Revisiting Berthold et al. 1992

In a paper in Nature in 1992, Peter Berthold, Andreas Helbig, Gabriele Mohr and Ulrich Querner provided experimental evidence to show that central European blackcaps (Sylvia atricapilla) had evolved a new winter migration route, and established a new winter home over 1000 km away from their old one, in less than 30 years. Twenty-four years after the paper was published, I spoke to Peter Berthold about the making of this study and what we have learnt since then about the migratory behaviour of this species.

(Interview conducted via Skype on 27th July 2016)

Citation: Berthold, P., Helbig, A. J., Mohr, G., & Querner, U. (1992). Rapid microevolution of migratory behaviour in a wild bird species. Nature 360: 668-670.

 

Hari Sridhar: At the time when you published this paper, in 1992, you had already done a lot of work on migration, especially on blackcaps. What got you interested in the work presented in this paper?

Peter Berthold: We were really astonished by how rapidly changes in migratory behaviour can occur. When I was a student, I had learnt that, say, for changing a migratory direction or migration time by a week or so would take hundreds, if not thousands or tens of thousands, of years. And some people even doubted whether, after the Ice Age, any novel development of migration in Europe could have occurred. So of course, in the first instance, we couldn’t believe that within, let’s say a few decades, birds could change their migratory direction from a hitherto south-south-westerly-south-easterly direction to northwest, to England. This was baffling for all of us. And also for geneticists to whom I had spoken about it. This was the main reason to publish it.

 

HS: This paper has four authors. Could you tell us how this group came together and what each person brought to this study?

PB: Andreas Helbig was a PhD student, Ulrich Querner, at that time, was one of my main technical assistants, and Gabriele Mohr was also a technical assistant.

 

HS: Was Andreas Helbig your PhD student?

PB: Oh yes, he was in my lab and also in the laboratory of Wolfgang Wiltschko. You may have heard about the name Wiltschko. They are a scientist couple living in Frankfurt who have been the leading authorities on orientation research for a long time in Germany. Wolfgang Wiltschko discovered magnetic orientation in birds.

 

HS: Did Helbig continue in a career in research after his PhD?

PB: Yes, for a number of years, but then, unfortunately, he died of cancer. It was very sad.

 

HS: I’m sorry to hear that.

HS: In your paper you say you transported these birds back from Britain to Germany to do the experiments. Can you tell us a little about how you actually did this?

PB: This is as we have always done this – they were trapped with mist-nets and then put in small cages. There is a critical time in the beginning, especially on the first day, when you need to make sure that the birds will take food in the cage because otherwise they will die. Therefore, we have developed very specific methods to do this. The rest is very easy – to take them into a car, or from other countries, even by plane. This is something we had developed in our institute in a unique way. In this respect, we have been the world champions.

 

HS: How long did it take to drive from Britain to Germany?

PB: Less than a day.

 

HS: Did Andreas Helbig do most of the experiments?

PB: The experiments were run in a large group of people, including many technical assistants. The scientific investigations we did together, step by step. I would say it was split about 50-50.

 

HS: I want to find out a little more about the sites in Britain where you trapped blackcaps. You acknowledge a couple of agencies for permissions. At that time, was it difficult to get permits to move birds from one country to another?

PB: [Laughs] Not on principle. But of course, you know how it is with Britain, you have belonged to Britain for a long time. In most countries it was very easy to get permissions to take birds – France, Spain, Portugal etc. But the British, they say – Oh, these are our birds, and we normally don’t give permits.  So we told them – Listen, these birds that we would like to take from Britain are birds from Europe. They come only to winter with you. They are very bad continental intruders, and you should be happy about every bird that’s leaving England a little bit earlier than normal. You should be grateful to us for taking these food robbers from the British islands back to the continent. Then they said – Oh yes, of course, you will certainly have the permits to take these birds away.

 

HS: How did you pick the site in England – near Western-super-Mare – to trap the blackcaps for this study?

PB: This was an area in southern Britain, and we had two reasons to trap here. First, this was an area which had one of the highest densities of wintering birds from continental Europe. And second, this is an area with a lot of traps in the dunes, where it’s easy to post mist nets and drive the birds. The British people are very critical about mist-netting, and don’t allow it in their house gardens. In mid-England we have faced a lot of difficulties. But in these coastal areas it was very easy. So let’s say we had chosen the area for good practical reasons.

 

HS: In the paper, you say you used a “modified Emlen technique” for the migration direction experiments. Can you tell us what the modification you made was?

