A female cuckoo, hidden in an ash tree, watching a pair of reed warblers. She parasitised their nest five days later.
Wicken Fen, 9 June 2014.
The heroes of this chapter are two of the greatest naturalist explorers of all time. On 20 April 1848, Henry Walter Bates and Alfred Russel Wallace set sail from Liverpool on the ship Mischief. Five weeks later, they entered the mouth of the Amazon and, as Bates recorded in his journal, they saw ‘the beauties of a tropical country for the first time’. Unlike Charles Darwin, neither came from a wealthy family, and to fund their expeditions they relied on selling the specimens they found to the British Museum and to professional collectors. Bates and Wallace spent much of their first year together in the forests. Their daily routine was to rise at dawn to study birds and mammals, then after breakfast they turned their attention to insects until the early afternoon, when they sought shelter from the heat of the day. In the evenings they made notes and preserved their specimens.
Wallace’s return to England after four years met with disaster. Three weeks into the voyage home, his ship caught fire. Along with the rest of the crew, he scrambled to safety in the lifeboats, but then watched in horror as, back on board, all his precious specimens and journals went up in flames. He was rescued 10 days later by a passing ship, claimed the insurance money on his lost specimens, and within 18 months, and with admirable lack of self-pity, was off to the Malay Archipelago on another collecting trip. Meanwhile, Bates stayed on in the Amazon until 1859, spending 11 long years in the forests and amassing over 14,700 specimens (mainly insects) of which over 8,000 were new to science. He sent them home on three separate ships to guard against the calamity suffered by his companion.
Bates was astonished by the diversity of tropical insects and by how closely many of them resembled inanimate objects: caterpillars like twigs, moths like bark or dead leaves, beetles with wing cases that shone like dew drops. He thought that such wonderful camouflage must protect them against sharp-eyed predators. However, not all prey escaped by hiding. Some startled their enemies, such as a hawkmoth caterpillar that reared up when disturbed and dilated its body to expose two large eyes, just like a venomous snake. He showed this to the native Indian villagers, who were all terrified by the display. He was fascinated to discover, too, that some palatable species of butterflies resembled the bright colours and lazy flight of distasteful species. So good was this mimicry that even with his expert eyes he had to catch them in a net and examine them closely to determine whether they were the model (the distasteful species) or the mimic (the palatable species). He suggested this was a form of protective mimicry which fooled predatory birds.
He published his findings in 1862, three years after his return to England, in the Transactions of the Linnean Society of London, in a paper modestly entitled ‘Contributions to an insect fauna of the Amazon valley’. Darwin’s The Origin of Species had just been published, and Bates suggested that his discovery of mimicry of a distasteful species ‘offers a most beautiful proof of the theory of natural selection’.
Darwin was thrilled and wrote to Bates, praising the paper as ‘one of the most remarkable and admirable papers I ever read in my life . . . but,’ he continued,
I have one serious criticism . . . and that is the title of the paper . . . you ought to have called prominent attention in it to the mimetic resemblances. Your paper is too good to be largely appreciated by the mob of naturalists without souls, but rely on it, it will have lasting value, and I cordially congratulate you on your first great work.
Darwin was right; this form of mimicry, where an undefended species (the ‘mimic’) resembles a defended species (the ‘model’), is widespread in the natural world. It is known as Batesian mimicry, in honour of Bates’s wonderful discovery.
In February 1858, while Bates was still continuing his labours in the Amazon, Wallace lay in his hammock on the island of Ternate in the Malay Archipelago, suffering from severe bouts of fever. It was during one of these fits that the idea of natural selection came to him, in a flash. He wrote an essay on his theory and sent it to Darwin for comment. This was the famous bombshell that arrived in Darwin’s post on 18 June 1858; Wallace proposed the exact same theory that Darwin himself had been working on for nearly 20 years. Their joint papers were presented to the Linnean Society just two weeks later, on 1 July 1858, and Darwin rushed to publish his great book the following year. Wallace never complained that Darwin got most of the credit, writing to Bates that ‘I could never have approached the completeness of his book.’ In 1869, he dedicated his book The Malay Archipelago to Darwin, ‘to express my deep admiration for his genius and his works’, and 20 years later he magnanimously entitled his own volume on natural selection Darwinism.
