Behavioral assessment of acoustic parameters relevant
to signal recognition and preference in a vocal fish
Jessica R. McKibbena)
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853
Andrew H. Bass
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853
and University of California Bodega Marine Laboratory, Bodega Bay, California 94923
?Received 19 April 1998; revised 11 June 1998; accepted 26 August 1998?
Acoustic signal recognition depends on the receiver’s processing of the physical attributes of a
sound. This study takes advantage of the simple communication sounds produced by plainfin
midshipman fish to examine effects of signal variation on call recognition and preference. Nesting
male midshipman generate both long duration ??1 min? sinusoidal-like ‘‘hums’’ and short duration
‘‘grunts.’’ The hums of neighboring males often overlap, creating beat waveforms. Presentation of
humlike, single tone stimuli, but not grunts or noise, elicited robust attraction ?phonotaxis? by gravid
females. In two-choice tests, females differentiated and chose between acoustic signals that differed
in duration, frequency, amplitude, and fine temporal content. Frequency preferences were
temperature dependent, in accord with the known temperature dependence of hum fundamental
frequency. Concurrent hums were simulated with two-tone beat stimuli, either presented from a
single speaker or produced more naturally by interference between adjacent sources. Whereas
certain single-source beats reduced stimulus attractiveness, beats which resolved into unmodulated
tones at their sources did not affect preference. These results demonstrate that phonotactic
assessment of stimulus relevance can be applied in a teleost fish, and that multiple signal parameters
can affect receiver response in a vertebrate with relatively simple communication signals. © 1998
Acoustical Society of America. ?S0001-4966?98?02412-6?
PACS numbers: 43.66.Gf, 43.80.Lb ?DWG?
The function and underlying mechanisms of communi-
cation in the acoustic modality have remained largely unex-
plored in the largest of extant vertebrate taxa, teleost fish.
Studies of teleost hearing have demonstrated fundamental
similarities with auditory processing in higher vertebrates, in
spite of differences in their auditory endorgans ?review: Pop-
per and Fay, 1993?; thus one might expect similar acoustic
dimensions to have been exploited by both fish and terrestrial
vertebrates for encoding behaviorally relevant information.
We used playback of synthetic signals to test which acoustic
features affect call recognition and attractiveness in a sound-
producing teleost, the plainfin midshipman ?Porichthys nota-
Acoustic signals, generated by vibration of intrinsic
swimbladder muscles, are a prominent feature of social in-
teractions in midshipman fish. Midshipman breed along the
west coast of North America ?Walker and Rosenblatt, 1988?
where the parental, or ‘‘type I,’’ males establish nests under
rocks in the intertidal zone ?see Bass, 1996?. From these
nests, the type I males emit long-duration, multi-harmonic
signals known as ‘‘hums’’ ?Ibara et al., 1983; Brantley and
Bass, 1994; Fig. 1A–C?. When a female enters his nest, a
male stops humming, and spawning may begin. Spawning
can take several hours as the eggs are affixed to the under-
surface of the rock, after which the female departs and the
male alone guards and maintains the developing embryos.
Whereas, in any breeding season, a female probably spawns
only once, depositing all her eggs in one nest ?DeMartini,
1988; Brantley and Bass, 1994?, a male may continue to hum
and attract mates and may have several clutches at different
stages of development in his care. Midshipman also have a
smaller, ‘‘type II,’’ male morph, which pursues sneak
spawning strategies, does not hum, and lacks the type I
male’s secondary sexual characteristics, including its special-
ized vocal system ?Bass, 1992, 1996?.
Midshipman hums can be continuous for minutes to an
hour or more, often with minimal variation in frequency or
amplitude ?Ibara et al., 1983; Brantley and Bass, 1994; Bass
et al., in press?. Hum fundamental frequency is linearly re-
lated to water temperature, increasing about 5 Hz/°C, and is
approximately 100 Hz at 16 °C ?Brantley and Bass, 1994;
also see Bass and Baker, 1991?. Ibara et al. ?1983? found
with simple playback experiments that recorded hums, or
pure tones in the same frequency range, were sufficient to
attract gravid females ?phonotaxis?. This finding, along with
aquarium observations of midshipman nesting behavior
?Brantley and Bass, 1994?, suggests the hum functions as a
mate call. Midshipman also produce brief ?50–200 ms?
