Five hobbies feasting on newly-emerged mayflies, high over the fen.
In the final paragraph of The Origin of Species, Charles Darwin uses the metaphor of an entangled bank to provide a poetic vision for how the diversity and ecological complexity of the natural world has resulted from natural selection:
It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us . . . growth with reproduction; inheritance . . .; variability . . .; a ratio of increase so high as to lead to a struggle for life, and as a consequence to natural selection, entailing divergence of character and the extinction of less-improved forms. Thus from the war of nature, from famine and death . . . the production of the higher animals, directly follows. There is a grandeur in this view of life . . . from so simple a beginning endless forms most beautiful and most wonderful have been, and are being evolved.
Not everyone might regard the habits of cuckoos as ‘most beautiful’. When visitors to Wicken Fen see me searching through the reeds and discover that I’m looking for cuckoo eggs, many say: ‘Oh good. Are you throwing them out?’ But surely everyone will agree that cuckoos are ‘most wonderful’, in the sense of strange, astonishing and marvellous to behold. Before Darwin, observers were full of wonder that the Creator would design a bird with no parental instincts. Today, naturalists are still full of wonder at how parasitic cuckoos have evolved from parental ancestry, and how their trickery has co-evolved with host defences.
Darwin himself expressed this continuing sense of wonder in the final pages of The Origin:
When we no longer look at an organic being as a savage looks at a ship, at something wholly beyond his comprehension; when we regard every production of nature as one which has had a long history; when we contemplate every complex structure and instinct as the summing up of many contrivances, each useful to the possessor . . . how far more interesting . . . does the study of natural history become! . . . When I view all beings not as special creations, but as the lineal descendants of some few beings which lived long before the first bed of the Cambrian system was deposited, they seem to me to become ennobled.
Once more, I am sitting by the Wicken Lode, the waterway that winds westwards through the centre of the reserve. Sitting on a bank seems a fitting way to contemplate Darwin’s entangled bank. In the reed fringes along the edge of the lode, several reed warbler nests have been parasitised and the warblers are now unwittingly incubating a cuckoo egg, a living time bomb that will destroy their clutch. Then, as I gaze down into the still waters below, I begin to think beyond my obsessions with the world of cuckoos and their hosts.
The oil paintings of my eldest daughter, Hannah, have taught me how to see the many layers in a reflected surface. Her paintings capture a brief moment as you walk along a street and glance at café window; a dream-like world, where reflections of passers-by and smudges on the glass surface intermingle with coffee cups and lights inside the café, which seem to float beyond. There are many layers, too, as I look in the water below me: first I see the reflections of blue sky and of a flock of swifts, high above, scything the air below a billowing white cloud; then I focus on the sheen of the water surface, and bright blue damselflies resting on the lily pads; finally I look through the water, where there are shoals of fish feeding in the mud at the bottom of the lode. And I begin to realise that through all these layers – the skies above, the water surface, and the depths below – there are interactions as beautiful and wonderful as those between cuckoos and their hosts.
Gilbert White spent the best part of 60 years in his beloved village of Selborne. I have been lucky to travel the world, though I have spent the last 30 summers on Wicken Fen watching cuckoos and their hosts. But one could spend a lifetime here, just sitting on this bank, and still always be discovering something new.
We begin our celebration of an entangled bank on the water surface, where a moorhen swims along the edge of the lode towards her nest, hidden in a clump of rushes and reeds. The nest has seven eggs; four have large reddish spots at the blunt end, three are smaller with fine speckling. One might wonder if two different females have laid eggs in the same nest. Twenty years ago, David Gibbons and Sue McRae, research students at Cambridge University, discovered that moorhens in the fens do indeed often play at cuckoos, by parasitising the nests of other moorhens. They colour-ringed a population of about 80 breeding pairs at a fenland site near Peterborough, so they could follow the behaviour of individuals, and used DNA profiles to identify parasitic eggs.
Sue and David found that 10 to 20 per cent of moorhen nests were parasitised by other moorhens, often with just one foreign egg, but sometimes with up to six. Some parasitic eggs came from females on neighbouring territories, laying a few parasitic eggs before they then laid a normal clutch in their own nest. These females were trying to augment their breeding success with a few extra eggs foisted on their neighbours. Others came from females whose nests were predated during the laying of a clutch on their own territories. These females were trying to salvage the remainder of their clutch by laying eggs parasitically next door. Finally, some came from females who couldn’t find space to set up a territory of their own and who were trying to get at least some success by parasitism.
