Revisiting Komdeur et al. 1997

In a paper published in Nature in 1997, Jan Komdeur, Serge Daan, Joost Tinbergen and Christa Mateman showed, through a combination of observation, experiment and genetic analysis, that, in the endemic and endangered Seychelles warbler, parents can manipulate sex ratio adaptively to improve their future reproductive success. Nineteen years after the paper was published, I spoke to Jan Komdeur about his motivation to do this study, his memories of field work and what we have learnt since about adaptive sex ration modification in the Seychelles warbler.

Citation: Komdeur, J., Daan, S., Tinbergen, J., & Mateman, C. (1997). Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature, 385(6616), 522-525.

Date of interview: 30th August 2016 (via Skype)


Hari Sridhar: How did you get interested in the Seychelles warbler? Was the interest, initially, in its conservation?

Jan Komdeur: No, not really. When I started work on the small island of Cousin in the Seychelles, I had to do some managing jobs. So there’s monitoring birds, turtles and so on, but I was really into scientific research. But then at a time I was employed by the BirdLife International organization. Had to focus mostly on monitoring and guiding around tourists on Cousin, a tropical paradise, but was allowed to spend some time on research. So I had to do tourists and management work and all this monitoring. I was allowed to do one third of my time research and I wanted to work on endemic land birds. And because there’s only three land bird species present on the small island where I lived, I had the option to choose between the Seychelles warbler or the Seychelles fody or the Seychelles sunbird. I found one article on the Seychelles fody and I thought, okay, I don’t want to do this because it has been studied.  And then the previous warden – she had studied Seychelles sunbirds. And I did not want to do that, because that has been done. But I was not able to find a proper article on the Seychelles warbler. So I decided to study that bird, and also because the whole world population was at that time only present on one small island. I thought if you study the whole world population, and if you’re not good at statistics, you don’t need to do statistics because you are studying all the birds!

So I wanted to study the Seychelles warbler. And I heard from somebody that they had a cooperative breeding system. And I was interested in that. But before I was able to think about any possible questions and answers, I first had to find out how many birds there were, and how many territories there are on the island. So I imported lots of batteries from Europe, because at that time you weren’t able to buy batteries in the Seychelles. And also I had tape recorders with recording of warbler song and so I did playbacks. And they were highly territorial. After a couple of months, I had all the territories located, about 110 – 116 on the island – and I tried to catch as many birds as possible with mist nets and tapes. So I lured them into the net, I put unique combination of colour rings on nearly all the birds and metal rings with unique numbers. And with the colouring combination, I was able to monitor each bird in the field. I knew all the individuals. In the end, I managed to catch all the birds; I couldn’t see any un-ringed birds anymore, so I assumed I had them all. But then I was worried because, after half a year, I never found a nest of the warbler. I found heaps of nests, but these were all from seabirds or Seychelles fodies or sunbirds. The first Seychelles warbler nest I found after a half year, in May-June. And then suddenly there were lots of Seychelles warbler nests, so they were having a breeding season – they don’t breed the whole year round. That is not what I expected because, in the tropics compared to Holland, I thought there would be lots of food available all year around. But it was not the case. So I found lots of nests. And also what I found is that they lay only one egg – most of the breeding pairs – and some of the breeding pairs were indeed assisted by adults. And then slowly I got many questions. At the time, I didn’t have any access to the library. I had only one chapter with me, by Nick Davies, from the book An Introduction to Behavioural Ecology. That was sort of my Bible.But I had to invent all the questions myself. I was not biased by the literature; I started from scratch. So that is how it all started.

To answer your question about conservation: The whole world population is entirely confined to one small island in the Indian Ocean and can be easily wiped out by introduced diseases or predators, such as rats and mice. Moreover, if there are historical records from other islands where they know that warblers existed, you should try to put the population back. I became friends with local wardens. And I started investigating the number of insects on the other islands, because the Seychelles warbler is an insect eater – it takes 98% of its food from leaves. So I monitored insect abundance every year, every month, and also the tree species.And I also monitored the other bird species on the island to make sure there’s an open niche available for the Seychelles warbler. And then in the end, I was sure that there was one open niche available for the warbler. So there was enough food on the other islands for warblers to sustain a healthy population. Also, from one island, I knew there were historical records that the warbler existed there, so it was ready to go. Initially, I did not get permission because my employer informed me that we first should have proven that the other island is suitable for the warblers. And then I said, okay, I’ve all the data, I wrote the report and then we translocated 29 warblers to the other islands. Note the total population size of warblers amounts to ca. 5000 birds present on five islands in Seychelles. So yes, conservation is important for me. But it’s really nice that we were able to combine conservation with pure scientific work.


