Authors: Tim Birkhead
Most co-operative breeders, many seabirds and small finches like the zebra finch spend a remarkable amount of time allopreening. In primates, the equivalent behaviour, allogrooming, is known to result in the release of endorphins, which result in the groomed individual appearing to be relaxed – presumably a pleasurable feeling.
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The tame African grey parrots studied by Irene Pepperberg also seemed to go into a state that resembled ‘relaxation’, with half-closed eyes and a relaxed body posture, while she tickled or allopreened them. If she stopped, they would request ‘tickle’, but if she inadvertently touched a growing pinfeather, which is presumably very sensitive, they would give her a threat bite, then relax again and request ‘tickle’ again. Another parrot tamed and trained to talk by the French psychologist Michel Cabanac used the word ‘
bon
’, good, in response to pleasurable events, including being preened or tickled – despite not being trained to do so.
37
Our best hope for better understanding the kinds of feeling birds might experience is through a combination of careful behavioural studies, like those that looked at how much debeaked hens used their beaks, and physiological studies that measure response to what are likely to be emotional situations, such as greeting displays, allopreening and separation from partners. Physiological measures include changes in heart rate, breathing rate, the release neurohormones from the bird’s brain, or changes in brain activity visualised by scanning technology. None of this is easy, and at the present time cannot be done on free-living birds. Yet I can imagine that in the not-too-distant future it will be possible to measure at least some of these responses in wild birds. I will leave you to decide whether, on the basis of the science I have described here, birds experience emotions. My impression is that they do, but as Thomas Nagel said when he asked what it’s like to be a bat, we can probably never know if birds experience emotions in the same way as we do.
In this book I have discussed the different senses of birds one at a time. I have done this for convenience and clarity, but in reality, of course, the senses are used in combination. Psychologists have shown that we utilise and process information from several different sense organs simultaneously and often subconsciously. When we meet someone for the first time, for example, our primary source of information is visual, but almost without knowing it we assess how they smell, how they sound, and, if we embrace them or shake hands, how they feel, too (how I hate a limp handshake). It makes sense that birds must also integrate information from their different sense organs, because doing so provides them with more information that in turn may affect their survival.
Sometimes it can be hard for researchers to figure out exactly which senses birds are using to assess their environment. The sight of a thrush, blackbird or American robin foraging for earthworms on a suburban lawn is a familiar one. The bird hops forward, stops, cocks its head to one side and waits – is it looking or listening? Then, with a rapid lunge, it snatches a worm from the ground. In the
1960
s the American ornithologist Frank Heppner studied the question of which sense American robins use to capture prey. He found that if he played ‘white noise’ to captive robins while they were foraging for worms, it made absolutely no difference to their foraging success. He concluded that robins hunted visually and that, when a bird cocked its head, it was
looking
rather than
listening
, using one eye to scan the ground for signs of a worm.
1
Thirty years later, Bob Montgomerie and Pat Weatherhead revisited this problem and came to rather different conclusions. They agreed that the head-cocked posture was entirely consistent with looking and that the angle of the bird’s head meant that the image of the ground was projected directly on to the bird’s fovea. But when they removed all visual cues – holes in the ground or earthworm casts – the birds were still able to find their prey. By a process of elimination, Montgomerie and Weatherhead showed that the robins found food by
hearing
the worms. If you put your ear over an earthworm’s burrow you can sometimes hear the worm’s tiny bristles rustling against the sides.
They also discovered that Heppner’s study was flawed because the birds could actually see the worms in their holes, so it was hardly a case of discovering how the birds detected ‘invisible’ prey. The take-home message from Montgomerie and Weatherhead’s study is an important one. It is this: even though our interpretation of a particular behaviour suggests that birds are using one particular sense it requires careful experimentation to be absolutely sure which one it is.
2
Outside the laboratory American robins undoubtedly make use of both vision
and
hearing while hunting. They may also use smell; they may even detect the worm’s movements in the soil through touch sensors in their legs and feet.
More spectacular than the American robin’s ability to detect worms is the facility with which arid-region waterbirds can sense rain falling hundreds of kilometres away. Thousands of greater and lesser flamingos suddenly appear within hours of rain falling at Etosha Pan, Namibia or the Makgadikgadi Pans in Botswana. In these arid regions rain is erratic, but once it falls the shallow pans fill rapidly with water. Those flamingos spend the winter at the coast, and without directly experiencing any rain themselves are somehow able to tell that rain has fallen and in response fly inland. They can not only detect distant rain, but also appear to be able to tell
how much
rain has fallen, abandoning their coastal winter quarters only if the rainfall is sufficient for breeding. Are the flamingos responding to the vibration of distant thunder? Possibly, but they often respond to distant rain even when there has been no thunder. Are they responding to the sight of towering cumulus rain clouds, visible from considerable distances on the ground and further still from the air? Are they responding to changes in barometric pressure?
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So far, no one knows what senses flamingos and other birds use to detect distant rain. Stephen Jay Gould’s essay ‘The Flamingo’s Smile’ celebrates the fact that flamingos feed with their heads upside down, filtering tiny prey items from the water. Gould assumed that the flamingo’s enigmatic smile was a consequence of its upside-down bill, but I prefer to think that they are amused by our puzzlement over their mysterious ability to sense distant rains.
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The clearest example of the way our own senses are used in combination relates to taste. If you hold your nose (and therefore temporarily remove your sense of smell) and bite into a (peeled) onion, you can do so without tasting it. Stop holding your nose and the taste of the onion instantly becomes apparent. Psychologists reckon that
80
per cent of taste occurs via our sense of smell. Taste and vision are also intimately linked, and brain scans show that simply looking at food lights up the taste regions of the brain. Do similar interactions occur in birds’ brains? The experiments are more difficult to do, of course, but it would be interesting to know.
