Reed warbler feeding a cuckoo nestling, 11 days old, with a bill-full of flies.
Reach Lode, 25 May 2014.
Is there anything more extraordinary in the natural world?
Early morning, a still summer’s day in mid-July, not a breath of wind; I’m searching along the edge of a reed-fringed ditch on Wicken Fen, a patch of ancient fenland just north of Cambridge, and Britain’s oldest nature reserve. This is a vast, flat landscape; big skies encircle me to the horizon and reflect in the water below, so sometimes I feel I am floating through the sky itself. The white sails of an old wind pump shine brightly in the sunshine. A marsh harrier appears over the reed tops and drifts close by on upswept wings, a young moorhen in its talons. On the path, there are fresh molehills of black peaty soil, the matted remains of old fen vegetation. The peat is resting on a bed of water and, as I walk along, the ground sways gently below my feet.
Just ahead, in the middle of the ditch, a reed twitches. From that exact spot I hear a loud, high-pitched and persistent, quivering call: ‘tsi . . . tsi . . . tsi . . . tsi . . .’ I approach slowly and with a long hazel stick, I gently part the reeds. The calling ceases. In the silence, I hear the dew that I have dislodged from the leaves dropping into the water below. Hidden in the darkness, halfway up the reeds, is a reed warbler’s nest. It’s a neat cup, woven from thin strips of old reed and suspended from three vertical stems about a metre above the water surface. Sprawled on top, with its wings draped over the nest rim on either side, is an enormous common cuckoo chick. It is two weeks old, fully feathered, and it sits perfectly still, with its bill shut tight, but it is watching me intently through brown beady eyes.
I lean out from the bank to get a better look; as I do so, the cuckoo suddenly rears up, its head feathers erect, and it opens its beak wide to reveal its gape, a blaze of bright orange. Then it makes a lunge towards me. Instinctively, I withdraw my hand as if expecting an attack. My heart is beating fast, but then I find I’m smiling in admiration at the cuckoo’s show of bravery. We look at each other for a moment; then I withdraw my stick and the reeds spring back, but not completely. Now there is a little gap through which I can watch the cuckoo from the bank just five metres away. I sit quietly and focus on it with my binoculars.
After a few minutes, the reeds twitch once again and a reed warbler emerges from the forest of reed stems, clinging to a reed just above the nest. It has a bright blue damselfly in its bill. The warbler gazes down and appears tiny next to the monstrous cuckoo chick below, some five times the warbler’s own weight. The cuckoo immediately begins a frenzy of calling, vibrating its open gape. Without a moment’s hesitation, the warbler bows deep into the enormous mouth to deliver the food. As it does so, the reed warbler’s head is almost completely engulfed. For a brief moment its small eye lies buried at the base of the gape, right next to the cuckoo’s large eye, and the warbler seems to risk being devoured itself. But the warbler withdraws just before the large gape clamps shut on the prey, leaving the tip of the damselfly’s abdomen sticking out. Another twitch of the reeds, and the warbler slips off to search for another meal.
I am amazed by what I have just seen. Reed warblers have many wonderful adaptations for their insectivorous life in the reeds. They navigate by the stars from their winter quarters in sub-Saharan Africa to breeding grounds in Europe. They must have an excellent memory for local landmarks, too, because adults that I have colour-ringed, so they can be recognised individually, return to exactly the same territory each summer. The females select their mates carefully, based on territory quality and song repertoire. Females then build exquisite nests, anchored to the supporting stems with woven strips of reed and spider silk, just the right size to keep a brood of four reed warbler young snug and warm, and deep enough to keep them safe as the reeds sway in the wind. The pair then select choice prey items for their young, rejecting prey that are unprofitably small (tiny midges) or too large to handle (large dragonflies). So the warblers are admirably careful in their choice of where to live, who to mate with and what to eat. Why, then, when confronted by a young cuckoo, so different in appearance and far too big to be one of their own chicks, are they apparently so stupid?
I am amazed by the cuckoo chick, too. How does this enormous chick stimulate the little warblers to bring enough food? It’s now mid-July and all the adult cuckoos left the fen two weeks ago. Some may already be in their African winter quarters while their last chicks are still being tended by reed warblers back in Britain. Why do cuckoos abandon their young and entrust them to another species?