HS: Do you remember which chapter of Nick’ Davies “Introduction to Behavioural Ecology” you had with you?

JK: This is the book I had with me. This is actually the copy of the book I had on the islands and I think it is chapter 12. Yes. “Cooperation and Helping in Birds, Mammals and Fish.” And it was a book given to me by a student from Cambridge, Georgia Mason, who visited me in 1989 to do her honours project with me. And this book is from 1981. And I had come to the island in 1985. This is still ancient.


HS: How did you discover the Krebs and Davies textbook?

JK: Ah yeah. First of all I observed there were helpers at the nest. And at that time I did not have the book so I was surprised to see adult birds that were sexually mature that did not reproduce themselves but helped other birds raising their offspring and incubating the egg. And then I also found out that the whole island was covered with territories. There was no empty space left on the island for other birds to establish new territory. So I thought maybe habitat saturation was a driver for cooperation. And then I mentioned this to a lecturer I knew in Holland. And he said, oh, you should read that book by Krebs and Davies. It was one of my old lecturers, and then he sent a copy of the chapter on cooperative breeding of that book to me (it took 3-4 weeks for the post to get it to me). I read that chapter and I realized that cooperation sort of has been observed in other bird species and mammalian species. However, I did observe other things which were not written in the book chapter. But at least, the book chapter formed the basis for my thinking. So it mentioned that habitat saturation may be a main cause for cooperation. But I also noticed that when, for example, a vacancy became available in a very low quality territory with hardly any food present, it may take days for the vacancy to be filled up. The helpers present on the surrounding territories remain there; they do not take up the vacancy. And I wanted to know why is that, and found out that the quality of a territory (expressed as insect food abundance) in which individuals live is also an important driver for cooperation; so not only saturation, but also territory quality. For example, if you are born in a high quality territory, it may be better for you to stay and help to have a longer life expectancy, and a better chance to find a territory later, than, for example, disperse immediately to a low quality territory where mortality rate is really high, and where it’s very hard to reproduce. So that is how it got started.


HS: How did you end up doing a PhD in Cambridge?

JK: Yes, I did my PhD in Cambridge on the Seychelles warbler.  I finished in 1991. When I started my job in the Seychelles in 1985 – it was December 1985 -I never wanted to do a PhD. I was quite annoyed with my university in the Netherlands.They promised that I could do a PhD and said, okay, you just get started and then the money will be there. So I spent a whole year doing work without pay. And then every time I asked, is the money there? they said, yeah, no worries, the money will be there. In the end, I decided to quit their job. I took on the warden job in the Seychelles, and I told everybody I never want to do a PhD because of what happened. Then, after two years, Martin Garnett, associated with Oxford, passed by on the island who asked, do you want to do a PhD? I said, no, I don’t want to do a PhD, for definite reason. And then, after half year, Martin Garnett and Mike Rands (director) from BirdLife International passed by and said, do you want to continue in science? I said, of course I want to continue with science. And do you want to do a PhD. I said, no. And then he said, if you want to continue in science you should do a PhD. Oh, I said, Okay, then I will do a PhD. And then he said, you should do a PhD at Oxford. I can make sure that you get selected and you do a PhD with Prof. Chris Perrins. So I decided to start my PhD. But on the way to Oxford, Nick Davies and Tim Clutton-Brock asked me whether I wanted to give a seminar in Cambridge. That was in September 1988. And after the seminar they asked, Jan, do you want to do a PhD with us, because your data is so exciting. I said,No, no,no, I can’t because I have to go to Oxford and I will start my PhD there. And then they said, no worries, we will organize that you don’t need to do your PhD in Oxford. So I discussed it with some other people and then said, yes, of course I would like to do a PhD with you two.

I hadn’t heard so much about Nick Davies and Tim Clutton-Brock, because at the time I lived on a small island. I didn’t realize they were very famous people. The next day I was interviewed, got through and did my PhD in Cambridge. That’s how it happened. And it was one of the best years of my life.


HS: Were Nick Davies and Tim Clutton-Brock your PhD supervisors?

