Authors: Tim Birkhead
The touch idea remained unchallenged for one hundred years, by which time two further possibilities were in the air. The first surfaced after the sinking of the
Titanic
in April
1912
. Impressed by the ability of blinded bats to avoid collisions, the engineer and inventor Sir Hiram Maxim wondered whether ships might similarly be protected from collisions with icebergs and other ships in foggy weather by an apparatus that could detect the returning echoes from powerful low-frequency sounds. He assumed that bats heard and responded to the reflections of the
low
-frequency sounds made by their wingbeats. In other words, Maxim was the first to suggest that bats might use sounds inaudible to the human ear.
The second idea was the brainchild of physiologist and sound specialist Hamilton Hartridge (
1886
–
1976
), who was reminded of the underwater object detection techniques developed during the First World War. He wondered whether bats avoided obstacles by the reflections of what he assumed were their
high
-pitched calls.
Of the two ideas, Hartridge’s high-frequency sounds seemed the more plausible and in the early
1930
s Harvard undergraduate Don Griffin decided to test it. He did so using the only piece of kit capable of detecting and analysing high-frequency sounds: electronic equipment constructed by the physicist George Pierce to detect the high-frequency sounds made by insects. It is not unusual for researchers to design and build their own research equipment, and Griffin was fortunate that Pierce was happy to share his technology. The outcome was remarkable, and confirmed beautifully that bats utter sounds beyond the range of normal human hearing. Most people can hear sounds with frequencies as low as
2
or
3
kHz, and as high as
20
kHz, but the bats that Griffin studied were uttering cries as high as
120
kHz.
44
Together with a fellow student, Robert Galambos, Griffin then began more detailed investigations. Their efforts in the early
1940
s resulted in the momentous discovery that bats not only utter a continuous stream of high-frequency sounds, but they do so at an increasing rate whenever they are negotiating particularly tricky objects. This provided strong circumstantial evidence for Hartridge’s idea that bats avoided obstacles using the echoes from their high-pitched cries. Coincidentally, it was also realised around this time that visually impaired people could detect obstacles by making sounds and hearing the reflections of these sounds, inspiring Griffin to coin the term ‘echolocation’ for the process. Ten years later, Griffin was able to show that, as well as using echolocation to avoid obstacles, bats also use it to hunt their insect prey. This, too, was totally unexpected. The conventional wisdom before he started was that tiny flying insects would not ‘return enough acoustical energy to yield audible echoes, and the whole idea seemed too far-fetched for serious consideration’.
45
Yet this is exactly what he found, confirming that the bat’s echolocation system was far more sophisticated than anyone had imagined.
Excited by his discoveries, Griffin next went in pursuit of oilbirds, to check whether they also used echolocation to orientate themselves in total darkness. In
1799
– the year Spallanzani died – the German naturalist and explorer Alexander von Humboldt was in tropical America with a botanical colleague, Amie Bonpland. At Caripe in Venezeula they visited the Guácharo Cave, an enormous cavern inhabited by thousands of nocturnal birds, which the local people were very reluctant to enter. As Humboldt says: ‘The cave at Caripe is the Tartarus of the Greeks, and the Guácharos which hover above the torrent, emitting plaintive cries, recall the Stygian birds.’
46
Humboldt named the bird
Steatornis caripensis
– the oilbird of Caripe – and although he was impressed by the tremendous noise the birds made as they flew around in the cave, he did not comment on their ability to navigate in total darkness.
It wasn’t until the ornithologist William (Billy) H. Phelps Jr of Caracas got someone to expose film in Humboldt’s cave (now known as
Cueva del Guácharo
) in
1951
, that there was evidence that the darkness in there was complete, and that the birds must be able to navigate in absolute darkness. Accompanied by Phelps, Griffin went to the Caripe cave to see for himself. Unlike Humboldt, who had endured a difficult climb to reach the cave, by
1953
it was poised to become a major tourist attraction and Griffin was able to drive directly to the entrance, where he was greeted by the cave’s custodian and guides. At that date the young birds were still being harvested for their fat, although not to the same extent as in Humboldt’s day when thousands were taken.
As Griffin’s party, consisting of Phelps and his wife, Kathy, Mr and Mrs McCurdy and Mr Zuloaga and his son, entered the cave, they walked past the oilbirds nesting in what he called ‘the twilight zone’, for their main objective was to establish the degree of darkness in which the birds could fly. In the deepest part of the cave – the part Humboldt’s local guide had refused to enter – Griffin’s party turned off their flashlights and sat in the dark to allow their eyes to adjust while the oilbirds circled noisily but invisibly
75
feet above them. After twenty-five minutes everyone agreed that there was absolutely no light this deep into the cave, a fact confirmed by Griffin’s film, which was exposed for a full nine minutes. ‘Our first question was thus conclusively answered; the guácharos did fly in total darkness . . .’ Nor were they silent: ‘Our ears were bombarded almost constantly by a variety of squawks, screeches, clucks, clicks and shrieks . . . But whether these weird cries of the guácharos were used for orientation was still uncertain.’
