Revisiting Davies & Brooke 1988

In a paper published in Animal Behaviour in 1988, Nick Davies and Michael Brooke unraveled, using a mix of natural history observation and clever experiments, the nature of the interaction between the brood-parasitic common cuckoo and its host the reed warbler. Their experiments showed that many facets of the cuckoo’s behaviour are likely to have evolved to deceive reed warblers. In turn, the warblers have evolved counter-strategies to decrease the success of cuckoos. Thirty-two years after the paper was published I spoke to Nick Davies about how he got interested in studying cuckoos, his memories of fieldwork in Wicken Fen and what we have learnt since about the arms race between cuckoos and their hosts.

Citation: Davies, N. B., & Brooke, M. de L. (1988). Cuckoos versus reed warblers: adaptations and counteradaptations. Animal behaviour, 36(1), 262-284.

Date of interview: 16 September 2020 (via Skype)

Hari Sridhar: How did you get interested in cuckoos and brood parasitism?

Nick Davies: Most of my ideas come from just birdwatching. Wicken Fen, just a short cycle ride from Cambridge, has a good population of common cuckoos, which parasitize reed warblers. Ever since I was an undergraduate here I have been astonished by the sight of a little reed warbler feeding an enormous cuckoo chick; why are they  fooled by a chick that’s seven times their own body mass? Steve Rothstein’s papers on cowbirds in North America had shown how one could do experimental work on host defences using model eggs. And it  occurred to me we could do exactly the same to try and work out whether reed warblers have defenses simply by playing the part of the cuckoo ourselves and parasitizing nests with model eggs. So, it was this mixture of bird watching and reading Steve Rothstein’s studies which inspired me.

There was also a wonderful paper by Richard Dawkins and John Krebs on arms races in nature pointing out that a lot of biodiversity evolves in response to interspecific interactions. That also bubbled around at the back of my mind as a theoretical boost to this study. But it was  pure natural history interest which really drove the choice of the reed warbler and the cuckoo. We just thought it’d be fun to go around Wicken Fen pretending to be cuckoos!

HS: How did you know Michael Brooke?

ND: We were doctoral students together in Oxford. And then he came to Cambridge as curator of birds in the museum here. We’re old friends and we decided to team up for the cuckoo study.

HS: Were you already on the faculty at Cambridge University when you began this work?

ND: Yes. I spent the first part of my time here studying dunnock mating systems in the Botanic Garden. Our children were very young then and I wanted to have a local study, so I could spend time with them. And then gradually, as they started to grow up a bit and go to school, I felt free to go further distance – not very far, only 20 miles away. I also wanted a change of scene. I knew Wicken Fen very well and thought this would be a good place.

HS: I’ll come back to the study itself in a bit. I wanted to step back a little and ask you about your interest in birds. Do you remember how and when that came about?

ND: When I was a little boy; six or seven years old. I remember making a hide out of an old deck chair at home and putting some seeds out and being thrilled by the sight of little birds coming to feed and watching them closely through my first pair of binoculars.  It’s just always been a  passion. I’m the only one in our family who has this obsession. I’ve no idea where it came from. I remember my mum saying, you’re spending too much time birdwatching, Nick; you’ll never get a job as a birdwatcher. It started just for the aesthetic joy of going to wild places and seeing beautiful animals doing interesting things. And then, once I got interested in evolution, the combination of watching and wondering made it intellectually thrilling as well.

HS: Do you know when you decided to make a career out of it?

ND: I specialized in biology in sixth form at school. And then I came to Cambridge as an undergraduate to study zoology. Even then, I really just wanted to birdwatch. Most of the course was physiology and molecular mechanisms and I was much more interested in whole animal behavior. It wasn’t until I went to Oxford to do my PhD at the Edward Grey Institute that I met people making a career out of academic studies of birds. That really inspired me and I knew then that that’s what I wanted to do.

HS: In addition to watching birds, were you reading about them? Were there particular books that inspired you?

ND: Yes, very much. I read Darwin’s Origin of Species as a young teenager and I was absolutely thrilled by that. Also, David Lack’s Life of the Robin and Swifts in a Tower, which were studies of the lives of individuals and got me thinking about how they solve problems, of where to find food, how to get a mate, how to defend a territory. And then Niko Tinbergen’s wonderful book The Herring Gull’s World showed how you could treat the natural world as a laboratory in which to do experiments, and tinker with things to test hypotheses. So, this mixture of watching and wondering and doing experiments, and the fun of being outside, all combined as a sort of soup; it really thrilled me and it still does.

HS: You did a PhD on the pied wagtail. And then there were a few studies on other animals, which, I’m guessing, you did after you joined Cambridge.