JK: Yeah, Nick Davies was my first supervisor, Tim Clutton- Brock was my external, but also I had an external from Birdlife International, Dr. Mike Rands. He was a new director, and extremely supportive. He supported me in translocating birds to other islands, and getting the part of the PhD financed from Birdlife International. So I had three supervisors.


HS: How did the authors of this paper come together?

JK: After my PhD I moved to Denmark. And, actually, my first paper on habitat saturation as a main driver for cooperation I published in Nature. Nick Davies said you should publish that in Nature.I’d never heard about Nature; I didn’t know what sort of journal it was. I thought it was just a nature observations sort of journal; sort of low standard. But then I published that paper and got the job in Denmark in an applied institution at Kalø, a small village near Århus. But I really wanted to go back to more pure science and missed university atmosphere with students. After three years, Nick Davies said if you want to go back to pure science you should try to do so within three years, otherwise, it will be very hard for you to become a postdoctoral fellow or have a scientific career. So I quit my job in Denmark, even though it was a permanent position and they didn’t want me to leave. They offered me a sabbatical for two years, so I was able to come back. So, I took a risk. I quit the job, took a two year post-doc position, to investigate the effects of territory quality and the number of helpers on sex ratio modification in the Seychelles warbler.  I applied for the Science Foundation grant to become a post-doc in the Netherlands with professor Serge Daan – he is the second author of this article – and Dr. Joost Tinbergen, who is a Professor now. He is a third author or on the article. Christa Mateman is the fourth author. She was the technician who helped me in sexing all of these blood samples. It started when I  gave a talk at a scientific meeting in Norwich (UK); that was in 1992. And there, for the first time I met with Serge Daan and Joost Tinbergen. I presented a talk on egg sex ratios and they said, that’s really exciting. We want you to be in our group; we should write a grant proposal. So that’s how it all started. And it was exciting indeed because it helped me to get another paper in Nature.


HS: Give us a sense of the field work during this study.

JK: I spent about five years non-stop on the small island of Cousin (1985-1990), and thereafter three to four months each year in the field. I was there on my own, and I had one or two students with me. Then in 1993-1995, I spent again four months in the field. At that time,Serge Daan and Joose Tinbergen visited me for three weeks. I think it was important for them also to have a feel for the Seychelles warbler  environment, to get ideas, and also to see how difficult it is to study warblers in a tropical rain woodlands. There are no paths on the island. And even though the island is small – 500 by 500 meters – you really have to know all the stones and all the trees on the island to at least know the territory borders, and for your orientation. So they were really excited to be there, but also got a feel for the difficulties in following the birds of course. And then later on, when we discussed Seychelles warblers, they had a good feeling for the site so I was able to discuss with them whether they think it is feasible or not. And then, in Holland, I worked at the University of Groningen and we met say every week – every week we had a seminar – or whenever there was a discussion needed. I discussed it with Serge Daan and sometimes with Joost Tinbergen,s ay every month. Christa Mateman was not involved in any fieldwork; with her I discussed all my problems I had in sexing the birds. I had to do it all myself and, at the time, it was really complex. So I visited her in Wageningen. That is the Netherlands Institute for Ecology,  about two hours drive from Groningen. She helped me in getting the molecular techniques correct and we managed to sex the birds’ blood samples. She was crucial for this


HS: Were you doing most of the field work on your own? Did you have any assistance in the field?

JK: Yeah I spent the first five years on the island myself with my former wife. It was remote but I like to be alone. And also Birdlife International warned me that they will only have a contract for one year because most of the couples split up and also people get insane because it is such a small place. But I was completely happy. I had my own dinghy, and I used the boat if I had to do some shopping every now and then. I had to drink rainwater. There was no electricity, no fridge, nothing. In the evenings you have to work with candle light. You are very happy if you can buy some paper in a local store and a pencil; or a notebook. It was very hard to buy all these things. I had a binocular. But I managed; I worked really hard. People in Seychelles told me that I worked too hard. I was there every day, all day. Normally people do a siesta, but I didn’t. I enjoyed the work a lot. I had no stress, I was in very good condition, so it was not as difficult as people thought it was. I did most of the work alone, although, when I started my PhD, I also got students from Holland, from England, from all over the place. They were essential as well, because without them, I would not have been able to do more elaborate work. My former wife helped me a lot as well.

