Male cuckoo, mobbed by a pair of meadow pipits.
Holme, North Norfolk, May 2014.
Gilbert White’s The Natural History and Antiquities of Selborne, the Hampshire village where he was born, died and served as parish priest, has been continuously in print ever since its first publication in 1789. With over 200 new editions and translations, it is reputed to be the fourth most published book in the English language, after the Bible, the works of Shakespeare and John Bunyan’s The Pilgrim’s Progress.
The book is a compilation of letters to his friends, Thomas Pennant, the leading zoologist of the day, and Daines Barrington, a barrister, explorer and naturalist. In these letters, White provides a precise and often affectionate account of his daily observations on the weather, fauna and flora of the parish. While other naturalists were travelling abroad to collect their specimens, often by shooting them, White never ventured further than Derbyshire and, as his biographer Richard Mabey comments, ‘was so overcome by the size of the Sussex Downs that he referred to them as a vast range of mountains’.
Rather than collecting and describing dead specimens, Gilbert White took his notebook outside to make field observations of living animals and plants, and in doing so became Britain’s first ecologist. He wrote:
Faunists are too apt to acquiesce in bare descriptions, and a few synonyms: the reason is plain; because all that may be done at home in a man’s study, but the investigation of the life and conversation of animals, is a concern of much more trouble and difficulty, and is not to be attained but by the active and inquisitive, and by those that reside much in the country.
In the preface to his book, he recommended that ‘stationary men [should] pay a more ready attention to the wonders of the Creation, too frequently overlooked as common occurrences,’ and concluded that ‘these his pursuits, by keeping the body and mind employed, have, under Providence, contributed to much health and cheerfulness of spirits, even to old age.’ Gilbert White spent some 60 years of his life in Selborne village. He was born in the vicarage on 18 July 1720, and died 100 metres away in ‘The Wakes’ on 26 June 1793. His letters demonstrate that a wonderful way to observe the changing natural world is indeed simply to stay in one place.
The Natural History of Selborne makes frequent reference to cuckoos. In Letter IV to Daines Barrington, written on 19 February 1770, Gilbert White muses on how the cuckoo chooses its hosts:
Your observation that ‘the cuckoo does not deposit its egg indiscriminately in the nest of the first bird that comes in its way, but probably looks out a nurse in some degree congenerous, with whom to intrust its young’ is perfectly new to me; and struck me so forcibly, that I naturally fell into a train of thought that led me to consider whether the fact was so, and what reason there was for it. When I came to recollect and inquire, I could not find that any cuckoo had ever been seen in these parts, except in the nest of the wagtail, the hedge-sparrow [dunnock], the titlark [meadow/tree pipit – White did not distinguish these], the white-throat, and the red-breast [robin], all soft-billed insectivorous birds . . . This proceeding of the cuckoo . . . is such a monstrous outrage on maternal affection, one of the first dictates of nature, and such a violence on instinct, that, had it only been related of a bird in the Brazils, or Peru, it would never have merited our belief. But yet, should it farther appear that this simple bird, when divested of the natural maternal instincts . . . may be still endued with a more enlarged faculty of discerning what species are suitable and congenerous nursing-mothers for its disregarded eggs and young, and may deposit them only under their care, this would be adding wonder to wonder.
Writing just a few years later in his famous cuckoo paper, Edward Jenner (1788) also commented on the cuckoo’s selectivity, noting the hedge-sparrow (dunnock), water-wagtail (pied wagtail) and titlark (meadow/tree pipit) as the three main hosts. He watched a pair of titlarks feeding a young cuckoo in their nest and, ‘as it is a bird less familiar than many . . . to satisfy myself that they were really Titlarks, [I] shot them both, and found them to be so.’ Jenner suggested that the cuckoo chose small birds as hosts, partly because small birds are more abundant, so there would be more nests available to parasitise, but also because in the nest of a larger host ‘the young cuckoo would probably find an insurmountable difficulty in solely possessing the nest, as its exertions would be unequal to the labour of turning out the young birds.’
Recent studies have confirmed Jenner’s suggestion that the cuckoo chooses host species that are abundant. In Britain, the three current favourite hosts are among the commonest species in their respective habitats: there are races of cuckoo specialising on reed warblers in marshland, meadow pipits in moorland, and dunnocks in farmland and scrubland. Other regular British hosts are the robin and pied wagtail, also fairly abundant species. However, the cuckoo avoids other potential host species, which are also common, have accessible nests and a suitable diet for raising young cuckoos. Why not use them too?