47
Griffin and his colleagues made their way back towards the cave entrance, and, as they did so, something remarkable happened. Outside, darkness was falling and the birds were beginning to leave the cave in search of fruit to feed their chicks. As the birds streamed out towards the cave entrance, instead of the ear-piercing calls they had uttered earlier, their calls were completely different: ‘a steady stream of the sharpest imaginable clicks’. Subsequent analysis confirmed that these clicks had a frequency within the range of human hearing and much lower than most of the bats Griffin was familiar with.
48
The next question was whether the oilbirds were using these audible clicks to navigate in the dark. An experiment was necessary. With some difficulty Mr Phelps and the local guides caught some birds by stringing a net across the cave entrance, and Mr Zuloaga arranged for Griffin to use the laundry room at the Creole Petroleum Corporation, where he worked, for the experiment. The room, from which all light was excluded, measured about
12
ft square by
8
ft high (
3
.
6
x
2
.
4
m) and the birds flew around this confined space without touching the walls. In the dark Griffin could hear their wingbeats and, of course, their clicking. However, he noticed that the birds were unable to avoid the cord from the electric light that hung from the ceiling, raising the question of whether they could detect something this small in nature.
The experiment consisted of blocking the birds’ ears with cotton wool, which they sealed with glue. If the birds relied on echolocation to orientate themselves, hearing would be essential. Taking the three strongest birds, Griffin duly plugged their ears, and waited a few minutes for the glue to set. The birds were released into the darkened room. The results were spectacular. In each case the birds clicked vigorously, but immediately flew into the walls. On the removal of their earplugs, the birds’ ability to avoid the walls was restored. When the light was on the birds avoided the walls, but also uttered far fewer clicks, suggesting that when there was enough light the birds relied mainly on their eyesight.
49
Overall, even though based on just a few individuals, Griffin’s simple experiments demonstrated convincingly that oilbirds use echolocation like bats. They also showed that, unlike bats that typically use high-frequency sounds barely audible to the human ear, oilbirds used a low-frequency sound.
These extraordinary results were later confirmed in the
1970
s by Masakazu Konishi and Eric Knudsen by showing that the oilbirds’ clicks had a frequency of two kilohertz, which coincided exactly with the most sensitive region of their hearing. Taking this result together with what was known about echolocation in bats, Konishi and Knudsen suggested that the oilbird’s echolocation might be fairly crude and limited to detecting relatively large objects. Bats use very high-frequency sound, but also project that sound in a narrow beam, whose echo they then detect using their very sensitive ears, enabling them to detect very small objects and even moths in flight. Konishi and Knudsen tested their idea by placing obstacles (plastic discs) of different sizes in a narrow part of the oilbirds’ completely dark cave, knowing that to pass this point the birds would have to detect these obstacles. Observing the birds, using infra-red light, they watched the birds blunder into discs less than
20
cm in diameter as though they did not exist. With larger discs the birds had no problem avoiding them.
50
One other group of birds relies on echolocation: the cave swiftlets of South East Asia. Like the oilbird, these birds breed in total darkness deep inside caves, but unlike the oilbird their nests are constructed of the birds’ dried saliva (and harvested for bird’s nest soup). Writing in
1925
, G. L. Tichelman described a two-hour canoe journey inside a cave in Borneo: ‘during the whole time one travels through a thick rain of the birds’ twittering. Countless swifts fluttered around close to the canoe. On the dirty white rocks in places numberless swift nests were built so close together that they resembled clusters of black pickles.’
51
The American ornithologist Dillon Ripley described another swiftlet cave in Singapore:
The entrance consists of two relatively narrow semicircular openings through which the birds dash without appearing to slacken speed. As they fly by they make a rending sound, like the tearing of silk. An observer who stands by the entrance will have birds pass within a foot or so of him, and the noise of their flight is a thrilling sound . . . It seems fairly clear that the clicking is a sonic device to prevent the birds dashing themselves into the walls of the cave; they seem not in the least to slacken speed as they dash into the darkness.
52
Later, using similar experiments to those performed with oilbirds, Alvin Novick confirmed that in total darkness cave swiftlets – like oilbirds – use low-frequency sounds to navigate via echolocation.
53
As Jerry Pumphrey pointed out, compared with the high-frequency sounds used by bats: ‘The practical disadvantages of employing . . . low frequencies for echo-location are so considerable as to suggest that the bird’s ear is incapable of being readily modified in the direction of increasing sensitivity to ultra-sonic frequencies.’
54
Overall, the sense of hearing in most birds is fairly similar to our own, with the notable exception of nocturnal species and those that hunt and navigate by sound, such as owls, the oilbird and cave swiftlets. For me, however, the bird that best captures the extreme sophistication of avian hearing is the great grey owl. Its ability to pinpoint a mouse, invisible under the snow, by means of asymmetric ears, leaves me speechless.
3
A mallard duck dabbling in mud. Thumbnails show (
left
) the inside of the upper bill showing the tips of the touch receptors in the rim of the bill, and (
right
) a single touch receptor (
enlarged
) with its two types of nerve endings: Grandry (
small
) and Herbst (
large
) corpuscles – pale spheres.
In birds . . . the horny beak appears unlikely to be a suitable vehicle for a refined sense of touch . . . the presence of end-organs
[nerve endings]
. . . suggest that it is in fact the part of birds which is tactually the most sensitive.