PB: You know, Emlen used these funnels and inkpads on the ground. The birds would sit on ink pads and when they try to leave the cage they produced these footprints on a white paper. In our technique, developed by Wiltschko and Helbig, we used rubber paper on which the feet, and especially the nails or claws, produce small scratches. These scratches are much more easily counted and investigated. For analysing all these scratches we have developed a specific computer program, which would take all the papers with the scratches and calculate the mean value of the direction and other necessary statistical values.

 

HS: Is migration still studied with similar apparatus?

PB: I think it’s rarely used now. The Wiltschko group continues to fit the data by eye. Now, in Germany, we have no other institute that’s really doing orientation research with songbirds. Only with larger species. In America they continue to use Emlen’s method.

 

HS: Have you gone back to the site in UK where you trapped birds, since you did this study? Do you know what the status of the site is?

PB: The site is the same as it was then. It is a protected area. But, of course, with climate warming, there will be changes!

 

HS: Have the blackcap numbers changed in this site?

PB: They have increased, and are still increasing. This development, started during my time there and is still going on. Now we have blackcaps wintering not only in Great Britain, Scotland and Ireland but also in southern Norway up to Finland. So the whole north is now a large, more or less closed, wintering area of blackcaps coming from continental Europe.

 

HS: Has this increase been documented systematically?

PB: It has been studied systematically by the British people. It’s quite easy because all British blackcaps are leave the breeding area during winter, and so the blackcaps you observe wintering in England are all from the continent. And the bird counts in Britain, as you know, are, by far, the best in the world. They count every individual.

 

HS: Do the outdoors aviaries that you used during these experiments still exist? Are they still used for experiments today?

PB:  Yes, they exist, but they have been changed. They have been enlarged. I’m retired for about 10 years now, and my successors no longer work with blackcaps. They work with blackbirds – Turdus merula – and the blackbird is, of course, a larger bird than the blackcap, and so the aviaries have been enlarged. What we used to called blackcap city is now blackbird city!

 

HS: Who did most of the writing for this paper and how long did it take?

PB: It was written by Helbig and me. Writing itself was very easy. It was done in three days or so. What took time was running the experiments – doing the orientation experiments took time, and the statistics to some extent. Once you are at the stage where you can start writing, it is very easy after that.

 

HS: Were the other two authors also involved in the writing?

PB: No, they were only involved in running the experiment and compiling the raw data.

 

HS: How did the writing actually happen – would you and Helbig sit together and work, or would you share drafts on a computer?

PB: At that time we didn’t use the computer. Till today, I do all my writing, even of books, by first hand-writing, then by dictating and getting it typed into a computer. Still in the very old fashion way.

 

HS: So you would sit and write it together?

PB: No, we would each sit each somewhere in a corner and write, and then come together and exchange what we have written. It doesn’t really work to sit at a table and do it in a combined way. That way you talk about everything but science!

 

HS: How were the figures in this paper drawn?

PB: They were hand drawn, just on a sheet of paper. The orientation figures, as I already mentioned, were made by a computer from the very beginning. The computer did all the analysing and also the printing.

 

HS: In the paper you thank C. Mead, G. Pudney and T. Parsons. Could you tell us who these people were and how they helped?

PB: They were all people from England. Mead was the head of the ringing office of the British Trust for Ornithology (BTO) in England. He was a good friend of mine and we asked him to help us get the permission to trap. The other two were ringers of the BTO, who helped us trap birds in the field.

 

HS: You also thank someone by the name of H. Dingle for comments.

PB: Yes, Hugh Dingle. He is an American. He was and still is working in the University of Davis. Hugh Dingle is a very famous investigator on birds and insects. He has written an interesting book on bird migration, as I have done, but his main focus was on partial migration. I had invited him to come to Germany, to stay here in my institute, as a Humboldt Research Prize winner, for half a year. This was a very fruitful time during which we discussed all aspects of the genetics of bird migration. And he also gave a lot of input into this specific paper.

 

HS: Did this paper have a relatively smooth ride through peer-review?

PB: Oh yes. It was very easy. We got a few very small comments. The reviewers were really enthusiastic about the paper, and so it ran through.

 

HS: And Nature was the first place you submitted this to?

PB: Oh yes, of course.

 

HS: How was this paper received at the time it was published? Did it get a lot of attention?

PB: Oh yes. All over the world. And, of course, also in the Max Planck Society. In the meantime we have published a number of papers that are very similar in their content. But this was something like a small revolution, because of the idea of how rapid and how quickly and how efficiently micro-evolution, and therefore evolution as a whole, can work in the living world.