For example, in farmland and scrub, blackbirds are usually more abundant than dunnocks and robins. Why isn’t there a cuckoo race specialising on blackbirds? Tomáš Grim and his colleagues tackled this question by field experiments in the Czech Republic and Hungary. They took newly hatched cuckoo chicks from reed warbler or great reed warbler nests and placed them, singly, in blackbird nests with eggs. The cuckoo chicks quickly ejected the blackbird eggs, so they had no problem ejecting a larger egg from a larger nest than normal. However, the blackbird parents were reluctant to feed a cuckoo, and none survived beyond a few days. This was not a case of rejecting a lone chick, because blackbirds happily raised a single blackbird chick.
The researchers then tested cuckoo chicks cross-fostered to song thrush nests, another potential host that cuckoos do not use. Surprisingly, the cuckoo’s problems here were of a different kind. The cuckoo chick was unable to eject the thrush’s eggs, mainly because a thrush nest is deeper and has steeper sides than a blackbird nest, but also because, unlike blackbird nests, song thrush nests are lined with mud and the cuckoo’s legs kept slipping on the hard, smooth surface. Experiments showed that cuckoos also failed to eject reed warbler eggs from song thrush nests, so the problem was the steep and slippery nest walls, not the large egg. However, if the researchers gave the cuckoo a helping hand, by removing the thrush’s eggs, they found that it was fed very well by the thrushes and grew even better than in reed warbler nests. So a diet of mainly worms, with some snails, is fine for raising a young cuckoo. Finally, cuckoo chicks were placed together with a brood of song thrush chicks, but now they fared poorly in competition with host young and none of them survived to fledging.
These experiments suggest cuckoos avoid blackbirds, simply because blackbirds won’t feed them. It’s not yet known why this is so. Blackbirds feed their young mainly on worms, and this diet was fine for cuckoos raised in song thrush nests. So the problem is not one of diet. Perhaps the cuckoo’s begging signals are not appropriate for blackbird foster parents? Cuckoos avoid song thrushes for a different reason: the young cuckoo would be raised successfully if it was the only chick in the nest, but it cannot eject the host eggs from such a steep and slippery-sided nest and doesn’t survive in competition with the host young.
What about other potential hosts that cuckoos usually avoid? Experimental ‘parasitism’ of their nests with model cuckoo eggs reveals that some of these are very strong rejecters of eggs unlike their own. This applies, for example, to reed buntings, blackcaps, tree pipits, chaffinches, spotted flycatchers and willow warblers. Many of these species are even stronger egg rejecters than the cuckoo’s favourite hosts. How did they evolve such strong rejection? We have already seen that species which have never engaged in an arms race with cuckoos, because of an unsuitable diet or an inaccessible nest, are acceptors of eggs unlike their own. This suggests that strong rejection of eggs must have evolved in response to past parasitism by cuckoos. So they are likely to be old hosts, which still bear the scars of the arms race their ancestors ran long ago, just as we have wisdom teeth and an appendix, signs of our ancestry.
If this interpretation is correct, we are left with the question: why did these cuckoo races go extinct? One possibility is that their hosts won the arms race, evolving such good egg signatures and such good egg rejection that their cuckoos couldn’t keep up with successful forgeries. The other possibility is that their cuckoo races went extinct for ecological reasons. Perhaps these hosts were more abundant in the past, and a decline in their density meant that they were no longer profitable as a cuckoo host. In this case, no matter how well a cuckoo race was adapted to its host, it would be doomed to extinction as its niche faded away. Now that these hosts are no longer parasitised, their egg signatures might fade and they may lose their egg rejection behaviour, too. If so, they will become available once more as suitable cuckoo victims, and the arms race might be repeated all over again.
This brings us to a question that is still unresolved: how do the various races of the common cuckoo, each with a particular egg type suited to its host species, remain distinct? The most likely explanation has been discussed ever since the days of Edgar Chance, namely that a female cuckoo inherits her egg type genetically, and then she comes to choose to parasitise the same host species that raised her, by learning its features when she is a nestling or fledgling. For example, a young female cuckoo raised by reed warblers would imprint on the characteristics of her foster parents and then, when adult, would choose to parasitise reed warblers. The green egg laid by her mother obviously fooled her reed warbler foster parents: she is the living proof of this. So, if she inherits this same green egg type and chooses reed warblers in turn, then the match between cuckoo and host eggs will be maintained across the generations.
