Echolocation Call Design and Limits on Prey Size: A Case Study Using the Aerial-Hawking Bat
Nyctalus leisleri
Author(s): Dean A. Waters, Jens Rydell, Gareth Jones
Source: Behavioral Ecology and Sociobiology, Vol. 37, No. 5 (1995), pp. 321-328
Published by: Springer
Stable URL: http://www.jstor.org/stable/4601146
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(CSpringer-Verlag1995
Behav Ecol Sociobiol (1995) 37: 321-328
Dean A. Waters * Jens Rydell * GarethJones
Echolocation
calldesignandlimitson preysize: a case studyusingthe
leisleri
batNyctalus
aerialwhawking
Received: 28 October 1994/Accepted after revision:4 June 1995
Abstract The echolocation calls used by Nyctalus leisleri during search phase in open air space are between
9 and 14 ms long, with the peak energy between 24
and 28 kHz. The pulses are shallowly frequency-modulated with or without an initial steep frequencymodulated component. The diet consists primarilyof
small flies (Diptera), including many chironomids
(wingspan 9-12 mm) and yellow dung flies (Scatophaga;wingspan24 mm), but also of some largerinsects
such as dung beetles (Coleoptera; Scarabaeoidea),
caddis-flies (Trichoptera) and moths (Lepidoptera).
The echo target strength of some prey items was measured. Contrary to models based on standard targets
such as spheresor disks,the echo strengthof real insects
was found to be virtually independent of the emitted
frequency within the 20-100 kHz frequency range. A
model was used to calculate probable detection distances of the prey by the bat. Using narrow-bandcalls
of 13.7 ? 2.7 ms duration, a bat would detect the two
smallest size classes of insect at greatest range using
calls of 20 kHz. The results may thereforeexplain why
many species of large and medium sized aerial-hawking bats use low-frequencycalls and still eat mostly relatively small insects. The data and model challenges
the assumption that small prey are unavailableto bats
using low-frequencycalls.
Key words Bat Echolocation Feeding ecology
Ultrasound Target strength
D.A. Waters (1) G. Jones
School of Biological Sciences, University of Bristol, Woodland
Road, Bristol BS8 IUG, UK
J. Rydell1
Departmentof Zoology, University of Aberdeen, Tillydrone
Avenue, Aberdeen AB9 2TN, UK
Present acldress:
'Department of Zoomorphology, University of Gothenburg,
Medicinaregatan18, S-41390, Gothenburg, Sweden
Introduction
For predatorsin general, prey size normally increases
with predator size, and a wider range of prey sizes is
usuallyavailableto largepredatorsthan to smallerones.
This is because large predators are able to catch both
large and small prey, while smaller predators are
restrictedto small prey (e.g. Rosenzweig 1968). However, this hypothesis assumes that large predators are
equally well adapted to detect and catch small prey as
are the smaller predators.
For aerial-hawkinginsectivorousbats which always
use echolocation to find their prey, the assumption of
equal detectabilitymay not hold, and hence the usual
relationship between predator size and prey size may
not apply. The principal reason for this is that small
prey may be less availableto large bats, which tend to
echolocate using relativelylow frequencieswith a correspondinglylong wavelength.These long wavelengths
are predictedto be unsuitablefor the detection of small
targets (Barclayand Brigham 1991).
Echolocation of insects in air operates over a short
range,usually only a few meters(Kick 1982;Kalko and
Schnitzler 1989). This is partly because the effective
range of echolocation is severely limited by the small
proportion of acoustic energy that is reflectedfrom a
small target, termed "target strength" (Mohl 1988),
which is low for small insect targets. In addition, the
geometric spreadingof sound and severe excess attenuation of high-frequencysound by the atmospherealso
limit the range at which echolocation can operate
effectively (Griffin 1971; Kick 1982; Lawrence and
Simmons 1982).