I spent five years on the islands. I didn’t want to go home. When after two and a half years, we (me and my wife) had a short holiday, we went to Africa instead, for three or four weeks, to do some hitchhiking. We didn’t have a valid visa , but I thought I can bribe the guy from Kenya to Tanzania, Tanzania to Rwanda. We wanted to see the gorillas. But I did not realize when you get in, you have to get out. So we had to hide in a truck. And there was some way and I had to bribe the drivers, but it was really…We will never do that again, but we saw the gorillas.

I was so happy there in the Seychelles and I still go down. So I told you that I was only allowed to stay there one year, but then people visited us and they really thought that we were a great couple, so we were allowed to stay for another one and a half year. But then I started my PhD in Cambridge, and I needed to be in the Seychelles for three years. And then they offered me a post-doctorate on the Seychelles magpie robin on Fregate – that’s another island – but in the meantime, I was able to spend one and a half month to continue studies on the Seychelles warbler. And then after five years, I wanted to leave. I didn’t want to study warblers anymore. So I left. But I didn’t realize at that time, that the big journey had just started, because we’re still working on these birds, and there are so many new research questions to explore.


HS: Can you tell us a little more about the people you acknowledge – how you knew them and how did they help?

JK: Lars Gabrielsen was a Danish colleague of mine. He was a PhD of mine when I worked in Denmark. He assisted me during one field season in 1993 and 1994 to collect blood samples and to do nest observations. And the same is true for Andres Datema. He was a student of mine from Waganingen who also helped out in 1994-1995. They were both involved in field work. Cor Dijkstra was a colleague of mine from Groningen. And he was really nice. He was the pioneer of sex ratio studies in kestrels, in birds of prey, and I had lots of good discussions with him, and learned a lot from him. He advised a lot also in the data analyses and interpretation of data. I also notice here that I thank Cor Dijkstra for double-scoring the sex of nestlings. I forgot to mention it. That was really important. I first sexed the blood samples myself, to tell whether it was a male or a female. And then Cor did the same, for every sample, to validate my classification.

Okay, I thank Dr Kate Lessells and Prof. Patty Gowaty for comments on the manuscript. Yeah, I knew Kate Lessells in 1993. She was the one who started out sexing of embryos and young chicks based on the blood sample DNA extraction. That was in her molecular lab. Kate was the first one who managed to sex birds in the Netherlands. And I had a good discussion with her in 1993. She also sexed some pilot samples I gave her because we wanted to know whether it was possible to determine the sex of blood samples taken from Seychelles warbler nestlings. If that was not possible, I would not have written a grant application. But it was possible,and so I wrote a grant application and we got funding. Patty Gowaty, I met in the States several times at conferences.She studies sex ratios in another cooperative breeder  – eastern blue birds (US). We became very good friends. At that time when I met her  we had dinner together, we discussed work and we had email conversation. She was intrigued by the findings in the Seychelles warbler, and helped me commenting on the manuscripts, and so I’m very grateful to her as well. Patty is already retired a while ago.


HS: How long did the writing of this paper take? When and where did you do most of the writing?

JK: I think the writing in itself didn’t take that long. However, grasping the concepts and ruling out alternatives and doing the analyses did. I wanted to be absolutely sure that the analyses were correct. So I also sent all the data blindly to Tinbergen and Daan. Joost Tinbergen is an extremely good expert in statistics and he re-analyzed the data and reached the same conclusion. So that took some while.

I did all my writing at the university and shared drafts with the other authors. Serge was really good at seeing the red line through the manuscripts, and where to start,where to end. We had several discussions, and I also presented at some meetings. So I got feedback from the students, from post-docs and other staff members and slowly we got the whole idea for this paper.And then when we were writing the paper we could only use 1700 words, the word limit for Nature. It was difficult to decide what to include and what to leave out, but after we knew exactly what to include, the writing was not so hard. Christa Mateman commented on the red line of the paper and contributed to data analyses. I shared drafts to all the authors at frequent intervals.


HS: How were the figures for the paper made?

JK: At that time we were in a luxury position that we could make draft figures in an SPSS package. At that time, that was the statistical package that we used. The figures were made by our graphical designer Dick Visser. I don’t know whether I quoted him but he finished and drafted the figures for us. First, we had some draft figures and then he polished them up and made them really nice.At the time he used a software program that has more possibilities to make some good figures.


