The frequency sensitivity of hearing in the grey swiftlet, Collocalia spodiopygia, was determined by neuronal recordings from the auditory midbrain (MLD). The most sensitive best frequency response thresholds occurred between 0.8 and 4.7 kHz, with the upper frequency limit near 6 kHz. Spectral analysis of echolocation click pairs revealed energy peaks between 3.0 and 8.0kHz for the foreclick, compared to 4.0-6.0 kHz for the principal click. The relationship between good hearing sensitivity and click energy peaks in the swiftlet extends about an octave higher than it does in the oilbird (Steatornis caripensis)

Coles, Roger B.

Konishi, Masukazu

Pettigrew, John D.

English

Caltech Authors - Main

J. exp. Biol. 129, 365-371 (1987) 365
Printed in Great Britain © The Company of Biologists Limited 1987
HEARING AND ECHOLOCATION IN THE AUSTRALIAN
GREY SWIFTLET, COLLOCALIA SPODIOPYGIA
BY ROGER B. COLES
Zoologisches Institut, Universitdt Munchen, Luisenstrasse 14, 8 Miinchen 2,
West Germany
MASAKAZU KONISHI
Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA
AND JOHN D. PETTIGREW
Department of Physiology & Pharmacology, University of Queensland, St Lucia,
Queensland 4067, Australia
Accepted 3 February 1987
SUMMARY
The frequency sensitivity of hearing in the grey svviftlet, Collocalia spodiopygia,
was determined by neuronal recordings from the auditory midbrain (MLD). The
most sensitive best frequency response thresholds occurred between 0-8 and
4*7 kHz, with the upper frequency limit near 6 kHz. Spectral analysis of echolocation
click pairs revealed energy peaks between 3'0 and 8'0kHz for the foreclick,
compared to 4'0—6-0 kHz for the principal click. The relationship between good
hearing sensitivity and click energy peaks in the swiftlet extends about an octave
higher than it does in the oilbird (Steatornis caripensis).
INTRODUCTION
Echolocation is known to occur in only two families of birds. The Steatornithidae
is represented by one species, the oilbird {Steatornis caripensis), which is known to
echolocate and is a nocturnal frugivore from South America (Griffin, 1953; Konishi
& Knudsen, 1979; Suthers & Hector, 1985). In the Apodidae a number of swiftlet
species (Collocalia spp.) are also known to echolocate and are diurnal insectivores
(Novick, 1959; Medway, 1959). Swiftlets are common to south-east Asia (Medway,
1962) including the north-east regions of Australia (Smyth, Pecotich & Roberts,
1980). Although the oilbird and echolocating swiftlets have contrasting life-styles,
they both use echolocation solely for navigation in the dark caves where they roost
and nest. Detailed study of the echolocation system of these birds has been limited
since they inhabit fairly remote neo- and palaeotropical regions. Usually such studies
have been restricted to the recording of echolocation clicks (Griffin, 1953; Medway,
1959; Novick, 1959; Medway & Pye, 1977; Fenton, 1975; Hollander, 1971; Konishi
& Knudsen, 1979; Smyth, 1979) and determining target resolution by obstacle
Key words: swiftlet, hearing, echolocation click, midbrain.
366 R. B. COLES, M. KONISHI AND J. D. PETTIGREW
avoidance during echolocation (Griffin & Suthers, 1970; Fenton, 1975; Konishi &
Knudsen, 1979; Griffin & Thompson, 1982; Thompson & Suthers, 1983). Detailed
analyses of the click production mechanism have been reported recently for the
swiftlet and oilbird (Suthers & Hector, 1982, 1985).
To understand the adaptations for echolocation in birds, it is necessary to examine
the auditory system as well as the vocal system. To date the only published data
concerning auditory sensitivity in echolocating birds has been reported in the oilbird
and was based on the frequency sensitivity of forebrain-evoked potentials (field L)
and cochlear potentials (Konishi & Knudsen, 1979). This paper reports the first
recordings from auditory neurones in an echolocating bird, the grey swiftlet
(Collocalia spodiopygia), made in order to determine the frequency sensitivity of the
auditory system. These results are compared with an analysis of the energy spectra of
echolocating clicks to establish the emitter-receiver relationship.
MATERIALS AND METHODS
Grey swiftlets (average mass 10 g) were mist-netted at the cave entrance of a large
colony in a limestone karst near Chillagoe in North Queensland, Australia. For
physiological recordings, the birds were brought immediately to a temporary
laboratory (a motel room) in the nearby town. Swiftlets were anaesthetized with a
combination of ketamine (20mgkg~') and rompun (1 mgkg"1) and the responses of
single neurones from the midbrain auditory nucleus (MLD) were recorded by
tungsten-in-glass microelectrodes using conventional extracellular techniques. Each
bird was placed in an elevated position facing a 10 cm diameter speaker (Pioneer TS-
162DX) at a distance of 34 cm. Sound pressures at the position of the bird's head
were recorded with a 1 -3 cm Bruel & Kjaer microphone (type 4133) by measuring the
output voltage of the microphone on an oscilloscope screen or by using a portable
digital voltmeter. The free field sound pressure level (SPL) re. 20/iPa was calculated
in decibels (dB) with reference to the calibrated sensitivity of the microphone.
Acoustical stimuli were repetitive tone bursts in the frequency range 0-2-8 kHz with
2 ms rise/fall time and 20 ms plateau duration. The birds were heated from below
with a hot water heater and the air temperature close to the bird's head was
maintained between 29° and 33 °C.
Sound recordings of echolocation clicks were obtained from a tethered bird
attempting to fly in a small, dark, sound-absorbing chamber (approximately 1-5 m in