Since target strength is generally dependent on the
ratio of the size of the target (the prey) and the wavelength of the sound (M0hl 1988), the detection range
would be expected to decrease with decreasing target
size for sonar signals of a fixed frequency.Small prey
items may therefore be particularly difficult or even
impossible to detect at great enough distance to allow
322
successful pursuit and capture, particularlyfor large,
relativelyunmanoeuvrablebats.This constrainton prey
availability may demand extraordinary manoeuvrability and agility, hence restricting the size of aerialhawking bats (Barclay and Brigham 1991).
However, the assumption that large bats are effectively limited to large prey does not seem to agreewith
the observation that the diet of several medium-sized
to large (10-30 g) aerial-hawkingbats in Europe are
dominated by small dipterans like chironomids and
mosquitoes rather than by moths, beetles and other
relativelylarger prey items (Sologor 1980; Petrusenko
and Sologor 1981;Bauerov'aand Ruprecht1989;Rydell
1989, 1992a, b; Sullivan et al. 1993; Catto et al. 1994;
Jones 1995). Hence, this study was motivated by the
apparent discrepancy between theory and empirical
data regardingthe diet of aerial-hawkingbats, particularly by the somewhat unexpected exploitation of
relativelysmall prey items by some medium-sizedand
large aerial-hawking bats. Specifically, the following
problems were addressed: Firstly, what is the lower
limit on prey size, i.e. which insects are acoustically
"small" and therefore effectively unavailable as individual prey items to aerial-hawking bats? Secondly,
what are the predicted detection ranges for prey of
differentsizes, given the frequenciesused during search
flight, and are these ranges sufficientto avoid temporal overlap with the outgoing pulse, which may interfere with the detection of echoes?
For the calculationsseveralgeneralassumptionsare
made:
1. Prey detection is enhanced by the wing movements
of the prey,i.e. that the echolocation pulses are long
enough in duration to produce "glints" (maximum
target strength), occurring when the insect wings
are perpendicular to the transmitted sound, such
that the pulses are longer than the wing beat
cycles of the prey (Schnitzleret al. 1983; Schnitzler
1987).
2. Echoes that overlap temporally with the emitted
pulses interferewith detection and hence that prey
detection is most likelyto occur duringthe time window between pulses, i.e. that the minimumdetection
range is determined by the duration of the pulses
and the maximum range is set by the duration
of the interpulse intervals (Kalko and Schnitzler
1993).
3. The bats' hearing threshold for echo detection is
near 0 dB SPL (Sound Pressure Level) (Neuweiler
et al. 1984; Coles et al. 1989).
4. That the intensityof an outgoing pulse used in search
for prey in open air spaces is near 110 dB peSPL
(peak equivalentSPL, Stapells et al. 1982) at 10 cm
(Shimozowaet al. 1974;von Joermannand Schmidt
1981; Surlykke et al. 1993; Waters and Jones
1995).
Materials
andmethods
Study site
Recordings and visual observations of foraging Nyctalus leisleri
were made near a maternityroost used by a large colony (150-200
females plus their young), situated in central Bristol, England
(51?30 N, 02?40'W) during September 1993. Droppings from the
month of Septemberwerelatercollectedfrom underneaththis roost,
which was located c. 10 m above the ground in a large stone house.
Our observationsand recordingswere largely confined to the area
near the roost, although some individuals of N. leisleri were also
detected while foraging in other parts of the city.
Recording and analysis of echolocation calls
Foragingbats were recordedusing PetterssonD-960 and D-980 bat
detectors (L. Pettersson Elektronik, Uppsala, Sweden), which
allowed high frequencydigital samplingof the input (samplingrate
350 kHz) and output at x 10 time expansion, hence lowering the
frequency to within a range suitable for recording on a Sony
ProfessionalWalkmanWM-D6C. Recordingswere made when the
environmentalconditions were approximately 12?C and 80-90%
relative humidity. Analysis was performed on a Kay DSP 5500
sonagraph. Call durations were taken from waveforms and maximum, minimumand peak frequencieswere taken from power spectra using a 1024 point fast Fourier transform with Hamming
window.
