Bird Sense (18 page)

As a boy I was an avid birdkeeper and I remember looking at the ads in
Cage & Aviary Birds
, the UK birdkeepers’ newspaper, and seeing buffalo weavers offered for sale. But times change and when I looked again, some thirty years later, there were no buffalo weavers on offer. Undeterred, we decided to catch some of the Namibian birds and take them back to Britain. I cannot quite believe we did this now: applying for permits, arranging air transport, veterinarians’ certificates of health and so on, and I suspect that it was only because the birds were considered a pest species that we were allowed to take them. We actually sent the birds to southern Germany, to the Max Planck Institute for Ornithology, where some of my colleagues worked and where a technician, Karl-Heinz Siebenrock, was an enthusiastic and expert birdkeeper.

The birds – twelve males and eight females – were soon building nests out of the hawthorn branches that Karl-Heinz provided as a substitute for the spiny acacia they would normally use. I was optimistic that the birds would at least copulate. Before starting the study I had visited Chester Zoo where Roger Wilkinson (he of the vasa parrots) was curator of birds, and where they had three male buffalo weavers in a very large aviary. We had been to look at them, and Roger had even invited us to bring our captive birds there (I declined because I felt that the warmer summer climate of southern Germany might be more conducive to reproduction). As we walked into the zoo’s giant aviary looking for the buffalo weavers among the (inappropriately) lush tropical vegetation, an unusual movement caught my eye and, lifting my binoculars, an extraordinary sight met my gaze. One of the buffalo weavers was copulating vigorously and repeatedly with a small, slightly dazed-looking dove. On and on the weaver went, copulating with the dove which squatted low and clung on to the branch for dear life. A lack of female buffalo weavers was obviously causing some frustration, but this casual observation suggested that males were both highly motivated to copulate, and did so in a protracted manner.

Our captive males were just as enthusiastic, but they did have the additional stimulation of genuine female buffalo weavers. Mark stayed in Germany to observe, sending me regular reports on his and the birds’ progress. In fact, once the males were fired up and in breeding condition, their sexual enthusiasm knew no bounds. One of the things we wanted was semen samples, and, previously, using the much more modest zebra finch as our study species in captivity, we had developed a novel technique for obtaining some. Presenting a male zebra finch with a freeze-dried female mounted in a soliciting posture was often sufficient to encourage him to court and copulate, allowing us to collect his semen from the false cloaca with which we had fitted the female. I suggested that Mark try something similar using a dead female buffalo weaver we had found. The result, Mark informed me, was spectacular. Males mounted the dummy female immediately and went through their entire, lengthy copulation performance, and provided us with the much-needed semen samples. Later, when Mark showed me a photograph of his mounted female, I was horrified: it was a mere caricature of a bird, with a wire frame for a body, topped by head and wings. But it did the trick, and the males couldn’t resist her.

The male buffalo weavers’ unbridled sexual motivation was a godsend since it meant we could handle them without seriously disrupting their activities in our quest to understand the function of their phalloid organ. Almost any other species would have given up attempting to breed, but not the buffalo weaver. There were plenty of copulations with the real females, and, using a variety of techniques, Mark showed conclusively that, contrary to my expectations, the phalloid organ was not inserted into the female’s cloaca during copulation. First, close-range video provided no evidence for penetration of the female; second, in dummy females fitted with a small piece of sponge inside their artificial cloaca, the sponge was never displaced during copulation; and third, the male’s phalloid organ was rarely damp after copulation, whereas a model phallus gently inserted inside a female usually was.

The most surprising result of all was that, after the full thirty minutes of vigorous venery, the male buffalo weaver appeared to experience an orgasm. This was unheard of: no other bird in the world was known to climax. In a state of high excitement, Mark phoned from Germany to tell me. I was sceptical at first: ‘How do you
know
the male is experiencing an orgasm?’ Indeed, how would one tell whether the male of any other species experienced ecstasy in a similar way to ourselves? The way Mark discovered the answer may sound weird, perverse even, but biologists sometimes have to do funny things in their search for the truth.

Reasoning that what the male was doing was simultaneously stimulating both himself and the female by rubbing his phalloid organ around her cloacal region during his extended mounting, Mark decided to massage a male in the hand for the same time to see what happened. After twenty-five minutes of manipulation Mark gently squeezed the phalloid organ. The result was spectacular: the wingbeats slowed to a quiver, the entire body shuddered, the feet clenched tightly on to Mark’s hand and the male ejaculated.
49

Here was as convincing evidence as one was ever going to get that birds – well, the buffalo weaver at least – have a well-developed sense of touch in their genital region. The result flew in the face of those early researchers who failed to find any evidence of nervous tissue in the phalloid organ. How could there not be? To elicit such a dramatic response, there had to be some sensory mechanism inside the phalloid organ. It prompted me to have another look.

Using two male and two female buffalo weavers shot by farmers, I sent their phalloid organs to a neurobiologist, Zdenek Halata, in Germany. After making thin sections for examination under the light microscope and ultra-thin sections for examination with an electron microscope, Zdenek looked for nervous tissue. It was there: obvious in the males, but much less so in the females, comprising free nerve endings and touch-sensitive Herbst corpuscles (albeit much smaller than he had encountered on other parts of the body in other species). It was difficult to say more than that, but perhaps it was enough.

