Bird Sense (25 page)
Authors: Tim Birkhead
Smell seemed a likely candidate, mainly because of the abundant anecdotes of whalers, fishermen and birdwatchers. In addition, studies by Tom Grubb, a PhD student at the University of Wisconsin (and later at Ohio State University) in the
1970
s, showed that Leach’s storm petrels – the same species we had discovered in Labrador – invariably returned
upwind
to their breeding islands in the Bay of Fundy. Much more significantly, Tom, working with Betsy Bang, showed how petrels whose olfactory nerve had been cut (an operation that renders birds anosmatic – smell-blind) were unable to relocate their colony, whereas unoperated-upon birds could do so, and from as far away as Europe.
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Smell was clearly important in allowing Leach’s petrels to relocate their nesting colony. But this was only half the story. Gaby Nevitt was interested in whether smell also played a role in their finding food. She started by repeating the kinds of experiments Loye Miller and others had carried out, pouring smelly slicks on to the ocean and seeing how quickly birds were attracted, compared with their attraction to some other, unsmelly, substance. In
1980
, Bernice Wenzel’s graduate student Larry Hutchinson had shown that ground-up krill poured on to the ocean attracted sooty shearwaters, indicating that something in the krill pulled in the birds. As Nevitt soon found out, conducting experiments on oceans where
12
-m waves are the norm was far from easy. She used vegetable oil laced with raw krill extract and unadulterated vegetable oil as a control. The studies confirmed that the smell attracted birds like petrels and albatrosses very effectively, but it didn’t really answer the question of whether krill give off a particular odour that helps the birds locate them.
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Then, in
1992
, in unusual circumstances, Gaby met Tim Bates, an atmospheric scientist. In her own words:
I was doing a cruise down near Elephant Island (off Antarctica) and we ran into some very bad weather . . . I got thrown into a tool chest in a storm and injured my left kidney. Of course I didn’t know that at the time but the pain was so bad that I was confined to my bunk which was down in the bowels of the ship. We were within a week of getting into Punta Arenas and I swear it was the longest week of my life. Anyway, when we got there, I was not very mobile. The new chief scientist was Tim Bates, and he was kind enough to let me stay aboard to wait for transport home. During this time his team was outfitting the ship for their atmospheric cruise on dimethyl sulfide (DMS).
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DMS is a biogenic substance released from the bodies of phytoplankton when they are eaten by zooplankton such as krill. DMS dissolves in seawater and is then released into the atmosphere, where it lingers for hours or even days.
Gaby continued:
Once I was able to see some of their transect data and smell DMS and get some pain killers the world changed. The profiles he showed me were like mountain ranges or landscapes. DMS was just one tractable compound, but it suddenly seemed that ‘tracking the ephemeral plume to the prey patch’ was the wrong model for large-scale questions. Instead, the ocean was overlain with odour landscapes tied in part to bathymetric features, shelf breaks, sea mounts, etc, and that changed my thinking entirely. When I think back on it, if I hadn’t had such a bad accident, I wouldn’t have met Tim, and I would probably still be chumming fish guts without seeing the bigger framework.
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A stream of experiments followed, including one showing that even at their breeding colony (rather than out at sea) Leach’s petrels were attracted to DMS. A study of Antarctic prions – another petrel species – showed that they were attracted to artificially created DMS-laden slicks at sea. Particularly revealing was an experiment that was actually a rerun of one performed by Wenzel in her early research, which involved measuring changes in heart rate in response to specific odours. Working on Ile Verte in the Kerguelen Archipelago, in the southern Indian Ocean, Antarctic prions were gently removed from their breeding burrows and taken to a nearby temporary laboratory. Electrodes were carefully (and temporarily) attached to the skin, allowing Nevitt and her colleague Francesco Bonadonna to measure the birds’ heart rate on an electrocardiograph, as air, with or without DMS, was passed over the birds’ nostrils. The crucial part of this study was that the concentrations of DMS experienced by the birds during these brief experiments were similar to those they would experience out at sea. In response to pure air, none of the birds showed any change in heart rate, but in response to DMS all ten birds exhibited a pronounced increase, thus providing some of the best evidence so far that naturally occurring odours may help birds like prions navigate across the ocean.
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Nevitt began to wonder whether substances like DMS might provide oceanic seabirds with an olfactory landscape, or rather, an olfactory seascape, superimposed on the surface of the ocean. Areas where phytoplankton accumulate, such as fronts and upwellings, attract predatory zooplankton like krill. As the krill consume the phytoplankton, DMS is liberated into the air, creating a plume of odour downwind from the source. Wind and wave action will render the plume patchy and irregular and, of course, weaker and weaker the further it is from the source. How might we expect a bird to behave if it was using such airborne information to find prey, the source of the odour plume? The answer is to fly crosswind to maximise the chances of locating a plume and, once it has been detected, to fly upwind in a zigzag manner – casting from side to side – to retain contact with the odour trail until it finds the prey.
The match between Nevitt’s prediction and some early observations of foraging petrels is striking. In his account of how New England fishermen caught petrels to use as bait, Captain J. W. Collins wrote this in
1882
:
On many occasions during the prevalence of dense fog, when not a bird of any kind has been seen for hours, I have thrown out as an experiment, pieces of liver to ascertain if any birds could be attracted to the side of the vessel. As the particles of liver floated away, going slowly astern of the schooner, only a short time would pass before either a Mother-Carey Chicken [storm petrel] or a Hag [hagdon, hag-down or greater shearwater] . . . could be seen coming up from the leeward [upwind] out of the fog, flying backward and forward across the vessel’s wake, seemingly working up the scent until the floating pieces of liver were reached.