I am not the first to experience this astonishment, of course. These marvellous interactions between common cuckoos and their hosts have fascinated human observers since ancient times. It has long been known that the cuckoo lays its eggs in the nests of other species. Over 2,300 years ago, Aristotle (who lived from 384 to 322 BC) recorded that ‘it lays its eggs in the nest of smaller birds after devouring these birds’ eggs’. He knew that the cuckoo then relied entirely on the host species to raise the young cuckoo: ‘they do not sit, nor hatch, nor bring up their young.’ And he also knew that the newly hatched cuckoo chick ejected the host eggs and young and so became the sole occupant of the nest: ‘when the young bird is born it casts out of the nest those with whom it has so far lived.’
In 1248, the Holy Roman Emperor, Frederick II, a keen falconer and fascinated by bird behaviour, also described the cuckoo’s parasitic habits:
The bird called cuckoo makes no nest nor lays eggs on the plain ground, nor feeds young, but obligately lays its eggs into foreign nests, for instance those of blackbird or praeni [a meadow-nesting songbird] or other birds, which incubate its egg and rear its young. Once I got a nest of praeni with an untypical nestling having a large gape. After having reared this nestling with thorough care by my helper we realised that this is a young cuckoo. Therefore, we know clearly that the cuckoo does not build its own nest, but lays its eggs into the nests of foreign birds.
There are also frequent references in old literature to the cuckoo’s odd behaviour. This bird riddle, translated from Old English, is in The Exeter Book, a manuscript dating from AD 950–1000, and surely refers to a cuckoo egg and then the cuckoo chick being cared for by foster parents:
In these days my father and mother gave me up as dead; nor was there a spirit for me as yet, a life within. Then a certain very faithful kinswoman began to cover me with garments, kept me and protected me, wrapped me in a sheltering robe as honourably as her own children, until I, under the garment, as my fate was, grew up, an unrelated stranger. The gracious kinswoman fed me afterwards until I became adult, could set out further on my travels.
The young cuckoo’s vigorous begging in the host nest must also have been familiar. In Chaucer’s poem from c.1382, The Parlement of Foules, the young cuckoo is chastised as a symbol of greed (line 612):
Thow rewtheless glotoun!
And the adult cuckoo’s lack of parental care often comes to symbolise a life with no love at all. In another fourteenth-century poem, The Cuckoo and the Nightingale by Sir John Clanvowe, an opposition is set up between these two birds. The nightingale argues that love is the mainspring of
al goodnesse, al honour and al gentilnesse . . . perfyt joy.
The cuckoo replies that the nightingale’s complicated song, with its embellished phrasing, is obscure, while his own simple call, ‘cuck-oo’, ‘trewe and pleyn’, is easily understood by everyone. His message is that ‘lovyng is an office of dispaire’, that will bring nothing but pride, sorrow, envy, distrust, jealousy and eventual madness.
These two birds continue their dispute in a German folk poem from the early nineteenth century, set as one of the songs in Gustav Mahler’s 1892 song cycle Des Knaben Wunderhorn (The boy’s magic horn). Here, the argument is over which is the finer singer. The cuckoo’s cunning nature is revealed when he suggests they ask the donkey to act as judge, ‘for he has two big ears, all the better to tell which is best’. The nightingale goes first, but its song is too intricate for the poor donkey. When it’s the cuckoo’s turn, the donkey immediately appreciates the simple call and, with a cry of ‘ey-aw’, pronounces the cuckoo the winner of the contest.
The cuckoo is also associated with betrayal, a ‘cuckoo in the nest’ becoming a symbol of an illegitimate child, the violation of a man’s own domestic nest. In Love’s Labour’s Lost, written in the 1590s, Shakespeare makes a play on the words cuckoo and cuckold, a man whose wife has been unfaithful and so who might be raising another man’s child as his own:
When daisies pied and violets blue
And lady-smocks, all silver white,
And cuckoo-buds of yellow hue
Do paint the meadows with delight,
The cuckoo then on every tree
Mocks married men, for thus sings he
Cuckoo!
Thus the call of the cuckoo comes to instil a fear of cuckoldry. Milton’s ‘Sonnet to the Nightingale’, from about 1629, when he was a student at Cambridge, refers to the superstition that hearing the cuckoo in spring before the nightingale foretells bad luck for a lover:
O Nightingale, that on yon bloomy spray
Warblest at eve, when all the woods are still,
Thou with fresh hope the lover’s heart dost fill,
While the jolly hours lead on propitious May;
Thy liquid notes that close the eye of day,
First heard before the shallow cuckoo’s bill,
Portend success in love; O if Jove’s will
Have linked that amorous power to thy soft lay,
Now timely sing, ere the rude bird of hate
Foretell my hopeless doom in some grove nigh;
As thou from year to year hast sung too late
For my relief, yet hadst no reason why.