This last category of females had very low breeding success, perhaps partly because they were poor-quality individuals, but also because any attempt to breed purely by parasitic laying is likely to be unrewarding for a moorhen. A cuckoo can easily survey many host territories from a concealed perch. A moorhen is clumsy and conspicuous in flight and has to walk from one territory to the next. It would find it much harder to watch hosts and to gain access to sufficient nests at the correct stage of egg laying to beat the rewards from nesting and bringing up its own young.
When a moorhen lays in another moorhen’s nest, she doesn’t remove a host egg, but simply adds her egg to the host clutch. Parasitic eggs that appear in an empty nest are quickly ejected or pecked and eaten by the hosts. But once the host has begun her clutch, she doesn’t eject parasitic eggs. It might be difficult for a female to recognise a foreign egg, because her own eggs are often variable in colour and markings. Nevertheless, hosts often desert a nest if they are parasitised early on in laying, or if several parasitic eggs appear at once. Moorhens do not have the benefit of DNA profiles, but even the limited knowledge that ‘there are more eggs here than I can have laid myself’ can be a useful rule for rejection.
Moorhens lay their eggs in the evening, usually just after darkness falls. At this time, the male takes over the duties of incubation and nest defence, perhaps because he is larger than the female and better able to chase off nocturnal predators. Parasitic eggs are laid in the evening too, so this raises the possibility that the host male might copulate with the intruding female and fertilise either the parasitic eggs, or some of the eggs that she lays later in her own nest. Sue McRae’s DNA profiles revealed that this never happens. All the parasitic eggs are fertilised by the parasite’s mate, and he also fathers all the eggs that a parasite lays back home in her own nest. This means that both members of the host pair should try to keep parasitic females at bay.
Sue set up video cameras with image intensifiers, so she could film laying behaviour during dusk and by moonlight. During normal laying, the female arrives at her nest, stands next to it and calls softly ‘puck, puck’ to her sitting mate. She has her head raised, she is relaxed, and she often preens while she waits for him to leave. He then steps aside and stands nearby while she settles on the nest. She sits there for about half an hour to lay. Then she leaves, and the male sits on the nest once more.
Parasitic laying is a remarkable contrast. The parasite’s mate stays at home, so she arrives in the dark alone. Her entry to the territory is probably easiest at night, when the male is on the nest, because during the day, when the female is incubating, the male patrols the territory and is vigorous in evicting all intruders. The parasite female charges quickly towards the nest in silence, and with her head held low. She has no hesitation and must know the exact location of the nest from previous scouting visits. Sue filmed nine parasitic layings. In one case, there were no hosts present and she laid in peace, though she was clearly nervous. In two cases, the host female was on the nest, laying her egg for the evening. She sat tight, while the parasite squeezed alongside, facing in the opposite direction and trying to protect her head from the resident female’s pecks. In one of these cases, the host female called and her mate arrived to join in the attack.
In the other six cases, the host male was on the nest when the parasite female arrived. Once again, she squeezed alongside him, head to tail, and sat there quietly while his blows rained down on her. Parasites never fought back and always remained motionless. The hosts may have limited their aggression because a more violent struggle would have cracked their own eggs. Parasite females laid quickly, in two or three minutes, and then ran off back to their own territories, often pursued by the host male. These remarkable film sequences show that the parasite females need a combination of stealth, speed and bravery to succeed.
Occasional parasitic laying has now been recorded for over 200 species of birds. This ‘part-time’ cheating is a regular tactic for trying to produce at least some offspring when a female is prevented from nesting normally, by shortage of nest sites or territories, or because her clutch has been taken by a predator. But birds are not the only creatures to foist care of their eggs onto other parents. We now change our gaze from the water surface and peer into the depths of the lode, where one of the most abundant fish, the bitterling, has a remarkable relationship with freshwater mussels.
Bitterling are small fish, up to seven centimetres in length. In spring, the males become colourful, with red eyes, a dark violet back, a pink-red flush underneath, and a vivid green stripe along the side. They set up territories around freshwater mussels, which live half-buried in the mud at the bottom of the lode. Most territorial males defend just one mussel, but some may have several mussels in their territory. If another male approaches, he is head-butted and chased off.
