Bird Sense (15 page)

Primates and socially living birds have much in common. In primates, any kind of stressful interaction, such as an attack by a more dominant individual, is often followed immediately by the victim seeking grooming, as though for reassurance. Humans do the same: we might touch someone lightly on the arm or shoulder in a gesture of reassurance or comfort. Among European magpies that I studied around Sheffield, allopreening was sufficiently rare that I made a note whenever I did see it. As in many other birds, it only ever occurred between pair members, but more interestingly it happened only after another magpie had made an aggressive incursion into their territory. Typically the intrusion resulted in a territorial skirmish, after which the pair would retreat to a tall tree, sit close together and the female then allopreened her partner – very rarely the other way round. The association with a stressful social encounter was therefore very obvious, and it is even more obvious in another bird, the African green woodhoopoe studied by Andrew Radford and Morne du Plessis.

With its spectacular iridescent green-purple plumage and scarlet down-curved bill, the green woodhoopoe is a highly social, co-operatively breeding bird. It lives in groups of six or eight individuals, comprising a breeding pair and several helpers, which are usually young from previous breeding seasons. Each night the entire group roosts together in a tree cavity, rendering them vulnerable to picking up ectoparasites from one another, so allopreening may serve a hygienic function. This seems particularly plausible since, as in other birds, the preening focuses on the head and neck. In addition, though, allopreening has a clear social function. Conflicts with neighbouring woodhoopoe groups are common and are invariably followed by allopreening between group members, just as with magpies. Allopreening under these circumstances, however, is focused on the body plumage rather than the head. The more intense the woodhoopoes’ battle with their neighbours, the more intense the allopreening afterwards. Losers in intergroup conflicts also allopreened more than individuals in the winning group, presumably because losing was more stressful than winning. These birds allopreen a lot, up to
3
per cent of their day, and, as in primates, preening or grooming seems to reinforce particular social relationships.
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The only study so far that has explored the link between allopreening and stress reduction in any bird species has been conducted on ravens, and seems to confirm what has been found in primates: ravens that allopreened each other more often produced less of the stress hormone corticosterone. More studies are needed before we can be confident that this is a general phenomenon in birds, but my guess is that it is.
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The way allopreening occurs in guillemots, magpies, ravens and woodhoopoes obviously involves touch receptors in the recipient’s skin. As with ourselves, a bird’s skin has lots of different receptors that are sensitive to pressure, pain, movement and so on, but birds also have specially modified feathers that probably play a central role in allopreening.

There are three types of feather. The most abundant and obvious are the contour feathers: these include the long, strong wing and tail feathers, but also the short feathers that cover the body and rictal bristles around the mouth. The second type are fluffy, down feathers, lying out of sight under the contour feathers close to the body. Their role is to act primarily as insulation, hence their effectiveness in a down-filled sleeping bag or jacket. The third type of feather is much less familiar and you are likely only to have noticed them if you have ever plucked a bird like a chicken or a pigeon. Once all the contour and down feathers have been removed, what’s left are the filoplumes, fine hair-like feathers sparsely dotted over the entire body surface and always rooted close to the base of a contour feather.

Filoplumes consist of a shaft, sometimes with a tiny tuft of barbs at the tip, and, like the down feathers, they are usually hidden beneath the contour feathers. In some songbird species, though, the filoplumes protrude beyond the contour feathers, as on the nape of the chaffinch or on the back of the eponymous hairy-backed bulbul. In others, the filoplumes have been co-opted as display structures, notably in cormorants, where they form the crest, but most spectacularly in the whiskered auklet. This small North Pacific seabird – it weighs just about
120
g – is extraordinarily beautiful during the breeding season, with sooty black plumage offset by a stunning white iris with a pinprick pupil, and a cluster of facial ornaments, a black, forward-pointing crest made up of modified contour feathers, and three tracts of silvery filoplumes. One set of filoplumes runs from in front of the eye down the neck, the second originates behind the eye and also runs down the neck, parallel to the first, and the third set lies above the eye and projects like antennae a few centimetres behind the head. The birds are nocturnal at the colony and, as in other auklet species, their facial ornaments probably play a role in mutual mate choice. But they also operate like the whiskers of a cat, helping the auklets avoid collisions when they disappear underground into the total darkness of their rocky breeding crevices.
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They may do even more than this, for the whiskers (technically, vibrissae) of rats and other mammals are so sensitive that they can distinguish between smooth and rough textures, as well as objects of different sizes.
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For a long time the function of regular filoplumes was unknown. Indeed, a major dictionary of ornithology published in
1964
referred to them as ‘degenerate, functionless structures’,
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this despite the fact that in the
1950
s a German researcher, Kuni von Pfeffer, presciently proposed that filoplumes transmit vibrations via touch sensors, allowing birds to monitor and adjust their feather postures. She was right: the filoplumes are highly sensitive and when moved trigger a nerve impulse alerting the bird so that it can readjust its plumage.
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Filoplumes must play a particularly important – albeit indirect – role in social displays. Just think of the staggering variety of feather postures birds use, including the fan-like opening of a peacock’s train, the snapping of a manakin’s wing feathers, the flamboyant fluffing of a displaying great bustard male and the sleeked plumage of an intimidated blue tit. The sensitivity of the filoplumes means that must also be important during allopreening, either by being moved by the allopreener directly, or indirectly, by the allopreener touching nearby contour feathers.