Whether the Muse, or Love call thee his mate,
Both them I serve, and of their train am I.
How did early observers explain the cuckoo’s strange behaviour? We are so familiar with our own strong parental feelings, and with sights of animal parents working hard to feed and defend their young, that the cuckoo’s habit of abandoning its offspring seems both cruel and unnatural. The seventeenth-century naturalist John Ray regarded the beautiful fit between an animal’s design and its mode of life as evidence for the wisdom of God. For him, the cuckoo simply didn’t make any sense at all:
The Cuckow her self builds no nest; but having found the nest of some little bird, she either devours or destroys the eggs she there finds, and in the room thereof lays one of her own, and so forsakes it. The silly bird returning, sits on this egg, hatches it, and with a great deal of care and toil broods, feeds and cherishes the young Cuckow for her own, until it be grown up and able to fly and shift for it self. Which thing seems so strange, monstrous and absurd, that for my part I cannot sufficiently wonder there should be such an example in nature; nor could I have ever been induced to believe such a thing had been done by natures instinct, had I not with my own eyes seen it. For nature in other things is wont constantly to observe one and the same law and order agreeable to the highest reason and prudence: Which in this case, is that dams make nests for themselves, if it need be, sit upon their own eggs, and bring up their young after they are hatched.
Perhaps it’s not surprising, then, that early accounts suggested that there were abnormalities in cuckoo design. One view was that the cuckoo’s parasitic behaviour was bestowed by a benevolent Creator to compensate for the lack of parental instincts. In The Fowles of Heaven, written in 1614, Edward Topsell expresses his admiration for
that natural discretion with which the Grand Creator hath bestowed upon this siely fowle for the propagation of her oune kinde . . . it understandeth her oune frigiditie, or coldness of nature, utterly disabling it to hatche her oune kinde. Nature being defective in one part is wont to supply by another . . . want of streingth is recompenced with witt . . . the worke of God is wonderfull, and his mercy to his Creature magnificent.
Others thought that the cuckoo’s defect lay not in its behaviour but rather in its anatomy. In 1752, the French anatomist François Hérissant noted that the cuckoo’s stomach was unusually large and protruded low into the belly, and he suggested that if the female cuckoo were to sit on her eggs she would surely smash them. A few years later, in 1789, the famous British naturalist Gilbert White describes in his Natural History of Selborne how he dissected a cuckoo, concurring with Hérissant that: ‘the crop placed just upon the bowels must, especially when full, be in a very uneasy situation during the business of incubation.’ However, when he dissected some other species that did care for their young, including the nightjar and swift, he found that they too had cuckoo-like guts and concluded that:
Monsieur Hérissant’s conjecture, that cuckoos are incapable of incubation from the disposition of their intestines, seems to fall to the ground; and we are still at a loss for the cause of that strange and singular peculiarity in the instance of the cuculus canorus.
Gilbert White regarded the cuckoo’s habits as unnatural: ‘a monstrous outrage on maternal affection, one of the first great dictates of nature’.
At about the same time that Gilbert White was cutting up cuckoos, Edward Jenner was testing Hérissant’s theory by experiment. He placed two partly incubated pied wagtail eggs under a two-week-old cuckoo nestling that was being raised in a dunnock nest. A week later, the wagtail eggs hatched. Jenner concluded that if a young cuckoo could incubate eggs successfully then an adult cuckoo should be able to do so too. Instead he proposed another explanation for the cuckoo’s parasitic habits, namely that its early departure from the breeding grounds at the beginning of July left no time for parental care and compelled it to be a parasite.
This argument seems odd today, now that we are familiar with the variable migratory habits of many species. Reed warblers, for example, if they fail to raise their late summer broods successfully, migrate several weeks earlier than those still busy raising young to independence. Jenner has surely got his argument back to front: the adult cuckoos choose to depart early precisely because they have no parental duties to perform. On Wicken Fen, their departure in early July coincides exactly with the time reed warblers cease to start new clutches, and so marks the end of the summer’s opportunities for parasitism.