ND: Yes, my two long-term studies were both done in Cambridge. First, the dunnock mating system study, which we did in the Botanic Garden here, showed how sexual conflict drives various mating outcomes. The novelty back then was combining DNA profiling with behavioral studies. And then this experimental study of coevolution in cuckoos and warblers. These two studies have been my passions for the last 40 years.

HS: Do you remember when you first saw a cuckoo in a reed warbler nest?

ND:  Yes, when I was an undergraduate, on Wicken Fen. Reed warblers do so many wonderful things: they migrate from African winter quarters, set up breeding territories, build nests and choose mates carefully; all these lovely, exquisite adaptations. And then they are fooled by this monstrous chick! How does the cuckoo get away with it?

HS: Coming back to the paper, you talk about early observations on cuckoos.

ND: Yes. The first really detailed study was by Edgar Chance, an egg collector who made wonderful observations in the 1920s His book reads like a hunting diary. To collect cuckoos’ eggs, he had to know a lot about how the cuckoos behaved. Edgar Chance deserves the credit for discovering how the cuckoo lays her egg. Our experiments aimed to discover why does the cuckoo behave in this way?

HS: How difficult was it for you to find information about earlier work on cuckoos, dating from Aristotle?

ND:  I’m a fellow of Pembroke College, with academics specializing in many different subjects. I asked a classicist friend, Michael Reeve, where would be the best place to look up Aristotle’s work. I remember being thrilled by this old literature, and amazed that Aristotle already knew that the young cuckoo threw the host eggs out of the nest. Edward Jenner is given the credit for the first detailed study, but Aristotle knew all about it 2,300 years ago. And then I really enjoyed Gilbert White’s observations of cuckoos in The Natural History of  Selborne (1789). There’s a chapter in The Origin of Species on how behavior can evolve, and the ‘instincts’ of the cuckoo is one of Darwin’s prime examples. In a brief and brilliant paragraph, Darwin first points out that being a parasite is  advantageous, because freed from the burdens of parental care parasitic cuckoos can lay more eggs. Second, he argues that hosts accept cuckoo eggs not from benevolence, to give cuckoos a helping hand, which some early observers had thought, but because they get tricked or follow what Darwin calls a “mistaken instinct”. And then, Darwin’s third point is that the cuckoo’s parasitic habits evolved from parental ancestry. These three points have inspired much of the recent research on cuckoos.

HS: Did Wallace also write about it? In the paper you mention his ideas about mimicry being selected for by predation.

ND: Yes. Darwin suggests that the reason the cuckoo’s egg has evolved to match the host’s egg is in order to fool the hosts. But Wallace had a different idea, namely that cuckoos and hosts have independently evolved the same camouflage pattern to beat predators. So, in theory, even in the absence of any discrimination by hosts, the match could evolve by convergent evolution. I found that a thrilling idea, and wanted to test it. And then, Mike Brooke and I came up with a third idea: the cuckoos themselves might select for mimicry, to prevent a second cuckoo from spotting a cuckoo egg and selectively removing it from the nest. So, now we had three hypotheses: –Darwin’s host discrimination, Wallace’s camouflage against predation, and selection by the cuckoos themselves, all of which we could test by experiment. That made it much more fun, to have three hypotheses rather than one.

HS: At that time, you thought that the major predators of these nests were probably cuckoos. Has that been borne out by subsequent observations and study?

ND: During our study, some of the predators were clearly, crows and mink. They’re clumsy and big predators. We’d find the nest completely trashed or pulled away from the supporting reeds, and the whole clutch gone. However, sometimes, we’d find the whole clutch gone, but no disturbance at all to the nest. And then we began to realize that perhaps the cuckoos themselves were one of the major predators. Now, it was known from Edgar Chance’s work, and also some work done by Karsten Gärtner in Germany, that female cuckoos would  selectively predate nests where incubation was already underway and so it was too late to parasitize that nest. Predating the nest forces those hosts to build a new nest and lay a replacement clutch and thereby makes available a new opportunity for the cuckoos to parasitize. And so, by selectively farming nests in her territory through the season, the cuckoo can make available more opportunities for parasitism. It’s a very clever strategy…

HS: You earlier said that Darwin, in that short paragraph, provided pretty much the right explanation for what’s happening. I was curious about something you said about earlier interpretations being wrong. What were some of these earlier explanations?