We still do not know whether egg colour and pattern is inherited in cuckoos, but it is in other species of birds, so this seems very likely to be true. Neither do we know whether cuckoos imprint on their hosts. Edgar Chance himself tried to determine whether a female cuckoo victimised the same host species that raised her as a youngster. In 1923, he collected 17 cuckoo eggs or newly hatched cuckoo chicks from the vicinity of Pound Green Common, and placed them into the nests of meadow pipits, stonechats or skylarks. He ringed the nine that survived to fledge in the hope that some would return to the Common to breed, but none was seen again. In the 1970s, Ian Wyllie ringed a large number of cuckoo nestlings raised in reed warbler nests in the fens, but again none returned to his study site to breed. In 1987 and 1988, Mike Brooke and I tried a different technique, raising cuckoos in captivity with either robins or reed warblers as hosts. However, when we tested these cuckoos as adults they showed no propensity to breed, so we could not determine whether they had imprinted on their host species. A lot of hard work produced no results whatsoever!
In another captive study, Yvonne Teuschl and Barbara and Michael Taborsky, from the University of Vienna, hand-raised cuckoos in one of five different ‘habitats’ (these were cages containing objects of different colours and shapes). When the cuckoos were tested as adults, a year or two later, both males and females preferred their familiar habitat when given a choice. This suggests that habitat imprinting might increase the chance that a cuckoo encounters the host species that raised it. However, even within the same habitat there are likely to be several potential host species, so imprinting on the hosts themselves (their appearance, songs and calls, or nests) would be necessary to refine host choice to one species.
Although there is still no direct evidence for host imprinting in cuckoos, recent experiments have shown that it does occur in another brood-parasitic bird. In Africa, there are 19 species of finches in the genus Vidua, and they are all brood parasites, laying their eggs in the nests of grassfinches (Estrildidae). These hosts are remarkable for the striking mouth patterns of their chicks, which vary between species. Each Vidua parasite species specialises on one estrildid host species. The parasite chick is raised alongside the host young and shows remarkable mimicry of the host chicks’ mouth pattern.
The village indigobird, widespread in sub-Saharan Africa, has been particularly well studied. It is a little smaller than a sparrow; the males have a glossy blue-black plumage and the females are streaky brown. It lays its eggs in the nests of just one host species, the red-billed firefinch. If you look in a red-billed firefinch nest, it is difficult to pick out the parasite chick because it looks exactly like a host chick. The host young have bright orange gapes, with extraordinary white swellings and blue spots on the edge of the mouth, and black spots on the roof of the gape. These patterns are specific to red-billed firefinches and are as striking as any signatures you will see on an egg. The indigobird chick mimics this complex mouth pattern to perfection. Robert Payne and his colleagues from the University of Michigan tested how red-billed firefinches would respond to chicks with different mouth patterns by cross-fostering chicks of other species into their nests. The firefinches were more reluctant to feed chicks with mismatching mouths, so the indigobird’s mouth mimicry is important in ensuring it gets fed properly alongside the host young.
Therefore, a female village indigobird has to ensure she parasitises only red-billed firefinches, the one host for whom her chick has a matching mouth. It’s also important that she mates with a male of her own species, to ensure her offspring have the correct mouth pattern. If she mated with another species of indigobird, her hybrid offspring might have a different mouth pattern, and so her chicks would not survive so well. Her choice of mate is not as straightforward as in many other birds, because there are several indigobird species which look very alike. How does the female village indigobird solve these problems of host choice and mate choice?
In aviary experiments, Robert Payne and colleagues cross-fostered eggs so that some indigobirds were raised by Bengalese finches, a domestic form of an Asian finch, the white-rumped munia, which, of course, indigobirds would never encounter in the wild. Others were cross-fostered to be raised by their normal red-billed firefinch hosts. When these nestling indigobirds became adults they were given a choice of hosts in an aviary with a mixture of breeding species. Female indigobirds that had been raised by red-billed firefinches chose to parasitise the nests of red-billed firefinches, while females raised by Bengalese finches chose Bengalese finches as hosts. This is a beautiful confirmation that a female parasite’s host choice occurs through imprinting on the host species that raised her.