Diet analysis
The droppingswere softened by soaking them in a mixtureof water
and alcohol, the latter included to eliminate the surface tension,
and then teasing them apart under water under a dissectingmicroscope by using dissecting needles and fine forceps. One hundred
droppings of approximatelyequal sizes were analysed. The prey
remains were identifiedto order and in the case of dipterans further, by comparison with a collection of whole insects and a variety of availableguides includingseveralvolumes of ThleHandbook
for theIdentificationof BritishInsects(Royal EntomologicalSociety,
1949-1993), Chinery (1986) and McAney et al. (1991).
For each dropping,the minimumnumberof each prey type was
determined (Swift et al. 1985) and also the approximate volume
representedby each (Whitaker1988).The frequency(percentageof
the numberof recoveredprey items) of each prey type was obtained
by adding the numbersfrom each dropping. This method tends to
overestimate the importance of larger items, parts of which may
appear in several droppings. The relative volume representedby
each prey type was estimated for each dropping separately,later
adding the percentages,assuming that each dropping represented
one percentof the whole sample(Rydell 1989;Jones 1990).Volume
gives an estimate of the importanceof each prey type, in terms of
energy or biomass, while frequencygives a picture of the number
of items in each category that were pursuedand captured.
Echo intensity measurements
In order to model the maximumtheoreticaldetection range, target
strengthwas determinedfor a variety of Diptera and Lepidoptera
of differentsizes (Table 1). Target strength is defined as the logarithmic ratio of incident acoustic energy to the reflected energy,
measured at a certain distance from the target along its acoustic
axis (M0hl 1988). Our reference distance was defined as 1 m.
Atmosphericconditions duringmeasurementswere 120 C and 82%
323
Table 1 Insects from which target strengths were measured, together with some of their measurementsin mm (means ? SD)
Wingspan
Moths (Lepidoptera)
Noctua pronuba(Noctuidae) 53.7 ? 2.5
Agrotis segetum (Noctuidae) 32.3 ? 1.6
Body length
n
24.8 ? 2.5
14.3 ? 1.2
5
5
40
12.4 ? 0.46
10.7 ? 0.67
4.8 ? 0.26
5.1 ? 0.62
__
30?
L
Flies (Diptera)
Trichoceridae
Culicidae
t
20 -
L
~
-10
ms_
_
10
6
5
Time
relativehumidity. Insectswere mounted to dry with their wings flat
and spread perpendicularto the body. This posture was aimed to
imitate the "glint"situation, i.e. with maximum wing surface perpendicularto the directionof the sound, giving maximalecho intensity. A 0.08-mm diameternylon thread was run from the floor to
the ceiling in a 4 x 4 x 2.6 m sound-proofedroom lined with sound
attenuating foam. The insects were glued to the thread with the
wings parallelto the speakermembraneof an Ultra Sound Advice
ultrasound loudspeakerat a distance of 1 m for large insects (the
two moth species) and 0.5 m for smaller ones (the two Diptera
species). Constant frequencysound pulses of 2.5 ms duration were
generated and shaped by a custom-made sine wave generator and
pulse shaper (total harmonic distortion <1 %). Signals were
amplified prior to broadcasting at the insect and adjusted incrementally over the frequencyrange 20-100 kHz in 5-kHz steps. The
echoes from the insects were recorded via a QMC PSM-3 ultrasound microphone placed immediately above the speaker. The
angular separation between the speaker and the microphone was
4.50 for the 1-m targets and 90 for the 0.5-m targets. Output and
echo levels were recordedas speaker and microphone voltages on
a Tektronix 5113 oscilloscope. The echo levels with the insect subsequently removed from the thread were then subtractedfrom the
insect echo levels to adjust for echoes from the supporting tether.