The other well-known feature of the human sensory system is ‘compensatory enhancement’ (or, more technically, cross-modal plasticity) – the ability to develop certain senses if one is impaired or lost. There are two explanations for this. One is that without the ability to see, for example, people simply pay more attention to sounds or other sensory inputs. The other is that, deprived of one sense, the brain reorganises itself to enhance the other senses. Both seem to be true. The fact that the brain can reorganise itself in this way is compelling evidence for the sophisticated integration of sensory information. I wondered whether the ability of our blind zebra finch, Billie, to distinguish footsteps (see page
75
) might be an example of this type of compensation, or whether a fully sighted zebra finch could do the same. It would have been relatively easy to check, but by the time I thought of it Billie had passed away.
One of the most impressive examples of compensatory enhancement is the ability of blind people to echolocate. Unsighted people often learn to navigate around their home by listening to the echoes of sounds bouncing off the furniture – a phenomenon known as
passive
echolocation because it does not require the person to make any noise. As I worked on this book, I thought about passive echolocation, and noticed that I was sensitive to echoes, too. In fact, I discovered (not very usefully) that I could tell as soon as I opened one particularly noisy door where I work (and without being able to see) whether there was someone already in there. Once I had detected this ability, each time I visited this room I tried to predict on opening the door whether I was right: my success rate was about
85
per cent. Far more impressive, though, is the fact that some blind people use
active
echolocation to enable them to go mountain biking. As they ride they click their tongues about twice a second, and using the echoes they hear are able to stay on the track and avoid obstacles!
5
I described earlier how oilbirds and swiftlets actively echolocate inside dark caves, but I wonder whether other cave-dwelling or nocturnal birds might also employ passive echolocation.
Using our own sensory system provides our only starting point for understanding how birds experience the world, and as long as we recognise that they have senses that we do not possess, and as long as we don’t automatically assume that even the senses they share with us are identical, then we can begin to gain some understanding of their world.
The ability to visually recognise individuals provides a nice example. We are extraordinarily good at recognising faces: we know within a fraction of a second if we’ve seen a particular face before, and we have an extraordinary capacity to recognise someone we know. In the chapter on seeing, I described an incident that suggested to me that, on the basis of vision alone, guillemots can identify their partner in flight at a distance of several hundred metres. This seems extraordinary not because the eye of a guillemot is that different from our own, but because to the human eye most guillemots are utterly indistinguishable even at point-blank range. My example is a mere anecdote, but it is consistent with other observations that suggest that guillemots and, indeed, many other birds are very good at recognising individuals. The most obvious and well-established way that birds recognise other individuals is through their voice. We know this because hearing lends itself to elegant testing through so-called playback experiments in which birds are played recordings of calls and songs (which exclude all other cues) to see how they react. Hundreds of such experiments show unequivocally that voice and hearing are important ways for birds to recognise each other.
Working out whether birds use other senses to identify individuals is rather more difficult, but, again, anecdotal evidence suggests that they do. The peck order in chickens, for example, relies on birds being able to recognise each other by sight. My colleagues Tom Pizzari, Charlie Cornwallis and I inadvertently demonstrated this in an unexpected way. We were conducting experiments to establish how many sperm cockerels transfer to hens during mating. If we presented the same hen to the same cockerel every few minutes over an hour or so, the number of sperm showed a predictable decline with each successive mating. If, however, we swapped the female halfway through the experiment, the male’s sperm count shot up. Since the cockerels always seemed to look at the hen before mating, visual recognition seems the most likely explanation. Other birds are known to be capable of recognising other individuals by sight. The turnstone has an individually distinct pattern of black and white plumage on its head and upper body, and by making models painted to resemble particular individuals Philip Whitfield confirmed that visual cues were crucial in individual recognition. In more sophisticated tests in the laboratory, pigeons can also recognise other pigeons they see on a video screen.
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This ability of birds to visually recognise particular individuals, and sometimes from a distance, seems all the more remarkable in the light of other observations and experiments. The facts that young herring gulls can be duped into responding to a two-dimensional cardboard cutout of an adult gull’s head, or that a buffalo weaver is willing to copulate with a model female consisting of little more than a wire frame with wings, or a duckling can imprint on a human (or a boot) and behave towards it as though it was its mother, all suggest that some fundamental differences in perception exist between birds and ourselves. However, a moment’s reflection should make us cautious of jumping to such a conclusion. With only a modicum of imagination, we can probably think of human equivalents to all three of those bird examples. Our ability to be duped by our sensory system is extraordinary: we are fooled by holograms, befuddled by optical illusions such as Necker’s cube, Penrose’s triangle or Escher’s endless staircases, and, because of the way our brain is wired, we are incapable of seeing an upside-down human face objectively. Understanding why our senses are fooled by such tricks has provided extraordinary insight into the way our sensory systems function. The same kind of approach might increase our understanding of the way birds perceive the world – as far as I am aware, no one has yet used it, but I guess they soon will.
7
A psychologist recently commented that this – the early twenty-first century – is the golden age of sensory research in humans.
8
I like to think that the golden age of sensory research in birds is still to come. I have tried to summarise what we currently know and also what we don’t know about the senses of birds. Our understanding of the human sensory system is advancing in leaps and bounds, and, if history is anything to go by – and I think it is – then it is inevitable that what we discover about the senses of humans will allow us to make similar studies of birds. History also shows very clearly that what we discover about birds (and other animals), including their seasonal remodelling of the brain, or their regeneration of hair cells in the inner ear, have huge implications for humans, too. At the present time we have a good basic understanding of at least some of the senses of birds, but the best is yet to come.