Bird Sense (17 page)

It is well known that the European cuckoo chick eliminates any competition by pushing host eggs or chicks out of the nest directly. Like the honeyguide chick, it hatches with its eyes closed and relies on an acute sense of touch to detect and eject host eggs or young. Prior to Edward Jenner’s direct observation of the nestling cuckoo’s ejection behaviour, in
1788
, many people thought that the adult cuckoo was responsible for the disappearance of host eggs or young. What’s more, many people found it almost unbelievable that a newly hatched cuckoo chick could – or would – behave in such an apparently evil manner. However, once Jenner had alerted them, the sceptics soon witnessed the behaviour for themselves. ‘A monstrous outrage on maternal affection,’ Gilbert White called it in
The Natural History of Selborne
. Starting a few hours after hatching, the cuckoo chick begins to manoeuvre itself so that the host eggs or young are lodged, one at a time, in a small pit in the middle of its back, between its scapulars. Bracing itself against the sides of the nest with its legs, the young cuckoo heaves each victim up and over the side of the nest. Although it has not been investigated, the pit on the young cuckoo’s back must be loaded with touch receptors, triggering the ejection response each time something the size of an egg or nestling touches it. After a few days, the cuckoo chick’s ejection response wanes, by which time it has usually removed any host eggs or young, or sometimes even another cuckoo egg or chick.
43

The main focus of my own research is promiscuity in birds: the behaviour, anatomy and evolutionary significance of avian infidelity. Since some birds copulate for long periods of time or copulate many times each day, a question I am often asked is: do birds enjoy sex?

In some species, like the European dunnock, copulation is so rapid – it has been timed using high-speed photography at one-tenth of a second – it is hard to imagine it generating much pleasure. On the other hand, so much of a bird’s life is speeded up that perhaps to a dunnock one-tenth of a second is equivalent to several minutes for a human. In fact, most small birds copulate for only a second or two and show no sign of any physical pleasure in what has been euphemistically referred to as a ‘cloacal kiss’.
44

There are other birds that copulate for much longer, and still show no signs of pleasure, let alone ecstasy. The greater vasa parrot of Madagascar, for instance, has one of the most protracted copulations of any birds, up to one and a half hours, with the added complexity of a copulatory tie, exactly like that seen in dogs. On witnessing a canine copulatory tie for the first time, dog owners are often confused about what is going on, not least because the two animals face away from each other – because the male turns round. In the vasa parrot the copulatory tie is rather more polite in that the two animals remain perched side by side, the male nibbling his partner’s head feathers (and appearing to whisper sweet nothings to her), while locked in their genital embrace. Strictly speaking, the male vasa parrot (unlike a dog) has no penis, but he does have a large, globular cloacal protrusion that, once inside the female, becomes engorged with blood (much as does the dog’s penis), effectively locking the male inside the female’s cloaca. The two birds sit side by side, but with little movement and even less indication of pleasure. The function of this unusual behaviour and its extraordinary accompanying anatomy, is, as my PhD student Jonathan Ekstrom demonstrated, sperm competition: vasa parrots are among the most promiscuous of birds.
45

I became intrigued by this species when a colleague, Roger Wilkinson, who was then curator of birds at Chester Zoo, sent me some photographs of his vasa parrots before, during and after their protracted and bizarre copulation. Not long afterwards, and quite independently, I received a message from another colleague, Andrew Cockburn, who had been birdwatching in Madagascar and had seen wild vasa parrots copulating: ‘knowing of your interest in avian copulation’, his message started, and then went on to describe what was effectively the same behaviour as in Roger’s captive parrots. I decided this would make an interesting research project for an intrepid and enterprising student. Jonathan fitted the bill, and it was indeed a tough project. As well as coping with high temperatures and high humidity, and climbing up into the canopy and then down through the hollow trunk into the base of gigantic baobab trees, where the parrots nested, he also acted as amateur doctor to the desperately undernourished local people.

Despite all this, he obtained some remarkable results. Briefly, the birds’ breeding system is unlike any other. Females sing to attract males; males appear from the forest and copulate with females – several males over several days. The female incubates the eggs alone, but when the chicks hatch she emerges to sing again, and males appear once more, this time to give her regurgitated fruit which she takes back to the chicks. DNA fingerprinting analyses revealed that almost every chick in a brood has a different father. The remarkable thing is that the males that comprise the fathers of a brood are the fathers of offspring in nests dotted across the Madagascan forest – there are no bonds of exclusivity. Like Willughby and Ray, I am happy to leave it to others to figure out why such an unusual system has evolved. What we can be reasonably confident about is that the protracted copulation in this species has almost certainly evolved in response to the intense sperm competition mediated by the females’ promiscuity. By copulating for a long time – a process facilitated by the unique copulatory tie – a male probably maximises his chances of fertilising the female’s eggs. Whether the females or her several partners derive any pleasure from their copulation is not known, but to be able to perform the behaviour at all must require at least some tactile sensitivity.
46

There is one bird, however, where sexual pleasure is strikingly apparent: the red-billed buffalo weaver, a starling-sized African bird. In February
1868
, when he was preparing his book on sexual selection, Charles Darwin wrote to his favourite cage-bird informant, John Jenner Weir, to ask if he could ‘call to mind any facts bearing . . . on the selection by a female of any particular male – or conversely of a particular female by a male – or on the allurement of the females by the males – or any such facts’. Weir wrote back immediately describing the courtship and mating behaviour of several birds he had in captivity, including the buffalo weaver, saying that there was ‘nothing particularly striking’ about this species.
47

How wrong he was. For lying just in front of the male buffalo weaver’s cloaca is a false penis: a two-centimetre-long fleshy finger-like appendage. Seeing the bird going about its everyday business you wouldn’t know there was anything unusual about its anatomy, for the false penis is obscured by the black body feathers. Holding the bird upside down in your hand, and blowing gently on its underside, reveals the full glory of this bizarre structure. First described in the
1830
s by prolific French naval apothecary and naturalist René Primevère Lesson (
1794
–
1849
), buffalo weavers are unique among birds.