ND: Some early observers thought there might be some defect in cuckoo behavior or anatomy that prevented them from raising their own chicks. A French biologist, Herrisant in the 18th century, suggested that cuckoos might have bulging stomachs, so  if they tried to sit on their own eggs they would surely crack them. Gilbert White shot a cuckoo and dissected it to test this idea. He found that the guts were no different from those of other birds. And then, Edward Jenner noted that cuckoos departed on migration very early in the summer. He thought that left no time for parental care, and so forced them to be a parasite. He just got the causal arrow the wrong way around – it’s not the early departure that forces them to be a parasite, it’s their parasitic habits that enable an earlier departure, because there’s no need to stay behind to look after their chicks. Actually,  flipping the causal arrow around often gives you new insights.

HS: I just want to see if I’ve understood this correctly: you chose to focus on reed warbler hosts because of their numbers on Wicken Fen?

ND:  Yes. Cuckoos parasitize several hosts across the UK. In moorlands, up in Scotland and in the West Country, there is a genetic race that parasitizes meadow pipits. The genetic race of cuckoo we have here in the Fens lays a green egg, and they go for reed warblers. Actually, of all the hosts that cuckoos go for,reed warblers are the easiest to study, simply because their nests are easy to find.

HS: Can you give us a sense of whether Wicken Fen has changed in any way from the time of this study?

ND: The number of reed warblers has remained more or less stable over the 30 years we’ve been studying them, but cuckoos have declined dramatically, as they have across most of Europe. We now have only about one third of the cuckoos compared to when we started the study 30 years ago. One of the things we’ve found is that reed warblers have dropped their defenses in concert with the reduction in parasitism risk.

HS: I know it’s a long time ago, but what memories do you have of the fieldwork for this study? What was your daily routine?

ND: Mike and I partitioned the Fen into two halves. He had one territory, and I had another territory. When you map out a field site, you almost feel you’ve taken possession of your patch.  And you become quite protective of your nests.  I remember one of the wardens once telling me that an old man had been  reported looking for nests along my stretches. I had a sleepless night thinking somebody might be collecting eggs on my study site. Then I woke up the next morning and realized that the old man, obviously, was me!

Our daily routine was to look for new nests and to check the nests we’d already found to monitor their progress. It was the thrill of the hunt as much as anything and tremendous fun  to see what happened to the model eggs in our experiments

HS: In the paper, you use this phrase “cold searching for nests”. What does that mean?

ND: You have a stretch of reeds along a waterway, and you just go along the bank with a stick parting the reeds every few meters looking for nests. Sometimes, we found nests by watching birds building. But there were so many nests we couldn’t find all of them in this way. So, just going through every five days or so with a stick enabled us to find all the nests. Most of them were found at the early building stage,and then we could monitor their progress right through, from the start of laying through to fledging.

HS: How did you make the model eggs?

ND: We borrowed a couple of cuckoo eggs from the museum here and made a mould around each of them using Silastic rubber. The mould was in two halves, into which we poured resin and then stuck the two halves together. These resin egg models were then exactly the same dimensions as a real cuckoo egg, and the same mass too.We then painted them using acrylic paints to match the variety of eggs which cuckoos lay. Different cuckoo races lay different eggs. One race, for example, lays a pure blue egg and goes for redstarts.The reed warbler race of cuckoo lays a greenish spotted egg, which looks just like areed warbler egg. And there’s a meadow pipit strain of cuckoos, which lay brownish spotted eggs. We painted these varieties of egg types, so we could examine the response of reed warblers to their own race of cuckoo – namely, a mimetic egg, and to the eggs of other races of cuckoos, which would be non-mimetic for them.

HS: I don’t know if I understood this correctly. In the paper, do you say that you can actually identify the individual cuckoo based on the eggs?

ND: Yes. We didn’t study the cuckoos themselves, but we had color-ringed many of the reed warblers, so we could follow their behavior. But you can recognize individual cuckoos indirectly from their eggs because, although they all laid greenish spotted eggs, there are little individual differences in colour and pattern that are very obvious even to the naked eye. Identically-marked eggs occurred in little territories, so it was very obvious that individual female cuckoos defended a territory containing maybe 20 to 40 pairs of reed warblers. We could plot cuckoo territories from the different egg types. It also became clear that there were some cuckoos that didn’t have such well-defined territories, because, occasionally, we’d get a different cuckoo egg appearing within a resident cuckoo’s territory. These intruding cuckoos popped up all over the Fen. They try and sneak in, and lay eggs into another female’s territory. That’s why you sometimes got a second cuckoos parasitizing the same nest. Of course, a female cuckoo would only ever lay one egg in each host nest, because the young cuckoo is going to reject all the other eggs from the nest. But a second cuckoo, presumably, wouldn’t know which nests had already been parasitized, and would come in and try and sneak a parasitism. This observation led to the idea that maybe  cuckoos are trying to hide their eggs from other cuckoos through their egg mimicry.

