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Authors: Tim Birkhead

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Guillemots also look out for each other’s offspring in another way. If a parent guillemot leaves its chick unattended, a neighbour will usually brood the chick – keeping it warm and keeping it safe from predatory gulls.
10
This form of communal care is rare among seabirds. In most other species unattended chicks would simply be eaten.

For guillemots breeding on the Isle of May, on the east coast of Scotland in
2007
, something extraordinary happened. The sand eels they rely on to feed themselves and their chicks were in very short supply, and there was nothing else. In hundreds of field seasons of guillemot-watching by dozens of researchers at many different colonies, nothing quite like this had been seen before. As the parent birds on the Isle of May struggled to find food for their starving chicks, their normally harmonious behaviour disintegrated into chaos. Many adult guillemots were forced to leave their chicks unattended as they searched further afield for food, but their neighbours, instead of sheltering and protecting the unattended chicks, attacked them. Kate Ashbrook, who was studying the guillemots there, told me this:

I remember watching in horror as one chick, stumbling into a puddle to escape attacking adults, was repeatedly forced face-down into the muddy water by pecks from a different adult. After a couple of minutes the attacker gave up and the chick struggled to stand up, but it was too weak and died shortly afterwards. It became just one of the many muddy little bodies that littered the breeding ledges. Other chicks were picked up by neighbours and swung around in the air, before being tossed off the cliff. These attacks were shocking and extremely tragic.
11

This unprecedented anti-social behaviour seems to have been a direct result of chronic stress caused by the severe lack of food. In the following years, the food situation improved, and these same individual adult guillemots resumed their normal amicable behaviour.
12

A similar response to a shortage of food has been seen in another bird, the white-winged chough. John Gould, one of the first ornithologists in Australia, commented in the
1840
s on this species’ intense sociality: ‘It is usually met with in small troops of from six to ten in number feeding upon the ground . . . the entire troop keeping together . . . and searching for food with the most scrutinising care.’ Gould came close to recognising that the chough was what we now refer to as a co-operative breeder, a species in which a breeding pair is assisted by non-breeding individuals, called helpers.
13

Groups of white-winged choughs, comprising between four and twenty individuals, often remain together for years. They consist of a breeding pair, and the offspring from several previous breeding seasons, and sometimes unrelated individuals as well. All group members help to construct the bizarre mud nest – unlike any made by a European bird, it is a robust cup glued on to a narrow horizontal branch some ten metres above the ground – and all individuals take turns to incubate and to feed the chicks. Co-operative breeding is rare in Europe and North America, but is common among Australian birds, and the white-winged chough is an extreme example in that it is
always
co-operative. The species simply cannot reproduce as a conventional pair. The explanation lies in the chough’s habitat. Digging for worms or beetle larvae in the dry ground is hard work. Young choughs rely on their parents for food for eight months – eight times longer than almost any other bird. Even after the adults have ceased to feed them, young choughs take several years to perfect their foraging skills. Essentially they serve a foraging apprenticeship in their parents’ territory, and in return they perform household duties – defending the territory, watching for predators and helping at the nest. Food is so difficult to acquire that a minimum of two helpers is needed for a breeding pair to have any chance of rearing offspring. When researchers provided choughs with additional food, breeding success soared – confirming that the difficulty of finding sufficient food really does limit the birds’ activities.

Chough groups function because a suite of behaviours keeps individuals bonded together. The birds do everything together: playing, roosting, dust-bathing and, during periods of rest, the birds line up along a horizontal branch and allopreen each other. What has this got to do with emotions? Being part of a tightly-knit group hinges on social interactions, both with other group members but also with the individuals of other groups. As Rob Heinsohn, who studied these birds for twenty years, said: ‘The chough’s chronic need for help leads to fascinating politics, especially when the weather turns bad.’
14

As drought kicks in, the choughs experience several things simultaneously. The shortage of food increases their stress levels; the birds are forced to spend more time searching for food, and less time keeping an eye open for predators. If food is really short the birds use up all their body fat and start to use the protein reserves in their breast muscles. This in turn impairs their ability to fly, so that if a predator such as a wedge-tailed eagle does attack they have less chance of escaping. Stress is increased further as birds squabble over food. Whereas group members might once have shared food, as hunger bites individuals become extremely selfish and try to keep food for themselves. Larger or more dominant birds simply push the smaller individuals aside and steal their food; resistance is useless, for the stress of losing a fight may be more damaging still.

The difficulty of finding enough food under drought conditions eventually causes groups to disintegrate. The social bonds that once held individuals together dissolve – presumably in a sea of stress hormones – and individuals break off into smaller units, scouring the dry countryside for food. While such a tactic may increase the chances of finding something to eat, it also renders individuals more vulnerable both to harassment from other choughs and to attacks by predators.

Like many other birds, choughs probably have an innate response to the sight of an aerial predator like an eagle or falcon, by giving an alarm call and taking evasive action. Ethologists in the
1930
s and
1940
s studying this behaviour in young chickens and geese worked out exactly what it was about a shape moving overhead that triggered the response: it was a long tail, short neck and long wings.
15
Later, in
2002
, researchers showed that the sight of a predator flying overhead (actually a model) resulted in an increase in the stress hormone corticosterone in the bloodstream, suggesting that birds experience the sensation of fear.
16

The value of using a hormonal measure of stress rather than relying simply on behaviour to infer what kind of emotion the birds were experiencing was shown in a clever experiment in which captive, wild-caught great tits were allowed to see, on separate occasions, a Tengmalm’s owl (a serious predator of great tits and other small birds) and a brambling (a finch, and no threat to the great tit). The great tits’ behavioural responses to the owl and the brambling were identical, but only the owl elicited a surge of the stress hormone corticosterone, clear evidence that the great tits were more frightened by the owl.
17

The rise in corticosterone in response to stress occurs rapidly, but decreases slowly. Researchers investigating the stress response in birds have employed a simple and harmless assay, which comprises holding the bird in the hand. On being held, the bird’s heart rate, breathing and corticosterone levels all increase, and it is assumed that the bird responds much as it would do if it were captured by a predator. In other words, all three physiological changes indicate that the bird is frightened. While the increase in heart rate and breathing occur within seconds, it takes about three minutes for corticosterone to appear in the blood. Similarly, after the bird is released, heart rate and breathing return to normal within a few minutes, but depending on how stressful the experience, it may take several hours for the corticosterone to return to its normal levels.