 

HS: What impact did this paper have on your future research itself? Did it open up new lines of investigation?

PB: This was a milestone in our own research. Following this, we thought about many aspects that could be followed up and that led to a whole series. It finally led to a totally novel theory on avian migration. We found that it was possible, through selection, to make birds from a partially migratory blackcap population from southern France either exclusive migrants or exclusive non-migrants within a few generations. Just in about 5-6 generations. Then the discussions with Hugh Dingle really showed us that partial migration is, in fact, a common habit in all kinds of animals and even plants. From the oldest pre-Cambrian bacteria up to humans, you have partial migration. Wherever you look around partial migration is there. This is probably a habit as common as, let’s say, circadian rhythmicity in plants and animals. Then we looked carefully into the literature on the world’s bird species – now about 10,000 – and found that in more than 80% there is some evidence for partial migration. And even among the remaining, some proportion might be migration. Take the house sparrow.  As you know, house sparrows are normally resident, but if you look carefully at them – like it has been done by Professor Parkin in England – about 1-2% of the birds are migratory. It’s a small amount, but still. So even one of the most typically resident bird species all over the world is a partial migrant. Based on all this evidence we developed the theory that partial migration is a basic equipment of all living avian species. Therefore it would be very easy for birds to adapt to all kinds of environmental changes, whether ice ages or climate warming, because even a species like the house sparrow could easily develop in 10-20-50-100 years a fully migratory population, if conditions at home become unfavourable. Or the other way around – a population of barn swallows, now a migrant in Europe, could develop, in about 40 years or 25 generations, a totally resident population, something that I think we will have in the next 50 years or so. All this was initiated by the paper in Nature at that time.

 

HS: Its now 24 years since this paper was published. Would you say that the major conclusions from this paper still hold true, more-or-less?

PB: [Laughs] No, it doesn’t only hold true; it has become, let’s say, a common sense. At that time we wrote that this maybe a unique rapid micro-evolutionary process that we have observed. Since then we have come to learn from many other papers, many other plants and animals, that this is not an exception. This is normal. But it was absolutely overlooked before we did this experiment. You may have heard about Peter and Rosemary Grant from America, from the Princeton University. They have worked for decades on the Galapagos Islands. They were astonished when, once, after a big drought, a specific population of ground finches went almost extinct, but after a while started to not only survive but also to increase the population again. This was due to the fact that they had developed, in a very short time, extremely strong beaks with which they could open the only seeds that could be harvested in the extreme drought. And when the normal climatic conditions came back to the Galapagos the size of the bill was again reduced to normal size. All this happened within about 10 generations. We have so many more examples – e.g. snakes that lay one more egg in a clutch and so on.  And all this can happen within a few generations, in about 10 years or so. So this is now a general biological aspect. Therefore, I would say, the paper opened an area of understanding of how rapid and effective evolution can work everywhere in the world.

 

HS: If you were to redo this experiment today, would you change anything, given the developments in technology, theory and statistical techniques?

PB: No, certainly not. The only way to show this was to do some breeding and selection experiments. That was the only way. Today, in parallel, we would also look in detail for the genetic structure of the individual birds, i.e. for the genes itself. This is, of course, very very difficult way in birds, but we have managed to do this. We have also found at least one gene now that’s responsible for at least some aspects of migration. That’s something we would do in addition, but the rest would be done as before. There’s no other way around.

 

HS: And you would still use the modified Emlen funnel?

PB: Oh yes. That is the best way you can do it. There’s nothing better in the world.

 

HS: In the paper you flagged a few topics about which not much was known, and which you felt needed to be researched further. One of these is the genetic basis of this migratory evolution. Do we know more about that now?

PB: No, this is still not possible. Because you see, while you can easily find differences in the genomes of different species, between populations you find only very very slight differences. You have no idea to what they are really related. So it will be some more decades before that will be possible.

 

HS: You say “Overall mean directions suggest a breeding origin between Belgium and central Germany”. Do we now know, with more certainty, where these birds wintering in Britain come from?

PB: Oh yeah, we know now. There have been many more ringing recoveries, and many other investigations, based on which we can say this is an area that roughly goes from the south, from Switzerland and Austria, up to Vienna in east Austria, and then up to about almost the whole Germany, up to the area of Hamburg and east Germany. This is the big patch from where the birds that nowadays migrate to England are coming.

