A meadow pipit feeding a fledged young cuckoo.
Dartmoor, 29 July 2007.
Sumer is icumen in,
Lhude sing cuccu!
Are we about to lose our harbinger of spring?
The dramatic decline in cuckoos across England during the last three decades is reflected by the changes we have recorded on Wicken Fen. In 1985, the first year of our study, there were 14 female cuckoos parasitising reed warblers on the Fen, recognisable by their individually distinctive eggs. In the last four years, to 2013, there have been just one or two females. In 2012, not a single cuckoo chick was raised to independence on the Fen, the first time this has happened during the 30 years of our study, and perhaps the first time for hundreds of years.
Our records show that reed warbler numbers on the Fen have not changed, so the decline in cuckoos has led to a marked reduction in parasitism, from 24 per cent of reed warbler nests in 1985 to just 1 per cent in 2012.
Humans are not the only ones to have noticed that cuckoos are becoming scarcer. Remarkably, the reed warblers have noticed it too. Our experiments show that reed warblers are now much more reluctant to approach and mob an adult cuckoo than they were back in the 1980s, and they are also less likely to reject a cuckoo egg. This is not simply a general reduction in their response to any threat, because reed warblers have shown no changes during the last three decades in their responses to other enemies, such as sparrowhawks (a predator of adult reed warblers) or jays (a nest predator).
Why have reed warbler defences against cuckoos declined, now that there is little threat of parasitism? Their change in behaviour makes good economic sense. We have seen in previous chapters that defences are costly. Cuckoos resemble hawks, so it is dangerous to approach a cuckoo-like enemy at the nest. A mistake could be fatal. Cuckoo eggs resemble host eggs, so egg ejection is costly too: sometimes hosts reject their own eggs in error. If reed warblers assess that there are few or no cuckoos, then their best option is to avoid these risks of making mistakes. We invest less in costly defences of our property when the risk of burglary is low. Reed warblers, too, invest less in their cuckoo defences when the risk of parasitism declines.
How have reed warblers adapted so rapidly? Sometimes populations adapt to a changing world by genetic changes. Darwin assumed that such evolution by natural selection would proceed so slowly that we would never be able to observe the changes in progress. Indeed, The Origin of Species does not document any cases of natural selection in action, only the outcomes of past selection, and in a famous passage Darwin wrote:
natural selection is daily and hourly scrutinising, throughout the world, the slightest variations; rejecting those that are bad, preserving and adding up all that are good . . . [but] we see nothing of these slow changes in progress, until the hand of time has marked the lapse of ages.
However, we now know of many examples where genetic variants have such a strong selective advantage in nature that we can watch evolutionary change taking place even within a few years.
Peter Berthold and colleagues from the Max Planck Institute at Radolfzell, Germany, have discovered a wonderful example of evolutionary change in migration due to climate change. During the past 40 years the number of blackcaps wintering in Britain and Ireland has steadily increased. At first, it was assumed that these must be British and Irish breeders, remaining in response to milder winters. However, ringing recoveries indicate that they are breeders from central Europe with an entirely new migration habit of going northwest in the autumn instead of following the traditional route, southwest to the Mediterranean. Berthold was able to study the migration direction of blackcaps in the laboratory by keeping them in small cages. During the migration period, the birds flutter against one side of the cage, indicating the direction they want to fly. When blackcaps wintering in Britain were tested, they exhibited a northwest preference in autumn, a 70-degree shift in direction from the traditional southwesterly route. Furthermore, when these birds that wintered in Britain were bred in aviaries, it was found that their offspring inherited this new autumnal orientation.
In past times, when winters were more severe, mutant blackcaps with this new migration direction would have been eliminated by natural selection. But now the new migration habit is flourishing because of milder weather and more winter food in Britain, both from garden feeders and from winter-fruiting bushes planted in recent decades. This new population of migrants not only enjoys a shorter distance to winter quarters, but also an earlier arrival back in the central European breeding grounds in spring. Stuart Bearhop and colleagues, from the University of Exeter, have shown that this enables them to gain the best breeding territories and to produce more offspring. They also discovered that the difference in arrival times on the breeding grounds results in matings between individuals from the same wintering area. For example, males wintering in Britain arrive early on the breeding territories and tend to pair with early-arriving females, which have also wintered in Britain. The consequence is reduced gene exchange between individuals with different migration habits, which has speeded up the evolution of the new migration behaviour.
