Download Species-Recognition in the Field Cricket

AMER. ZOOL., 22:597-607 (1982)
Species-Recognition in the Field Cricket, Teleogryllus oceanicus:
Behavioral and Neural Mechanisms1
RONALD R. H O Y , GERALD S. POLLACK, 2 AND ANDREW MOISEFF 3
Section of Neurobiology and Behavior, Langmuir Laboratory,
Cornell University, Ithaca, New York 14850
SYNOPSIS. Field crickets depend on acoustic organs to detect the presence of potential
predators as well as conspecific crickets. Predators are recognized largely on the basis of
spectral frequencies that are contained in their acoustic signals. Puffs of air and very low
frequencies activate a cricket's cereal receptors and ultrasonic frequencies activate their
tympanal organs. Both of these acoustic stimuli release "escape behavior," in the form of
evasive movements. An identified neuron sensitive to ultrasound is described. Crickets
recognize singing conspecifics by both frequency and temporal properties of cricket songs;
however species recognition requires specific temporal information in calling songs. While
previous studies have emphasized the role of songs on female behavior, males also recognize conspecific songs; sexual differences in recognition behavior occur.
' From the Symposium on From Individual to Species
Recognition: Theories and Mechanisms presented at the
the necessity of recognizing categories of
signallers—being able to tell predators from
crickets, for example. In the latter case we
refer to discrimination within a category—
homospecific from heterospecific crickets,
for example. In principle, crickets could
also perform individual recognition, but
thus far such has not been demonstrated.
The final question, "Where is it?" is not
directly related to the matter of recognition and will not be dealt with here.
The cricket's conspicuous acoustic signals are vitally important, for they mediate
social behavior—the calling song of the
adult male is stereotyped and species-specific and acts as a beacon to attract distant
conspecific females to his territory for mating. It is by discriminating between the
calling songs of different species that females find reproductive partners; this discrimination behavior serves as our operational definition of species "recognition."
In this brief review we do not have space
to describe the extensive and excellent work
on the many aspects of acoustic behavior
in the singing orthoptera. We must restrict
ourselves to acoustic behavior in field
crickets, and furthermore, we will focus
primarily on our own work on the Austra-
Annual Meeting of the American Society of Zoologists. 27-30 December 1980, at Seattle, Washington.
2
Current address of G. S. Pollack is: Department
of Biology, McGill University. Montreal, Canada.
3
Current address of A. Moiseff is: Division of Biology. California Institute of Technology, Pasadena,
California.
interested reader should consult the excellent reviews of acoustic behavior in other crickets and insects that can be found in
Michelsen and Nocke (1974), Eisner and
Popov (1978), and Huber (1978).
INTRODUCTION
Field crickets are primarily active nocturnally and depend heavily on acoustic
signals by which they monitor their environment. Like other acoustically dependent animals they must solve three problems:
1) What is producing the acoustic stimulus? Among the relevant sources of sound
in the cricket's world are other crickets,
other kinds of singing insects, and acoustic
predators of various species.
2) Who is producing the sound? Crickets
must be able to discriminate among different species of sympatrically singing crickets in order to differentiate their own
species signals from those of others.
3) Where is the signaller located in the
environment? Obviously, crickets must be
able to localize the sources of sounds,
whether they emanate from conspecific
crickets or from potential predators.
The questions "What is it?" and "Who is
it?" are related to the issue of signal recognition. In the former case we refer to
lian field cricket, Teleogryllus oceanicus. The
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HOY ETAL.
T H E PRODUCTION AND RECEPTION OF
ACOUSTIC SIGNALS
Among crickets only males sing; they do
so by rubbing their forewings together, a
behavior called stridulation. Each closing
stroke of the wings produces a relatively
pure tone (field crickets songs are pitched
in a range between 3 and 8 kHz, depending on species) due to the frictional mechanics and resonant properties of the
wings themselves (Michelsen and Nocke,
1974). The opening stroke is silent. Thus,
the calling song is composed of a train of
tones in a rhythm determined by the timing of the contraction cycles of opener and
closer muscles; this rhythm is neurogenic,
stereotyped, and species-specific (Huber,
1962, 1964, 1978; Bentley and Kutsch,
1966). Differences among calling songs of
different species focussed attention on the
calls as species-isolating mechanisms (Alexander, 1962). As an example, the call
rhythm of Teleogryllus oceanicus is shown in
Figure 1.
