Revisiting Şekercioğlu et al. 2002

In a paper published in PNAS in 2002, Çağan Şekercioğlu, Paul Ehrlich, Gretchen Daily, Deniz Aygen, David Goehring and Randi Sandi showed. using data from forest fragments in Costa Rica, that the ability to move through the deforested matrix was the best predictor of persistence of understory insectivorous birds in small forest fragments. Bird diets, invertebrate community composition, and microclimate of the fragments, and habitat specificity of bird species had little effect on the pattern of persistence of bird species in fragments. Fourteen years after the paper was published, I spoke to Çağan Şekercioğlu about his motivation to do this study, memories of fieldwork and what we have learnt since about the persistence of understory insectivorous birds in habitat fragments.

Citation: Şekercioḡlu, Ç. H., Ehrlich, P. R., Daily, G. C., Aygen, D., Goehring, D., & Sandí, R. F. (2002). Disappearance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences, 99(1), 263-267.

Date of interview: Initial interview in 29 September 2016 (via Skype) with follow up questions over email in 2020.

Hari Sridhar: What was your motivation to do this work as part of your PhD?

Çağan Şekercioğlu: Prior to my PhD, I was at Harvard and did an undergraduate thesis there. And I studied the Kibale forest National Park of Uganda, where I compared the bird communities in unlogged forest, selectively-logged forest, and a conifer plantation. The selectively-logged forest was logged at two intensities: heavy and light. Okay. That was three months of fieldwork where I did point counts, mist-netting and vegetation surveys, with a local guy I trained as an assistant: Katabe Deo. I found out that the most sensitive group was the understory insectivores. While working on my thesis I read the literature and I found that, in the tropics, that group is consistently the most sensitive forest guild to fragmentation and disturbance and logging. So, basically, I came to Stanford planning to focus on understory insectivores, and to understand what makes them so sensitive. My hypothesis was that they were diet-limited.

HS: Stepping back a bit, how did you get interested in birds and in tropical forests?

CS: Well, I was always interested in nature and biodiversity, growing up in Istanbul. My interest in birds started when I was 14, again in Istanbul, and I became a bird \watcher. My interest in the tropics was just a natural result of my interest in wildlife and biodiversity, because, as I read, I realized that tropics are where biodiversity is the highest. I really wanted to work in the tropics one day. Actually, I became Turkey’s first tropical biologist as a result. I’m the first Turkish citizen who’s done a PhD in the tropics and I still work in the tropics.

HS: Was your PhD with Paul Ehrlich?

CS: Yes, Prof. Paul Ehrlich.

HS: How did you decide to work in this particular site in Costa Rica for your PhD?

CS: Well, that was partially due to Paul Ehrlich. I actually wanted to work in Manu National Park in Peru. But Paul Ehrlich was already working at this site in Costa Rica. He said it’s a very comfortable site. You know, we’ve got a research station, they make your bed every day, they have three course meals! But, actually, for me, that was a negative thing because I like working in remote, unstudied locations, because the more comfort you have, the more civilization you have, the more impacted the forest is. I had been to Manu National Park the year before my PhD – I was deciding where to work – and I went to Manu, Madidi, Yasuni and Tiputini in the Amazon basin, and I decided, okay, I’m going to work in Manu: remote, uncomfortable, but you know, world’s top bird biodiversity: more than a thousand bird species in a national park. So I told that to Paul, and he said, “well, you are free to work there, but if you work there I cannot provide you with research funding. But if you work in Costa Rica, I can pay for it.”

You know, sometimes, when you’re a grad student with no research money, you have to be practical. So I said “alright, I guess I have to work in Costa Rica”. Because I was working in Costa Rica, I actually end up changing my research question. My initial question was not about fragmentation because Cocha Cashu is not fragmented – it’s just prime beautiful rainforest. I wanted to study the community ecology of understory insectivores there. So, I ended up changing my question and focusing more on fragmentation. That actually ended up working out, and it ended up being an interesting study and a well-cited paper. For a scientist, there are always many interesting questions. So, just changing the study location is not the end of the world; you just rephrase and rethink the questions.