Is the rapid decline in reed warbler defences against cuckoos on Wicken Fen also a case of evolutionary change by natural selection? My colleagues and I doubt this, not only because our calculations show that the decline has been too fast to reflect a genetic change in behaviour, but also because we know from experiments that individuals have remarkable flexibility in their levels of defence. When we presented mounts of adult cuckoos at nests, reed warblers were more likely to reject eggs. Their mobbing calls also attracted neighbours, which then increased their defences back at their own nests. The magnitudes of these individual changes in defences are similar to the declines we have seen over the last three decades. Therefore it is likely that the changes we have recorded in the population are entirely a reflection of flexible behaviour: reed warblers monitor local cuckoo activity, and they have reduced their defences because they perceive parasitism risk to be lower.
Why should reed warblers have such flexible cuckoo defences? Across most of Europe and throughout the UK, their populations are often restricted to small islands of wetland in a vast sea of agriculture. Cuckoo numbers are therefore often also small on a local scale, so parasitism is prone to chance variation between neighbouring sites and between years. Furthermore, although ringing recoveries show that some young reed warblers return to breed at their natal site, some disperse to breed up to 200 kilometres away (their average dispersal distance is 50 kilometres), and so they are likely to encounter different parasitism rates from those experienced by their parents. Whenever there is such fine-scale spatial and temporal variation in encounter rate with enemies, it makes good sense for individuals to vary their defences in response to local risks.
For example, in the mid-1980s, cuckoo parasitism on Wicken Fen was high (16 to 24 per cent annually), and our experiments there showed that reed warblers rejected 74 per cent of our model cuckoo eggs that differed in appearance from their own eggs. However, in a small reed bed just 11 kilometres away, where there were no cuckoos, the reed warblers accepted all our model cuckoo eggs. A wider analysis, comparing different populations across Europe, also shows that reed warblers vary their strength of egg rejection in response to parasitism risk. Once reed warblers are equipped to respond to this local variation in parasitism, they are bound to show rapid declines in defences as cuckoos decline.
There are other examples where birds have adapted to a rapidly changing world by individual flexibility in behaviour, rather than by genetic change in the population. In Wytham Woods, near Oxford, female great tits have advanced their egg laying by 14 days over the 47-year period 1961 to 2007. The main changes have been from the mid-1970s, since when there has been a marked increase in spring temperatures. This has led to the earlier emergence of oak leaves and of winter moth caterpillars, which feed on the oak leaves and are a key food for nestling great tits. The earlier laying of the great tits has tracked these earlier springs perfectly, so they still have chicks in the nest at the right time to coincide with the caterpillar peak. Anne Charmantier, Ben Sheldon and their colleagues from the University of Oxford have shown that this change in egg-laying date is entirely due to flexibility in the timing of laying by individual female great tits, perhaps a direct response to spring temperature or leaf burst or some other cue of the timing of the food peak.
Reed warblers and great tits have tracked their changing world by individually flexible defences and breeding times. However, their ability to respond so effectively depends on reliable cues of change, such as observing fewer cuckoos or detecting earlier springs. When cues are not available, it will be impossible for an individual to track change by varying its behaviour. For example, many long-distance migrants, which spend the winter in Africa south of the Sahara, now arrive too late to catch the earlier spring food peak in their northern European breeding grounds. This is because their spring departure from African winter quarters is triggered by changes in day length, unaffected by climate change. Natural selection will now be favouring individuals whose response to day length leads to earlier departures, but it will take time for a population to evolve a new habit. It is still unclear to what extent genetic change will enable animals to keep pace with our rapidly changing world.
Animals and plants have evolved in response to environmental change ever since life began, for example with changes on the grand scale of shifting continents and ice ages. For thousands of years they have been faced with human-induced changes, too, as our ancestors cut down forests, burnt grasslands, and flooded or drained the land. But the current scale and pace of change is unprecedented, involving climate change, habitat destruction and fragmentation, ever more intensive farming and fishing, urbanisation, and a new biotic environment of invasive species, pathogens and parasites. When I was a young boy, I thought there would always be cuckoos calling to greet the spring, and swifts would forever scythe the skies on hot summer days. But the alarming declines in populations of these and many other familiar species mean that our generation will surely be the last to take the natural world for granted. The title of a recent seminar by my colleague at Cambridge, Andrew Balmford, Professor of Conservation Science, neatly captures our dilemma: ‘How to feed the world without costing the earth’.
