Bird Sense (14 page)

Jerry Pumphrey,
1948
, ‘The sense organs of birds’,
The
Ibis
,
90
,
171
–
99

For several years while my children were growing up, we had a pet zebra finch named Billie. Born blind, Billie thrived on human company and was particularly fond of my daughter, Laurie, who had reared him from a chick. He knew her voice, but more impressively he recognised her footstep, although how he did this was a mystery, for Laurie is an identical twin and Billie never became excited at the sound of her sister’s footfall. On hearing Laurie’s approach, Billie would burst into song, and would do so again as soon as she opened his cage door and he hopped on to her finger. After his initial excitement Billie would solicit Laurie to preen his neck, tipping his head to one side and raising the feathers on the back of his neck, adopting exactly the same posture as he would when inviting a zebra finch partner to preen him.
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Ornithologists refer to one individual preening another as allopreening (‘allo’ meaning ‘other’), to distinguish it from the more usual self-preening. If you have ever tried to allopreen a bird like a zebra finch, whose entire body is smaller than your thumb, a finger seems far too large and clumsy. My daughter, who has small hands, was able to perform something akin to allopreening by using her index finger and Billie loved it, keeping his eyes closed and occasionally twisting his neck as if to provide access to new areas, much like a human having his or her neck or back scratched. When I tried preening Billie, I was aware of how huge my finger seemed and how careful I had to be to ensure that I tickled rather than pummelled him. If I lost control and was a little clumsy, he’d snap out of his reverie and either peck me or move away.

As far as I could tell, Billie thoroughly enjoyed the sensation of being allopreened and the same seems to be true when male and female zebra finch pair members allopreen each other. While it is easy to infer that the recipient enjoys the sensation of being allopreened, it is rather more difficult to decide what the bird performing the allopreening experiences.

When I allopreened Billie’s neck, I was acutely aware of the sensation of my fingertip on his skin and feathers, and I used that information to regulate the tiny amount of pressure I was applying. When zebra finches allopreen each other, does the preener have similar feedback?

At first glance a bird’s hard and horny beak seems decidedly insensitive. To see what it would be like to allopreen with an inanimate beak, I sometimes preened Billie with a dried grass stem, which was even finer than a zebra finch beak. In fact, the grass stem was not as inanimate as I imagined since I could feel the sensation of touch transmitted through it and into my fingers. What’s more, Billie quite liked being preened in this more focused way.
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The truth is that a bird’s beak is far from inanimate. Tucked away in tiny pits in different parts of the beak (and the tongue) are numerous touch receptors, and it is these that enable the zebra finch and other species to fine-tune their allopreening.
3

Touch receptors – in human fingers – were first discovered in the
1700
s
4
but not in the beaks of birds until
1860
, when they were found in those of parrots and a handful of other birds.
5
Given the nature of their beak, parrots seem an unlikely bird to have a touch-sensitive bill tip, but they do, and this nicely explains their marvellous dexterity.

The bill-tip organ was discovered by the French anatomist D. E. Goujon in
1869
. In fact, he found that all the parrots he looked at, including the budgerigar, possessed this organ which consists of a series of pits in the upper and lower beak, full of touch-sensitive cells. Goujon’s brief account is wonderfully enthusiastic: ‘It is . . . not enough to know the exact topography of an organ, it is necessary to penetrate its very substance and to divine its fundamental elements where possible’, and this is exactly what he did with touch receptors.
6

In terms of keeping your fingers intact, if you want to examine a bird’s bill-tip organ, a duck is a much safer option than a parrot. When I first saw a drawing of the nerves in a duck’s beak,
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I was reminded of an experience I had as a zoology undergraduate in the late
1960
s, when one of my favourite books was Ralph Buchsbaum’s
Animals Without Backbones
,
first published in
1938
. Buchsbaum brought the biology of invertebrates to life in an extraordinary and compelling way. One chapter begins: ‘If all the matter of the universe except nematodes [threadworms] were swept away, our world would still be dimly recognizable . . .’
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In exactly the same way, if all the matter of a duck’s beak apart from the nerves was swept away, the beak would be clearly recognisable. Simply seeing that remarkable network of nervous tissue left no doubt in my mind that the avian beak, far from being an inanimate tool, must, in some species at least, be a highly sensitive structure.
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The remarkable arrangement of nerves in the duck’s beak was discovered by the English clergyman John Clayton, Rector of Crofton, in the late
1600
s, who wrote:

Dr Moulin and myself when we made our anatomies together when I was at London, we shewed to the Royal Society that all flat-billed birds that groped for their meat [food] have three pair of nerves that came down their bills; whereby as we conceived they had that accuracy to distinguish what was proper for food and what to be rejected by their taste when they did not see it; and as this was the most evident in a duck’s bill and head, I drawed a cut [i.e. an illustration] thereof and left it in your custody.
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Effectively, what John Clayton is saying is this: imagine being given a bowl of muesli and milk to which has been added a handful of fine gravel. How good would you be at swallowing only the edible bits? Hopeless, I suggest, yet this is precisely what ducks can do.

To understand how this is possible, first catch a duck. Then turn it over and open its beak so that you can examine its palate. The most striking feature is a series of grooves radiating around the curved tip, but you need to look beyond these at the outer edge of the bill. What you should be able to see now is a series of tiny holes or pores – some thirty of them. If you look on the lower jaw, you will find even more – about
180
. Examining these pores with a magnifying glass, you will see that from each one protrudes the pointed tip of a cone-shaped structure called a ‘papilla’, inside which is a cluster of around twenty to thirty microscopic sensory nerve endings – these are the touch receptors – that connect to the brain via that network of nerves.

Nineteenth-century German anatomists were the first to see touch receptors in the duck’s bill-tip organ. There are two types. The larger and more sophisticated ones were discovered by, and named after, Emil Friedrich Gustav Herbst (
1803
–
93
), who found them first in bone in
1848
, then on the bird’s palate in
1849
, then in skin in
1850
and on the bird’s tongue in
1851
. Herbst corpuscles, which are sensitive to pressure and hence touch, are oval-shaped structures about
150
µm in length and
120
µm wide (one µm is
1
/
1000
th of a millimetre), but occasionally up to one millimetre long. The second type, Grandry corpuscles, named after M. Grandry, a Belgian biologist who first found them in
1869
, are smaller (about
50
µm long and
50
µm wide) and simpler in design, and are sensitive to movement. The two types lie together in the cone-shaped body of the papilla, with the smaller Grandry corpuscles positioned over the Herbst corpuscles – in a most beautiful structure.

Elsewhere in the duck’s beak, both inside and out, there are large numbers of Herbst and Grandry corpuscles, particularly towards the tip and edges of the bill, but not bundled up together as they are in papilla in the bill-tip organ. Indeed, in just one square millimetre of a mallard’s bill there are several hundred receptors, all designed to pick up information about things in contact with the bill and what is inside the bird’s mouth.
11

When we watch a duck dabbling in muddy water at the edge of a pond, rapidly opening and closing its beak, it is straining food items from the mud, retaining what’s edible and rejecting the mud, gravel and water. It does this very quickly and without being able to see what it is doing, relying on its sensitive bill-tip organ together with the other touch receptors scattered throughout the mouth, and, as we’ll see in the next chapter, its taste buds. We simply do not have the sensory (or mechanical) apparatus to do the same, which is why we would fail the muesli and gravel test. Ducks do, of course, use their eyes when they forage but in a different way – for example, when they take a piece of bread out of your child’s hand; but as the bread is grasped, its texture is detected by the bill-tip organ, and then, if it tastes okay, it is swallowed.

How does a zebra finch manage to allopreen its partner with such sensitivity? Like that of the parrot and duck, the tip of the zebra finch’s beak is also packed with nerve endings.
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There are also a lot of touch receptors inside the mouth and on the tongue, whose main function is to facilitate the husking of seeds on which the zebra finch lives, and which is accomplished by sophisticated manipulation of the seed between the tongue and the upper mandible.
13
But these same touch sensors are also responsible for converting mechanical sensations into nerve impulses and the feedback from them allows the preener to control how much pressure it applies.