Both males and females hear by means
of specialized tympanal organs that are located on the forelegs. This "ear" lies internal to a distinct tympanal membrane upon
which sound waves act. The membrane has
a peak resonant vibration that corresponds
to the fundamental frequency of the male's
call (Johnstone etal., 1970; Dragsten etal.,
1974; Larsen and Michelsen, 1978). These
vibrations activate a group of about 70 auditory receptor neurons whose axons project to the prothoracic ganglion (Young and
Ball, 1974; Eibl, 1978; Esch et al., 1980).
There they activate an unknown number
of interneurons that carry auditory information to the brain and to lower motor
centers that control locomotion; several
auditory interneurons have been identified (Stout and Huber, 1972; Rheinlaender
et al., 1976; Casaday and Hoy, 1977; Popov etal., 1978; Wohlersand Huber, 1978;
Elepfandt and Popov, 1979).
RECOGNIZING PREDATORS BY EAR:
T H E PITCH IS THE SWITCH
In its world a cricket hears not only other crickets, it hears potential predators.
Crickets are sensitive to a surprisingly wide
range of frequencies; in fact, the frequen-
- Phrase- Chirp
-Trill
tnn
B mi*——ii' Intra
Htrillii ii M
I WHIHIH
-Intrachirp
-Inlertrill
FIG. 1. Temporal structure of the species-specific
calling song of T. oceanicus shown as an oscillograph.
Calling song is composed of a series of repeating stereotyped phrases. Each phrase is composed of an introductory series of pulses (chirp), followed by a series of doublet pulses (trills). The three types of
interpulse intervals are defined in the oscillograph.
The time bar equals one second.
cy band devoted to social communication
is only a narrow one considered in light of
the insect's auditory capabilities. Figure 2
shows a frequency range from zero Hz to
100,000 Hz—from infrasound to ultrasound. Crickets are sensitive over a good
part of this range; compare this with the
auditory sensitivity of humans, which spans
a range of 50 Hz to 15,000 Hz. Crickets
achieve this sensitivity to airborne vibrations through two kinds of auditory organs. They detect very low frequencies with
a pair of appendages called cerci that project from the tip of the abdomen. The sensitivity of the cerci extends from between
nearly zero Hz in the infrasound to almost
1,000 Hz. Depending on species, the rest
of the frequency range of sensitivity begins
at 1-2 kHz and extends to at least 100 kHz.
This wide band of higher frequencies is
detected by the tympanal organ, or "ear,"
in the tibia of each foreleg.
Toads are insectivorous predators that
capture prey by flicking out their tongues
at their victims. These prey-capture movements set up a pressure wave (low frequency vibrations) that activates particular
sensory hairs on a cricket's (or cockroach's)
cerci. Precisely which hairs become stimulated depends on the direction of the wind
or vibrational source. These receptors in
turn activate giant interneurons in the CNS
that mediate directional escape responses
in crickets and cockroaches (Roeder, 1967;
Matsumoto and Murphey, 1977; Camhi,
1980). In addition to cerci, other low frequency receptor organs exist but their behavioral role is uncertain (Dambach, 1972).
Other predators produce ultrasound.
SPECIES-RECOGNITION IN CRICKETS
S&9
FIG. 2. The range of hearing in field crickets. The frequency line is drawn logarithmically, from zero Hertz
(Hz), through the infrasound and terminating in the ultrasound at 100,000 Hz (100 kHz). Low frequency
stimuli are detected by the cricket's cerci, and higher frequencies are detected by its tympanal organ or "ear."
Below the frequency line are drawn typical sources of sound that fall within the cricket's range of audition:
terrestrial predators such as frogs produce low frequency vibrations, crickets produce middle frequency
vibrations, and flying bats produce ultrasound.