Fascinated by Lesson’s account, and one from the
1920
s by the Russian ornithologist Petr Sushkin, I decided to investigate further, convinced that this extraordinary structure must have evolved in relation to sperm competition. The first step was to see one for myself and by a fortunate coincidence I learned that the museum in Windhoek, Namibia, had a specimen I could have. The pickled specimen that duly arrived in the post was perfect: a male in full reproductive condition. The accompanying note explained that these were ‘trash’ birds in Namibia, considered a nuisance by farmers for building their enormous stick nests on windmills and disrupting the essential business of pumping water out of the ground on to the dry desert soil. My dissection confirmed everything that Sushkin said: the false penis was a rigid rod of connective tissue, with no ducts or tubes, no obvious blood supply, and, according to previous accounts, no nervous tissue either. This was odd, for the outward appearance of the phalloid organ screamed tactile sensitivity. Rarely in all my research on the reproductive biology of birds had I encountered a more pointed symbol of male virility.
48

Significantly, my dissection revealed that the bird had relatively large testes, a sure sign of female promiscuity and rampant sperm competition. One thing led to another and, before I knew it, I had a project on buffalo weavers in Namibia, with an enthusiastic young research student, Mark Winterbottom, conducting the fieldwork. At first glance, buffalo weavers seemed very easy to study. The birds were common and in some areas almost every windmill supported their conspicuous thorny nests, which were wonderfully accessible. Less conveniently, they also nested in acacia trees, including the one overhanging the house we rented on a game farm. Waking at first light each morning to the calls of male buffalo weavers was wonderful and seemed almost too good to be true.

It was. Nests – sometimes a metre or so across and containing multiple chambers – were often owned by two males operating as a team. This is unusual for birds of any kind and an arrangement that seemed to predispose them to sperm competition. The several nests above our house were occupied by several teams, or coalitions, as we called them, of males which we caught and colour-ringed so that we could see who was who. But there were no females. Males spent their early morning at the nest, adding a few sticks and performing the occasional display or squabbling with one of the others. Then, one morning, with no warning, our males suddenly launched themselves into a frenzy of display, fluttering, bowing and calling, as a small party of females flew overhead. They didn’t stop and our males’ enthusiasm evaporated as rapidly as the females disappeared. Eventually it dawned on Mark and I that the buffalo weavers’ breeding system was an opportunistic one, completely dependent on females taking a fancy to a group of males (or their nests) and deciding to stay and breed. The birds above our house were obviously hopelessly unattractive for, during that first four-month-long field season, no breeding occurred.

Elsewhere on the farm things were better and at another colony we soon witnessed the arrival of a group of females and the extraordinarily rapid onset of breeding. But it was copulation we were primarily interested in: how exactly did the male deploy his false penis?

The local black farm workers told us we were wasting our time for they knew why the males possessed this structure: it was a device, they said, by which the male carried thorny acacia twigs during nest construction. Our extensive observations, however, provided no evidence whatsoever for this. The local people must have known this, too, so it is curious that that particular bit of avian folklore persisted.

Witnessing copulations was tough. One morning I saw a female leave her nest chamber in what I recognised to be a purposeful way. Flying fast and low over the ground away from the colony, her unusual flight instantly alerted not only me, but also one of the two male nest owners, who immediately followed her. The two birds flew about
200
metres and landed side by side on a low branch of an acacia. I followed, too, but in
40
o
C heat running was hard work. Sweating profusely and barely able to hold my binoculars steady, I watched the two birds bobbing up and down beside each other in a kind of mutual display. Initially they bobbed out of synchrony, but soon they were bobbing in unison, faster and faster, and building up to a climax. Just at the moment when I thought the male would mount the female, and I would get to see what happened with the false penis, the female took flight again. The male followed; I followed, too, and we all repeated the same performance, but no cigar. They flew off again and again and I eventually lost them. They were indifferent to my presence, so it wasn’t me scaring them off: this was simply the female’s elaborate way of testing the male.

Over the three years of study Mark and I witnessed only a handful of copulations. Most were preceded by the synchronous bobbing display, and all the copulations were extraordinarily protracted. The male clung to the female’s back, leaning backwards in an extremely unusual posture, flapping his wings to maintain balance while maintaining what looked like vigorous cloacal contact. The female, on the other hand, seemed almost to be in a trance, stoically enduring the male’s endless bump and grind. What was most frustrating, though, was that we simply could not see what was going on with the false penis – we were too far away, and there were too many feathers in the way. If we were to crack this, watching wild weavers wasn’t the answer. We needed to be able to observe them in captivity.