diameter) made from fibreglass insulation batts. The recording chamber was situated
in the town hall, to provide a quiet environment. A microphone (Sennheiser Model
MKE401) was inserted into the chamber from the side so that a constant recording
distance of 34 cm from the bird was achieved. Under these conditions, click
sequences with uniform amplitude were emitted by the bird and recorded on a
portable tape recorder (Uher CR240). The recorded clicks were relatively free from
interference by background noise and echoes (Figs 1, 3), in contrast to field
recordings in caves, for example.
Hearing in the grey swiftlet 367
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Fig. 1. (A) Distribution of best frequency thresholds for 56 auditory neurones (circles)
from the midbrain (MLD) of a grey swiftlet (Collocalia spodiopygia). Open triangles are
data from unit clusters. (B) Distribution of energy peaks for five consecutive echolocation
clicks of C. spodiopygia. Foreclicks and principal clicks (for definition see text) analysed
individually by the fast Fourier transform (FFT) method (see Fig. 3). Horizontal arrows
indicate spectral peaks derived from the click pair shown in Fig. 3. (C) Narrowband
(45 Hz) and (D) wideband (300 Hz) sonagraphic analysis of echolocation clicks of C.
spodiopygia. Note the paired click structure (as shown in Fig. 3, inset).
RESULTS AND DISCUSSION
Recordings were made from 121 auditory neurones from 19 separate electrode
penetrations through the MLD in five birds. The MLD is a major afferent relay
nucleus and to determine the frequency sensitivity of the auditory system the best
frequency (BF), defined by the most sensitive excitation threshold, was obtained for
each neurone. Response thresholds were judged subjectively, relative to spontaneous
discharge levels, by listening to the amplified neural activity through headphones.
An example of the BF threshold distribution for 56 units recorded in one bird is
shown in Fig. 1A and indicates that most units with thresholds between 18 and
45 dB SPL have BFs ranging from about 0-8kHz up to 4-7kHz. A few units were
recorded with low BFs near 250 Hz, and occasionally it was possible to find units and
unit clusters tuned to high frequencies around 6-7 kHz (Fig. 2) but thresholds were
high i.e. at or above 70dBSPL. The room acoustics, especially background noise
and the difficulty of free field calibration, probably account for the minimum
thresholds being about 18dBSPL, but these were the most sensitive estimates
possible under 'field' conditions. Pooled BF data for all the birds studied are shown in
Fig. 2 as a histogram of BFs at one-quarter octave intervals. Unit BFs most
frequently occurred between 2 and 5 kHz, with some clustering of units around the
4-4-8 kHz band.
368 R. B. COLES, M. KONISHI AND J. D. PETTIGREW
25 i—
20
15
I 10
ffl
0-125 0-25 0-5 1 2
Frequency (kHz)
16
Fig. 2. Distribution of best frequencies for a sample of 121 neurones recorded from the
midbrain of Collocalia spodiopygia. Class interval is one-quarter octave.
The most sensitive auditory units in the grey swiftlet's midbrain prefer frequencies
between about 2 and 4-5 kHz and despite the small number of swiftlets studied, it is
unlikely that a population of high-frequency neurones was missed. Electrode tracks
were made throughout the rostrocaudal and mediolateral MLD, and electrode
penetrations traversed the full vertical extent of the nucleus. Typically these
penetrations showed a strict tonotopic sequence progressing from low to high BF as
the electrode was advanced dorsoventrally, similar to observations in other avian
species (Knudsen & Konishi, 1978; Coles, 1980). An interesting result from the
present study is the limited extent of high-frequency sensitivity, as very few units
have BFs above about 4-8kHz. Apparently the grey swiftlet does not develop its
high-frequency sensitivity to the same extent as similarly sized songbirds (Konishi,
1970) or acoustically specialized birds such as owls (Knudsen & Konishi, 1978).
Frequency sensitivity in the grey swiftlet resembles more closely that in the pigeon
and domestic fowl, for example (Sachs, Young & Lewis, 1974; Coles & Aitkin, 1979).
Unpublished data on the frequency sensitivity of cochlear microphonic potentials in
the echolocating swiftlet Collocalia fuciphaga are difficult to compare to present data
due to extreme variability in the results and the lack of absolute thresholds
(Hollander, 1971). However, there is some indication that the maximum sensitivity
to sound in both C. fuciphaga and C. esculenta lies between 1 and 4 kHz with a
marked reduction in sensitivity for higher frequencies (Hollander, 1971), and these
data are supported by the present observations in C. spodiopygia. Thus it is possible
to conclude tentatively that echolocating swiftlets extend their frequency sensitivity
up to 4-O-5-OkHz, which is significantly higher than the oilbird, in which auditory
sensitivity diminishes rapidly above 2-0—2-5 kHz (Konishi & Knudsen, 1979).
Echolocating pulses used by swiftlets are click-like signals (Medway, 1959;
Novick, 1959; Griffin & Suthers, 1970; Hollander, 1971; Fenton, 1975; Medway &
Pye, 1977; Smyth, 1979), which have been recorded from individual grey swiftlets
Hearing in the grey swiftlet 369
under controlled conditions (see Materials and Methods). Sonagraphic analysis of
echolocation clicks (Fig. 1C,D) reveals a paired structure with a constant interval of
about 18 ms between the first (foreclick) and second (principal) click (as defined by
Hollander, 1971). During echolocation, the interval between click pairs varies