‘‘grunt’’ sounds ?Fig. 1D–F? that probably serve an agonistic
function. Both females and type II males have been recorded
making infrequent, single grunts; but only type I males pro-
duce trains of grunts ?Fig. 1D–F?, emitted, during aquarium
observations, in response to intruder males ?Brantley and
a?Electronic mail: firstname.lastname@example.org
3520 3520J. Acoust. Soc. Am. 104 (6), December 1998 0001-4966/98/104(6)/3520/14/$15.00© 1998 Acoustical Society of America
This study first tests the hypothesis that the hum func-
tions as a mate call by examining the phonotactic responses
of gravid and spent females and of both male morphs. Then,
one- and two-choice tests with gravid females are used to
assess the importance of certain acoustic parameters to hum
recognition and attractiveness. Finally, we examine the ef-
fects of signal overlap. Midshipman nests are often clustered,
and males hum simultaneously; thus receivers must com-
monly process concurrent acoustic signals ?Bodnar and Bass,
1997; Bass et al., in press?. We chose to present playback
choices as they would be encountered in a natural situation,
that is, with alternative calls originating from closely spaced
sources and overlapping in time. Therefore, inherent in every
choice task presented here is the problem of identifying, lo-
cating and evaluating concurrent acoustic signals. The effect
of overlap on stimulus effectiveness is further investigated
by presenting two-tone beat stimuli.
I. MATERIALS AND METHODS
A. Experimental animals
Midshipman, including females and type I and type II
males, were collected from nests exposed at low tide along
Tomales Bay and San Quentin Point in Marin County, Cali-
fornia. Females and males ?type I and II? are distinguished
by the size and shape of the urogenital papilla, while the two
male morphs are easily further separated on the basis of size
and coloration. Gravid females typically have a very dis-
tended abdomen, which becomes flaccid and often darker in
coloration in spent females ?e.g., see Brantley and Bass,
1994; Bass, 1996?. Females taken from nests were in various
stages in the spawning process, with many having begun egg
deposition, but the majority were still conspicuously gravid.
Each fish was measured, weighed, and labeled either
with subcutaneous injections of poster paint, creating a
unique color/location pattern, or with a numbered tag sutured
just rostral to the dorsal fin. Most experiments were con-
ducted using gravid females (n?265), which ranged in size
from 8.9 to 20.4 cm ?mean 13.5?2.0 cm? standard length
and 9.3 to 121.8 g ?mean 33.8?18.1 g?. Fish were held for at
least 24 h prior to testing in outdoor, running sea water tanks
at the University of California Bodega Marine Laboratory,
where all experiments were conducted. The temperature the
fish were housed at varied with the temperature of the in-
coming seawater ?usually between 10 and 15 °C?. Live grass
shrimp, brine shrimp and goldfish, and chopped anchovies
were occasionally offered as food. Under these conditions,
females usually would retain their eggs and remain respon-
sive for up to several weeks.
Females and both type I and type II males were tested
for responses to humlike, continuous tones; but all tests of
comparative responses were done with gravid females. Due
to limited numbers of subjects, individual females were used
for multiple tests ?median number of tests per fish: 6, median
number of responses: 3?, and may have encountered the
same stimulus as one of the choices in different tests. Except
for serial one-choice tests, fish were used for no more than
one response per night; and, because some fish were used for
the same test on different nights or for tests that were later
grouped, only the first response of a fish to a stimulus pair is
included in the analysis. Variables such as length of time in
captivity and hormonal state could also have affected indi-
vidual responsiveness. However, since all tests involved
choices or response comparisons, loss of responsiveness was
controlled for. It is not possible to rule out experiential ef-
fects on preference strengths, although it seems likely that
any habituation to the artificial sound sources or stress due to
time constraints on egg viability would tend to decrease
rather than increase selectivity.