Voltages were later convertedto absolute dB peSPL values by calibration of the apparatuswith a Bruel and Kjaer 2204 sound pressure meter equipped with a 4135 6.35-mm microphone (with the
protection grid off). The data obtained were recalculatedto provide target strengthsat a standardiseddistance of 1 m. To estimate
the maximumtheoreticaldetection distance of the targetby the bat,
the targetstrength,distanceto target and excess atmosphericattenuation (from Bazley 1976) were modelled to provide the target distance at which the returningecho was at 0 dB SPL for a source
level of 110 dB peSPL at 10 cm. The attenuation model was based
on excess atmosphericattenuation at 120 C and 80% RH. Excess
atmosphericattenuation for these conditions is plotted in Fig. 1.
3.5
3-3
.02.5
Fig. 2 Sonograms of two typical search phase echolocation calls
of foraging Nyctalus leisleri recorded in Bristol, England, in
September1993. The first is a low bandwidth, long duration shallow frequency-modulated(FM) call, the second is a high bandwidth, shorterduration, more broadbandFM call. The two pulses
are 15 and 10.2 ms long, respectively
Results
Echolocation call design
The bats were recordedas they dispersed shortly after
emergence from the roost and a few recordings were
also obtained in the immediate vicinity later in the
evening. The light levels that prevailed shortly after
dusk also permittedvisual observationsof the recorded
bats. They usually fed along tree lines at 10-15 m elevation in relativelyopen parkland.
The search phase echolocation pulses were principally of two types, although intermediateforms sometimes occurred as well. They were either narrow-band
(shallow frequency-modulated)signals or narrow-band
signals that also included an initial broadband component (steep frequency-modulated).The narrow-band
pulses (n = 20) were 13.7 ? 2.7 ms long (mean ? SD),
with peak energy at 25.5 ? 2.3 kHz. The bandwidth
was generally less than 5 kHz in these cases. Pulses
which had an initial broadband component (n = 20)
were 10.3 ? 1.7 ms long, with peak energy at 28.0
? 1.6 kHz, highest frequency at 57.9 ? 5.1 kHz and
lowest frequency at 25.8 ? 1.4 kHz. In the recorded
sequences we analysed, broadband calls were not alternated with narrow-band calls. Sonograms of two
typical pulses, representingeach of the two types, are
shown in Fig. 2.
02-
Diet and prey size
~1.5
The recoveredinsect remains showed that the diet was
strongly dominated by flies (Diptera), which made
0.5
up 81% of the prey items (Table 2) and 77% of
the volume (Fig. 3). Moths (Lepidoptera), dung bee10
20
30
40
50
60
70
80
90
100 110
tles (Coleoptera; Scarabaeoidea) and caddis-flies
Frequency (kHz)
(Trichoptera)were also recovered,but in relativelylow
Fig. I Excess atmospheric attenuation at 12?C and 80% relative numbers (in total 18% of the items and 22% of the
volume). Among the flies, Nematocera, particularly
humidity (from Bazley 1976)
O
I
A
I,
,
,
I
I
__
324
Table 2 Frequencies(%) of various insect taxa recoveredfrom faeces collected in a maternity roost of Nyctalus leisleri in Bristol,
England. One hundredpellets were analysed
Insect taxon
Occurrence
Frequency Percent of total
(% of pellets) (number)
Diptera
Nematocera
Muscidae
Lepidoptera
Coleoptera
Trichoptera
Unknown
50
42
15
11
3
1
85
42
15
11
3
1
54.1
26.8
9.6
7.0
1.9
0.6
midges (Chironomidae) were most common, representing 54% of the total number of Diptera and 43%
of the volume. However, the yellow dung fly
[Scatophaga stercoraria (L.); Brachycera; Muscidae]
was also very numerous,comprising alone 27% of the
items and 12% of the volume.
To estimate the size of the insects eaten by the bats,
we used eye diameter as a correlate,because eyes were
the only parts that regularlywere recoveredwhole. The
smallest prey items recovered were chironomids, the
smallest of which had eye diameters of 0.3-0.4 mm
(Fig. 4). By comparison with whole chironomid specimens collected in the United Kingdom, this eye diameter corresponds to body lengths of 6-8 mm and
wingspansof 9-13 mm. The most common single prey
species, the yellow dung fly, had an eye diameter of
0.7 mm, a body length of c. 11 mm and a wing span
of c. 24 mm.