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

JK: Yep, I submitted to Nature first. I submitted the paper before I went to an ISBE conference in Canberra 1996 and when it got back it was preliminary accepted; we had to incorporate some comments from two referees, I think. But it was very fast.


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

JK: Yep, it came out when I moved to Australia, to work at university of Melbourne. I moved to Australian December 1996. I lived in Australia for one and a half year. And then I got phone calls from New York Times, from Radio Australia, newspapers all over the world immediately after arrival in Australia. So it attracted lots of attention. And I think I have all these clippings still.It was quite immense. So I had interviews, early morning hours, late night, because of the time shifts all over the world.


HS: What about in academia?

JK: Yeah, I also believe in academia, because I was told that this is a textbook example for sex-ratio modification in birds. So whenever you see a textbook, they refer to this paper and also include the figures. They always asked permission whether they can use the figures. Before this work, there were something known about offspring sex ratio modification in domestic quail and birds of prey in the wild, but very little about sex ratio modification at the egg stage and fitness consequences for the offspring and parents in wild bird species.And ever since, there are heaps of sex ratio studies in birds as well as mammals. And at least this showed that female birds were able to bias the sex ratio already at egg laying in the way they want. And in birds, it is the female who decides about the sex, whereas in mammals, it’s the other way around, i.e. it’s the male who decided about the sex.

This also formed the basis for many other questions. At first this seems adaptive for breeding pair because female offspring normally help and male offspring normally disperse and do not help. By producing female offspring on high quality territories these females remain on their natal territories to become a helper thereby improving future reproductive success for the breeding pair. By producing male offspring on low quality territories (which disperse after reaching independence), breeding pairs avoid having future helpers, and thus avoid future competition for food which would have led to lower future reproductive output. But then what are the long-term benefits of sex ratio modification for the breeding male, female, and also for the helper? You need long-term studies and you need more experimentation. So it stimulated lots of research into primary and secondary sex ratio modification, but also the causes – what makes birds do this? Is it hormonal? Is it environmental? Is it condition? So there are lots of people also studying sex ratio variation in captive pigeons; they are easy to hold and to manipulate as well. So you can inject them with hormones, check whether sex ratio changes. Ever since this study, sex ratio studies is an exciting field and they still working on sex ratios nowadays.


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

JK: This paper and also the previous paper I had in Nature opened up my career enormously. I’m really grateful to Nick Davies and Tim Clutton-Brock for the first Nature paper, and to Serge Daan and Joost Tinbergen for this one. I thing that once you get a Nature paper, that it’s relatively easy to get jobs. Although I don’t like this sort of nepotistic idea – I really admire people who have written thorough researches in normal journals – but the Nature papers also made it very easy to get major funding for further investigations into the Seychelles warbler to continue work on the warblers to investigate the adaptive significance of sex ratio modification in Seychelles warbler. It was quite easy to get funding at the time, so it had a big impact. And of course, you can then attract students, PhD students, so you get PhDs delivered, you have new findings, more publications in highly cited journals, more grants,  so it’s like a snowball effect. So, once you have done a good paper, an excellent paper, I think you have a better chance in your career, easier than, for example, if you struggle and struggle, and don’t manage to get any high impact papers. So, I’ve been lucky to have been working with Seychelles warblers.

When the paper came out, I applied for four jobs – Melbourne,Cape Town, Tour du Valat (France) and Oxford, was invited for an interview in all four of them and was offered three jobs. I decided to go to Melbourne. But I think that without this paper and the first one published in Nature (1992) it would have been much harder for me to find jobs.


HS: Today, 19 years after the paper was published, would you say the main findings and conclusions still hold true more-or-less?

JK: Yeah, the main conclusions are still true more-or-less. I’ve thought about this. So this is true for when there are birds living in a very stable environment. At a time,the inner part of the island was high quality and the outer surrounding part was low quality. So, in the inner part high quality territories,the birds mainly produced female eggs in order to have female helpers in the next year (because males normally disperse). On low quality territories they mainly produced male eggs, which will produce sons who will disperse. They don’t want to have helpers because in low quality territories they will compete for food with the parents and therefore the parents cannot produce successfully in the next few years if they still have a helper around. That is true if the island remains stable in terms of environmental (food) quality. But incredibly, over the years now, the whole island is high quality territory. Between 1920 and 1968, in the whole island the original vegetation was cut down and replaced/planted with coconut trees and only 24 -29 warblers survived, and it was in a mangrove area, which was a stronghold for the warbler population. The coconuts do not like wet fields, so they died, and then  the coconut trees were put down from 1968 onwards when the island was bought by BirdLife International, allowing the original endemic and indigenous threes to regrow. At the beginning,  the inner part was high quality (lots of vegetation) and the outer part low quality (less vegetation as a consequence of wind-blown salt spray from the sea). But then slowly the trees grow and grow all over the island.