B. Experimental layout
Tests were done outdoors in a cylindrical concrete tank
?4-m diameter, 0.75-m water depth? supplied with running
seawater. Since midshipman normally call next to the sub-
strate in water a few meters or less in depth, the boundary
conditions in the experimental tank were not entirely unnatu-
ral. Underwater loudspeakers ?UW-30; University Sound,
Buchanan, MI? were suspended just above the bottom from
water-filled PVC frames, so that no direct contact substrate
conduction was possible. The speakers were placed near the
center of the tank facing outward ?Fig. 2?, well removed
from the wall to reduce both the influence of reflected sound
and incidental approach by the fish, which tended to hug the
tank perimeter in the absence of sound stimuli. For experi-
ments conducted in 1995, the speakers were 137 cm apart
center to center and angled toward the release site ?configu-
ration C in Fig. 2?. These experiments include one of the
FIG. 1. Midshipman calls recorded in the field. ?A? Segment ?1 s? of a hum
waveform showing the nearly flat envelope. ?B? An expansion of the hum
waveform. ?C? Frequency spectrum of same hum showing peaks at the
107-Hz fundamental frequency and harmonics. Amplitude values are rela-
tive only. ?D? Waveform for segment ?6 s? of a grunt train. ?E? Expanded
waveform of single grunt. ?F? Spectrum of grunt shown in ?E?.
3521 3521 J. Acoust. Soc. Am., Vol. 104, No. 6, December 1998 J. R. McKibben and A. H. Bass: Signal recognition in fish
relative proximity to an individual source. Given the re-
sponse criteria applied in this study, it is also possible that
rejection of single-source beat stimuli occurs only after the
fish has approached the source. Indeed, fish were sometimes
observed to orient toward and begin to approach a speaker
playing a strongly beating waveform and then to swim away,
implying recognition of the summated waveform that oper-
ates at a distance but not at the source.
Alternatively, although the two speakers used here to
create the multi-source beat were side by side, it is possible
that, due to directional selectivity of sound transducing hair
cells in the fish ear, the angular separation of the sources was
sufficient to diminish the effective interference ?review of
directional masking data in Fay, 1988; Fay and Edds-
Walton, 1997?. In effect, each tone would be processed by a
separate channel, and beating would not be a problem.
IV. SUMMARY AND CONCLUSIONS
First, this study supports the conclusion of Ibara et al.
?1983? that the plainfin midshipman hum functions as a mate
call, and extends that finding by describing the phonotactic
response of both male morphs as well as of gravid females.
Second, results from one and two-choice tests show that fe-
male midshipman fish respond selectively to audible sounds
and are capable of differentiating and choosing between
acoustic signals that differ in duration, frequency, amplitude,
and spectral/temporal content. Although it is most straight-
forward to examine preference functions along one dimen-
sion, in reality there are probably interactions between vari-
ous signal parameters such that they create a multi-
dimensional preference space ?Doherty, 1985; Ryan and
Rand, 1993; Forrest and Raspet, 1994?. This study has not
directly addressed the influences of one parameter on an-
other, but it is apparent, for example, that, although fish can
discriminate small amplitude differences, they do not always
prefer the more intense signal.
In the absence of any data correlating hum characteris-
tics with male or nest quality, we do not know whether fe-
males would benefit from acoustic choosiness beyond that
necessary to locate a conspecific male. However, females do
make a large investment in one clutch of eggs that is appar-
ently deposited in a single nest ?DeMartini, 1988; Brantley
and Bass, 1994?, and search behavior could be costly. Thus,
selection would likely have favored acoustic discrimination
that enabled females to extract any available information
about mate or nest quality from male hums.
The midshipman’s simple acoustic signals and unam-
biguous phonotactic responses make it a promising system
for understanding the receiver mechanisms of communica-
tion, both in terms of behavioral decisions and the underly-
ing neural coding.
We would like to thank Margaret Marchaterre and
Deana Bodnar for logistical support and advice during this
study, and Deana Bodnar, Christopher Clark, Ronald Hoy,
and the reviewers for their comments on the manuscript.
This research was supported by a training grant from NIMH
?5T32GM07469?. a Clare Booth Luce Fellowship, and NIH
Grant No. DC-00092.
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