Echo intensity measurements
Targetstrength at various pulse frequencieswas measured for four different insect species ranging in size
from a large moth (Noctua pronuba)to a dipteran, a
mosquito of unknown species (Culicidae), about the
same size as the smallest prey items actually eaten by
the bats (Fig. 5). As expected, target strength generally decreased with insect size. Within each insect
species, however, there was no clear relationship
between target strengthand the frequencyof the pulse.
Using data from Mohl (1988), recalculatedto give target strengthsat 1 m, a disk of 10 mm diameter would
be predicted to have a target strength of -34 dB at
35 kHz (the model is only valid above a wavelength/
diameterratio of unity wherethe wavelengthat 35 kHz
is 10 mm), and -25 dB at a frequency of 100 kHz. A
sphereof 10 mm diameterwould have a target strength
of -52 dB at both 35 and 100 kHz. As would be
expected, the target strengths recorded for a disk of
comparablediameterto the wingspan of the insect are
>30 dB higher. It is likely that reflectionsfrom a complex target cannot be modelled using such simple
assumptions,and also likely that the actual biomaterials of the insect have some influence in determining
reflectiveproperties.
Modelled maximum detection distances (Fig. 6)
show that the maximum distance at which the bat was
predicted to be able to detect the two larger insects
decreaseswith increasingfrequency,mainly because of
excess atmospheric attenuation. The calculated detection distances for the two smaller insect classes remain
relatively stable with increasing frequency. The solid
horizontal line in Fig. 6 represents the distance at
which the echo from the target will overlap temporally
with an outgoing pulse of 13.7 ms duration,which corresponds to the mean duration of the narrow-band
pulses recordedfrom N leisleri in this study. The dotted lines represent the standard deviation of the call
duration. The distance at which pulse-echo overlap
occurs depends on pulse duration, and is hypothesized
to set the minimum detection range (Kalko and
Schnitzler 1993). At a 13.7 ms pulse duration, the
smallest of the two dipteranstested (the culicid) would
be detected if the bat uses frequencies near 20 kHz
(Fig. 6). At higher frequencies,detection distances are
likelyto enterthe zone of pulse-echooverlap.Therefore,
to use higher frequencies,the bat would also have to
shorten the pulses in order to detect the same sized
60
,_4030
O
20-
100
Fig. 3 Percent volume of insect taxa recovered from faeces collected
in
a
maternity
root
of
N
leI -
I
BIstol,
EngA
-
0.1
0.2
0.3 0.4 0.5 0.6
Eye Diameter(mm)
0.7
0.8
Fig. 4 Size distribution of dipteran eyes (diameter,n = 77) recovered from faeces collected in a maternity roost of N. leisleri in
Bristol, England
325
-30
-
-
V
V
20
is
-40
16
-50
14
13,7 ms puise-echooverlap
sd
distance+1
-60
Noctua pronuba
-70
-80
0
20
40
60
100
80
120
-30
-40T
k121z1
-60
-70
Agrotis segetum
-80
0
X
ci
Frequency
g Agro>gsegetumtE
J Novtuapron:ubo
-501
20
40
80
60
1oo
120
ire
1wzeridue
2 CulicIed
Fig. 6 Modelled detection distances (+SD) for four differentprey
items by an echolocating bat that uses narrow band pulses of 13.7
ms duration, in relation to the (hypothetical)frequencyused. The
solid line is the detection distance at which pulse-echo overlap
occurs. The dottedlinesare the pulse-echo overlap distances at ?l
SD of the call duration
-30
Trichoceridae
~-40
H-50
60
-T
-
-70
-80
0
20
40
60
80
100
120
100
120
-30 -
Culicidae
-40
-50
-60-
-70
-80
0
20
40
60
80
Frequency (kHz)
Fig. 5 Target strengths for Nocttuapronuba and Agrotis segelum
(Lepidoptera:Noctuidae), a dipteran(Diptera: Trichoceridae)and
a smallerdipteran,(Diptera: Culicidae).Data are mean?SD of one
determination at each frequency for each insect (n = 5-6, see
Table 1). Measurementsof these insects are given in Table I
insects. If a 10 ms pulse is used, the bat would be predicted to detect the small dipterans (Culicidae) within
the zone where temporal pulse-echo overlap is predicted to interfere with echo detection, regardless of
the frequencyused.