An increase in corticosterone is a general response to any kind of stress. In snakes – and I’m using a reptilian example here because there is no equivalent information for birds – males that lose a fight with another male (over a female) experience a surge in corticosterone, and as a result are much less interested in sex for several hours than are the winners.
18

That birds experience a similar physiological change in response to losing an aggressive interaction is suggested by a study of captive great tits in which exposing birds to an especially aggressive male in a cage for a few moments resulted in an increase in body temperature and a reduction in activity that lasted twenty-four hours. Similar results have been obtained in laboratory rats. Such tests are, by necessity, artificial since, however dramatic the results seem to be, the study birds are unable to ‘escape’ as they would in the wild. So, while such studies tell us that birds and other animals experience ‘fear’, the chances are that in the wild such effects are much smaller and the animals recover much more rapidly than they do in captivity.
19

Studying wild zebra finches in Australia I spent many hours sitting quietly in a hide watching the birds through binoculars or a telescope. Inevitably, I saw lots of other wildlife during those hours, including one spectacular predation event. Galahs – pink and grey parrots – were common in the study area and often flew in front of where I sat, squawking as they went. On one occasion a brown falcon dropped out of the sky and chased the galahs. The flock took evasive action, but the falcon quickly singled out one of the birds, grabbing it in mid-air in a puff of pink feathers. The seized parrot shrieked abominably and even after the two birds disappeared into the trees I could still hear the parrot’s plaintive cries, leaving me no doubt that the parrot was both terrified and in pain. My views, however, were later modified by another predation event I witnessed.

A puffin stepped out of its burrow at exactly the moment that a female peregrine was gliding along the cliff top. The falcon simply landed on top of the puffin, grasping it in its yellow talons. I know from capturing puffins myself that they are feisty and possess a powerful beak and sharp claws, so for a moment I thought the puffin might be able to escape. It didn’t. Instead, it lay still, looking up at its captor, which, avoiding its gaze, stared resolutely out to sea. I imagine that the peregrine was waiting for its powerful clenching claws to do their business and for the puffin to die. It didn’t. Puffins are tough birds, built to withstand intense pressure while diving for their own prey, and capable of withstanding high seas and gale-force winds. It was a stalemate. Five minutes passed with no obvious resolution in sight. The peregrine continued to gaze out to sea. The puffin wriggled slightly, its eyes were bright and it still looked full of life. Watching through my telescope, it was like a traffic accident, simultaneously appalling and compelling. Eventually, after fifteen minutes, the falcon started to pluck the breast feathers from the puffin, and five minutes after that began to eat the muscle from the puffin’s breast. Only after the peregrine had eaten its fill, a full thirty minutes after capture, did the puffin eventually expire. Did it feel any pain? I don’t know, for at no point during this grisly spectacle did the puffin show any sign of distress.

Jeremy Bentham (
1748

1832
), an early advocate of animal welfare, is perhaps best known for pointing out that the question is not whether animals can reason, but whether they can suffer.
20
It was, and remains, an important point, and Bentham was motivated by the fact that slaves were often treated appallingly and often no better than animals. A century earlier it suited the philosopher René Descartes to assume that animals were incapable of suffering, since denying the existence of pain helped to distinguish animals from ourselves, something the Catholic Church was keen to do. It also meant that animals could be abused without guilt. For others, like the naturalist John Ray, Descartes’ contemporary, it was unimaginable that animals were without feelings. Why else did dogs cry during vivisection, he asked? The evidence seems irrefutable, yet objectively demonstrating the existence of pain in animals such as birds is tricky.
21

Some researchers think that birds are capable of feeling only a certain type of pain. Imagine you have inadvertently placed your hand on the hotplate of a cooker. Your first reaction is a sharp sensation of pain followed by the immediate withdrawal of your hand. This is an
un
conscious reflex. It works via the pain receptors, the so-called nociceptors (‘noci’ refers to injury) in the skin, sending a signal to the spinal cord that triggers the reflex that results in your removing your hand. This is the first ‘level’ of the pain response. The second is the transmission of a message between your hand via your nerves to your brain where information is processed to create the sensation or feeling of pain. This is conscious pain – what you feel
after
removing your hand from the hotplate. It has been suggested that to feel this kind of pain requires consciousness. If, as some researchers propose, birds do not have consciousness, they cannot experience this particular ‘feeling’ of pain.
22

This view presupposes that the unconscious pain reflex alone is sufficient for survival. Indeed, many other animals – both vertebrates and invertebrates – show the same kind of withdrawal reflex to unpleasant stimuli.
23
In terms of self-preservation the value of such a reflex is obvious. One has only to think of those unfortunate people who, because of a genetic mutation, are incapable of feeling pain and who routinely bite their tongue and cheeks while eating, or the Pakistani boy who makes a ‘living’ out of his inability to feel pain, by sticking knives into his arm for money.
24

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