A reed warbler feeding its brood of five young, now 7 days old.
Wicken Fen, 22 June 2014.
To sit quietly in the reeds on Wicken Fen, and watch a pair of reed warblers feeding their nestlings, is to experience another world.
The best way to do this is to tie some reeds and make a narrow channel, so the nest can be observed from the bank. Once you are sitting low down, you sense the sights and sounds from a parent reed warbler’s perspective: a dense green forest of vertical reed stems and long lance-like leaves, the occasional bright flash of a yellow hoverfly, a metallic red beetle or an azure blue damselfly, the glow of white and yellow from water lilies floating in the water below, the gentle whine and hum of insects in the still air, a sudden splash from a pike, the cluck of a moorhen swimming by, the squeal of a water rail, or the shadow of a marsh harrier passing overhead. You feel the reed warbler’s urgency, as it collects prey for its hungry chicks, and then broods them from time to time to keep them warm, all the while remaining alert to signs of danger amongst the background sounds, the swishing of the reeds and the loud cracks of the old reed stems drying in the sun. When you have become immersed in this intimate and hidden world for a few hours, it’s a shock to stand and be exposed once more to a human’s view of the fen, with huge skies and distant horizons.
When reed warblers on Wicken Fen have a cuckoo chick in their nest, they behave as if nothing was amiss; they feed and protect it just as if they were caring for a brood of their own chicks. They bring the same food: mainly bill-fulls of small flies or single large items, such as caterpillars, moths, butterflies, damselflies, hoverflies or dungflies. They also bring food at about the same rate to a cuckoo chick as they do to an average brood of four young reed warblers of the same age. The only difference is that the cuckoo is dependent for longer, 17–20 days in the nest plus 16 days after fledging, compared with just 11 days as nestlings plus 12 days as fledglings for a brood of host young.
In a study in the Czech Republic, Tomáš Grim, from Palacký University, found that reed warblers deserted 16 per cent of cuckoo nestlings when they were about 15 days old, when the normal nestling period expected for a brood of their own young had clearly been exceeded. However, this response is unlikely to be an evolved defence against cuckoos, because he found that a similar percentage of reed warbler broods was also deserted when the normal nesting period was prolonged experimentally, by replacing a brood with younger chicks from another nest. The occasional desertion of a cuckoo chick, therefore, was probably a by-product of the reed warblers protecting themselves from continuing to feed slow-growing broods of their own, which are likely to fail.
On Wicken Fen, by contrast, we have never recorded reed warblers deserting cuckoo chicks, despite their prolonged nestling period. How, then, does a single cuckoo chick persuade its reed warbler foster parents to work as hard as they would for a whole brood of their own young? Rebecca Kilner, David Noble and I spent two summers trying to solve this question by various experiments.
First, we wondered if the cuckoo’s bright orange gape was the key attraction for the hosts. This is certainly the case for rufous bush chats, a favourite host of the common cuckoo in southern Spain. Fernando Alvarez, from the Biological Station of the Coto Doñana, used non-toxic food dyes to colour the normally yellow gapes of nestling rufous bush chats bright orange. Their parents immediately brought them more food! So for these hosts, the cuckoo nestling’s orange gape works as a ‘super-stimulus’, producing a greater response than the gape colour that the parents normally expect. Reed warbler nestlings also have yellow gapes. However, when we used food dye to make them orange, the parent reed warblers did not bring more food, nor did they prefer an orange-gaped chick in among a brood of chicks with yellow gapes. So, for reed warblers, an orange gape does not work as a super-stimulus.
Next, we thought that the hosts might be stimulated simply by the cuckoo chick’s large size. If so, then a large chick of another species should be provisioned just like a cuckoo. We tested this by an experiment, done under licence, where we temporarily replaced a brood of reed warblers with a single blackbird chick, just for a few hours. (Meanwhile, we kept the reed warbler brood warm and well fed in an artificial nest.) We predicted that if the parent reed warblers’ provisioning was determined by the size of the chick in their nest, then they should bring as much food to a single blackbird as to a single cuckoo of the same weight.
Reed warblers have their chicks rather late in the summer, in June and July, by which time most blackbirds have finished breeding, so it was hard work finding blackbird broods from which we could borrow a chick for our experiment. A further practical problem was that at first this experiment didn’t work because the blackbird chick crouched in the reed warbler’s nest and would not beg. We then realised why: the blackbird was used to a stable nest in a bush, not one that swayed in the wind. So we anchored the nest, by tying the supporting reeds to a bamboo cane in the mud. Once the nest was made steady, the blackbird chick began to beg beautifully, and the reed warblers immediately responded by feeding it. However, the results of this experiment at several nests showed that the blackbird was fed at a much lower rate than a cuckoo chick of the same weight. (At the end of these experiments, of course, the blackbird chicks were returned to their rightful nests and the reed warblers were given back their own broods. Their parents continued to care for them as if nothing usual had occurred, unaware of the contribution to science their offspring had made.)