Discussion
The low proportion of large prey items in the diet of
N. leisleriand the correspondinglyhigh proportion of
small dipteransmay seem surprisingin the view of the
relatively large size (11-20 g) and powerful flight of
this species. However, the result agrees very well with
a previous study of the diet of NMleisleri in Ireland
(Sullivan et al. 1993), where small dipterans,including
chironomidsand yellow dung flies, also constituted the
bulk of the prey. Furthermore,the diet of NVleisleri is
similar to those of all other European aerial-hawking
bats that use high intensity echolocation calls and
frequencies between 20 and 30 kHz, e.g. N. noctula
(Jones 1995), Eptesicus nilssonii (Rydell 1989, 1992a),
Eptesicus serotinus (Sologor 1980; Catto et al. 1994)
and Vespertiliomurinus(Petrusenkoand Sologor 1981;
Bauerovaand Ruprecht 1989;Rydell 1992b). This suggests that there must be a general explanation for the
low occurrenceof largerprey and the high occurrence
of smaller prey items in the diets of such bats.
One factor that contributes to the relative scarcity
of large prey in the diet of these bats is that high intensity,low frequencyand long durationecholocationcalls
are easily detected by tympanate insects such as, for
example, many families of moths (Fullard 1987) and
lacewings (Miller 1984). On hearingecholocation calls,
these insects exhibit escape responses making them
more difficult or perhaps even impossible to catch
(Roeder 1962; Miller and Olesen 1979; Dunning et al.
1992), hence lowering the profitability of such prey
items compared with smaller, mostly non-tympanate
ones like dipterans (Roeder and Treat 1962).
The calculated target strengths of real insects
illustrate that they may not obey standard rules for
modelling simple shapes such as spheres or disks.
For spheres, targets with diameters larger than the
wavelengthof the sound reflect all frequenciesequally.
Reflection from disks increases as the ratio of wavelength/diameteris reduced.Reflectionsfrom an insect's
wing would be expected to approximate to a planar
target and show a high-pass characteristic.For a 1-cm
disk (1 cm is the wavelength at 34.4 kHz), the target
326
strength would be predicted to rise 9 dB over
the range 35-100 kHz (Mohl 1988). In contrast to that
of spheresand disks, target strengthsfrom real insects
are more difficult to predict, and the empirical results
reported here appear to accurately representa maximum target strength likely to be encounteredby a foraging bat. Provided that our experimentation and
modelling efforts representa reasonable model of the
real situation (see Pye 1993), our results suggest that
detection distances are limited by the excess atmospheric attenuation at high frequencies, and that low
attenuation at low frequenciesallows the detection of
even small targets at greaterrange.