HS: Was this the major paper from your PhD dissertation?

CS: Well, it was the major field study. But I would consider the major paper from my thesis, the ecosystem consequences of bird declines paper, which is actually my second most-cited paper. It’s a global analysis of threatened birds, based on their different specializations, guilds, habitats and regions. And that paper is still getting cited, you know, 70 times a year. I still work on those topics and my 2016 book Why Birds Matter is about birds’ ecosystem services and the consequences of bird declines and extinctions.. And it’s, again, on birds’ ecosystem services and the consequences of bird declines and extinctions.

HS: In the paper you say you did the fieldwork between July 1999 and September 2000. And there are so many different things that you did – sample birds, sample invertebrates, sample bird diet and vegetation as well. Could you give us a sense of this fieldwork, i.e. what your daily routine was like and whether you had people to help you in the field?

CS: Well, yeah, so one good thing about, you know, working there with Paul Ehrlich’s support is that I did have the funding to hire local research assistants. Also, I had four Stanford undergraduates who came as part of an undergraduate research experience program and they were paid by Stanford University. Consequently, I did have a lot of help. I also had a colleague of mine, who was a second author on the paper, and she came also; she was an ornithologist. So, basically, we had two teams; she led one and I led one. Every morning, we would go to a different site, set up 12 nets, sample the bird community for six hours, band them, measure them and also get the diet samples by making them vomit. In the afternoon, I, primarily, would go over the diet samples under a microscope and try to understand what they ate. In the meanwhile, the undergraduates would go through all the invertebrates we collected and sort them to order and dry them and weigh them. Also in the afternoon is when we did the vegetation surveys. And at all aspects of fieldwork, we had about four local assistants, helping it. Local farmers working with the research station, so they learnt very well how to help with this type of research.

HS: Can we go over the names of the people you acknowledge to get a sense of how you knew them and how they helped?

CS: Okay.

HS: Tom Davis.

CS: Yeah, so Tom Davis was a volunteer, actually, a retired guy from Silicon Valley and he just came for, I think, two weeks to help out.

HS: Forrest Fleischmann.

CS: Stanford undergraduate, who was with the research experience program.

HS:  Angelina Sanderson.

CS: Same.

HS: Jason Sandi.

CS: Actually, this is a mistake. There was only Jeisson Sandi, a teenager and Randi’s brother.

HS: Audrey Tapia

CS: Local guy.

HS: Parker Van Valkenburgh

CS: Oh, Parker. Stanford undergraduate.

HS: Richard Bierregaard

CS: He’s a professor of tropical ornithology, and he was one of the reviewers.

HS: Carol Boggs

CS: Former Stanford faculty, and a part of our research group, who provided reviews and comments.

HS: Chris Canaday

CS: He reviewed the paper. He also wrote an earlier paper from Ecuador on insectivores. So basically, colleague who reviewed the paper

HS: Marcus Feldman

CS: Stanford professor who provided comments.

HS: Oliver Komar

CS: Colleague ornithologist who works in El Salvador, who provided comments.

HS: William Laurance

CS: Major professor, friend and colleague who commented on the paper.

HS: Gary Luck

CS: He was, at the time, a postdoc at Stanford. He also commented on the paper.

HS: Harold Mooney

CS: Top Stanford professor and my PhD committee member.

HS: Philip Stouffer

CS: Major colleague, professor who commented on the paper and gave advice during the research.

HS: Peter Vitousek

CS: My committee member. Stanford prof.

HS: How did this group of authors come together? Paul Ehrlich was, of course, your supervisor. Was Deniz Aygen the person who led one of the field teams?

CS: Yes, exactly. She led one of the banding teams.

HS: What about Gretchen Daily?

CS: Gretchen Daily was my PhD committee member and, at the time, she was a professor working with Paul Ehrlich. She provided feedback on the project and the paper,

HS: David Goehring

CS: Undergrad researcher who did a lot of the insect work.

HS: Randi Sandi?

CS: Local guy, who was the leader of the field assistants. I mostly worked with him in the field, like personally.