Clearly, the cuckoo’s large size is not a sufficient stimulus on its own to persuade the reed warblers to bring it enough food. Then we realised that parents don’t simply look at their chicks, they listen to them too. When a reed warbler chick begs for food, its call is a high-pitched ‘tsi . . . . . . tsi’. When a cuckoo begs, its call is much more rapid: ‘tsi. . tsi. . tsi. . tsi’. In fact, to our ears, the cuckoo didn’t sound like a single chick; it sounded more like a whole brood of hungry chicks. Was this vocal trick the one that spurred the hosts into treating it like a brood of host young?
We tested this by repeating the experiment with a single blackbird chick in a reed warbler nest, but this time the blackbird was given a helping hand. We placed a little loud speaker next to the nest; whenever the blackbird begged, we broadcast cuckoo begging calls through the speaker. The reed warblers reacted quickly to the extra begging cries and became much more active in collecting food. We did this experiment at several nests, and the results were clear: with the extra stimulation from cuckoo begging calls, the hosts now brought as much food to the blackbird as they did to a cuckoo of the same weight. In further experiments, we found that broadcasts of the calls of a brood of reed warblers had the same stimulating effect. So the cuckoo’s exuberant calling, which sounded like a hungry brood of host young, was indeed the key. An important finding was that the blackbird chick itself did not beg more in response to our broadcast, so it was certainly the calls that spurred the reed warblers on to working harder.
We discovered later that we were not the first to come up with this idea, although we were the first to test it. In 1743, a book was published whose German title is translated as Winged Theology: an attempt to inspire humankind to admiration, love and reverence for their creator by a closer consideration of birds. The author, J. H. Zorn, had certainly considered cuckoos closely. He wrote:
The young cuckoo cries as loud as a whole brood of host nestlings. The reason is to enhance the feeding by the foster parents.
He had beaten us by more than 250 years!
In an essay written in 1926, the mathematician and philosopher Alfred North Whitehead suggested that the guiding motto of every natural philosopher should be ‘Seek simplicity and distrust it.’ How wonderful it was to think that the cuckoo tricked the hosts with visual mimicry in eggs and vocal mimicry with chicks! But this explanation is too simple. At a week of age, the cuckoo chick’s begging call does indeed match the calling rate of a week-old brood of four reed warbler chicks. But as the cuckoo gets older, its calling rate increases still further: by two weeks, the rate is equivalent to two broods of reed warblers. Yet it is still fed like one brood of four young.
Why does the cuckoo have to call faster and faster as it grows? It was Becky Kilner who realised that the way the cuckoo chick’s call works is both more subtle and more interesting than by simple vocal mimicry of a brood. When reed warblers provision a brood of their own young, they respond both to a visual cue – the total area of begging mouths on view, and to a vocal cue – the begging call rate of the brood. The visual cue gives the parents a rough guide to how much food to bring, because it is related to chick number (more chicks, more mouths) and chick age (older chicks, larger mouths). The vocal cue enables parents to fine-tune their provisioning in relation to chick hunger (hungrier chicks call more rapidly). So if reed warblers have more chicks, or older chicks, they work harder, and if they hear their chicks calling more rapidly, they work harder still.
How does the cuckoo chick exploit this system? The young cuckoo needs as much food as four young reed warblers. Its problem is that it presents just one begging mouth. A cuckoo chick’s mouth is, of course, much larger than the mouth of one reed warbler chick. But it is smaller than the total mouth area of four reed warbler chicks, which is the visual stimulus that the hosts use to calibrate the demands of four young reed warblers. As the chicks get older and increase in size, the cuckoo chick’s visual stimulus, a single mouth, becomes relatively even smaller in comparison with the four mouths of a host brood of the same age. The cuckoo’s trick is to compensate for its increasingly deficient visual stimulus by boosting its vocal signal. At a week of age, calling at the same rate as a brood of four reed warblers is sufficient, but at two weeks it needs to sound like eight hungry chicks to persuade the hosts to bring enough food.
So the cuckoo chick’s begging trick is a subtle one: it has ‘tuned in’ to the way the hosts integrate visual and vocal cues when they raise a brood of their own young. Nestling honeyguides, which use their bill hooks to kill the host young, also sound like several chicks, so rapid begging calls may be a regular trick in parasitic birds that are raised singly.