Clearly,the model of calculated detection distances
is sensitiveto the values of the target strengthdata, the
level of atmosphericattenuationand the validity of the
assumptions.Irrespectiveof the assumptionsabout call
intensity and hearing thresholds,the data support the
hypothesis that bats using low frequencycalls are able
to detect individual Diptera with wingspans smaller
than 1 cm, and that a low call frequencythereforedoes
not limit the perception of such small prey. Different
values of emitted intensity will increaseor decreasethe
detection distances, as will differentvalues of hearing
threshold, but our conclusions remain sound. An
important considerationis whetherpulse-echo overlap
does put a lower bound on detection distance, as at
short ranges the returningechoes may be masked by
outgoing pulses. Field studies have shown that pulseecho overlap is avoided in bats with low duty cycle
echolocation (Schnitzler et al. 1987; Kalko and
Schnitzler 1989, 1993). Avoidance of pulse-echo overlap is also supported by data on middle ear muscles,
which contract duringpulse emission to protectthe ear
(Henson 1965; Suga and Jen 1975), and by inhibitory
neuronal mechanisms activated in the brainstem during calling (Suga and Schlegel 1972), although psychophysical data on this effect is lacking. There is
however some evidence to suggest that, at least in laboratory studies, a small degree of pulse-echo overlap
does not affect target discrimination(Simmons et al.
1990). If we assume that pulse-echo overlap does constrain minimum detection distances, then for certain
combinations of emitted intensity, auditory sensitivity
and atmospheric attenuation, small insects will be
detected using long duration calls before pulse-echo
overlaponly if low frequency(< 25 kHz) calls are used.
The distances calculated for detection corresponds
well with establishedempirical data on prey detection
ranges in the lab and in the field (Griffin et al. 1960;
Novick 1977; Kick 1982; Fenton and Bell 1979;
Schnitzler et al. 1988; Kalko and Schnitzler 1989).
However,we emphasisethat our calculationsare based
on the assumption that the bats were able to detect the
glints, which occur only periodicallywhen the moving
wings of the insects are perpendicularto the transmitted sound. Therefore, the ranges calculated probably
reflect a maximum and the averagetarget strength of
individual insects will be much lower (Roeder 1963;
Moss and Zagaeski 1994). If the insects are flying in a
swarm however, it is much more likely that the bat
would detect an insect in the glint position. It is also
probablethat the target strengthof an insect swarmis
higher than that of the individual insects within it,
making the swarm detectable at a greater range. This
effect remains to be quantified.
The conclusions reached here may have some general implications for the evolution of echolocation
systems and foraging strategies in bats. Since excess
attenuationis so severe at high frequenciesthat detection of prey within a biologically realistic distance
may be hindered by pulse-echo overlap, the evolution
of echolocation systems employing high frequencies
would be severelyrestricted.Such high-frequencycalls
would be advantageousfor exploitingtympanatemoths
whichhavepoor high-frequencyhearing(Fullard1987).
For aerial-hawking bats, use of higher frequencies
would also mean that shortersearchpulses would have
to be used, in order to minimise the problemof pulseecho overlap.Since shorterpulses also result in shorter
average detection distances, and hence less reaction
time,this strategywould only workin combinationwith
25
Vm
20
*
315
Sn
S
Es
o
En
CNr
g:10
l
0
H
Ln.
r
Pko *
-
S
O
20
Lao
Cv*
Pr
G
*Tp
*P4
Ec Ns
Ms
P
*b
I
30
40
*Ma
h
I
50
60
I
70
Frequency
(kHz)
Fig. 7 The relation between pulse duration and frequency containing most energy of the calls in vespertilionidbats which use
FM/CF echolocationcalls. All measurementsare from searchphase
calls recordedin the field. Acronyms and sources are: Le Lasiurus
cinereus (Barclay 1986), Ef EptesicusJuscus, Ec E. capensis, Pr
Pipistrellusrueppelli,Sv Scotophilusviridis,La Laephotisangolensis, Pn Pipistrellusnanus, Sn Scotophilusnigrita, Ns Nvcticeinops
schleffeni, Ph Pipistrellus hesperus (Fenton and Bell 1981), Nn
Nycvtalusnoctula, En Eptesicus nilssonii, Es E. serotinus, Vin