Yeah, so, at the time the vegetation was still changing, and this is how it was until 99 – 2000. But now the low quality areas have also turned into high quality areas. And then you see that birds that produced male eggs on low quality territory, the same birds, if you followed them for example, 5-8 years later, they produce female eggs. So they adjust towards changing environmental qualities.

So now, I thought, okay, there will be an excess of female birds on the island because most of them switched to female eggs. But that was not the case.They produce equal male and equal female eggs all over the islands, and it seems like that sex ratio allocation is not so much adjusted to territory quality anymore. Because the whole island is high quality territory, there is no adaptive reason to do egg modifications anymore. We are analyzing this and we are in the process of writing this up into a long-term study on sex modification. I also concluded in my paper that it is adaptive for the breeding pair to produce a male on low quality and a female on high quality territories. But that’s in the short term. And, of course, you will have helpers on high quality territory one or two years later. But then we also found out that female helpers can lay an egg into a nest of the mother and compete for breeding with the mother. At that time, we were not able to do paternity –  that was possible later on, and then we found out that 44% of all these female helpers produced eggs, and a lot of them produced an egg in the nest of the mother. Sometimes the mother skipped a breeding season and allowed the daughter to lay, and even helped in nest building. But even though the mother skips a breeding year, in the long term, it pays for her to allow the helper to lay an egg, because by allowing a helper to produce, the helper then is more inclined to stay and you will reap the benefits of helping for a longer time. So the conclusions haven’t overall changed, but we have to be careful because this is only based on one breeding event. Breeding females make multiple nests in the life. So, for example, if as a breeding pair produce one female, and in the next year, still have the female, you may produce another female egg, but then in the long-term may have lots of offspring produced and it is still beneficial then to produce female eggs on high quality territory or maybe better to switch to males. So you need to do long-term monitoring and you need to calculate the inclusive fitness benefits of producing an egg – male or female. How many offspring will you be able to produce through help is bit complex, but you need to calculate inclusive fitness benefits and that requires thorough and thorough investigations.


HS: Do you continue to work in this study site? When was the last time you visited this place?

JK: Yeah, I do continue to visit the site and work there.But, as you may know, I’m a professor now and there’s lots of administrative work. I also work in Spitsbergen now and go there quite often, as well as in China, Chile and Australia, but also have many projects running in the Netherlands. At the moment, we have a total of five post-docs, nine PhDs and four technicians working on the Seychelles warbler. And the warblers are now distributed over five islands as a consequence of translocations of some warblers to other islands we conducted in the past. It takes quite some effort, as well as money and logistics to make sure that, every year, the warblers have been monitored. Because you don’t want to have a gap; you want to have continuous monitoring. And whenever it’s necessary I go there. The last time I was there was five years ago. I want to go there again for research next year; this year and the year before I had to go to other places, and so you have to take turns. Normally what I do is, when research goes well, and I have good post-docs, and PhD students, I do not join them myself in the field. I’d rather go to places where you have to set up new work and help out new PhD students and post-docs. Cousin Island has changed a lot since I was there. Every time when I go there it feels like home. But if I look at the soil, I know still most of the pebbles and stones, but the trees are different to me. I can walk there blindly, more or less, but I have to look at the composition of stones, rocks, special trees etc. to orientate myself in the dense tropical woodlandbut still, it’s fairly familiar when I go there. The smell is familiar. And it feels like I haven’t been away.


HS: What’s the current status of the birds you translocated? Have you continued doing translocations?