However, the story is even more intriguing. Male indigobirds play no part in choosing which nest to parasitise, but their experience as a nestling also colours their future behaviour because they copy the songs of the host species that raised them; male indigobirds raised by red-billed firefinches sing red-billed firefinch songs, while those raised by Bengalese finches sing Bengalese finch songs. So when a male indigobird sings, he announces the identity of the host species that raised him!
Female indigobirds do not sing, but they nevertheless imprint on their host’s songs and prefer to mate with a male indigobird which sings that same song. Therefore, a female indigobird ensures she mates with a male raised by the same host species that raised her, so host imprinting determines both her host choice and her mate choice. The result is that female and male indigobird lineages remain faithful to the one host species, and their mouth mimicry is maintained across the generations.
It would be wonderful to perform such cross-fostering experiments with cuckoos, but they are much more difficult to keep in captivity than finches. When Mike Brooke and I sought advice from Miriam Rothschild, who had hand-reared cuckoos in the 1960s, she warned us that they would be tricky to keep. In fact, she suggested we abandon all hope of studying host imprinting and instead used cuckoos as a model for schizophrenia! When they are being hand-fed by humans, or fed by hosts, she told us, cuckoos are remarkably tame and unperturbed by the events around them. However, once they become independent, she warned us, they change character within a few hours and become wild and easily disturbed. Perhaps we should have heeded her advice; it would have saved a fruitless experiment.
The alternative way to test for host imprinting is by field experiments. Some young cuckoos from reed warbler nests, for example, could be transferred to the nests of sedge warblers. The prediction would be that these young would imprint on the wrong host species and, when they returned the next year to breed, would choose to parasitise sedge warbler nests. There would be the problem of finding these cross-fostered young the following summer, because although young cuckoos tend to return to the general area where they were born, they often breed 10 to 20 kilometres away. Now satellite tracking of birds has become feasible, it should be possible to follow young cuckoos by tagging them just before they fledge but, even so, large samples would be needed because of heavy mortality of young before they return to breed.
My guess is that cuckoos do imprint on their hosts, just like parasitic finches, and that this explains how the cuckoo races remain distinct. Although there is no direct evidence for host imprinting, we do know that individual female cuckoos are usually remarkably host-specific when they lay their eggs. We have already seen evidence for this from Edgar Chance’s study on Pound Green Common, where Cuckoo A and her successors favoured meadow pipits, almost exclusively, even though there were other potential hosts in the same habitat. Chance also collected a series of nine eggs one summer from a female cuckoo which specialised on spotted flycatchers, and another of 14 eggs from a female who specialised on yellowhammers. These two unusual hosts are sparsely distributed, and both female cuckoos must have ignored many other host species in their territory.
Recent studies also show remarkable female host fidelity even within the same habitat. In two marshland sites in the Czech Republic, Marcel Honza and colleagues from the Academy of Sciences, Brno, followed female cuckoos by a combination of radio-tracking, to determine where they laid their eggs, and DNA profiles to determine maternity of cuckoo nestlings. This is a particularly valuable study because at one site there were three, and at the other four, very similar host species, all warblers in the same genus (Acrocephalus), and all breeding in close proximity within a female cuckoo’s territory. Indeed an individual female cuckoo could potentially watch all three or four host species from the same vantage point. Nevertheless, seven of the nine females targeted just one host species: two females specialised on reed warblers; one specialised on great reed warblers; three specialised on marsh warblers; and one specialised on sedge warblers. Such fine host specialisation within one marshland habitat strongly suggests female cuckoo are imprinted on their host species.
Along the Chikuma River, in the suburbs of Nagano City, central Japan, female cuckoos were likewise host-specific. DNA profiles were used to assign maternity for 98 cuckoo nestlings, a combination of a truly heroic field effort by Hiroshi Nakamura and expertise in the laboratory by Karen Marchetti and Lisle Gibbs, of McMaster University, Canada. Twenty-two of the 24 female cuckoos at the study site parasitised the nests of just one host species. Sixteen females specialised on great reed warblers, and six specialised on azure-winged magpies.