Many moth species have ears, and are sensitive to the ultrasonic echolocation sounds
of insectivorous bats; the acoustically mediated evasive behavior of moths to bats is
well-known through the classic work of
Kenneth Roeder (1967). Some species of
crickets also fly at night (Ulagaraj and
Walker, 1973; Popov etal, 1975) and would
be vulnerable to bat predation. While critical observations of bats actually hunting
down crickets on the wing are lacking,
studies from our laboratory indicate that
if crickets were pursued by echolocating
bats, they would be able to make evasive
maneuvers to escape them (see also Rheinlaender et ai, 1976). Crickets can be induced to fly in the lab by placing them on
the end of a tether and directing a stream
of wind past them; while these "flying"
crickets flap their wings and respond to directional sources of sound by making directed movements of their abdomens and
hind legs that can be interpreted as steering movements (Moiseff et al., 1978) that
are analogous to comparable steering behavior in other tethered, flying insects
(Dugard, 1967).
Figure 3A-C shows diagrams taken from
photographs of flying crickets responding
to acoustic stimuli. In the absence of sound
a cricket flies with a symmetrical flight posture, with its longitudinal body axis perfectly straight. When a series of sound
pulses consisting of pure 5 kHz tones is
played from a speaker on the cricket's left,
the insect bends its abdomen and legs to
the left, a rudder-like action that would
propel the insect toward the speaker, were
the insect not tethered. However, when the
sound pulses are composed of 40 kHz
tones, the cricket's abdomen and legs
abruptly veer to the right; in free-flight this
would propel the cricket away from the
sound source. Thus, 5 kHz tones elicit positive phonotactic movements and 40 kHz
cause negative phonotactic movements.
The sign of the movements makes behavioral sense: 5 kHz is the carrier of fre-
40 kHz
i
ill
i
iii
II
I I
3 4 56 8 0
20
Frequency (kHz)
j_
1
i
i
i i
r
40 60 80 100
FIG. 3. Crickets shown during an instant of tethered flight. Drawings are made from photographs taken
with a strobe-flash. In A, the cricket is shown flying in the absence of acoustic stimulation. In B, the cricket
is played a 5 kHz calling song from a speaker on its left; note that the abdomen, legs, and one antenna are
oriented toward the sound source. In C, the acoustic stimulus was played at 40 kHz from the same speaker
as in B. Note that the abdomen and legs are now oriented away from the sound source; such movements of
the appendage would steer a free-flying cricket away from the sound. In D, the frequency sensitivity of
steering behavior is demonstrated; the data are drawn from experiments on 12 animals. The filled circles
represent the median threshold intensities and the bars indicate the ranges. The animals are most sensitive
to narrow frequency band between 4 and 6 kHz; a secondary area of sensitivity ranges broadly in the ultrasound between 20 and 100 kHz. From Moiseff et ah, 1978.
SPECIES-RECOGNITION IN CRICKETS
quency of the calling song of Teleogryllus
oceanicus; female crickets are attracted to
this frequency. Forty kHz is in the ultrasonic range and occurs in the vocalizations
produced by insectivorous bats (Griffin,
1974); crickets attempting to escape from
echolocating bats would be expected to
react to 40 kHz aversively.
The frequency sensitivity of steering behavior can be ascertained by examining a
behavioral tuning curve (Fig. 3D) made by
measuring the threshold sound intensities
required to elicit a phonotactic response as
a function of the tone frequency. T. oceanicus is most responsive to tones in the range
4-6 kHz, with peak sensitivity at 5 kHz; a
second area of sensitivity occurs in the ultrasound, from 25-100 kHz. While these
data reflect the spectral sensitivity of phonotactic behavior, it is from the direction,
or sign, of phonotaxis that its behavioral
importance can be inferred. In Figure 6
we see that crickets steer toward middle
frequency tones (3-10 kHz) but steer away
from ultrasonic tones (above 15 kHz). We
believe that these data define the information content contained in the frequency
spectrum of a sound: middle frequencies
are interpreted by crickets as other crickets, and are therefore approached; ultrasonic frequencies are interpreted as something to avoid (predacious bats?). The data
in Figure 3, provide insight into the way
that simple acoustic information (in this
case, frequency) is translated into adaptive
behavior. In addition, flight phonotaxis is
a powerful behavioral assay for the investigation of the mechanisms that underlie
species recognition (Pollack and Hoy, 1979,
1981).