JK: Good point. In 1988 I translocated first birds to Aride island, which were high quality. On Aride island, all the birds established high quality territories, and they all formed pairs within a couple of days. They produced the first eggs within a week. And because they all established high quality territories, they nearly always  produced females. That lasted for about three years. After that, I think about 60% of all the eggs laid on Aride over time contained male embryos. I was able to repeat what I found on the island of Cousine. And then slowly the warblers occupied lower quality territories and these other birds produced male eggs. So ostensibly it’s not adaptive for them to produce female eggs because it took a while for the translocated birds to grow. Because if you produce mainly females, there are no partners. But now on Aride, the population is estimated to be about 2500 birds. There was a census about 3-4 years ago. And then I translocated the birds to Cousine in 1990, and the population there at habitat saturation is about 260 birds. Then in 2004, we translocated birds to Denis, and the population is still not saturated. Three years ago, we observed for the first time cooperative breeding that was more than15 years after the translocation. There the birds had a problem because of the introduced Indian myna. We had video evidence of the mynas attacking and killing warblers when they were incubating. They are on the nest and it’s very easy prey to the mynas. Because only female birds incubate, quite a lot of females were killed, which resulted in an extreme bias towards adult male birds in the population about 80% of birds are males  – adults – it is extremely biased and it still holds true 10-12 years later. So we are writing that up. It took a while for them to grow because of all these high mortalities and also eggs that were predated upon, but then slowly they can get off and now the population is estimated to be about 180 birds. And then we translocated the birds to Fregate in 2011. And there they do quite well, but we have only monitored the population for two years after the translocation. We reckon there’s about another 200 birds present there. Oh yeah, and also last year, the warbler was no longer on the list of endangered species . It is one of the few examples of species that have come out of the list of endangered species. So this is good news. It was even on TV and news worldwide, and Seychelles named one of their airbus after the warbler ‘Merle des Isle’ (creole name for Seychelles warbler)  It was good.

Normally warblers don’t fly off the island. I analyzed the flight muscles using some dead specimens and compared them with well-flying Acrocephalus species –great reed warbler and Australian warbler  – who can fly easily up to 4000 kilometres – and they are quite similar in the flight operators (wing span and wing surface) and flight muscles corrected for body mass. So, ostensibly, they can fly, but they don’t. I think there’s no selection pressure for them to fly to other islands, because originally all the islands were covered with warblers. But then, in 1990, I translocated a male to Cousine and he produced offspring there with a wife for three years, and then flew back to Cousin, kicked out the male from his old territory and established position back in his old territory. Also from Fregate island, two birds came back to Cousin. It is quite interesting. But most of the birds, of course, stayed on the island where they were translocated.


HS: If you were to redo this study today, would you change anything?

JK: I will do most of it the same way. But nowadays, there’s more politics involved. Then I was on my own, so I didn’t need to discuss things. Whenever I had an idea (sometimes a good one), I was able to do it straight away in the morning when I woke up. But now if I have an idea, I have to make sure that everybody’s happy, or that we get permission. We now collaborate intensively with Nature Seychelles. At that time, you didn’t have any ethics approval ; you just do the things you want to do. But now it has to go through approval. This is, of course, important, because they are endangered birds, and before you do any things, you must make sure you don’t harm the bird, and also that all are happy what you do.

But, I think, yes, overall, I will do the study the same way as I did it then. Of course I wanted to have as large sample size as possible, but this is all we could have. There were no more bird nests available. This is what I had to live with.


HS: Since then, have there been studies that have documented adaptive sex ratio modification in other species?

JK: Yeah, there is a parrot species, the Eclectus parrot showing extreme egg sex ratio modification. Yeah, there’s quite some studies,\ I have seen, on zebra finches, showing that if you  pair females with  high quality and attractive mate they change the sex ratio of their eggs towards sons (who may inherit the characteristics of their dad, and be attractive for females in the future). Also this has given a boost to studies in the wild studying adaptive sex ratio modification. When I started the study, it was already known for kestrels, that they bias the first laid egg towards males. Because in birds of prey, males are the smaller sex, so by biasing the first egg towards males, and the second or third act towards females, you get equal sizes, i.e. because first egg hatches earlier than the second or third egg. So, within-nest sex-ratio bias that was already known, but sex ratio bias related to habitat quality was not known before this study. Since then, there been several studies on house sparrows, on other birds of prey,  blue tits, laughing kookaburra, great tits; heaps of passerine species have been studied ever since. And I must say, whenever I read those studies, they refer to this paper, stating that one of the reasons they wanted to study this study system is that apparently it seems like their birds can bias their eggs like the Seychelles warblers.


HS: Have you ever read this paper after it was published? Do you find it different from the way you write today?