HS: Do you remember how long, approximately, you took to write this paper, and when and where you did most of the writing?

CS: I did the writing at Stanford. I guess the analyses and the first draft took six months, but then it took another year of reviews and getting it published.

HS: Did you write the first draft and then share it with the other authors? What was the process?

CS: Mainly between Paul Ehrlich and Gretchen Daily and Deniz.

HS: Was it all done over email?

CS: No. At the time, both Paul and Gretchen would comment on printed versions, and I would incorporate that.

HS: Did this paper have a relatively smooth ride through peer review? Was PNAS the first place it was submitted to?

CS: No. I submitted it to Nature and Science, but it was turned down. But both of them reviewed it, so that helped a lot. It made it better and then PNAS accepted it.

HS: Did the paper attract a lot of attention, both within academia and the popular press?

CS: Not in the popular press. PNAS wanted to do a press release on the paper, but their version was a bit exaggerated. I can’t remember what it was, but it was inaccurate. I, basically, had to go over the press release and say, you know, this is not the way it is. But then once I corrected it, I guess they didn’t find it as sensational, so they dropped the press release. But as far as impact, papers normally take a little time. But, you know, within a year this paper was attracting attention and citations, and it was steadily growing in impact. And, it went on for quite a while. And it’s still being cited highly, 50 times in 2020 alone. So, it’s still getting cited quite a lot.

HS: The paper is set up to test among four different hypotheses. Was that the motivation right from the beginning?

CS: Yeah, absolutely.

HS: And you found support for the limited dispersal hypothesis. Today, 19 years later, what have we learnt about these different hypotheses?

CS: More research has shown that these birds are truly sensitive to fragmentation. There is some recent evidence from Puerto Rico about the impact of insect declines, but, to my knowledge, I haven’t seen any paper that’s strongly showed that dietary limitation is what’s going on. That being said, I haven’t noticed another test of this hypothesis that was as intensive as ours because it is a lot of work. Looking through 800 bird vomit samples is not fun. But yeah, I mean, overall, it is a pretty good consensus that understory insectivores are very area sensitive, they are not good dispersers, and so they disappear from fragments. And, in fact, I created my world bird database, while working on this paper, because I wanted to see, globally, whether understory insectivores are sensitive to fragmentation in general. I decided to enter the diet of all bird species into a database, and it became this monster database that we’re still working on and publishing on. So, using that database, we did a global analysis of fragmentation effects on birds, with Joe Tobias and Tom Bregman in 2014. That was a big global meta-analysis. And it turns out that tropical insectivores are sensitive to fragmentation whereas temperate insectivores are not. And that’s because temperate insectivores tend to be mostly migratory, highly mobile species, most tropical insectivores are sedentary, resident, understory species. So, the global picture also supports our initial limited dispersal hypothesis.

HS: Do you continue to work in this site in Costa Rica?

CS: No, not anymore. Not since I moved to the University of Utah, and shifted my focus to Ethiopia and Ethiopian forests, which are very understudied. But I continue to publish from the site. I published a paper on manakins in 2015 and just published in 2019 another PNAS paper from Costa Rica. It is my most comprehensive one, based on analysis of all the bird banding data of more than 57,000 birds in seven habitats during my 12 years in Costa Rica.

HS: When was the last time you visited this site?

CS: I was there, I believe, in 2011.

HS: Would you would you say that these sites have changed a lot since the time you work there?

CS: Not a lot, but they’ve been changing in a favorable manner. Las Cruces Reserve belongs to the OTS. When I was there, they had started a restoration campaign and also a campaign to connect this isolated reserve to the big Guaymi (Ngäbe-Buglé) Indian Reserve, through reforestation and purchasing forest fragments in between. That has been making steady progress. Las Cruces Forest Reserve is now bigger than when I worked there, due to reforestation and restoration. And they’re still working on connecting it to the bigger forest in the west.

HS:  What about the fragments? Do you know what has happened to the fragments?

CS: I do not, to be honest. I can’t imagine them getting better, because they are, mostly, private property surrounded by pastures and coffee plantations. Even while we were there, occasionally, somebody would cut a tree, even though it’s illegal. So, it would be hard to improve them.