HS: What is the current understanding of why egg mimicry evolved?

ND: The results of our study clearly supported the host rejection idea. The hosts were more likely to reject non-mimetic eggs than mimetic eggs. There was no difference in predation across the different egg types. And there was no evidence that second cuckoos selectively removed odd eggs from the nest, whether those odd eggs were real cuckoo eggs or even model eggs that we’d put in. In Norway, Arne Moksnes, Bard Stokke and Eivin Roskaft were  studying common cuckoos at the same time, and we all came to similar conclusions from experiments with different hosts. You might think it’s obvious that hosts would discriminate.. But it wasn’t obvious until we had done the experiments.

There are some bronze-cuckoos in Australia that don’t lay a mimetic egg, but they lay a cryptic egg, a very dark egg that is difficult to see against the nest lining. These cuckoos parasitize dome-nesting hosts. This crypsis might hide the cuckoo’s egg to prevent selective removal by other cuckoos.

HS: In the paper, there is a clear logical sequence to the experiments. To what extent does this reflect how the experiments were actually done? Was it planned in this way, right at the start?

ND: No, it emerged during the study. We started with the question, why do you get egg mimicry? And then, in discovering the answer to that, namely, that mimetic eggs are less likely to be rejected,we began to wonder, well, is the stage of parasitism important? What if you put a mimetic egg in before the hosts themselves began to lay? We found that those eggs were all rejected. So, the cuckoo has clearly got to wait until the host has begun to lay. And then we wondered, why does the cuckoo remove an egg before she lays her own, and why is the egg so small and so on? But that came after doing the initial egg mimicry experiments.

The results we got from egg discrimination were, more or less, what we expected. But sometimes our results were a surprise; Mike and I thought surely the hosts would count and notice an extra egg in the nest, so that’s why it’s important for the cuckoos to remove an egg before they lay their own. We were  amazed to find that’s not true; our mimetic eggs were equally likely to be accepted whether we removed a host egg to make room, or simply added them to the clutch. So, we had to come up with new hypotheses for why cuckoo removes an egg. We thought, well, maybe she’s getting a free meal. If so, why doesn’t she remove all the eggs and have a bigger meal? We did experiments to show that if you remove too many host eggs -if the clutch is reduced too much – then the host would dessert. That was a very exciting result because then it raised the question, well, if the host will desert a single egg, why don’t they desert a single chick? Our observations showed that the host never deserted a single chick so the cuckoo chick can happily eject all the nest contents. So, it’s the fact that there’s a lower limit to the number of eggs that hosts will attend but not to the number of chicks, that explains why it’s the cuckoo chick that has got to do the ejection. And then that raises the question, of course, why do hosts desert a single egg but not a single chick? And I think again there’s an economic answer;, that if your clutch has been reduced too much, it’s not worth spending a whole season raising a tiny brood, because within a few days you can start a replacement clutch, and do better from a full clutch. But by the time the chicks hatch, the season’s now getting late and so maybe the best thing to do is stick with what you’ve already got. I suppose the main message there is the cuckoo’s adaptations have evolved in relation to economic decisions made by the host.

HS: Do you remember if you started writing after you finished all the experiments? Were both you and Michael Brooke involved in writing?

ND: Yes, we waited until all the experiments were completed before we began the paper. Mike and I worked very much as a team, with the experiments and the writing and the analysis. There was definitely a trend in those days to produce lots of short papers. I’ve never really liked that. I wanted to write one big paper where we tied all our ideas and all our experiments together to make a complete story. Actually, one of the reviewers said our paper was “excessively long”, but the editor kindly let us keep it as a  long and rather chatty paper. Looking back, I’m pleased we were allowed to do this. I like the mix of history, natural history and experiments and the comparative analyses, with all our egg and chick experiments, to produce one big story.

HS: Do you remember if Animal Behavior was the first place you submitted this paper to?

ND: Yes, I don’t think any other journal would have taken it! Animal Behaviour was my favorite journal in the old days, because they allowed you to publish longer papers, with a mix of natural history and detailed quantification.

HS: In the Acknowledgments You thank Chris Thorne and Max Hobbs of the Wicken Fen group for color-ringing the warblers?

ND: They helped us color- ring the warblers for individual recognition. We were also interested in distinguishing young reed warblers from older ones to see if young reed warblers are more likely to accept odd eggs.