Breeding females are dull coloured, grey-green on the back with silver sides, but it is easy to identify them when they are ready to spawn by their long ovipositor, a tube hanging down below that may be as long as the female’s body. When a female with an extended ovipositor approaches, the male displays to her by quivering his body alongside, and then he leads her to his mussel. Mussels extract food particles and oxygen from the water by passing a stream of water over their gills. Water enters through an inhalant siphon and exits through an exhalant siphon. The female bitterling inspects the exhalant siphon, determining the suitability of the mussel by the oxygen concentration in the water passing out.
If she decides this is a suitable place to lay her eggs, then the next sequence happens with tremendous speed. She sweeps down, inserts her ovipositor deep inside the exhalant siphon, extrudes from one to six large eggs in less than a second, and then swims off. The male then immediately ejaculates sperm into the inhalant siphon, where they will be swept inside the mussel by the inflowing water to fertilise the eggs. For the next minute, the male is especially aggressive, and with good reason because neighbouring males sometimes try to sneak in to fertilise the eggs, and sometimes a whole shoal of up to 60 non-territorial males rush past and release sperm too. Both the resident male and these sneakers sometimes also compete by releasing sperm into the mussel’s inhalant siphon before the female lays.
The bitterling’s eggs become lodged deep in the mussel’s gills, which provide a safe haven for their development. They hatch 36 hours later, then the fish embryos live on their yolk reserves for about a month, growing to one centimetre in length before emerging through the exhalant siphon into the dangerous outside world.
Some mussels are laid in repeatedly by the same or several female bitterlings, and may end up with 100 or more young bitterlings in their gills. They may suffer damage to their gills and disruption to the water flow, and the young bitterlings also compete for oxygen with the mussel’s own developing larvae. In many ways, therefore, the relationship is like that between the cuckoo and its hosts. Do mussels defend themselves against bitterling parasitism? Recent studies by Martin Reichard, Carl Smith and colleagues from the University of St Andrews show that indeed they do, but defences take time to evolve, just as they do for cuckoo hosts.
In Turkey, mussels and bitterlings have lived together for at least two million years. Here mussels have strong defences: they are quick to close their exhalant siphons if stimulated by touch, which must make it difficult for the female bitterling to lay her eggs, and they often dislodge bitterling eggs and embryos by contracting their shell valves, to pass a stream of water over their gills, and then they eject them through the exhalant siphon. In central and western Europe, by contrast, including the lodes of Wicken Fen, bitterling are recent colonists, within the last 100–150 years. Here, the mussels do not have these strong defences. As with many cuckoo–host interactions, this will be a wonderful opportunity to watch evolution in action, as the mussels begin to defend themselves against the new invaders.
We remain sitting on our bank, but now we change our gaze once more, this time to the skies above. On a few warm mornings in May there is a sudden and spectacular mass emergence of thousands of mayflies from the lode. The young stages, the nymphs, are aquatic and live for a year or two, feeding on algae and vegetation. When they emerge from the water and become winged adults, they live up to their name, the Ephemeroptera, lasting but a day (ephemeros) on the wing (ptera). Adult mayflies do not feed; they live for just a few hours, during which they find a mate, lay eggs and die. They have large wings and long tails, which act as parachutes, and they shimmer as they dance and float through the air, but they are weak fliers and provide a feast for predators.
We are watching a flock of 12 hobbies swooping fast and low over the lode, enjoying this bonanza of food. These are the most agile and graceful of falcons. Their long, scythe-like wings sometimes give them the appearance of a large swift, and indeed they can catch swifts and swallows on the wing, dashing at tremendous speed to pluck one out of the skies with their talons. But in the spring hobbies often feed on insects, which they seize with their claws and then hold up to their beak to devour in flight. They hunt the mayflies with a regular beat, flying into the wind for 100 metres or so to catch prey, and then turning away from the lode and flying back downwind to repeat the circuit. By choosing the best place to sit on the bank, we can watch them speeding past and catching mayflies just a few metres away.