It is in this book Darwinism that Wallace applies the insight of his friend Bates to the appearance of the cuckoo. Wallace points out that many parasitic cuckoos look remarkably similar to birds of prey, particularly Accipiter hawks, such as the sparrowhawk. They share a close resemblance in size and shape: an elongated body, long wings and a long tail. They have a similar plumage pattern: greyish or brownish above, paler and barred below. And they both have a swift, direct flight. This similarity in shape, plumage and flight gave rise to an ancient belief that the disappearance of cuckoos from Europe during the winter months came about because they transformed themselves into hawks. Aristotle dismissed this possibility, pointing out that cuckoos lack both talons and a hooked bill. Nevertheless, the resemblance is sufficiently close to often cause human confusion. During Edgar Chance’s pioneering studies of the common cuckoo on Pound Green Common, the female that he followed closely for five seasons (Cuckoo A) was mistaken by a local villager for a sparrowhawk and was about to be shot, when Chance intervened just in time.
Hawks and cuckoos are not closely related, so why are they so similar in appearance? Wallace noted that cuckoos are ‘an exceedingly weak and defenceless group of birds’, and he suggested that the resemblance was an example of protective mimicry, in which cuckoos had evolved to resemble hawks to reduce hawk attacks. Wallace may be right, because cuckoos are indeed more rarely taken by hawks than expected from their abundance relative to other potential prey. Nevertheless, hawk-like plumage, with barring below, is more prevalent in parasitic than in non-parasitic cuckoo species, which suggests that it might also somehow help cuckoos in their battle to slip past host defences.
On Wicken Fen, reed warblers encounter both common cuckoos and sparrowhawks every day. Are they fooled by their similarity? To test this, Justin Welbergen and I presented taxidermic mounts next to reed warbler nests during their laying period, when they would be vulnerable to cuckoo parasitism. We found that the reed warblers were reluctant to approach a mount of a sparrowhawk. They usually had a quick look and then retreated immediately and hid in the reeds, perfectly still and silent, several metres away. Their extreme caution makes good sense, because sparrowhawks are dangerous predators of small birds. Sparrowhawks usually make surprise attacks, dashing by the edges of vegetation or along watercourses, ready to pick off any unsuspecting small birds from a perch or in flight by shooting out their long legs and grasping them in their powerful talons. They can twist and turn though dense vegetation with astonishing dexterity, and will crash through leaves and branches to make a final kill. The intensity of a sparrowhawk’s hunt is beautifully captured by Kenneth Richmond’s description of one standing on its kill with a ‘lunatic, pitiless glare’. In a poem by Ted Hughes, the sparrowhawk announces: ‘My manners are tearing off heads’.
Cuckoos cannot damage adult songbirds. Nevertheless, at some nests the reed warblers treated the cuckoo mount as if it was a sparrowhawk. They were reluctant to approach, and hid in the reeds. At other nests, however, the warblers immediately attacked the cuckoo, striking it with their bills and feet, giving loud rasping calls ‘skrr . . . skrr’, and snapping their bills while they hopped about close by in agitation. Clearly, then, some pairs could tell the difference. But why were others so cautious?
To test whether it was the similarity of the cuckoo to a sparrowhawk that made some warblers cautious, we manipulated the appearance of the cuckoo mounts to vary their hawk resemblance. We did this by pinning a piece of silk below, which obscured the natural barring. The silk was either pure white (so the cuckoo no longer had hawk-like barring) or had bars made with a felt-tip pen, of the same width and spacing as natural bars (which retained the hawk-like appearance). We found that reed warblers were much more reluctant to approach and mob a cuckoo mount with barred rather than unbarred silk underparts. Therefore, the hawk-like barring did indeed deter the hosts and so would facilitate a cuckoo’s access to host nests. This protective mimicry is ‘Batesian’ because the adult cuckoo is otherwise defenceless against host attack. However, the cuckoo is not harmless to its enemies, in the sense that a palatable butterfly is harmless to a predatory bird, because its mimicry helps it to parasitise host nests. Perhaps the cuckoo is better described as a ‘parasite in wolf’s clothing’.