HS: What kind of an impact did this paper have on your career?

CS: Yeah, well, it’s got me to think about doing long-term studies. Because, you know, after I did the paper, I had a lot of other questions, like some of them you were asking, and I realized, that a lot of these questions you cannot answer in one or two research seasons. You have to do these long-term population biology and community ecology studies, which I’ve been doing ever since. In fact, I ended up working at Las Cruces for 12 years, which is quite a long time.

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

CS: Well, there has been a lot of other work in the tropics on forest bird communities and understory bird communities. So, when other people find that understory insectivores are the most sensitive group, they cite this paper in support of that. So, it’s mostly tropical ornithologists and conservation biologists. But it does get a range of citations from other topics; sometimes surprisingly. But it’s mostly on this topic.

HS: Towards the end of the paper you say, “More research comparing the movement, foraging, and breeding patterns of understory insectivores and other guilds in both forest fragments of various sizes and in open countryside is needed to reveal the actual mechanism(s) of the disappearance of understory insectivores.”To what extent has this happened?

CS: I’ve done some of it at Las Cruces later, radio-tracking different species, both in forest and countryside, and also studying their reproductive success. So, some has happened, definitely. But, you know, we have more than 6000 tropical-limited bird species, many of which we still don’t know enough about their life-history and behavior and population dynamics. A lot of the tropical studies are still limited to one or two seasons, and they tend to be limited to point counts or mist-netting for a couple seasons. So they’re basically surveys. There are far fewer studies that actually go and radio-track birds across multiple years and study their breeding success and study different parts of their life cycle. Yeah, so it’s definitely not at a level that is satisfactory. In our 2019 PNAS paper from Las Cruces, we analyzed all our banding data from 12 years. More than 57,000 birds mist netted in 19 sites and 7 habitats. We looked at changes in the communities and populations. Sadly, insectivores are continuing to decline and disappear from fragments and coffee plantations, even the Las Cruces Forest Reserve.

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

CS: I have. Yeah, I did. But, it’s been a while.

HS: In what context?

CS: Well, I mean, a couple times, I was referring to this paper in another publication. So, I just read it to make sure I was referring to it correctly. But also, a couple of times I read it because I needed a reference, and I thought I had cited it in this paper, you know, and I found it there.

HS: If you compared this paper to the papers you write today, do you notice any striking differences in the way you write?

CS: That’s a good question. Well, yeah, I mean, with this paper, I was pretty focused on my own data and analysis and results, so I first finished those. Whereas, currently, when I write a paper, I first read all the relevant literature. And I take longer reading literature and preparing the Introduction, so by the time I get to the methods and results, I actually know the relevant literature much better. So that, when I’m writing the results of discussion, it’s easier for me to emphasize the novelty of our findings and the relevance of our findings and how they relate to the current literature. That would be the main difference, I’d say.

HS: Would you count this as a favorites among the papers you’ve written?

CS: Oh, absolutely. I mean, your first PhD paper is always one of your favorites. It’s also a favorite because it was a ton of work, and, of course, you always worry when you start your PhD, if you’ll discover something truly important, and if you’ll get it published in a good journal, and if it’s going to attract attention. All these happened, and I learned a lot doing it. So, yes, definitely, I’d say one of my top five.

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

CS: Absolutely. I mean, one thing I would do, these days, is I wouldn’t be trying to ID invertebrates under a microscope.  I would use genetic methods to analyze the vomit samples, and I’m sure I’d be much more accurate than using a microscope. So that would be probably the biggest difference.

HS: What would you say to a student who’s about to read this paper today? What should he or she take away from this paper published 19 years ago? And would you add any caveats?

CS: Well, let’s see. I mean, of course, with any paper, I recommend students to read the papers critically, and think about ways they can improve the paper, and also think about alternative hypotheses that could explain the data. Most importantly, while reading the paper, it helps a lot if they have their own related questions, and if they read the paper with an eye towards how they could answer those questions and how they could improve their research, so that they get better answers.

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