To summarize, the spectral frequency in
a sound pulse carries important information having to do with predation:
1) Very low frequency sounds activate the
cereal system and mediate escape behavior
in walking crickets.
2) Ultrasonic frequencies activate the
tympanal system and also mediate escape
movements in flying crickets.
Thus, particular frequency bands are
"labelled" and stimuli falling within them
elicit escape responses. The task of "recognizing" predators is relatively easy and
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is done by frequency analysis of a sound.
In a narrow frequency band ("middle" frequencies), approximately 2-8 kHz, are
found most cricket calls. The role of frequency in species recognition will be dealt
with later.
ULTRASOUND SENSITIVITY:
A NEURAL ANALYSIS
Escape behaviors in invertebrate animals
have been fertile ground for a neuroethological analysis, for example: crayfish
swimming (Wiersma, 1947; Wine and
Krasne, 1972); grasshopper jumping
(Pearson, 1980); moth flight (Roeder,
1967); and cockroach running (Roeder,
1967; Camhi, 1980). We have made an attempt to analyze the ultrasound mediated
"escape" behavior of Teleogryllus oceanicus
(Moiseff and Hoy, 1979; Moiseff, 1980).
An identified auditory interneuron in the
CNS of the cricket Teleogryllus oceanicus (in-
terneuron-1—Casaday and Hoy, 1977) has
been shown to be highly sensitive to ultrasonic stimulation, including artificial pulse
trains designed to resemble bat echolocation signals. Figure 4 shows a diagram of
the neuron in the prothoracic (auditory)
ganglion, and its response to a train of ultrasonic stimuli delivered from an electronic sound generator arranged to simulate a bat echolocation signal; this identified
interneuron is sensitive to ultrasonic stimuli from 20-100 kHz (Moiseff and Hoy,
1979; Moiseff, 1980). Its response resembles the sensitivities of neurons in the auditory systems of many moths known to be
preyed upon by bats (Roeder, 1967). Perhaps the most interesting feature of this
neuron is its dichotomous response characteristic: while it is excited by ultrasound,
its activity appears to be suppressed by
lower frequencies—4 to 10 kHz—precisely
those frequencies used by crickets for social communication. In fact, peak inhibition occurred at 5 kHz, the carrier frequency of the oceanicus call. This was shown
by performing a two-tone inhibition experiment (Fig. 5) which was suggested by
our colleague, R. Capranica. First, the neuron was excited by a pulse of ultrasound
to establish a standard excitatory response
(Fig. 5A). Then, a 5 kHz tone was pre-
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HOY ETAL.
E only
E+145
B
60
80
LULL
WLL
W1L
JULL
lllllll
FIG. 4. lnterneuron-1 and its response to ultrasonic
pulses. At the top is shown a camera-lucida drawing
of interneuron-1, made from a whole mount of the
prothoracic ganglion (see Casaday and Hoy, 1977)
stained with cobalt. The neuron has a major dendritic
arborization in the auditory neuropile (AN) and it
sends its axon (A) to the brain; its cell body (S) is seen
in the contralateral hemiganglion. In the lower panels
are shown the responses of int-1 to simulated bat
echolocation pulses. The first panel shows int-1 responding to 0.5 msec, 30 kHz-tone pulses delivered
above threshold (here, 80 dB SPL); the repetition rate
is 10 pulses per second. In the second panel, the pulse
repetition rate was increased to 300 pps, a rate found
in the terminal phase of echolocation. The recordings
were made from int-1 intracellularly, with a dye-filled
micropipette.
sented simultaneously with the 40 kHz excitatory tone (Fig. 5B-D). When played
loudly enough, the 5 kHz tone added to
the 40 kHz tone reduced the cell's excitatory discharge; the combination tone was
inhibitory compared to the excitatory tone
alone. Thus, int-l's activity is inhibited by
frequencies that occur in the social signals
of its own species. The hypothesis that it
functions to detect the ultrasonic calls of
bats is attractive and we present Figure 6
to support it; the lower graph shows the
phonotactic performance of tethered flying
crickets as a function of stimulus tone frequency; the upper graph shows the effect
of tone frequency on the interneuron's state
of activity. At those frequencies that "attract" the cricket (promote positive phonotaxis) the interneuron is inhibited from firing, whereas at those frequencies that
stim.