Our experiments revealed the importance of barring for a cuckoo’s hawk-like disguise, but barring is unlikely to be the only cue. In further experiments in which we modified the underparts of mounts with pieces of silk, we found that reed warblers were more afraid of a barred cuckoo than of a barred dove. Therefore other hawk-like features of the cuckoo must combine with the barring to deter the hosts. And reed warblers continued to be frightened of sparrowhawk mounts even when they were unbarred below. So, just like us, birds use a combination of features to distinguish friend from foe.
The common cuckoo, therefore, employs two forms of mimicry as it attempts to slip past host defences. First, the adult cuckoo mimics a hawk to deter host approach. This is a case of appearing dangerous, whereas in fact the adult cuckoo could safely be attacked. Second, the cuckoo egg mimics the host’s eggs to avoid host rejection. This is a case of appearing harmless, whereas in fact the cuckoo egg is dangerous to host reproduction. We have already seen that if hosts see through the cuckoo’s egg disguise they can save their clutch by rejecting the cuckoo egg. If hosts see through the adult cuckoo’s disguise, and launch an attack, can they deter the cuckoo from laying?
Female cuckoos can certainly be very persistent, and will sometimes lay in a host nest even while they are being attacked by the hosts, as shown in the early film by Edgar Chance. Nevertheless, when Justin and I tested some 200 pairs of reed warblers with cuckoo mounts at their nests, we found that those which attacked the mount were four times less likely to be parasitised by cuckoos than those that treated the cuckoo as a sparrowhawk, and were too nervous to approach.
Why do cuckoos avoid parasitising the nests of more aggressive hosts? Cuckoos are sometimes damaged by host attacks. There is one report of a great reed warbler attacking a female cuckoo so viciously that she fell into the water below the nest and drowned. Reed warblers are only a third the size of a great reed warbler, but even they can pull out the cuckoo’s feathers. However, the risk of physical damage may not be the main deterrent. When reed warblers attack a cuckoo, their loud rasp calls and bill snaps might attract predators, which would increase the chance of the cuckoo’s egg being eaten. Furthermore the commotion appears to alert the whole neighbourhood: as soon as reed warblers begin to give rasp calls, other reed warblers approach from nearby territories to see what’s going on. If neighbours are alerted, perhaps they would be more likely to watch out for cuckoos. And, as our previous experiments have shown, if they see a cuckoo at their nest they are more likely to reject the cuckoo’s egg.
These ideas stimulated another set of experiments on Wicken Fen. First, Justin and I tested whether it really was the loud rasping calls of the reed warblers that attracted neighbours, rather than other signals, for example the movements of the reeds or the sight of the enemy itself. We placed small loudspeakers in the reeds, away from any nests, so our results would not be confounded by the calls of reed warblers themselves. When we broadcast rasp calls, ‘skrr . . . skrr’, reed warblers quickly approached from up to 40 metres away. We could see the reeds twitching as the warblers climbed up the stems to peer over the tops, and then they made short flights to the speaker. Sometimes, up to six neighbours came over to investigate. When we broadcast a control call, the territorial call of a male chaffinch, ‘hreet . . . hreet’, reed warblers were rarely attracted, so neighbours were alerted specifically by the alarm calls of their own species.
Next, Justin and I tested what reed warblers might learn from investigating the cause of alarms on a neighbouring territory. For this experiment, we placed a cuckoo mount next to a reed warbler’s nest and alongside we placed a loudspeaker, which broadcast reed warbler rasp calls, to ensure the neighbours came to see what was going on. We used several cuckoo mounts and several different broadcasts to make sure the responses were not due to unusual features of particular mounts or broadcasts. Once again, neighbours approached, and this time they saw the cuckoo mount. It was remarkable to watch the reed warblers trespassing right into the middle of a neighbour’s territory, something they would not normally dare to do. Sometimes the territory owners chased them off.