HS: Jan Parr

ND: Jan is my wife. We’d often spend long evenings painting model eggs together. In the paper we also acknowledge Bruce Campbell, who was one of the best nest recorders in the country. He  came across one of our experimental nests and reported our model egg  as a real cuckoo egg! So, unwittingly he convinced us that our model eggs were realistic. Subsequent studies, by Cassie Stoddard and collaborators, have examined  egg mimicry in much greater detail and have showed mimicry occurs across all wave lengths seen by birds. including UV. They have also analyzed the spotting patterns in tremendous detail. Our results were quite crude, just asking if an egg that was mimetic to our eyes was more likely to be accepted than a non-mimetic one. The details of the mimicry have been worked out much better since our early studies, but our conclusions were correct.

HS: I’ve watched a short video online in which you show how closely the model eggs resemble the real ones.

ND: One of the things I  remember with great pleasure is watching the reed warblers reject the eggs. You can make a little channel through the reeds from the bank and just sit quietly, and the reed warblers will come and sit on the nest. We saw both males and females pecking at the model eggs. So, it’s very clear that both sexes  rejected eggs. At one nest the male was quite happy with the odd egg in the nest,but the female decided she didn’t like it. She started to dismantle the nest to build a new nest nearby, while the male continued to incubate. You could imagine him thinking, what on earth is she doing? And of course, once the nest was dismantled, he had to agree to the move!. I just remember that as a bit of natural history that I found absolutely fascinating, that males and females both reject, but they wouldn’t always agree on whether rejection should take place or not.

HS: What about the cuckoo and jackdaw models? How were those made?

ND: The model cuckoos were actually stuffed real cuckoos – taxidermic mounts, which we got from the museum. We only had two. Of course, reviewers these days could rightly point out that there’s lots of pseudo replication, thatwe’re using the same model again and again. I think we could defend that by saying even getting one stuffed cuckoo was pretty amazing, because these are protected birds,and we were relying on specimens that the museum allowed us to have. Subsequently, we’ve done lots of work with other stuffed cuckoos, and with wooden cuckoos painted to resemble real cuckoos,to show that you get exactly the same effect. That was one of the findings that thrilled us most, not that the reed warblers mobbed the cuckoo at the nest – we’d expected that – but that the sight of a cuckoo would alert them to even stronger egg rejection. This suggested that rejection decisions are harder for the reed warblers than you might imagine,and that they’re on the lookout for other cues of parasitism risk to modulate their rejection behavior. So, there’s information warfare going on, with the cuckoos trying to hide their presence by secrecy and speed, and the reed warblers looking out for cuckoos to modulate their rejection behavior. Moreover,reed warblers depend not only on their own sightings of cuckoos, but also on social information; if they hear neighbors mob, they quickly go across to see the source of that mobbing, and if it’s a cuckoo, they up their own rejection behavior. That means cuckoos have got to be doubly secretive, not only to avoid alerting the target, but also to avoid alerting the whole neighborhood. Being a parasite is tough.

HS: You mention that the paper doesn’t address other kinds of adaptations and counter adaptations that happen before the laying itself, what you call frontline defense. Has that been an area of research you pursued subsequently?

ND: Yes, we’ve certainly been very interested in that. Egg rejection is the obvious defense. But there are things you could do before that.For example, you could choose a site which is less likely to be at risk of parasitism. It’s clear that nests built further away from trees are less likely to be parasitized. That’s simply because cuckoos need a secretive lookout perch to watch the hosts build and time their parasitism correctly. Nevertheless, lots of hosts still choose to nest near trees. That’s a good unsolved question: why do they choose these high risk sites when, potentially,there are lots of lower risk sites available? Maybe high risk sites are also better for food or whatever; nobody’s looked at that. And then there are frontline defenses in terms of nest architecture. You could build a nest that is harder for a cuckoo to get into. For example, there’s very good evidence that weaver birds add tunnels to their nest entrance to make it harder for cuckoos to get into. Mobbing cuckoos might also be a frontline defence to reduce parasitism risk.

HS: Going back to the list of people you acknowledge, the next name is Ian Wyllie.

ND: He’d done a prior observational study of cuckoos in a reed bed not far from Wicken. He’d also radio-tracked cuckoos to look at their behavior. He provided lots of data on parasitism rates of host nests at different stages, which we analyzed in our paper to boost our sample sizes. He wrote a very nice book called The Cuckoo. So, we acknowledged his advice and provision of some data.

HS:  David Gibbons, who you thank for helping with the experiment.

ND: He was one of my PhD students who studied moorhens. At the very start of the study, there was the possibility he might join us but then he went off to do something else.

HS: Tim Bennett

ND: He was the Head Warden of Wicken Fen Reserve and we thanked him for allowing us to roam the Fens.

HS: And then you thank three people for comments on the manuscript: Steve Albon, Tim Birkhead and Chris Kelly.