-
^
^
—
•
FIG. 5. Two-tone inhibition in interneuron-1. In A,
the neuron was presented with an excitatory tone alone
(30 kHz at an intensity 10 dB above threshold). In B,
C, and D, the excitatory tone (same parameters as in
A) was paired with a 5 kHz tone at varying levels of
intensity, 45, 60, and 80 dB SPL respectively. The
effect of the combination tone was a diminished response from the neuron—the 5 kHz tone is inhibitory. The stimulus bar denotes the duration of the
stimulation period—220 msec, for both excitatory and
inhibitory tones.
"repel" the cricket (promote negative
phonotaxis) the interneuron is excited.
These observations are consistent with the
hypothesis that the interneuron plays a role
in the cricket's negative phonotactic behavior to ultrasound.
SPECIES RECOGNITION IN CRICKETS
A long history of phonotaxis experiments on crickets has shown that the temporal pattern of the calling song carries
critical information upon which speciesspecific discrimination is based (Walker,
1957; Zaretsky, 1972; Popov and Shuvalov, 1977; Pollack and Hoy, 1979, 1981).
While it is clear that carrier frequency is of
importance (Hill, 1974; Moiseff et ai,
1978), temporal pattern is the primary cue.
We will review the phonotactic behavior of
just one species, Teleogryllus oceanicus, the
subject of our own studies (Moiseff et al.,
1978; Pollack and Hoy, 1979, 1981).
In their natural habitat in Australia, 7Yleugryllus oceanicus females are able to discriminate between the calls of oreanims
males and those of a sympatrk speiies, 7".
SPECIES-RECOGNITION IN CRICKETS
100
Inh
0
Exc
100
100
Pos
0
Neg
100
1
1
8
O
20
30
40
Frequency (KHz)
FIG. 6. Possible role of interneuron-1 in phonotactic
behavior. The neural response (Top) of int-1 as a
function of frequency is compared with the phonotactic behavior (Bottom) of a tethered, flying cricket
responding to acoustic stimuli at various frequencies.
In the range 4—6 kHz, the response of int-1 is inhibited, and the flying cricket approaches these frequencies. From about ID kHz to 40 kHz, the interneuron
is excited, and at these frequencies flying crickets steer
away. The bars in the int-1 data indicate the percentage (of 8 experimental preparations) of neurons
that showed excitation or inhibition (measured by the
two-tone inhibition criterion). The bars in the behavioral data indicate the percentage (of 12 animals tested)
of animals that steered toward the sound source (positive) at a given frequency, or away (negative).
commodus (Hill et al., 1972). We have established laboratory colonies of both species
and investigated their phonotactic behavior, especially during tethered flight. We
have shown that T. oceanicus females prefer the calls of oceanicus to those of commodus in both walking and flight phonotaxis (Hoy and Paul, 1973; Pollack and
Hoy, 1979). Hereafter, we shall discuss only
data from flight phonotaxis experiments.
The role of temporal pattern in speciesspecific song recognition was studied by
making electronic song models of normal
and altered oceanicus calling song (Pollack
and Hoy, 1979, 1981). In Figure 7 the results of several phonotaxis experiments are
summarized. Figure 7B-D shows electronic song models of normal oceanicus call (B),
"altered" oceanicus call (C), and the call of
the sympatric species, T. commodus (D). The
orderly procession of chirp intervals and
trill intervals are species-specific characteristics and are distinctly different in ocean-
603
icus and commodus (Leroy, 1963; Bentley
and Hoy, 1972; Hill etal, 1972). The electronic song models were constructed from
the data of Bentley and Hoy (1972), and
the females responded as well to synthetic
as to real songs. The temporal stereotypy
of the normal species calls is manifested in
two ways. First, the pulse-to-pulse orderliness of pulse intervals is apparent from
the sequential interval plots (E, F). Second,
the relative proportions of each interval
type can be shown in a conventional histogram plot (H-J). Clearly, oceanicus and
commodus differ from each other in both of
these ways. The altered oceanicus song (C,
F, I) differs from normal oceanicus song in
that the sequential orderliness of pulse intervals has been "randomized," by repeatedly shuffling the ordinal positions of the
song intervals throughout an experiment.