There is an apparent contradiction here: on the one hand I’m saying that the bird’s beak is much more sensitive than is generally supposed, but on the other you may be wondering about woodpeckers using their bills as an axe. How can a beak be simultaneously sensitive and insensitive? The answer is: our hands work in exactly the same way. Formed as fists, our hands become weapons, but opened flat they are capable of the most sophisticated sensitivity – exemplified by Wilder Penfield’s hugely handed homunculus. A woodpecker hacks wood using the sharp, insensitive tip of its beak; it doesn’t use the much more sensitive inside of its mouth. My concern is for those wading birds like the woodcock and kiwi whose bill tip is relatively soft and incredibly sensitive. What happens if they inadvertently hit a rock by mistake when probing in the soil? Is this the human equivalent of banging your funny bone?

Several different types of touch receptors are sensitive to pressure, movement, vibration, texture and pain. They differ in their appearance (under the microscope) and their distribution on the bird’s body. Just as in humans, which have many more touch receptors on the fingertips than on the back of the hand, birds, which have touch receptors all over their body, have more in their beak and on their feet. Allopreening is regulated by Herbst corpuscles alone, but the manipulation of food in the bill is regulated by several different types of touch receptors and free nerve endings all working in concert.
14

Highly social bird species that breed either close together in colonies, or co-operatively like babblers and woodhoopoes, spend a lot of time allopreening. Why? A simple explanation for species like the zebra finch is that allopreening is a way of maintaining a pair bond. Just watching a pair of zebra finches nibbling each other’s napes, they look as if they are in love. Indeed, this is the very reason why the small parrots called lovebirds are so named. In the past there was a tendency to assume that almost any behaviour that occurred between partners – preening, billing and mutual feeding – served to ‘maintain the pair bond’, but I have always found this an incomplete explanation and until very recently there was little hard evidence that behaviours like these help to maintain pair bonds.

Another explanation for allopreening in birds – and allogrooming in primates – is that it serves a hygienic function, removing dirt or parasites. The evolutionary logic is straightforward: it would pay you, for example, to remove a tick from your partner, if only because it would reduce the chances of you being infested yourself. Removing a tick from your partner may also reduce the chances of it damaging your mutual offspring. In birds at least, there are two reasons for thinking allopreening has a hygienic function. First, the behaviour is usually directed towards those parts of a bird’s plumage that it cannot preen itself: the head and neck. Second, allopreening is particularly common in species that live in close proximity. The record-holder for high-density living is the common guillemot, which breeds at densities of up to seventy pairs per square metre, and in close bodily contact with its neighbours – the ideal situation for external parasites like ticks to creep from bird to bird. Guillemots also engage in a lot of allopreening, both with their partner, and also with their immediate neighbours with whom they are in direct bodily contact.

On Skomer Island I have hardly ever found a tick on the hundreds of adult guillemots I have handled, and I only occasionally find them on the breeding ledges. However, at Funk Island, which I visited in
1980
, there are around half a million pairs of guillemots and the gravel on which the birds breed was literally heaving with ticks. Sadly, I didn’t have the opportunity to see how badly the birds were infested or whether allopreening was instrumental in removing ticks. However, one anecdote in particular suggests that allopreening may be important. Not long after the
Torrey Canyon
supertanker disaster in
1967
– in which many thousands of seabirds, including guillemots, died from being caught up in the ensuing oil slick – small numbers of survivors were kept in captivity in an effort to find ways of cleaning their plumage. One of the researchers involved in that study told me that he noticed a guillemot with a tick infestation – ticks embedded in the skin on the back of the bird’s head – and how the other birds in the group fell over themselves to preen the infested individual. Clearly, the sight of a tick on the plumage was a powerful stimulus. In another study, Mike Brooke of Cambridge University showed that allopreening greatly reduced the number of ticks on wild macaroni and rockhopper penguins.
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