depending on the proximity of an object and maximum rates of about 25 s~' occur
when swiftlets approach the nest. The narrow band analysis in Fig. 1C indicates a
discontinuous energy spectrum with variable peaks between 3-5 and 55 kHz, both
within and between click pairs. A digitized click pair shown in Fig. 3 (inset) indicates
that the peak amplitude of the principal click has a duration of about 1-5 ms, with a
total waveform duration of up to 5 ms. The energy spectra of digitized click trains
were computed by an FFT algorithm (PDP 11/03) for each component in a click pair
and for several successive pairs. Individual spectra for a typical click pair are shown
in Fig. 3A,B, confirming that both the foreclick and the principal click have two or
three major energy peaks with relatively little energy above 6 kHz, as suggested in
Fig. 1C. In Fig. 3A the energy peaks for the foreclick occur at 3-3 kHz and 5-5 kHz,
compared to 4-1 kHz and 5-5 kHz for the principal click (Fig. 3B). Consistent low-
frequency peaks in the energy spectra were seen between 0*2 and 0-5 kHz but these
are unlikely to be part of the echolocation process, and may be due to background
l-O-i A Foreclick
10 ms
I i-o
 n B Principal click
y v -
0 1 2 3 4 5 6 7 8 9
Frequency (kHz)
Fig. 3. (A,B) Energy spectra for the foreclick and principal click of an echolocation pulse
of Collocalia spodiopygia based on fast Fourier transform (FFT) analysis. Inset: digitized
waveforms of an echolocation click pair. Foreclick precedes the principal click which is
larger in amplitude.
10
370 R. B. COLES, M. KONISHI AND J. D. PETTIGREW
noise in the recordings generated by wing flapping (see Fig. 3, inset). The energy
peaks of five consecutive click pairs are summarized in Fig. IB and, despite some
variability in the energy for both click components, the principal click energy peaks
are more consistent than for the foreclicks. The principal click energy peaks occur in
a band between 4-0 and 6-0kHz compared to a 3-0-8-0kHz energy band for the
foreclick. Based on the limited number of pairs examined here, most of the click train
energy in C. spodiopygia is restricted to a band between 4-0 and 5-5 kHz. The extent
to which swiftlets use echo information generated by either the first or second
component of each click pair is unknown, but the second component (principal click)
maybe more important since it always has the greater amplitude (see Fig. 3, inset).
Nevertheless, it has been suggested that there may be some advantage in the use of
pulse pairs for echolocation (Buchler & Mitz, 1980).
In comparison with the frequency sensitivity of the auditory midbrain (Fig. 1A),
the grey swiftlet uses echolocation clicks with energy bands that fall mainly just
within the upper frequency regions of good sensitivity to sound (Fig. IB). This high-
frequency bias in the swiftlet appears to be more marked than the relationship
between emitter and receiver recently shown for the oilbird, which coincide around
1-5-2-5kHz (Konishi & Knudsen, 1979). Presumably swiftlets make use of the
highest energy peaks in the clicks to get the best target resolution, but since clicks are
broadband, lower frequencies could also be used. Preferential use of the energy band
between 4-0 and 5-5 kHz cannot be stated categorically, and a much more exhaustive
analysis of click trains, the auditory system and behavioural performance is required.
The unit data in this study suggest that the most frequent BFs occur in the regions of
click energy peaks and the apparent clustering of units near 4-0—4-5 kHz is
particularly interesting. However, any such tendency must be confirmed by further
detailed mapping of the MLD. An over-representation of the major frequency band
for sonar (click) energy could conceivably occur in the auditory system of
echolocating swiftlets as in echolocating bats. The volume of the midbrain torus is
about 100% larger in Collocalia fugiphaga, an echolocator, than in C. esculenta, a
non-echolocator, but it is unclear whether it is the auditory nucleus (MLD) per se
which is hypertrophied (Hollander, 1971).
In summary, the click energy in swiftlets is significantly higher than in the oilbird.
This difference is also reflected in the receiver—emitter match, since the auditory
sensitivity in the oilbird is best around 2kHz (Konishi & Knudsen, 1979) compared
to C. spodiopygia where the frequency sensitivity extends about an octave higher to
4-5 kHz. Given the much larger size of the oilbird (400g; Snow, 1961) compared to
swiftlets (lOg) this may be useful, since swiftlets are able to fly through smaller gaps.
The nest is an acoustic target of major interest to the swiftlet during echolocation.
It is a small bracket-shaped structure glued to the cave wall and has an average
diameter of about 7 cm. These dimensions correspond closely to the sound
wavelengths used during echolocation but it is not known whether the swiftlet nest
has any special properties for echo reflection. In comparison, the oilbird nest is much
larger with a diameter up to 38 cm (Snow, 1961) and may be designed for an
echolocation system with longer wavelengths.
Hearing in the grey swiftlet 371
This work was completed as part of the 1980 Biosonar Expedition to Chillagoe,
Australia. We gratefully acknowledge funding by the NSF (grant no. BNS-79-
13968), the assistance of members of the Chillagoe Caving Club, Queensland
National Parks and Wildlife Service, and many other individuals whose help was
indispensable to the success of the expedition.
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Hearing and Echolocation in the Australian Grey Swiftlet, Collocalia Spodiopygia