However, it is identical to normal oceanicus
song in that the "dosage" of each kind of
interval is unchanged; the same interval
histogram is generated for oceanicus and
shuffled oceanicus songs. The relative attractiveness of these songs for oceanicus females during tethered flight is shown in
Figure 7, K-M, which summarizes the results from 36 crickets (12 for each experiment). The ordinate shows the proportion
of trials in which one song was chosen over
another, although both songs were presented to the cricket simultaneously. Crickets in tethered flight show their song preference by flexing their abdomens and
hindlegs in the direction of the speaker
playing the "favored" song; speakers are
set at 90° to the body axis. When oceanicus
females were presented with the choice of
oceanicus and commodus songs they overwhelmingly chose oceanicus (K); in a few
cases they did not make a choice (no postural change), and these are labelled "Nd"
on the abscissa. This result was expected,
for it corroborates the result for walking
phonotaxis (Hill et al, 1972; Hoy and Paul,
1973; Pollack and Hoy, 1979) in Teleogryllus. More surprising was the inability of
oceanicus females to make a phonotactic
choice between oceanicus song and the
shuffled version of oceanicus song (Fig. 7L);
the proportion of females that chose one
or the other was the same, and the major-
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HOY ETAL.
HIM iniii ii ii IMI mi m i n i nit
LL
Intrachirp
B
^J— Intratnl
C
Intertnl
D
MWHHHNHWHII
HI HUN I I I I I 1 Ml HI INI
6
I"
200
E 150
10
20
30
Interval number
ra 100
so
V
u
a>
a.
10
40 0
20
30
40
100
ISO
200
H
75
50
•
25
. 1 .
0
SO
100
. 1 .
ISO
200 0
50
100
ISO
200 0
Interval duration (msec)
M
1.0
1.0
1.0
0.5
0.5
0.5
0
L
Oc Nd Co
0
L
Oc Nd Sh
Sh Nd Co
FIG. 7. In A, oscillograph of T. oceanicus calling song showing the three types of interpulse intervals. In
B—D, oscillographs of electronically synthesized songs showing oceanicus, shuffled song, and T. commodus song,
respectively; time bars represent 1 sec. In E-G, sequential interval plots for the three songs shown directly
above; the abscissa represents the ordinal positions of intervals in each song and the ordinate shows the
duration of each interval; the orderliness of interval sequence seen in the T. oceanicus calling song is absent
from the shuffled song. In H—J, histograms showing the proportions of the three interval types in the three
songs; note that the oceanicus song and the shuffled song generate the same interval histogram, which is clearly
different from that for commodus. In K—M, phonotactic preferences of T. oceanicus females during two-choice
discrimination tests. Tests were made on tethered, flying animals; two different calling songs were presented
simultaneously, one from the animal's right, the other from its left. The results are given as the proportion
of trials in which the songs were selected (choices shown on abscissa). Abbreviations: Oc = oceanicus song
preferred. Co = mmmndm song preferred, and Nd = no discrimination, which meant that the cricket did not
make a steering movement toward either speaker during the experiment. Data drawn from 36 animals. (From
Pollack and Hov. 1979.)
SPECIES-RECOGNITION IN CRICKETS
605
ity of females failed to choose at all. The of such behavior differs depending on sex
inability to choose between normal and (Dawkins and Krebs, 1978). Whatever the
shuffled oceanicus songs could be inter- status of current theories, it seems likely
preted as their being equivalent. To test that further investigation of sex-linked difthis, females were presented with a choice ferences in acoustic communication in
between shuffled oceanicus and normal crickets will provide insight for behavioral
commodus songs. Again, females over- theorist and neuroethologist alike; e.g.,
whelmingly chose oceanicus (even when Cade, 1979.
shuffled) over the heterospecific commodus
SUMMARY
(Fig. 7M).