Before we leave the filoplumes, I should mention some similar, but more obvious, structures. First, in a number of birds, most obviously nightjars, oilbirds and flycatchers, on the corners of the mouth is an array of stiff, hair-like bristles. These are modified contour feathers, called rictal (mouth) bristles, and the presence of a well-developed nerve supply at their base betrays their sensory function. In nightjars and flycatchers the bristles help them catch flying insects. In the case of oilbirds, which are nocturnal, the bristles help them in flight to pluck fruit from forest trees in the dark. Second, certain frogmouths and potoos (nocturnal, nightjar-like birds of the tropics), kiwis and some seabirds, like the whiskered auklet, have crests or long wispy feathers on the tops of their heads. These are probably modified contour feathers rather than filoplumes, but like rictal bristles and filoplumes they probably also serve a sensory function. A recent study has confirmed this by demonstrating that birds with facial plumes are much more likely to live in complex habitats such as dense vegetation or tunnels or burrows rather than in the open, suggesting that the plumes function much like the whiskers of rats and cats and help them avoid bumping into obstacles.
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When Goujon discovered the bill-tip organ in parrots in the nineteenth century he said that he had also seen similar structures on the bills of wading birds such as snipe and sandpipers, species that probe in sand or mud for food. As a boy I was an avid collector of bird skulls and one of my most prized possessions was the skull of a woodcock, a probing bird, with enormous eye sockets and a distinctively pitted bill tip. These pits can be seen only after the leathery outer covering of the bill – the ramphotheca – has been removed.

Using their sensitive bill tips, probing birds like sandpipers, woodcock and snipe detect prey such as worms or molluscs either by touching them directly, by detecting their vibrations, or, more remarkably, by detecting changes in pressure in the mud or sand.
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Ingenious experiments by the Dutch ornithologist Theunis Piersma and his colleagues in the
1990
s showed how red knots were able to detect tiny immobile bivalves (like mussels and clams) hidden in sand. When the bird pushes its beak into wet sand it generates a pressure wave in the minute amounts of water lying between the sand grains. This pressure wave is disrupted by solid objects, such as bivalves, which block the flow of water, thereby creating a ‘pressure disturbance’ detectable by the bird. Rapid and repeated probing, so typical of these wading birds, is thought to allow them to build up a composite three-dimensional image of food items hidden in the sand.
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Piersma’s red knot discoveries resonated with two New Zealand researchers, Susan Cunningham and her PhD supervisor Isabel Castro, who wondered whether something similar might occur in the bill of the kiwi, the ultimate probing bird. Just as the sandpiper’s, the kiwi’s bill tip is a honeycomb of pits on both the upper and lower bill, both inside and outside the mouth. Interestingly, despite his careful dissections of kiwis in the
1830
s, Richard Owen seems to have overlooked these pits as he makes no mention of them, nor do they feature in the exquisite drawings of kiwi skeletons in his papers. It was Jeffrey Parker, professor of biology at the University of Dunedin in New Zealand, who first reported the unusual cluster of pits in the kiwi bill tip in
1891
, describing them as ‘abundantly supplied by branches of the dorsal ramus of the orbitonasal nerve’. In other words the pits are richly supplied with nerves.
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In his
Birds of New Zealand
(
1873
) Walter Buller provided a beautiful description of the way kiwis forage: ‘While hunting for its food the bird makes a continual sniffing sound through the nostrils, which are placed at the extremity of the upper mandible. Whether it is guided as much by touch as by smell I cannot safely say; but it appears to me that both senses are used in the action . . . That the sense of touch is highly developed seems quite certain, because the bird, although it may not be audibly sniffing, will always first touch an object with the point of its bill . . . and when shut up in a cage . . . may be heard, all through the night, tapping softly at the walls.’
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The orientation of the sensory pits in the kiwi’s bill tip provides a further clue to the way they are used to detect prey. The bill tips of knots contain neatly stacked Herbst corpuscles in forward-facing sensory pits, an arrangement that seems to be necessary to detect pressure disturbance patterns. Other sandpiper species,
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however, that detect prey by vibration, have outward-facing pits. Kiwis, however, have pits that face forward, outward and backward, indicating that they might use both pressure
and
vibrational cues to detect their prey. Despite the similarity in their bill structures, kiwis and wading birds are hardly close relatives, but constitute a nice example of convergent evolution in which similar adaptations evolve in response to similar selection pressures – that is, in response to the need to find food concealed beneath the surface.

There is one other ‘probing’ lifestyle where we might expect to find a well-developed sense of touch (and taste) – on the tips of the long tongues of woodpeckers, wrynecks and piculets.

Leonardo da Vinci was one of the first to comment on the extraordinary tongue of the woodpecker,
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but the best early illustrations are those of the Dutch naturalist Volcher Coiter (
1534
–
76
), who also recognised that the wryneck had a similar elongated tongue.
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Sir Thomas Browne, writing in the mid-
1600
s, commented on the ‘large nerves which tend unto [lead into] the tongue’ of woodpeckers,
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and his ornithological colleagues Francis Willughby and John Ray, after examining a green woodpecker, said: ‘The tongue when stretched out is of a very great length, ending in a sharp, bony substance . . . wherewith, as with a dart, it strikes insects.’ After what was clearly a very sophisticated dissection they wrote:

This tongue the bird can dart out . . . some three of four inches, and draw up again, by the help of two small round cartilages, fastened into the forementioned bony tip, and running along the length of the tongue. These cartilages from the root of the tongue take a circuit beyond the ears, and being reflected backwards to the crown of the head, make a large bow. Below the ligament they run down the sagittal suture . . . pass just above the orbit of the right eye, and along the right side of the bill into a hole excavated there, whence they have their rise or original [origin].

They go on to to describe the manner in which the tongue is protruded and retracted and finish by saying: ‘But we leave these things to be more curiously weighed and examined by others.’
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