 

HS: Do we also know more about why this change in migratory direction happened?

PB: Yes.  We must distinguish between the mechanism that has started this development, which was of course chance, and what maintains it. There is a lot of genetic variation and, by chance, some birds extended the westerly migratory direction to this slightly northern direction, and so by chance they reached England. If England would not have existed they would have gone into the Atlantic Ocean and the story would have ended. But fortunately there was England. And then the birds that entered England had, let’s say, a funny experience – a wonderful land, a mild winter, not so many birds in the winter, in comparison to Spain or France where so many birds from northern Europe were wintering. It was a paradise and therefore, of course, there was a strong selection pressure to increase the number of birds coming there. Now this work has been investigated in further detail. We had already, in our paper in Nature, the idea that this direction change could be accelerated by, so called, assortative mating. We knew already that birds wintering in Britain migrate back to the continent relatively earlier in the breeding season. Also the distance is relatively short. We have followed this up in more detail. We have looked in continental Europe for the very first breeding pairs of blackcaps. From these birds we have taken small amount from the claws, because the claws are growing in the wintering area, and in these claws must be stable isotopes that show exactly where the birds have been wintering. By this method we have found that the very first broods in central Europe are, more than expected, from parents that have both wintered in England. This means that, through assortative mating, there is an acceleration of the new migratory direction development. This has been published in a paper in Science in October 2005. The first author is Stuart Bearhop. In this we showed that there is a high selective advantage. The birds that winter in Britain come relatively early to Germany, choose the best habitats, mate assortatively, and have the possibility of having more than one brood. This is, I think, the main selection force behind the rapid development of these new migratory habits.

 

HS: Towards the end of the paper you say “Year-round residency has not yet evolved in British breeding blackcaps, but this may be only a matter of time”. Are there any indications that this is happening now?

PB: Oh yes. This will, of course, come in, sooner or later, due to climate warming. Experimentally, we have already shown that this can happen very easily. There was another paper from us in PNAS where we have shown that, in the blackcap, the genetic control of the migratory distance and the amount of migratoriness in partially migratory populations are controlled by one and the same genetic mechanism. So when a population is migrating shorter and shorter distances, due to climate warming, the number of resident individuals automatically increases. We have shown this in a very nice experiment. We took birds from an exclusively migratory population of blackcaps, in this case from south of Germany, and from these, chose the 30% with the lowest amount of migratory activity, i.e. the 30% with the shortest migratory distance. These birds we have selected for lower and lower amounts of migratory activity. In this way, after 4 or 5 years, we had the first 10% of non-migratory individuals from a hitherto fully migratory population. And from this we could calculate how long it would take for a totally migratory population, by directed selection, to convert to a non-migratory population. We found that would be about 40 years or 25 generations. And this is something that will happen in many many bird species during the next 100 years or so. You can read more about this in two places – one is my bird migration book – the English version that has been published by Oxford University Press. And then there is a paper in Advances in the Study of Behaviour where I have summarised all the genetic investigations that we have made in the blackcap. This was in 2003.

 

HS: Do you continue to work on this topic even today?

PB: No, this is absolutely impossible. I have given this up on retirement, because for this you really need a large institute and a large group of people. Now, I’m totally engaged in conservation issues and totally different things.

 

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

PB: I think I have read it a few times, when I was writing reviews on bird migration or when I had to write a new edition of my migration book – in German, it’s now in its 7th edition. Then, of course I go back into original papers. Sometimes, I also go back to it to see the wordings I used to deal with sophisticated concepts or ideas.

 

HS: When you compare this paper to those you write today do you notice any striking differences?

PB: No, the style has been about the same. I have been writing every week so there hasn’t been much change. The brain is still working to some extent.

 

HS: This paper has been cited over 300 times. Would you know what it is mostly cited for?

PB: No, I never have looked for citation index. This has never been, for me, of any interest. I was convinced that this was an important paper and that, sooner or later, it will be noticed. Citation indexes are very modern instruments and in many cases absolutely useless. We have had endless discussion in the Max Planck society about how to handle this. This is of no interest for me.

 

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

PB: Oh yes, absolutely. This is certainly one of the five best papers we have made.

 

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

PB: I think the most important thing is that if you have a good idea, and if in coming to a solution you have a lot of difficulties, like we had  – to get the birds from England, to take them over, to run long-term experiments and so on – do not give up and keep going. Because in the end you will either be happy to have excellent results or will anyway face many other problems but without any good results. So I think you should not hesitate to choose the hard way.

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