Sometimes nature’s inventiveness is truly astonishing. In Japan, Keita Tanaka and Keisuke Ueda, from Rikkyo University, Tokyo, discovered that the Horsfield’s hawk-cuckoo has an equivalent trick, but it exaggerates the visual component of the begging display. The young cuckoo has a yellow patch of skin under each wing, the same colour as its yellow gape. When the hosts (blue-and-white flycatchers) come with food, the cuckoo usually exposes one wing patch beside its mouth, which makes it appear as if there are two hungry mouths in the nest, rather than one. If it’s very hungry, it exposes both wing patches, so there now appear to be three hungry mouths! Sometimes, the hosts offer food to a wing patch. When Tanaka and Ueda blackened the wing patches, they found that the hosts then brought less food. Perhaps this cuckoo uses visual trickery, to look like several chicks, rather than vocal trickery, to sound like several chicks, because the host nests are particularly vulnerable to predators that locate nests by sound.
It might seem surprising that parent birds are fooled by such simple vocal and visual signals, when a closer look would surely reveal a cuckoo, not a brood of their own young. We might pride ourselves that we would never be tricked so easily. But we are manipulated in the same way by advertisements every day. My favourite example comes from an experiment done by Melissa Bateson and her colleagues in a coffee room at Newcastle University, where there was an honesty box for payment of drinks. Above the box, there was a notice reminding everyone to pay. In alternate weeks, an image was added above the notice: either some flowers or a pair of eyes. On average, people paid three times as much for their drinks when eyes were displayed. Remarkably, this was an unconscious response, because during debriefing at the end of the experiment, most said that they had never noticed the images. Eye images on notices can also be effective in reducing litter and bike thefts.
I sometimes imagine having a conversation with my reed warblers on the fen. ‘Why don’t you realise that there’s a cuckoo chick in your nest?’ I ask them. ‘We don’t see the world like that,’ they reply. ‘We just respond to begging mouths and calls.’ Then the reed warblers ask me: ‘Why don’t you realise that no one is really watching you? Those are just pictures of eyes.’ Just like the reed warblers, we often rely on fast, unconscious responses to make decisions, so we, too, are susceptible to manipulation by simple cues.
Persuading the hosts to bring enough food is only one of the cuckoo’s problems. It also has to contend with predators, such as jays and magpies, and sometimes mammalian predators, such as weasels. Most nestlings crouch when a predator approaches, in the hope that they will not be noticed. By contrast, the common cuckoo nestling has some remarkable defences from about a week of age. If you put your hand towards it, it erects its head feathers and opens its orange gape. Then it suddenly rears up and snaps down again. This is a shock even for someone familiar with the performance, and must surely be an effective deterrent against predators.
Edward Jenner provided a good description in his cuckoo paper from 1788:
Long before it leaves the nest, it frequently, when irritated, assumes the manner of a bird of prey, looks ferocious, throws itself back, and pecks at any thing presented to it with great vehemence, often at the same time making a chuckling noise like a young hawk. Sometimes, when disturbed in a smaller degree, it makes a kind of hissing noise, accompanied by a heaving motion of the whole body.
Perhaps the cuckoo’s orange gape makes the display even more effective. In addition, if touched, the cuckoo produces foul-smelling brown liquid faeces. These are quite unlike the normal faeces, which are white and contained in a gelatinous sac, which makes it easier for the hosts to carry them away.
Why has the cuckoo chick evolved these remarkable defences? One reason is surely the cuckoo’s unusually long nestling period, which will increase the chance that predators will find it. Young reed warblers leave the nest well before they can fly, clinging to the reeds with their strong feet. This suggests that a reed warbler’s nest is a vulnerable place to be, and should be escaped as soon as possible. But the cuckoo has to stay for longer, simply because it takes more time for a larger body to grow. The second reason is that the cuckoo’s loud and rapid begging calls are likely to attract predators to the nest. Certainly, the calls often led us to discover parasitised nests that we had missed at the egg stage. We now encounter another wonderful adaptation of cuckoo chicks which mitigates the costs of their exuberant begging calls.
When a predator approaches a nest, parent birds give alarm calls to warn their chicks of danger. These calls tend to vary between species; for example reed warblers give a low-pitched ‘churr’, while dunnocks give a higher-pitched ‘tseep’. Our experiments reveal that young nestlings respond only to the alarm calls of their own species. Thus, reed warbler chicks cease begging and crouch in the nest when reed warbler ‘churr’ calls are broadcast to them, but they carry on begging if dunnock ‘tseep’ calls are broadcast. Dunnock chicks do the reverse: they respond to ‘tseep’ but not to ‘churr’.