There is good evidence, therefore, that individual female cuckoos target one particular host species, even when very similar hosts are available. This suggests that female cuckoos are imprinted on the characteristics of one host. Now, what are male cuckoos up to? After a century of speculation, the picture is still confused.
One possibility is that a male cuckoo mates with any female he encounters, whatever her host preference. In the Chikuma River study, DNA profiles were used to assess paternity; seven out of 19 males (37 per cent) had offspring in the nests of more than one host, and so must have mated with females who were targeting different host species. Genetic analysis of cuckoos in lowland Britain also suggests that a male cuckoo often mates with females who have different host preferences. But now we have a problem: how could the distinctive egg types of the various races be maintained in the face of cross-mating by male cuckoos?
The answer is that, at least in theory, egg type might be under female genetic control, a suggestion made in 1933, back in the days of Edgar Chance, by R. C. Punnett, Professor of Genetics at Cambridge. This is a possibility in birds because of their mode of sex determination. In both birds and mammals, the sex of an offspring is determined by which sex chromosomes it inherits. In mammals, females have two X chromosomes (XX), so all their egg-cells have an X chromosome, while males have one X and one Y (XY), so their sperm have either an X or a Y chromosome. Therefore offspring sex is determined by the father: if an egg (X) is fertilised by a Y sperm it produces a son (XY), if it is fertilised by an X sperm it produces a daughter (XX).
In birds, it is the other way round: the female has two types of sex chromosome (WZ), so her egg-cells have either a W or a Z chromosome. The male has two Z chromosomes (ZZ), so all his sperm have a Z chromosome. So now it is the female who determines the sex of the offspring. Egg-cells with a W sex chromosome, on fertilisation, produce daughters (WZ), while those with a Z sex chromosome, on fertilisation, produce sons (ZZ). If egg colour was determined by genes on the W chromosome, then daughters would always lay the same type of egg as their mother. Not all the genes influencing egg colour need be on the W chromosome. Most could be on other chromosomes, inherited from either parent, with the mother’s W chromosome genes determining which of these other genes get ‘turned on’: those making green eggs for the reed warbler race, those making brown eggs for the meadow pipit race, and so on.
In this scenario, only female cuckoos would be in separate races, and a male could mate with females from any race because he has no influence on his daughters’ egg type. Indeed, cross-mating by males would maintain the cuckoo as the one species. This would explain very neatly why all the races of the common cuckoo look the same. There are no differences in appearance, for example, between cuckoos specialising on reed warblers and meadow pipits. They differ only in the colour of eggs they lay.
The inheritance of egg colour and pattern in cuckoos has still not been studied. However, in other bird species genes from both the mother and the father have equal influence on egg colour. This is true, for example, in the village weaverbird in Africa, where we have seen that the remarkable variation in egg colour and spotting acts as signatures, enabling individuals to recognise their own eggs. If, as in other species, genes from both parents influence egg colour, not only would a female cuckoo have to remain faithful to the host species that reared her, she would also have to restrict her matings to male cuckoos raised by the same host as she was, otherwise the egg mimicry would break down in the next generation. In this scenario, the different races of the cuckoo would be genetically isolated, just like different species.
A recent study in northwest Bulgaria, by Frode Fossøy and colleagues from the Centre for Advanced Study, Oslo, has revealed that cuckoo races can indeed sometimes be genetically isolated, even when they live side by side in the same small area. They studied the DNA of cuckoo nestlings raised by three hosts: marsh warblers, which bred in herbaceous vegetation, great reed warblers, which bred in reed beds, and corn buntings, which bred in bushy grassland. These three habitats were distributed in a patchy mosaic within an area of some 10 square kilometres, so here cuckoos that parasitised the three hosts would certainly all wander over the same geographic area. Nevertheless, there were clear genetic differences between cuckoos raised by the three hosts, showing that in this area, despite intermingling, matings must usually be between female and male cuckoos raised by the same host species.