ND: Steve Albon gave us statistical advice about a G-test, partitioning effects of model type and presence of a cuckoo at the nest. Tim and Chris  were colleagues who read and commented on the manuscript.

HS: This was a really exciting time in animal behavior, wasn’t it? A lot of the theory was developed at this time, and a lot of it came from Cambridge and Oxford. Were you also tapping into this larger community to discuss ideas, you know, at conferences or even through casual meetings?

ND: Yes. I particularly remember conferences and seminars being really important. There was a tremendous buzz. The idea of looking at behavior in terms of decision making with costs and benefits, an economic approach which is so familiar to us now, was really quite new in the 1970s.And then there was Game Theory.  I think the main message I got from games and the work of John Maynard-Smith and Geoff Parker is to expect variability in nature; if some individuals are doing one thing, it might pay other individuals to do something different. Field workers like me were thrilled by this because it made complete sense. Everything we looked at involved variability, and the theoreticians were saying,don’t worry, that’s exactly what we predict. The third new insight was the importance of kinship. Natural selection judges success not only through your own reproduction but through your interactions with kin too.

HS:  Was the grant from NERC specifically for the cuckoo work?

ND: Yes, the NERC grant paid Mike’s salary and our travel and equipment expenses.

HS: When you reflect on how animal behavior research has changed since that time, do you think there are still areas of research where there is the scope to do the kind of work you did in this study?

ND: Yes. I still think that that hardest part of research is getting a good idea. My dunnock work was stimulated by Trivers’s and Parker‘s ideas of sexual conflict, which led to a fresh look at mating systems. And the arms race idea of coevolution led us to have a fresh look at cuckoos and realize that you could test this by experiment. Of course, new techniques are important too, for example to look at mimicry through a bird’s eye and for genetic studies of egg markings, and of race formation in cuckoos.

HS: Why do parasitic cuckoos lay small eggs?

ND: It’s very clear that parasitic cuckoos lay an unusually small egg compared to non-parasitic cuckoos. Our experiments show that egg size is certainly one of the factors by which hosts discriminate foreign eggs. Egg discrimination might not be the only factor involved – small hosts might not be able to incubate a large egg.  And smaller eggs are less expensive, so a cuckoo could lay more eggs in the season. I think we have to be wary of the idea that there’s just one selective pressure favoring a particular trait.

I do have something else to say on egg size. The common cuckoo’s egg is often a little bit bigger than the host eggs. Hosts might favor bigger eggs among their own clutch because these would be the most valuable ones, the ones most likely to produce a big surviving chick. Cuckoos might play on that, by giving hosts a slightly super-normal egg. And that might make up for any mismatch in colour and markings. Now, we have techniques to make 3D printouts of eggs. It would be nice to manipulate egg size more finely to ask whether a mismatch in color and spotting could be compensated for by extra size, which might play on the hosts’ predispositions. That would be a nice study to do.

HS: And then, you talk about how quickly the cuckoos lay eggs, that it’s done in less than 10 seconds.

ND: Yes, that’s amazing. Our experiments with stuffed cuckoos show that it’s very important for the cuckoos to avoid alerting the host. Some parasitic insects also lay their eggs on a host in a flash, to avoid host detection and attacks. Speed and secrecy are really important for brood parasites.

HS: Let’s talk about the cuckoo chick.

ND: When we discovered all these host defenses at the egg stage, Mike and I thought, well heavens,why isn’t the same sort of fussiness shown at the chick stage too? Dawkins and Krebs had suggested that although the cuckoo chick didn’t look like the host young, its large size and exuberant begging cries were a supernormal stimulus – something the host couldn’t resist any more than a junkie could resist his fix. Their idea was that a cuckoo chick might act like a drug on the host nervous system. So in a series of experiments we gave reed warblers a chick of another species (dunnock, robin, reed bunting)in among their own brood. These chicks, which look very different from reed warbler young, were all accepted and raised just as if they were one of the reed warbler’s own young. That suggested two things to us: One is that the reed warblers really weren’t rejecting odd chicks in the same way they were rejecting odd eggs. And also, there was no special drug-like stimulus from a cuckoo needed to induce acceptance, because even other species were accepted and fed. So then, we did another experiment where we strapped two nests side by side. If reed warblers were feeding a brood of their own, we strapped another nest next to it with a cuckoo chick, or if they were feeding a cuckoo, we strapped a nest alongside with a brood of reed warblers. When the reed warblers came back,we could see them looking a little puzzled at first, at the two nests side by side, but eventually they treated them as one nest. And they quite happily fed the contents of both nests. We did this with a small sample size, but we presented the raw data in the paper, and it was very clear they would feed both chicks. Even with their own chicks alongside for comparison, they would still accept the cuckoo chick. This suggested that ejection of eggs by the newly-hatched cuckoo chick wasn’t important to prevent the hosts from comparing the cuckoo chick with their own young. We also showed, in subsequent work, that the reed warblers don’t treat a cuckoo chick as a super normal stimulus.They bring food to a cuckoo chick at about the same rate as they would to a brood of their own. You’ve interviewed Becky Kilner about another subsequent paper we did showing how the cuckoo chick’s rapid begging calls manipulate the hosts by sounding like lots of hungry host young. I like the idea that the cuckoo is fooling hosts with visual stimuli at the egg stage, and then with vocal trickery at the chick stage. The poor hosts are being bombarded by all these sensations!