If early writers considered the cuckoo had to be a parasite to compensate for its bad design, how did they explain the host’s acceptance of the cuckoo chick? A common suggestion was that this was an act of benevolence. For example, Bechstein, writing in 1791, thought that the hosts would be only too honoured to raise a cuckoo chick, rather than a brood of their own, and he mistook the host alarm calls for cries of glee:
It is wonderful to observe what great apparent delight the birds show when they see a female cuckoo approach their abode. Instead of leaving their eggs, as they do when disturbed by the approach of other animals, they seem quite beside themselves for joy. The little wren, for example, when brooding over its own eggs, immediately quits its nest on the approach of the cuckoo, as though to make room to enable her to lay her egg more commodiously. Meanwhile she hops round her with such expressions of delight that her husband at length joins her, and both seem lavish in their thanks for the honour which the great bird confers upon them by selecting their nest for its own use.
In 1859, these quaint views, of bad cuckoo design and host benevolence, were swept away for ever by Charles Darwin. In chapter 8 of The Origin of Species, he discusses the parasitic habits of the common cuckoo as a prime example of how behaviour can evolve by natural selection. Darwin knew that some species of American cuckoos are not parasitic, but have normal parental behaviour. They build their own nests, incubate their eggs and raise their young to independence just like most birds. Back in 1794, this had been a source of pride for Charles Willson Peale, who created the Philadelphia Museum with admission tickets bearing the slogan ‘The birds and beasts will teach thee.’ He contrasted cuckoos from the Old World, ‘notorious symbols of infidelity for their practice of planting their eggs in the nests of other birds’, with cuckoos from America, with their admirable family values, and he was ‘proud to believe that they are faithful and constant to each other’. However, Darwin learnt from his correspondents that these parental cuckoos were not so virtuous after all and occasionally laid eggs in the nests of other species. He then proposed this evolutionary sequence:
Now let us suppose that the ancient progenitor of our European cuckoo had the habits of the American cuckoo, and that she occasionally laid an egg in another bird’s nest. If the old bird profited by this occasional habit through being enabled to migrate earlier or through any other cause; or if the young were made more vigorous by advantage being taken of the mistaken instinct of another species than when reared by their own mother, encumbered as she could hardly fail to be by having eggs and young of different ages at the same time; then the old birds or the fostered young would gain an advantage. And analogy would lead us to believe, that the young thus reared would be apt to follow by inheritance the occasional and aberrant habit of their mother; and in their turn would be apt to lay their eggs in other birds’ nests, and thus be more successful in rearing their young. By a continued process of this nature, I believe that the strange instinct of our cuckoo has been generated.
This paragraph still dazzles me with its originality, and even today biologists are busy investigating its three main suggestions.
Darwin’s first point is that far from being defective behaviour, parasitic laying can be a positive advantage and bring better reproductive success than parental care. Relieved of the time and energy commitment of parental duties, a parasitic adult could indeed migrate earlier; but more importantly, we might add, it could use the saved resources to lay more eggs per season. In fact we now know that parasitic cuckoos are especially prolific in their laying. A parental cuckoo might have time to raise at most two clutches in a season, each of three eggs. The parasitic common cuckoo, laying one egg in each host nest, lays an average of eight eggs per season, while many individuals lay 15 or more and the maximum recorded from one female is 25. Similarly, another parasitic bird in North America, the brown-headed cowbird, can lay 40 eggs or more per season, compared with two clutches of four for a typical parental species in this same family of American blackbirds. Furthermore, as Darwin points out, common cuckoo chicks are raised alone in the host nest and so escape competition for food. Perhaps they grow better than they would if reared in a brood by their own parents. Far from being defective, therefore, parasitic laying seems positively advantageous. So the worry of Gilbert White and Edward Jenner should really be turned on its head: why haven’t more species become parasitic, to exploit the workforce of so many honest parental species?
According to the latest estimate, there are about 10,000 species of birds in the world. Precise estimates vary depending on how full species are separated from subspecies, exactly the kind of uncertainty predicted by evolutionary change, because divergence between species is a gradual process, not a sudden event. Of these, 102 species are obligate brood parasites; that is to say, they always lay eggs in the nests of other species and rely on these as hosts to incubate their eggs and raise their young. The parasites comprise 59 species of parasitic cuckoos (Cuculidae), five species of parasitic cowbirds (Icteridae), 17 species of honeyguides (Indicatoridae), 20 species of African parasitic finches (Estrildidae) and one duck (the black-headed duck from South America). Clearly, success as a parasite depends on a good supply of host species. But if, as Darwin suggests, brood parasitism is so advantageous, why have only 1 per cent of all bird species evolved this lifestyle?