How could a female recognise a male from her own race? One possibility is there might be subtle differences in voice. Gilbert White himself pioneered the idea that differences in voice could be as characteristic of a species as differences in appearance. He was the first to realise that there were three species of willow-wrens in Britain, though in appearance they all look rather alike. These are the little, yellow-green warblers now classified in the genus Phylloscopus (‘leaf seekers’), which flit through the summer foliage catching small insects. On 17 August 1768 (letter XIX to Thomas Pennant in The Natural History of Selborne), White wrote:
I have now, past dispute, made out three distinct species of the willow-wrens, which constantly and invariably use distinct notes . . . I have specimens of the three sorts now lying before me; and can discern that there are three gradations of sizes, and that the least has black legs [chiffchaff], and the other two flesh-coloured ones [willow warbler and wood warbler]. The yellowest bird is considerably the largest . . . and makes a sibilous grasshopper-like noise [this is the wood warbler] . . . Ray . . . [the] great ornithologist, never suspected that there were three species.
Three years later, in Letter X to Daines Barrington, written on 1 August 1771, Gilbert White notes that although they have a simple two-note call, ‘cuck-oo’, individual male cuckoos can also sometimes be distinguished by their voice:
A neighbour of mine, who is said to have a nice ear . . . finds upon trial that the note of the cuckoo (of which we have but one species) varies in different individuals; for, about Selborne wood, he found they were mostly in D: he heard two sing together, the one in D, the other in D sharp, who made a disagreeable concert . . . and about Wolmer-forest some [sing] in C.
Could there be subtle differences in voice between cuckoos of the different races? So far, there has been just one study to investigate this, by Tibor Fuisz, from the Hungarian Natural History Museum in Budapest, and Selvino de Kort, from Leiden University, the Netherlands. They recorded the calls of 142 male cuckoos in Hungary in two habitats: forests, where the main host is the robin, and reed beds, where the main host is the great reed warbler. To control for any geographical variation in calls, they compared adjacent pairs of forest and reed-bed habitat in three widely separated regions, at least 200 kilometres apart, in the north, the south and the east of the country. There were slight differences in calls between these three regions, mainly in call duration and the pitch of the first note ‘cuck’, but the major difference was between the habitats; forest cuckoos had a markedly lower-pitched second note ‘oo’ than reed-bed cuckoos.
These findings are intriguing; clearly there’s more to a simple ‘cuck-oo’ than we had first assumed. But it is too early to say whether this will be a ‘eureka’ moment, like Gilbert White’s discovery that there was more than one species of willow-wren. It is possible that the call is not a sure mark of cuckoo race. Lower-pitched calls travel best through dense foliage, and individual males might learn to adjust their call to suit their habitat. Even if a male’s call did signify his race, it still remains to be shown whether females choose mates based on such call differences, and whether the result is mating between male and female cuckoos raised by the same host.
Perhaps our current confusion about the exact nature of cuckoo races is because cuckoo mating behaviour varies between populations. In some areas, the races might be isolated genetically and best regarded as subspecies, perhaps in the process of evolving into different species. Over 50 years ago, in 1954, H. N. Southern, from the University of Oxford, noted that egg mimicry seemed to be best in those cuckoo races that occupied large tracts of uniform habitat, for example Hungarian reed beds (great reed warbler hosts) and Scandinavian forests (redstart hosts). Here, there would be plenty of opportunity for matings to occur between males and females of the same race. By contrast, in other areas more affected by human activities, Southern noted that egg mimicry is often poorer. He supposed that this was because the habitat was broken up into such small patches that male cuckoos more often encountered females of other races, and frequent interbreeding disrupted the egg mimicry.
In support of this idea, both studies showing that male cuckoos often mated with females of more than one race have been in areas extensively modified by humans, namely along the Chikuma River in the suburbs of Nagano City, Japan, and across lowland Britain. Perhaps, as we continue to destroy natural habitat and fragment the cuckoo’s landscape still further, we are slowly eliminating the distinct cuckoo races across many parts of Europe.
How did the various cuckoo races evolve in the first place? Now we can bring together all the various studies in this chapter to suggest a likely sequence of events. Although individual female cuckoos certainly have favourite hosts, they will parasitise another species if a nest of the main host is not available. For example, Edgar Chance’s cuckoos sometimes laid an egg in the nest of a skylark or yellowhammer if they failed to find a suitable meadow pipit. From their study of host clutches in museum collections, Arne Moksnes and Eivin Røskaft estimated that in 5 to 10 per cent of cases a common cuckoo egg was laid in the ‘wrong’ host nest. Hiroshi Nakamura’s radio-tracking of females in Japan revealed a similar level of mistakes, with 8 per cent of eggs laid in the nests of alternative hosts.