We then considered whether this eavesdropping experience affected how reed warblers responded to a cuckoo mount at their own nests. It certainly did! Having observed their neighbours mobbing a cuckoo, the warblers became much more responsive to a cuckoo on their own territory: they were quicker to approach a cuckoo mount at their own nest, and they behaved more aggressively towards it, giving many more rasp calls. Furthermore, this increase in aggression was specific to cuckoos; the reed warblers did not change their responses to mounts of other species. In effect, the hosts have a neighbourhood watch, where the word gets round that there is a particular threat at large, so everyone is on alert and defences are increased specifically to that enemy.
Let’s now summarise the various host defences and cuckoo tricks that have been unravelled by these experiments:
(1) Hosts reject eggs that differ from their own in colour and pattern. In response, cuckoos evolve such good forgeries that the hosts cannot be completely certain whether they have been parasitised, simply by inspecting their clutch.
(2) Hosts therefore watch out for cuckoos to determine their risk of parasitism. If they see a cuckoo at their nest, they are more likely to reject an egg. In response, cuckoos are very secretive and quick when they lay, to avoid alerting the hosts.
(3) Hosts also attack female cuckoos, which deters the cuckoo from laying. In response cuckoos mimic hawks, which makes the hosts more wary of approaching them.
(4) Hosts now widen their source of information about local cuckoo activity, not only watching out for cuckoos on their own territory, but also listening out for whenever neighbours give alarms. If they see a cuckoo being mobbed on a neighbouring territory, they are more likely to risk close approach and to attack a cuckoo at their own nest. As we shall now see, the cuckoo combats this last host defence, too. It does so by coming in different guises.
All adult male common cuckoos are plain grey above. But females come in two plumage types, or morphs: some are grey above, like the males, while others are bright rufous. When I first saw a rufous female cuckoo flying past, I failed to recognise it for a moment because I was so used to expecting cuckoos to be grey. Could different guises baffle the hosts too?
Rose Thorogood and I tested this by presenting reed warblers with either grey or rufous cuckoos. We used wooden models this time, to be sure that the cuckoos were identical except for their colour. My artistic wife, Jan, made the models, so art and science came together for these experiments. We repeated our ‘neighbourhood watch’ tests, in which we presented a cuckoo at a reed warbler nest, together with the broadcast of reed warbler alarm calls, to attract neighbours. But this time we sometimes presented a grey cuckoo, sometimes a rufous cuckoo.
As before, we found that reed warblers increased defences back at their own nests if they had witnessed a neighbour mobbing a cuckoo. However, they only increased their response to the cuckoo morph that they had seen their neighbours mobbing. If they had seen neighbours mobbing a grey cuckoo, they were alerted only to grey cuckoos at their own nest, while if they had seen neighbours mob a rufous cuckoo, they were alerted only to rufous cuckoos at their own nest. Therefore, whenever hosts became alerted to one cuckoo morph, the alternative morph was more likely to be undetected.
In the fens, grey female cuckoos are much more common than rufous females. Perhaps grey females have the extra advantage of looking like sparrowhawks, while rufous females simply get an advantage from being rare, and so are less likely to be recognised as an enemy when hosts are on the lookout for grey cuckoos? However, in some other parts of Europe rufous female cuckoos are the more common morph. The reasons for this geographical variation are not yet known.
Variable plumage is characteristic of other species of parasitic cuckoo, too, and is likely to have evolved to confuse enemy recognition by hosts. Just imagine how easy it would be for us to recognise a thief if all thieves were like those in cartoons, with masks and bags labelled ‘swag’. But thieves come in many guises: some are smartly dressed, some appear to be friends rather than foes. Most of us will get tricked at some time in our busy lives.
Spare a thought for the reed warblers, then, rushing to raise their brood during a short British summer. Your arch enemy sometimes appears hawk-like, but is sometimes very different in its dress; it is secretive and incredibly quick when it invades your territory; and it appears to leave no trace – no change in the number of eggs in your nest, nor in their appearance. You incubate the clutch, and then something extraordinary happens; one of the chicks throws all the other eggs out of the nest and grows to eight times your own body weight. At last, surely, you will realise you have been duped . . .