HS: I’ve also heard about this fascinating example of a cuckoo in which the young have wing patterns that look like open gapes.  

ND: Yes, the Horsfeld’s hawk-cuckoo in Japan has an equivalent trick of simulating extra chicks in the nest, but it’s not a vocal one. This cuckoo chick has a bare yellow skin patch on the underside of the wing which mimics its yellow gape. And it waves this patch whenever the hosts come to feed it. The host will sometimes even offer food towards the wing patch! The researchers blackened the wing patch and showed that the feeding rate dropped. So, simulating, visually, an extra gape in the nest is another way of tricking the hosts into bringing enough food. It is absolutely wonderful.

HS:  There’s another intriguing idea in your paper about why hosts might build nests on top of earlier ones.  I was wondering if we know more about this today.

ND: No, we’ve not followed that up. It’s really interesting. When a nest has been predated reed warblers often use the same material to build a new nest nearby. This can fool you when you’re doing your transects and can’t find a nest. Sure enough, there’ll be a new one just a few meters away. I think that shows that nest material  is expensive to collect, especially the spider silk  used to bind the nest together and to anchor it to the reeds, so it’s worth conserving. However, sometimes the new nest is built from fresh material, right on top of the old one. So you now have a nest two stories high. From a cuckoo’s point of view, a nest in a new location would obviously be a new nest, one that they could parasitize. So one of the ways that hosts could try and trick the cuckoo would be to build a new nest right on top of the old one. Then, if the cuckoos rely on location, they might regard that nest as already parasitized and leave it alone. We’ve never tested that, but that will be nice to do.

HS: At the time when the paper was published, do you remember if it attracted attention of any kind, either in academia or in the popular press. I know that, recently, there’s been some attention, in the form of a podcast and radio shows.

ND: Yes, we did have some media attention,in newspapers and articles. And I’ve since done several BBC radio programs on the fun of watching and studying cuckoos, and a BBC Natural World film, where David Attenborough did the commentary, based on our long term studies on Wicken Fen.

HS: What about within academia? Were there discussions around the findings and was it considered controversial at that time?

ND: I don’t think it was controversial. There’s still discussion about the importance of recognition errors in egg rejection. I’m very keen on this idea. I think one of the most important findings of the study was that, when there’s a mimetic egg in the nest, reed warblers’ rejection decisions are compromised by recognition errors. They sometimes reject one of their own eggs rather than the cuckoo’s egg. And this potential cost might make reed warblers reluctant to be too fussy, and hence rely on other cues to parasitism risk before they decide whether to reject eggs. We’ve done a signal detection model of how these recognition errors might modulate rejection behavior. There’s a balance between the frequency of parasitism and recognition errors that determines whether it’s best to reject eggs or not. But another subsequent study has suggested that recognition errors are not always important.

HS: I want to you read out some lines from the Discussion, just to get a sense of what you feel about them given all that we have learnt subsequently.  You say “Our experiments show that many aspects of the cuckoo’s behaviour, revealed by observers from Aristotle to Chance, are for better deception of hosts. These include egg mimicry, waiting until the hosts have begun to lay before parasitizing the nest, afternoon laying, a small egg, and rapid, secretive visits to the host nest. When we, as cuckoos, changed these procedures the model cuckoo eggs were more likely to be rejected. Other parts of the cuckoo’s strategy are not involved in host deception but improve cuckoo success for other reasons. Parasitism early during the host laying period probably increases the cuckoo chick’s hatching success and survival, and the removal of a host egg by the female cuckoo both provides her with a free meal and probably results in better incubation of the cuckoo egg.”

ND: I think that’s fine. I still believe all that.

HS: Then you go on to talk about the hosts. You say, “For their part, the hosts have evolved counter adaptations to decrease cuckoo success including egg discrimination, a response to the sight of a cuckoo at their nest and also, perhaps, the habit of building a new nest over the top of a parasitized nest. The delay in rejection shown to real and model cuckoo eggs may also be of adaptive advantage.”