Vespertilioinurinus(Ahlen 1981), P4 Pipistrelluspipistrellus,
45 kHz
crypticspecies, P5 P. pipistrellus,55 kHz crypticspecies(Jones and
Parijs 1993),Pk Pipistrelluskuhli,Pn P. nathusii,Hs Hvpsugosavii,
Ms Miniopterusschreibersii,Ni Nvctalus leisleri (Zingg 1990), Mai
Miniopterus australis, Cg Chalinolobusgouldii, Sg Scotorepens
grejii, Ep Eptesicuspumilus(Jones and Corben 1993), Lnilasionvcterisnoctivagans(Barclay 1986), Cv Clhalinolobus
variegatus(Obrist
et al. 1989), Tn Tylonycteris pachvpus, Tr T robustula, Gt
Glisochropusty/opus;Hb Hesperoptenusb/anfordi(Heller 1989).The
regression line is v =40.7 1-8.91 ln(x), F],9= 44.6, P < 0.001,
=0.56
327
a reductionin body size, necessaryfor extrememanoeuvrabilityand agility.Such links may partly explain why
aerial-hawkingbats are small (Barclay and Brigham
1991). If pulse-echo overlap did constrain minimum
detection distances, pulse duration would be predicted
to reduce as call frequency increased. There is indeed
a close logarithmic correlation between echolocation
call frequencyand pulse duration among aerial-hawking bats using frequency modulated/constant frequency (FM/CF) calls, based on data availablein the
literature(Fig. 7, P < 0.001, r2= 0.56). A logarithmic
relationshipmay well be appropriatesince atmospheric
attenuation approximatesto a logarithmicfunction of
frequency(Bazley 1976). Logically,the inflectionof the
relationshipwould be expectedto be in the other direction, high-frequencycalls havingto be reducedin duration by a proportionally greater amount than
low-frequency calls. However, this does not occur
because as a bat emits higher frequencies,the detection distance of the target decreases due to greater
atmosphericattenuation.Because the bat is now closer
to the target, the relative contribution of attenuation
due to spreadinglosses then increasesover that due to
excess atmospheric attenuation (Lawrence and
Simmons 1982). The net effect of this is to reduce the
impact of excess atmospheric attenuation as the bat
raises its frequency and approaches the target more
closely.It could be arguedthat the relationshipbetween
call duration and frequency in the field data may be
produced as a consequence of the calls of higher peak
frequencyalso having a higher maximum frequencyin
the initial FM sweep. These higher frequencieswould
be attenuatedmore and lead to an apparentreduction
in call duration.However,since the calls consist mainly
of a long duration CF portion, preceded by a short
durationFM component, this effectis likelyto be small.
One evolutionary pathway towards combining long
durationpulses with high frequencieswould be through
the use of constant frequency pulses in combination
with a Doppler-shift compensating mechanism. Such
a system, as is currently employed by the Rhinolophidae, some Hipposideridae and Pteronotusparnellii
(Mormoopidae), removes the problem of temporal
pulse-echo overlap entirely, because pulses and echo
detection are separatedin the frequencydomain rather
than in time (Schnitzler 1968; Neuweiler et al. 1980).
Separationof pulse emission and echo detection in the
frequencydomain allows echoes to be processedwhile
pulses are being emitted, and allows the bats to gain
benefits from using long duration calls (which encode
echoes from many insect wing beats) at high frequencies. However, because small prey would still only be
detected at a very close range,the necessityfor extreme
agility and manoeuvrabilityremains.
In summary, it appears that low frequency echolocation calls may not limit aerial hawking bats to
detectingand capturinglargeprey items.If the assumption that FM/CF bats are constrained by pulse-echo
overlap is valid, then under certain conditions, using
low frequencycalls may be the only way in which bats
can detect small prey items outside the zone of pulseecho overlap.
AcknowledgementsWe thank K. Watt and M. Young for help with
entomological literature and A. Entwistle, P.A. Racey, I. Wallis
and Brock Fenton for comments on the manuscript.The study was
fundedby a Scienceand EngineeringResearchCouncil Studentship
to D.A.W., the Swedish Natural Science ResearchCouncil to J.R.
and a University Research Fellowship from the Royal Society to
G.J. Three anonymous refereesprovided helpful comments on this
manuscript.
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