In human males, orgasm involves free nerve endings and other touch sensors, and a lot more besides. Indeed, the orgasm has been defined as ‘an integration of cognitive, emotional, somatic, visceral, and neural processes’ – or more poetically as a ‘shower of stars’.
50
Intriguingly, in human males the sensory receptors in the penis are not essential since men who have lost their genitalia through warfare or accident are sometimes still able to experience orgasm.

Our main question was why it was necessary for the male buffalo weaver to experience orgasm – and surely, after all that stimulation, the female should have enjoyed an orgasm, too? Perhaps she did, but there were no outward indications to suggest that she had.

Perhaps the most significant question for us was what the advantage of such protracted copulation was for the male. It seemed fairly clear that the phalloid organ has evolved in response to female promiscuity. Our molecular results showed that the two males in a coalition shared paternity, and that females also copulated outside the coalition, so sperm competition was rife. One possibility was that males used their phalloid organ to persuade females to retain their sperm, and the greater the degree of physical stimulation, the more likely they were to do so. In other words, males were trapped in a kind of arms race, to see who could stimulate the females the most through a combination of protracted courtship, a special organ and prolonged mounting. We had no way of testing this with buffalo weavers, but studies of a promiscuous beetle showed that exactly this kind of phenomenon was possible. After inseminating the female, the male beetle performed a kind of copulatory courtship by stroking her with his legs before dismounting. When the researchers prevented males from performing copulatory courtship, the female beetle retained significantly less of that male’s sperm.
51

To sum up, it is clear that the sense of touch in birds is better developed than we might imagine, but I cannot help feeling that researchers have barely scratched the surface, so to speak. There is clearly much more to discover. Sadly, Billie is long gone, but if the opportunity to have another tame zebra finch or other bird arises, I would jump at the chance since it would be relatively simple to devise some simple, non-invasive tests to further explore their tactile world.

4

Taste

Hummingbirds can taste the sugar concentration in nectar. Here a long-tailed sylph licks nectar from a flower – note the tongue protruding from the bill tip: the taste buds are inside the mouth not on the tongue.

These facts and many more of a similar kind . . . fully authorize us, we think, to conclude, that some birds at least are endowed with the faculty of taste; though this is expressly or partially denied by certain authors distinguished for accuracy of observation.

James Rennie,
1835
,
The Faculties of Birds
, Charles Knight

One morning in
1868
, John Weir, an enthusiastic amateur birdkeeper, goes into his aviaries with some caterpillars for his birds to eat. They love natural food like this and prefer it to their usual artificial diet, but on this occasion Weir notices that, while the birds rapidly consume some caterpillars, they leave others untouched. Looking more carefully, he realises that the caterpillars the birds are eating are all cryptically coloured while those they are avoiding are brightly coloured. Wondering whether this has anything to do with their taste, Weir later offers his birds some caterpillars of the ermine moth, which he knows to be distasteful. Most of the birds refuse even to try them, but the one or two that do try them reject them immediately, shaking their heads and wiping their beaks, and are clearly agitated. Weir has witnessed the first evidence that birds have a sense of taste.

John Weir conducted this experiment at the request of Alfred Russel Wallace, with Charles Darwin the co-discoverer of natural selection. Darwin and Wallace were both fascinated by the colour of animals – and by birds in particular – and by the fact that males are usually brighter than females. Darwin’s explanation for this difference between the sexes lay in what he called sexual selection – that females preferred to mate with brighter, more attractive males.
1

The colours of one group of animals, however, the caterpillars of butterflies and moths, could not be explained in this way because as larvae they are sexually immature and incapable of reproduction. Searching for an alternative explanation – he was preparing his book on sexual selection at the time – Darwin sought the advice of Henry Bates. A superb naturalist, Bates had travelled extensively in the Amazon in the
1850
s and written detailed accounts of the insects there. Bates in turn suggested that Darwin ask Alfred Wallace, who had been with him in South America.

Wallace wrote to Darwin on
24
February
1867
saying: ‘I saw Bates a few days ago and he mentioned to me this difficulty of the catterpillars [sic]. I think it is one that can only be solved by special observation.’ Wallace then speculates that:

Birds . . . I presume are great destroyers of catterpillars. Now supposing that others, not hairy, are protected by a disagreeable taste or odour, it would be a positive advantage to them never to be mistaken for any of the palatable caterpillars, because a slight wound such as would be caused by a peck of a bird’s bill almost always I believe kills a growing catterpillar. Any gaudy and conspicuous colour therefore, that would plainly distinguish them from the brown and green eatable catterpillars, would enable birds to recognise them easily as a kind not fit for food, and thus would escape seizure which is as bad as being eaten.
2

He continues: ‘Now this can be tested by experiment, by any one who keeps a variety of insectivorous birds. They ought as a rule to refuse to eat and generally refuse to touch gaudy caterpillars, and to devour readily all that have any protective [i.e. camouflage] tints. I will ask Mr Jenner Weir of Blackheath about this.’

John Jenner Weir and his brother, William Harrison Weir, were knowledgeable and trustworthy birdkeepers from whom Darwin regularly sought information. In response to Wallace’s request, John Weir, who was an accountant by profession, conducted the necessary experiments in his spare time and early in
1868
he reported to Darwin what he had observed.