Richard Nicoll has spent many hours photographing the wildlife on Wicken Fen, and I have one of his superb photos, which captures the grace and precision of a hobby about to make a catch. Both hobby and mayfly are in perfect focus. The hobby’s yellow feet have swung up, so the claws are held directly in front of its beak. Its long grey pointed wings are in perfect balance, so although this is a frozen moment you can sense the speed as the hobby closes in on its kill, its dark eyes intent on the floating mayfly just a few centimetres ahead.
At first, this seems a one-sided arms race, with the slow-flying mayfly no match for the accuracy and speed of a hobby, and easy prey for other predators, too. But the synchronous emergence itself provides safety in numbers and is the mayfly’s key trick for defence. When all the adult mayflies emerge together, the predators enjoy a brief bonanza, but their capacity to capture prey is swamped. Individual mayflies are safest from predation during these peaks of emergence. An alternative explanation for why mayflies all emerge together is that it might enhance an individual’s mating success. A neat test of this idea is possible, because some species of mayfly are parthenogenetic; these species have only females, which give virgin birth to offspring genetically identical to themselves, and so adults don’t need to mate. These parthenogenetic species have exactly the same synchronous emergence as sexual species. So reducing individual predation through predator swamping is probably the major selective pressure favouring synchrony.
We could sit on the bank for a lifetime to admire countless other tricks which predators have evolved for finding and capturing their prey, and defences which their prey have evolved for concealment and escape. But arms races involve not only battles between different species: predators versus prey or parasites versus hosts. There are also intense conflicts within species: between rivals for mates, and between males who are keen to mate and females who are reluctant to do so. These also provide an intriguing part of Darwin’s entangled bank.
We return our gaze to the water surface. Water striders, or pond skaters as they are sometimes called, are skating over the surface of the lode. Their legs are long and slender. The middle pair is the longest and is used for rowing, the hind pair is for steering, and the front pair, held forward, has claws for grabbing prey. They detect the ripples from struggling spiders and insects that have fallen into the water, dash over to grab and pierce them, and then suck out the juices inside.
Male water striders are also searching for mates. When a male encounters a female, he pounces on top of her and then tries to secure a mating by grasping her with elongated genitalia at the tip of his abdomen. It pays a male to try to mate even with females who have already mated, because his sperm will displace previous sperm from the stores inside the female’s tract, to give him paternity of her eggs. However, a female tries to avoid superfluous matings because, with a male on her back, she is less mobile, has lower feeding success, and is more likely to be caught by a predator. The female has a weapon for resisting unwanted males: a spine on the tip of her abdomen, which she jabs up into the male as he attempts to grasp her.
There are many species of water striders. In species where the males have the most elaborate grasping genitalia, females have the longest spines. Therefore male structures to force matings have co-evolved with female structures to resist. This arms race between the sexes within a species is an exact analogy of our arms race between cuckoos and hosts, where better cuckoo trickery to deceive (egg mimicry) has co-evolved with better host resistance (egg rejection).
Other female insects try to avoid superfluous matings by deception rather than by force. In many damselflies, some females are brightly coloured, and look like males, rather than having the typical dull female colouration. Females that mimic males are less likely to be harassed by males in search of matings, and so are better able to lay their eggs in peace. This raises the question: why aren’t all females brightly coloured? One possibility is that brighter individuals are more conspicuous to predators. They may be more likely to end up in the mouth of a hungry reed warbler, so the proportions of females that are bright or dull may reflect a balance of selective pressures. The other possibility is that as more and more females mimic males, the deception becomes less effective. Indeed, if all females were mimics, then clearly it would pay a male to check every bright individual closely, to determine if it was a potential mate. So the outcome of evolution might be a mixture of female guises, dull and bright females, like the mixture of grey and rufous female cuckoos that has evolved to thwart host defences.
Darwin’s entangled bank is clothed with interactions every bit as strange as those between cuckoos and hosts. The ‘war of nature’, entailing the ‘famine and death’ of natural selection, has given us much beauty and wonder: from the dances of mayflies and the speed and grace of the hobby, to the guile of moorhens, water striders and damselflies, struggling to outwit their own kind. We are all familiar with climate change and with the idea that animals and plants must adapt to changes in the physical world. But even if the physical environment remained constant, evolution wouldn’t come to a halt. The organic world is forever changing, and organisms will continue to evolve, simply to keep track with changes in their predators, parasites and competitors. Watching cuckoos and their hosts provides a window onto the wonders of this extraordinary entangled bank.