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To test her ideas, Gaby Nevitt and colleagues employed some stunning new technology on the world’s largest seabird, the wandering albatross. This species forages over thousands of square kilometres in search of its squid or carrion prey and, like other tubenoses, has an exceptionally large olfactory bulb. It is also known to be attracted to fishy odours, making it a prime candidate for a study of odour detection. Nineteen wandering albatrosses, rearing their chicks on Possession Island in the Southern Indian Ocean, were fitted with GPS (global positioning system) locators that allowed the researchers to follow with extraordinary precision the birds’ oceanic flight paths prior to the capture of prey. The birds were also fitted with a stomach temperature recorder that detects when a bird has eaten something.
If the albatrosses were foraging by sight, it was predicted that they would fly pretty much in a straight line towards their prey, but if they were using odour they should adopt a zigzag flight path. In fact, about half of all feeding events involved zigzag flights, suggesting that these albatrosses use odour plumes about half the time when finding prey. This remarkable study provides further convincing evidence that olfaction plays a fundamental role in the albatross’s foraging, but, just as in other species, olfaction is used in conjunction with other senses, in this case, vision.
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The idea of an olfactory seascape is relatively new; the idea of an olfactory landscape is not. In the
1970
s, prior to the start of Gaby Nevitt’s career, Italian researchers led by Floriano Papi suggested that pigeons used olfaction as part of their repertoire of navigational abilities. In contrast to Gaby Nevitt’s olfactory seascape, the idea that pigeons use olfactory cues to facilitate their homing abilities has had a rocky ride. Part of the difficulty has been in disentangling the role of olfaction from the ability to sense the earth’s magnetic field. Making the pigeon problem even more intractable is the nerve (the ophthalmic branch of the trigeminal nerve (VI)) that connects to putative magnetoreceptors in the upper part of the beak.
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Because it is extremely difficult to cut the olfactory nerve without also cutting this nerve, most previous experiments cut both, thereby ‘knocking out’ both senses. Recent work by Anna Gagliardo, at the University of Pisa, in Italy, however, has dealt with this problem, and concludes that olfactory cues are indeed necessary for the development of the navigational map in pigeons.
Let’s finish this chapter by returning to João dos Santos’s honeyguides. Kenneth Stager – who corrected Audubon’s erroneous conclusions about olfaction in turkey vultures – conducted his own simple honeyguide experiment in the
1960
s. During fieldwork in an area of Kenya where honeyguides were common, Stager placed a pure beeswax candle in the crotch of a tree. Unlit – he doesn’t say for how long – the candle attracted no honeyguides, but within fifteen minutes of lighting it a single lesser honeyguide had appeared, and after thirty-five minutes there were no fewer than six honeyguides near the candle or nibbling the soft melted wax. Stager took his study one step further and collected ‘cranial material of three [honeyguide] species’. His subsequent dissections confirmed that all three species have exceptionally large olfactory conchae, which, as he said, strengthened ‘the belief that olfaction may well play an important role in the behaviour of honeyguides’.
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6
Bar-tailed godwits on migration. Guided by a magnetic sense, these birds fly from Alaska to New Zealand in a single, non-stop, eight-day, 11,000 km flight.
A faculty sometimes hypothetically invoked, but not known to exist
.
Arthur Landsborough Thomson entry for ‘Magnetic sense’,
1964
,
in
A New Dictionary of Birds
,
Thomas Nelson & Sons
I am on Skomer Island climbing carefully down a steep, rocky slope towards an unsuspecting group of guillemots. Most of the birds are brooding a single chick, each of which, I like to think, is imagining where its next meal might be coming from. Far below, the waves are crashing on to the black basalt rocks, and away to the east under a clear blue sky I can see the hazy outline of the wild Pembrokeshire coast. I stop just above a group of guillemots and edge forward with my modified fishing pole. After making myself secure, I carefully hook one of the adult birds round its leg. As I draw the bird towards me, it is a few moments before the bird is aware that something is amiss. But too late! Before it realises what is happening, I have the guillemot firmly in my grasp. This apparent stupidity, tameness or lack of awareness was what in the past gave this species the name ‘foolish guillemot’. Luckily for me the birds
are
a touch naive and, one after another, over the next hour I capture a total of eighteen birds. As each one is caught we place a metal ring (band) on one of its legs, and on the other leg we place a specially modified plastic ring which carries a tiny device, a geolocator, that will record the amount of daylight every ten minutes, until the battery runs out in two or three years’ time. The amount of light at different latitude and longitude varies, allowing us to establish where the bird has been. As soon as each device is attached we release the birds into the air: they hurtle out to sea, describe a large arc and, a few minutes later, with a flurry of wings, are back on the ledge and reunited with their chick.
I have been studying guillemots on this island since the
1970
s and, as I write, it is now
2009
. I’m working alongside Tim Guilford and his students from Oxford, and my long-time colleague from Sheffield, Ben Hatchwell, who also studied Skomer’s guillemots for his PhD research.
Twelve months on and I’m roped up again for the descent to the same small group of guillemots. This time it is different: once caught, twice shy. The guillemots know what to expect and, despite being emotionally tied to their chick, are determined not to fall prey to my hook again. It is me who is beginning to look foolish, for my colleagues and I are desperate to recover the geolocators so that we can see where our birds have been over the past year. Little is known about where Skomer’s guillemots spend their winter other than what has been gleaned from the recovery of ringed birds found dead – a crude and possibly biased picture.