The inability of oceanicus females to dis- It is clear that acoustic behavior in the
tinguish between normal and shuffled cricket requires that its auditory system be
oceanicus songs, but to clearly prefer shuf- able to analyze spectral frequency as well
fled oceanicus to commodus songs, can be in-as temporal pattern in a signal. Spectral
terpreted as meaning that oceanicus fe- frequency is "labelled" in the sense that an
males recognize the temporal structure by extremely broad range of frequencies is dithe dosages of the three interval types con- vided into several categories of sender-antained in the song. Thus, the strict sequen- imals (Fig. 2). Very low frequencies actitial ordering of each interval within a song vate receptors on the cerci, prominent
phrase is not necessary for recognition; it abdominal appendages, and signal the
is sufficient to provide intervals in species- presence of possible land predators. At
specific proportions.
high frequencies (ultrasound), we have
A recent and important turn in this story shown that flying crickets make vigorous
warrants mention. All of the phonotaxis efforts to fly away from the sources of ulexperiments reported above were per- trasound. This behavior is mediated by
formed on female oceanicus. However, male tympanal organs located on the forelegs.
oceanicus also fly and perform in-flight Presumably, such a behavior evolved from
phonotaxis. Like females, they are attract- predation by echolocating bats which hunt
ed to the song of homospecific oceanicus flying insects at night; we make this specover the heterospecific commodus. How- ulation by analogy with the clearly demever, unlike females, males prefer normal onstrated acoustically-mediated escape beoceanicus over shuffled oceanicus songs and havior of moths when chased by bats
they prefer shuffled oceanicus to commodus (Roeder, 1967). Using ultrasound we have
songs; in experiments thus far, 11 male been unable to provoke escape responses,
oceanicus have preferred normal oceanicus such as hopping or running away, from
song to none for shuffled song, and 27 crickets that are walking or standing still.
failed to disciminate; however, when tested Presumably, on land, predators give themagainst commodus song, 11 males preferred selves away by issuing forth infrasound vithe shuffled song to none for commodus; brations or puffs of air, but not by ultraagain, 27 males failed to make discrimi- sonic signals. However, to a cricket on the
nations in the tests (Pollack, unpublished wing, it is ultrasound by which a predator
results). Thus, sex differences occur in the announces its presence.
acoustic communication in crickets, as have
Cricket sounds occur in a narrow band
been reported in the singing behavior of of "mid-range" frequencies (3-8 kHz).
songbirds (Nottebohm and Arnold, 1976; While different species of crickets may inNottebohm, 1980). These and other sex- deed call with different carrier frequendifferences in song attractiveness (Pollack, cies, the divergence between two sympatric
1980) may reveal important differences in species may be as little as 500-1,000 Hz.
the information content or meaning of the There is no doubt that carrier frequency
species-specific calling song that depend on in the sound pulses of the call carries imthe sex of the recipient of the signal. Re- portant information. However, differcent speculations on the evolution of com- ences in temporal pattern are critical for
munication behavior stress that the pay-off species-specific recognition. Thus, in social
606
HOY ETAL.
communication, crickets utilize both cues,
frequency and temporal pattern of acoustic stimuli.
It has been easier to make a neural analysis of behaviors due to low frequency auditory stimulation (Matsumoto and Murphey, 1977; Edwards and Palka, 1974) and
ultrasonic stimulation (Moiseff and Hoy,
1979) than of social communication. Undoubtedly this is due in some measure to
the ease with which escape responses can
be reproduced in the laboratory and the
participation of "giant" neurons in the
neural circuits that underlie escape in the
cricket as well as other animals. However,
studies on crickets are going on internationally to understand precisely what it is
that crickets are saying to each other and
what is going on in their nervous systems
that explains that elusive behavioral act
called "recognition." An important contribution of modern ethology has been to
demonstrate the utility of the comparative
approach in the study of animal behavior.
It is to be expected that comparative studies will prove equally enlightening in neuroethology, and that understanding mechanisms of recognition in the auditory
behavior of crickets will be informative for
similar analyses in higher animals.
ACKNOWLEDGMENTS
We wish to acknowledge the contributions of our neuro-behavioral colleagues at
Cornell, particularly in Dr. Bob Capranica's and Dr. Jeff Camhi's lab groups. Drs.
Bruce Land and Melvin Kreithen, and
Margaret Nelson provided facilities and
advice at critical times. Drs. Margaret Nelson and Jean Fraser commented on the
manuscript. We acknowledge, gratefully,
the support of the NIH (NINCDS) for a
postdoctoral award to G.S.P., and research
and RCDA grants to R.R.H.
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