Acoustic orientation in the cave swiftlet.

Acoustic orientation in the oilbird,

Acuity of echolocation in Collocalia hirundinacea (Aves: Apodidae), with comments on the distribution of echolocating swiftlets and molossid bats.

Acuity of echolocation in the oilbird, Steatornis caripensis.

Adaptations for echolocation in cave swiftlets {Collocalia).

Comparative neurophysiological studies of hearing and vocalizations in songbirds.

Discharge patterns of single fibres in the pigeon auditory nerve.

Echolocation among Collocalia.

Echolocation and the systematics of swiftlets.

Echolocation by cave swiftlets.

Functional organization of auditory centres in the midbrain of birds.

Mechanism for the production of echolocating clicks by the grey swiftlet Collocalia spodiopygia.J.

Notes on the distribution and breeding of the grey swiftlet, Aerodramus spodiopygius.

Sensitivity of echolocation in cave swiftlets.

Similarities in design features of orientation sounds used by simpler, nonaquatic echolocators.

Space and frequency are represented separately in the auditory midbrain of the owl._7.

Studies of echolocation in the grey swiftlet, Aerodramus spodiopygius.

The natural history of the oilbird, Steatornis caripensis, in

The oilbird: hearing and echolocation.

The physiology of vocalization by the echolocating oilbird, Steatornis caripensis.

The response properties of auditory neurons in the midbrain of the domestic fowl (Gallus gallus) to monaural and binaural stimuli.

The swiftlets (Colhcalia) of Niah Cave,

https://authors.library.caltech.edu/32078/1/COLjeb87.pdf

Hearing and Echolocation in the Australian Grey Swiftlet, Collocalia Spodiopygia

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