One of the ways we must help is by preserving and creating more suitable habitat for wildlife. For example, there are now plans to extend the areas of wetland in the old fens of eastern England, partly to compensate for the imminent loss of coastal wetlands, which are threatened by rising sea levels. The new reserve of the Royal Society for the Protection of Birds (RSPB) at Lakenheath is an inspiring example of what can be achieved in a short time. From 1996 to 2004, a 200-hectare area of wetland was created to the south of the Little Ouse River, on the Norfolk–Suffolk border, from land that had been drained at various times from the seventeenth to the nineteenth centuries and converted to arable land in the 1950s. The development of the reserve, led by Norman Sills, the first site manager, and Graham Hirons, chief ecologist at the RSPB, involved transforming carrot fields to a mosaic of washland, pools and wet grassland, with new reed beds created by the planting by hand of over 300,000 reed seedlings and stems. At the time the reserve was set up, the purchase cost of the land plus the capital cost of converting it to a wetland reserve was 1.5 million pounds, about the same as the cost of a large four-bedroomed detached house in a smart part of Cambridge.
By 2010, this new reserve already had thriving populations of Britain’s most characteristic wetland birds, including 12 marsh harrier nests, which produced 30 fledged young that year, four bittern nests, over 100 pairs of bearded tits, several hundred pairs of reed warblers, and, most exciting of all, the first cranes to breed in the fens for 400 years. William Turner mentions cranes in his 1544 book: ‘Cranes . . . breed in England in marshy places. I myself have very often seen their pipers [young].’ However, it is likely that they became extinct as a breeding bird in Britain during the sixteenth century, 100 years before the extensive draining of the Fens. The menu for King Henry III’s banquet in 1251 points to the likely cause of their demise: it included 115 cranes, along with 430 red deer, 1,300 hares, 2,100 partridges, 395 swans, 120 peafowl and lampreys ‘without number’.
With their elegant stature, strength and grace in flight and melancholic bugling cries, cranes have a rich mythology as symbols of vigilance, wisdom, longevity and good fortune. They are often regarded as birds from heaven, whose powerful wings can transport humans to greater spiritual enlightenment. They are the perfect symbol of wilderness, an ‘umbrella species’ whose protection will ensure the survival of wider biodiversity. Cranes are now spreading to other fenland reserves, which are being restored and extended around the washlands of the Great Ouse and Nene rivers. There are also plans to create a large wetland linking the two National Nature Reserves, Woodwalton Fen and Holme Fen, and to extend Wicken Fen, too, perhaps as far south as Cambridge.
As I write these last paragraphs, it is early April and I’m back on Wicken Fen once more, preparing for another season. Cuckoos and reed warblers will have left their winter quarters south of the Sahara, and will be on their way north. I am excited at the prospect of their arrival – hearing their songs once again, finding the first reed warbler nest of the summer and the first clutch with a cuckoo egg.
Marsh harriers are already building nests in the reed beds, and I lie on my back to marvel at the males’ wonderfully exuberant skydiving displays, high over the fen. As thermals develop in the warmth of the early-morning sunshine, they begin to soar, silently, on upswept wings, and to such great heights that they become difficult to pick out with the naked eye against the blue of the sky or billowing white clouds. Then, when they reach the summit of their ascent, they begin an undulating flight, with slow flaps, interspersed with spectacular dives and somersaults, the silver undersides of their wings flashing like mirrors in the sun, and calling all the while with a shrill two-note ‘way-ee, way-ee’. The display may last for 10 or 20 minutes as the male plunges down with closed or partly closed wings, spinning and twisting as he descends, sometimes looping the loop as he flips through a complete revolution before sweeping up again to maintain his elevation.
As I watch, I think of the vast wilderness their ancestors would have surveyed in William Turner’s time, and I wonder if their descendants will soar again one day over a wetland that stretches the 15 kilometres to my home city of Cambridge. Meanwhile, in a week or so, my reed warblers will drop from the night skies to this little patch of fen. My hopes are that some cuckoos will follow them, to thrill naturalists once more with their curious breeding habits, and as harbingers of a new spring.