This specific response is not simply an outcome of experience, because when nestlings are cross-fostered to be raised by another species they do not tune in to their foster species’ alarms, but still retain a selective response to their own species’ alarms. This suggests that newly hatched nestlings already have their brains pre-tuned to their own species’ signals. This enables them to pick out their parents’ alarms against a background of irrelevant sounds (for example, the calls of other species or noises from vegetation). It also means they can respond appropriately the first time danger threatens. A correct first response might save their lives.
On Wicken Fen, when reed warblers have a cuckoo chick in their nest, they give ‘churr’ alarm calls in exactly the same way as when they are protecting a brood of their own, which is further evidence that they do not recognise the impostor. My colleagues, Joah Madden and Stuart Butchart, and I tested how cuckoo chicks responded to these alarms by presenting them with broadcasts of recordings. As with the reed warblers’ own chicks, we found that cuckoos raised in reed warbler nests tuned in specifically to reed warbler ‘churr’ alarms, and ignored the alarms of other species. In response to ‘churr’ alarms, not only did they cease begging calls, they also opened their orange gapes wide, a preparation for defence.
How do cuckoo chicks become so specific in their response? To test if learning might be involved, we cross-fostered some newly hatched cuckoos from reed warbler nests to the nests of dunnocks or robins, and then tested their alarm responses when they were six days old. Remarkably, they had not tuned in to the different alarm calls of these new foster parents, but still had a specific response to reed warbler ‘churrs’. This suggests that the race of cuckoo that specialises on reed warblers is pre-tuned to reed warbler alarms, just like the hosts’ own chicks. Pre-tuning might be essential so that the cuckoo responds correctly the first time an alarm is heard. Continued begging when a predator is nearby might be fatal; the cuckoo’s first mistake might be its last. So this cuckoo race has both well-matched eggs and well-tuned chicks. Further studies are needed to test other cuckoo races.
The common cuckoo’s need for special begging tricks is the result of a problem of its own making. By ejecting all the host eggs and young from the nest, it is guaranteed every meal that arrives. But this benefit comes at a price: the cuckoo now has to do all the work of soliciting food from its foster parents. Some other cuckoo species have the opposite problem: the cuckoo chick tolerates the host young and so gets their help in stimulating the host parents to bring food to the nest, but now the cuckoo has to compete with the host chicks once the food arrives.
The problem of how a cuckoo competes with the host chicks has been particularly well studied in great spotted cuckoos in southern Spain, where the main host is the magpie. This species of cuckoo does not eject the host eggs or chicks, so it is raised in a brood alongside magpie young. The begging cries of several chicks in the nest stimulate the magpie parents to bring more food than they would to a cuckoo on its own. The cuckoo then takes advantage of the extra food with two tricks that persuade the magpie hosts to give it an unfair share.
The first trick, discovered by Manuel Soler and colleagues from the University of Granada, is that the cuckoo chick has white papillae on the roof of the mouth, which the hosts find particularly alluring. The second trick, discovered by Tomas Redondo and colleagues from the Biology Station of the Coto Doñana Reserve, is that the cuckoo chick exaggerates its begging calls to sound like a particularly hungry chick. A magpie chick gradually increases its begging intensity as it gets hungrier, with more frenzied gaping and more rapid calling. By contrast, a cuckoo calls with maximum intensity even when it has just been stuffed full of food. As a result, the cuckoo gets the most food, grows to be the largest chick in the nest, and yet still persists with its famished cries. This begging performance was so disturbing for a visitor to Redondo’s laboratory that she insisted he fed the ‘poor starving’ cuckoo every few minutes, until she realised she was being deceived.
Why should magpie parents favour a large and seemingly still hungry chick? In fact this makes good sense in normal circumstances, when the nest is not parasitised. Magpies adjust their brood size in relation to the food available by allowing the smallest nestlings to die if food is scarce. They feed the largest nestling first, and only when this is satiated does the next-largest get fed. If food is in short supply, the smallest chicks then quickly die and the magpies raise a few healthy young. This is much better than spreading scarce food out evenly, which would produce a large brood of weedy chicks, none of whom might survive.
The great spotted cuckoo chick’s exuberant begging exploits this system, which works so well for the magpies in unparasitised nests. Faced with a stimulus of a large chick which never seems to get satiated, the magpie hosts are tricked into diverting most of their hard-won food to the cuckoo, even while their own young perish alongside.