Most of these eggs laid in alternative host nests will be doomed. For example, linnets feed their young on seeds and never successfully raise a cuckoo to fledging. Nevertheless, they are still occasionally parasitised, probably by desperate cuckoos which specialise on dunnocks and cannot find a suitable dunnock nest. Other cuckoo eggs will no doubt be rejected because they are a poor match for the host eggs. Once in a while, however, some of the mistakes will produce a surviving offspring. If these lucky survivors imprint on the new host species, then this will be their chosen victim when they become adult, and a new cuckoo race will be born.
Many of these new races will be short-lived, perhaps lasting for just one or two generations, because the adult cuckoos will not produce sufficient surviving offspring to maintain the race. But sometimes the new race might proliferate. At first, cuckoos specialising on the new host might do even better than those that stick to the old host. There might be less competition for the new host’s nests, and the new host might also be less likely to reject cuckoo eggs, especially if it has not been exploited before. As the new race increases in numbers and the hosts begin to evolve rejection of eggs unlike their own, the stage is then set for a new cuckoo egg type, one that matches the new host. Note that in this sequence, the behavioural specialisation comes first, through imprinting, followed by the evolution of egg mimicry later on.
Hiroshi Nakamura and his colleagues have recently witnessed the birth of a new cuckoo race in central Honshu, Japan, which follows this sequence of events. Sixty years ago, the three most common cuckoo races here were those that specialised on bull-headed shrikes, great reed warblers and Siberian meadow buntings. Nowadays, these first two hosts continue to be cuckoo favourites, with 10 to 20 per cent of their nests parasitised in many areas. However, although the bunting is still abundant, it has become a rare host, with less than 1 per cent parasitism. Nakamura’s experiments with model eggs show that it is the most discriminating of the three hosts, so although the cuckoo egg is often a good match, copying the little brown scribbles on the host eggs, it is possible that this race is being driven to extinction by host rejection.
In its place, a new cuckoo race is evolving, one that parasitises azure-winged magpies. These magpies have spread dramatically in recent years, particularly into areas of higher elevation, and as a consequence have come into more contact with cuckoos. The first records of parasitism were of single nests in 1956, 1965 and 1971. Since then, the magpie has become one of the cuckoo’s main hosts in central Honshu. The increase in parasitism has been documented at Nobeyama Heights, an area first colonised by the magpies in 1967. From 1981 to 1983, 30 per cent of magpie nests were parasitised, but by 1988 it had reached 80 per cent, with many nests containing several cuckoo eggs. Similar rapid increases have been reported elsewhere, with 30 to 60 per cent of magpie nests parasitised by the 1980s.
This remarkable spread occurred because many female cuckoos simultaneously began to use the magpies as secondary hosts, as the magpies spread into their range. The cuckoo eggs that appeared in the magpie nests were particularly variable, reflecting their origins from all three former races. Cuckoo nestlings raised in magpie nests presumably imprinted on the new host, because Nakamura’s radio-tracking shows that many female cuckoos now specialise on magpies. As a result, the new host is suffering much higher parasitism than the old hosts. In some areas almost every magpie nest is parasitised.
It seems unlikely that this situation can persist. Some local magpie populations have declined due to the heavy parasitism or have been wiped out altogether. In other areas, the magpies are fighting back, by defending their nests against female cuckoos, by ejecting cuckoo eggs, or by deserting parasitised nests. In some areas, 40 per cent of the cuckoo eggs are being rejected. This must be exerting strong selection for egg mimicry by this new cuckoo race. It will be fascinating to see if the cuckoos can evolve effective forgeries before the magpies drive them to extinction.
These observations of old host species that have apparently beaten the cuckoo, by evolving strong egg rejection, and of new hosts evolving defences, show that life as a brood parasite is not easy. Yes, cuckoos and their kind avoid the burdens of parenting and so have the potential to lay more eggs than a normal nesting bird. They may enjoy a temporary advantage when their hosts are naive. But the hosts fight back, and in the end cuckoos need a complex toolkit of trickery to succeed. Perhaps, just as full-time cheats in human society are usually caught in the end and pay a price, so host defence might limit the evolutionary success of the brood parasites, explaining why they comprise just 1 per cent of all bird species. After long days searching for host nests at a suitable stage for my model eggs, I often think that if I was a bird, building a nest and raising my own young would make for an easier life than that of a cuckoo.