JK: Yes, I have read the paper since. Whenever I write papers, and I incorporate my earlier papers into them,  I always read the papers again to make sure that what is mentioned in the papers is correctly been cited. Of course, I still try high journals. At the moment we are about to submit a paper to Nature, but that is not written by me, but by a post-doc of mine. But I have one in line for Science; that’s a paper I wrote myself. So yes, I will make sure I spend one or two days a week, if possible, to write myself. Many people who are professors don’t write papers anymore. They rely on their PhDs to write papers. But I’m primarily a researcher. Of course, I also have lots of administrative work, lots of board meetings and committees, but I chose to study biology; to do research. I’m an explorer and I like to find answers. And that makes me happy. So if I cannot go into field myself or if I cannot write myself anymore, then I’m a full administer and that is what I don’t like. It keeps you sharp as well if you write yourself, but also if you have a very nice research group for discussion ideas, research and results.. I am fortunate to have a nice research group and to work with extremely nice colleagues.


HS: Would you count this paper as a favourite among all the papers you have written?

JK: Um, good question. It’s one of my favourites because it reminds me of the excellent time I had in the Seychelles and also in Holland. I shared an office with a nice lady at the time and  – maybe I should not say this – we had good conversation about research at the time, she was doing a PhD when I was a post-doc and she helped me a lot in getting discussions going. After my divorce seven years ago, I contacted my office mate and we are happily together and married ever since. And so whenever I see this paper I have a big smile. So it is one of my favourites, but I have many other favourite papers. But I do like research papers more than reviews or books, because if you write a research paper based on your own data or in combination with, you are trying to investigate something novel.


HS: What would you say to a student who is about to read this paper today? Would you guide his or her reading in anyway? Would you add any caveats he or she should keep in mind when reading this paper?

JK: The takeaway message of this paper is that birds can bias the sex ratio of the single egg. And this is not based on differential mortality, for example, if the less adaptive sex present in the egg dies so it won’t hatch. Instead, the egg sex modification happens already inside the mother before the egg is laid. And that is extremely novel. So, it is the mother who decides sex in birds.It is the mother who’s the heterochromatic sex so she can tell the sex of the offspring. And then, birds also bias the sex based on environmental cues, e.g. habitat quality in this case. There’s a very distinct shift from males to females, from low to high quality territories. And it seems to be adaptive. But the caveat is the long-term fitness benefits of egg sex modification.In this paper I conclude it is beneficial to a breeding bird to have males on low quality and females on high quality territories, because males disperse. So they don’t compete and females stay on high quality territories and help the breeding birds. And I have also shown before that the presence of helpers on high quality territories is positive for the breeding birds, resulting in higher reproductive output. And the presence of helpers on low quality is not positive, resulting in lower reproductive output because of competition for food between the breeding pair and the helper. So I did experiments to remove helpers, to demonstrate that the presence and absence of helpers on the same territory actually caused changes in reproductive output.This is all clear. But the caveat is that females can produce offspring that may compete with the mother for offspring production. And so, whether I analyzed the fitness benefits correctly, is still the question, because it was only based on the presence of helpers. But what you should do is calculate the long-term benefits of producing males on low and females on high quality territories. So what are the benefits eight years later, or five years later or three years after egg production? That requires more thorough investigations. Also, I said it’s adaptive for the mother, but what about the male breeder? Is it still adapted for a male breeder to have a female offspring on high quality territory and son on low quality territory? Maybe for the male, it is even more attractive to have a female offspring on high quality territory, because it can also produce offspring with the daughter. And we know that incestuous matings are common in the warbler. So there may be a discrepancy between fitness benefits of egg sex modification for males and females. There are studies necessary. But that they control egg sex ratio, that is evident from this paper, and it’s backed up with experiments. That is a good message of this paper.


What else would I say to students about to read this paper today? I also would ask the students, after reading this paper, how you would experimentally investigate the fitness benefits of sons produced on low quality and daughters produced on high quality territories. One answer is that you have to cross-foster chicks. So you have to select those breeding pairs that produce male egg on low quality territories and force them to raise female egg through cross fostering eggs, and similarly for those producing females on high quality territories. By swaps, you have to force them to raise male eggs and then you have to monitor what happens to male and female offspring. So is it true that breeding pairs producing, for example, females, have higher benefits than, for example those forced to produce sons on high quality territories. So I would ask the student, what have you learned about this paper, but also what will be your next experiments to investigate fitness? What are the shortcomings of this paper? I think this paper can form the basis for a solid discussion.



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