ND: The first two bits I definitely agree with, but the bit about building a nest on top needs to be tested experimentally. I find that a beguiling idea and it would be lovely to test that. The last bit about delay in rejection has been investigated by Arnon Lotem, who has shown that the way hosts come to reject eggs unlike their own is not by using the rule -reject the odd one out – but by learning what their own eggs look like, and then rejecting eggs that differ from that learned set. And that raises the question, how long should this learning period be before you build a picture of your own set? That’s very interesting. In this paper, Mike and I thought that the delayed rejection gave the reed warblers a better chance to pick out something that was odd. I don’t think we specifically said that,but that was our thinking. Whereas, Arnon Lotem points out that, actually, it’s more interesting than that – it might enable better learning of your own set.

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

ND: Until you asked me to read it, I’d not looked at it for ages. When a paper’s first published, you’re excited. And then you have a period where you just worry about all the little things that you could have done better… And then you put it aside for a while, and later, you think, oh well, it wasn’t too bad after all. Reading it after all these years helped me to remember the fun of being on the Fen, doing experiments and being surprised by some results, which then raised new questions. And then, the fun of working with Mike. We’ve known each other for 50 years, now. It just made it all the more fun to do it with a friend.

HS: Was there anything else that you were struck by, when you read it this morning, in terms of the style of the paper, or the nature of the work? I’m guessing the work you do and the papers you write today are very different.

ND: I think editors today might ask us to split it into three papers: one on egg mimicry, one on recognition errors and one on the absence of chick rejection. But I’m pleased that we put it all in one package, because I think comparing the eggs and the chicks in the same paper makes it more complete. Subsequent studies have done more detailed analysis of each of these topics. I’m also really grateful for the old style editors who allowed us to be chatty and put some long quotes from Darwin, Wallace and Aristotle. I think it’s lovely to pay tribute to these great naturalists. Lots of early cuckoo discoveries were really hard won, by Edgar Chance, for example. We’re so lucky to have this natural history to build on. As I said earlier, the hardest bit is doing the watching before you do the wondering.

HS: What would you say to a student who’s about to read this paper today? Would you guide her or his reading in any way, or suggest other things they should read along with this. Would you have any other advice for them when reading this paper?

ND: I’m sure many would think of better statistical analyses. But the most interesting thing would be, how would you take some of these ideas forward? I would ask them to design some experiments to test the idea that recognition errors and frequency of parasitism modulate the best decisions that read warblers could make.Design experiments to test whether second nest building on top is actually a defense against parasitism. Could some of these alternative hypotheses, like predation and second cuckoos, be important in other parasitic systems? What features of parasitic systems might favor those rather than host discrimination? Under what systems could a non-mimetic egg still survive in the natural world, given that there are costs of rejection? These sorts of questions might be interesting for students to think about.I also think there are other macro-evolutionary questions. This is very much a micro study, about adaptations within one system. You can ask bigger questions like, why there aren’t more species of parasitic cuckoos? Only 1% of bird species are parasitic. If parasitism is such a good thing, why aren’t more birds tricking others? That’s a good unsolved question. One answer might be that parasitism has a great short term advantage,but in the long term, just as human cheats, you get found out as hosts evolve defenses. And then life becomes more complicated, and you’re forced to specialize more and more. I remember reading E.O. Wilson’s book on Insect Societies, where he’s struck by the fact that the parasitic insects with the most sophisticated trickery often tend to be very rare. That suggested to him that parasitism might be a one-way ticket to eventual extinction, because hosts fight back and force you to become more and more of a specialist. And then, you might run out of niche, or are at greater risk of extinction due to chance events. So, I think this relationship between the intricacy of adaptation and macro-evolutionary patterns is very interesting. Just being perfectly adapted doesn’t mean you’re going to have a happy life. There’s another lovely example, by GC Williams in his book Adaptation and Natural Selection. He imagines a flea on a passenger pigeon. However well-adapted that flea might have been,it was doomed to become extinct when the passenger pigeons went extinct. Exquisite adaptation might not be the solution to everything.

HS: This is my final question. You said you retired recently. Do you plan to continue watching and studying cuckoos in Wicken Fen?

ND: I’m certainly going to carry on watching cuckoos. I’d like to do some more writing, particularly about the thrill of enriching watching by evolutionary wondering, following the footsteps of Darwin and Wallace. I enjoyed writing  a recent popular cuckoo book Cuckoo: Cheating by Nature.  I’ve got four young grandchildren to look after and I’m really enjoying that. We’ll see. I don’t have grand plans. But I’m certainly as fascinated as ever by bird watching and evolution.