Darwin’s second suggestion is that parasitic laying evolved gradually from parental ancestry. He had no direct evidence and simply argued that it was plausible for occasional parasitic behaviour to evolve, by stages, into full-time parasitism. However, we now know that this conjecture is correct. In 2005, Michael Sorenson and Robert Payne constructed a family tree for the 141 species of cuckoo in the world (family Cuculidae), based on similarities in their DNA. Only 42 per cent of cuckoo species are parasitic (59 species); the other 58 per cent (82 species) are parental species. The tree shows clearly that within the cuckoo family parasitic laying has evolved independently three times from parental ancestry: once in South American cuckoos (three related species in the genera Tapera and Dromococcyx), once in the crested cuckoos of Eurasia and Africa (four species in the genus Clamator), and once in another large group of parasites (52 species in 11 related genera, including our common cuckoo in the genus Cuculus).
Darwin’s third point is the one that has fascinated me for the last 30 years. It’s that hosts don’t raise cuckoos through benevolence, of course. How could they? Any reed warbler that spent its time preferring to raise cuckoos instead of its own young would fail to pass on those generous instincts to future generations. On the other hand, a reed warbler that refused to raise cuckoos and focused on raising its own young would pass on its selfish instincts to those offspring, so the selfish raising of one’s own young (or other genetic relatives) should be the habit we’d most expect to see throughout nature. And indeed it is. Darwin’s idea to explain acceptance of a cuckoo chick is simply that the hosts get tricked, or follow what he calls ‘a mistaken instinct’. ‘Wonderful and admirable as most instincts are,’ he wrote, ‘yet they cannot be considered as absolutely perfect; there is a constant struggle going on throughout nature between the instinct of the one to escape its enemy and of the other to secure its prey.’ Darwin likened the natural world to an entangled bank, where each species was forever evolving new defences or new tricks to combat its ever-changing competitors and enemies.
In theory, then, we should expect there to be what Richard Dawkins and John Krebs have termed an ‘evolutionary arms race’ between cuckoos and hosts. In response to parasitism by cuckoos, hosts should evolve defences, such as protecting their nests against laying cuckoos, and rejecting cuckoo eggs and cuckoo chicks. In turn, this would lead to the evolution of better trickery by cuckoos to beat host defences. Better cuckoo trickery would then favour the evolution of even better host defence, leading to further improvements in cuckoo trickery, further improvements in host defences, and so on. In other words, hosts and cuckoos should co-evolve, with changes in either party selecting for changes in the other party.
Are cuckoos and host evolving together in such an arms race?
A week later, I return to the reed warbler nest on Wicken Fen. Once more, I part the reeds with my stick. At first, I don’t see the cuckoo. The vegetation has grown and it takes my eyes time to adjust to the bright sunlight reflected from the stems and leaves. But suddenly there it is, sitting perfectly still in the depths of the reeds. The cuckoo is now three weeks old, much larger than before, with longer wings and tail, and it seems ready to fledge. The nest is in a sorry state. It is flattened, and one of the supports has become detached from the reeds. The cuckoo now perches on the ragged remains of the rim. I notice its toes, two pointing forwards and two back, the typical arrangement of all members of the cuckoo family. This time I daren’t approach closely in case it flies off. I retreat, sit back on the bank and peer through the narrow gap in the reeds. I can just make out the head and front part of the body, but it is hard to see in the dark interior. All is still and quiet and I become distracted by the dragonflies patrolling along the edge of the ditch; male four-spotted chasers defending their mating territories. For some fen creatures the summer has just begun.
A frenzy of calling ‘tsi . . . tsi . . . tsi . . .’ and I look towards the cuckoo once more. A reed warbler lands on the cuckoo’s back! The cuckoo turns it head and the warbler deposits a large black and yellow hoverfly deep into the enormous gape. This time the warbler’s head disappears completely, and for a moment I imagine that the cuckoo will swallow its host whole. But the feed is over in a couple of seconds, the warbler darts off through the reeds and the cuckoo becomes still and silent once more.
At that moment, Darwin’s suggestion that the hosts have been tricked seems to me more unlikely than ever. The cuckoo chick is now eight times the weight of the reed warbler. Surely a parent that has to perch on the back of such a monstrous chick in order to deliver a feed should realise something is amiss. Have reed warblers any defences against cuckoos? If so, how does the cuckoo chick manage to fool them so easily? To begin to answer these questions, we have to go back to the start of the summer to discover how the cuckoo lays her egg.