|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online November 1, 2006
Journal of Experimental Biology 209, 4444-4451 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02525
Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish
1 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY
14850, USA
2 Department of Oceanography, Florida State University, Tallahassee, FL
32306, USA
* Author for correspondence (e-mail: lrr4{at}cornell.edu)
Accepted 5 September 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: acoustic startle, predation, eavesdropping, natural selection, stress, communication, corticosterone
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Zuk and Kolluru,
1998). Most examples of this `conspicuousness tradeoff' occur in
species that rely on visual communication signals (e.g.
Endler, 1983;
Endler, 1987;
Endler, 1992;
Forsgren and Magnhagen, 1993;
Koga et al., 1998;
Evans et al., 2002).
Acoustic advertisement signals should also be susceptible to eavesdropping
[or `interception' (see Myrberg,
1981)] by predators. Empirical evidence supports the hypothesis
that acoustic signals become more cryptic in the presence of predators. For
example, nesting petrels reduce advertisement calling in response to playback
sounds of a predator, the brown skua
(Mougeot and Bretagnolle,
2000). Similarly, silver perch that are exposed to playback
whistles of the bottlenose dolphin [a primary predator
(Barros, 1993)] show a
transient reduction in population call amplitude
(Luczkovich et al., 2000). Bat
echolocation signals have also been shown to suppress or eliminate
advertisement calling in both male túngara frogs
(Ryan, 1985) and katydids
(Faure and Hoy, 2000).
Therefore, both predators and prey species monitor and respond to
`eavesdropped' acoustic information, although the proximate mechanisms for
anti-predator behavior by vocalizing prey species are not well understood.
Acoustic signaling is the primary mode of communication during the breeding
season in toadfishes, when males emit `boatwhistles' to attract females to
their nests and interact with rival males
(Fig. 1)
(Gray and Winn, 1961).
Toadfishes constitute approximately 13% of the diet of adult bottlenose
dolphins (Barros, 1993), and
Gannon et al. (Gannon et al.,
2005) recently showed that bottlenose dolphins exhibit positive
phonotaxis toward acoustic playbacks of the vocalizations of Gulf toadfish.
Thus, dolphin prey, such as Gulf toadfish, could be under selection to detect
dolphin acoustic signals and use this information to adjust mate advertisement
calling, though this possibility remains untested.
|
;
Kagawa and Mugiya, 2000;
Kavaliers et al., 2001;
Cockrem and Silverin, 2002;
Clinchy et al., 2004).
Although elevated circulating stress hormones are linked to anti-predator
behaviors such as defensive posture
(Blanchard et al., 1998), it is
unknown whether reductions in acoustic behavior and conspicuousness are also
linked to changes in glucocorticoids [some evidence indicates that
glucocorticoid levels vary in other systems in response to context-dependent
acoustic playbacks (e.g. Rukstalis and
French, 2005)]. Furthermore, glucocorticoids are known to cause
rapid increases in the output of a hindbrain-spinal vocal pattern generator
that establishes the temporal properties of natural calls in toadfishes
(Remage-Healey and Bass, 2004;
Remage-Healey and Bass, 2006),
but the relationship of this observation to natural behavior is largely
unexplored.
In this study, we test whether exposure to playback of vocalizations of
bottlenose dolphins elicits rapid changes in the vocal behavior and/or stress
hormone levels in a primary prey species, the Gulf toadfish. Bottlenose
dolphins employ a variety of vocalizations during social communication and
foraging. High-frequency whistles (5-20 kHz) are used during social
communication with conspecifics (Fig.
2A) (Tyack and Clark,
2000; Janik et al.,
2006) and echolocation clicks (20-100 kHz) are emitted during
navigation and foraging (Au,
1993; Johnson et al.,
2004). A third vocalization category, the low-frequency `pop', has
been recently documented during foraging bouts over habitats that may be less
amenable to high-frequency echolocation clicks, such as seagrass beds
(Fig. 2B)
(Nowacek, 2005). However,
dolphin prey species such as toadfish may be able to best detect low-frequency
pops emitted by foraging dolphins, since toadfish auditory frequency encoding
is most robust below 1 kHz (Fish and
Offutt, 1972; Yan et al.,
2000; Fay and Edds-Walton,
2000; Bass et al.,
2001). As shown here, using behavioral (vocalization) and
physiological (circulating cortisol levels) measures, Gulf toadfish can
apparently recognize the foraging pops of predatory dolphins.
|
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Playback, recording and blood sampling procedures were similar to those
presented previously (Remage-Healey and
Bass, 2005). Playback experiments were performed using enclosures
(70x70x10 cm) in the bay at FSUML, which has a water depth of
1-1.5 m. Enclosures were placed on the sea bottom (depth=1.5 m) within a
natural group of calling male toadfish with active nests. A section of PVC
pipe (8 cm diameter, 25 cm length) was inserted in the enclosure to provide
nesting and hiding space. A single male O. beta was placed inside
each enclosure and each male began emitting boatwhistles
(Fig. 1) within 48 h. A
hydrophone was placed in the center of the calling population (approximately
3-4 m from any one enclosure) and suspended 4 cm from the sea bottom by a
hydrophone stake.
Acoustic stimuli were used with permission from William Tavolga (marine
sounds atlas), and were brief clips of bottlenose dolphin and snapping shrimp
sounds, as presented in Fig. 2.
Stimuli were presented in a looped-mode playback (1 min loop comprising 45 s
of stimulus followed by 15 s of silence) for a 5-min playback period (see
below). Each fish received only one stimulus per experiment, and only one
experimental playback occurred during a 24 h period (within the hours 12:00 to
16:00). Each fish was only used in one experiment, to control for possible
habituation effects. Stimuli were broadcast from a portable compact disc
player (Memorex) connected to a 12 V powered amplifier (Mofset XAF340 340 W
2/1 channel power amplifier, Namsung, Kent WA, USA) connected to an underwater
playback speaker (Aquasonic 229, Clark Synthesis, Littleton, CO, USA). The
speaker was suspended from the side of the research boat so that it was 1 m
from the sea floor, directly above the calling population of toadfish. All
stimuli were presented at approximately 136 dB (see
Table 1) to minimize distortion
due to over-amplification. The range of instantaneous source levels for
dolphin vocalizations is 150-200 dB
(Janik, 2000;
Tyack and Clark, 2000) and for
snapping shrimp `pops' is 180-210 dB (Au
and Banks, 1998; Versluis et
al., 2000). Recorded dolphin pops used in this study were
repetitive trains of brief, broadband signals that had significant energy
<1 kHz (see Fig. 1 and
Table 1), and are similar to
the low-frequency `pops' previously reported to be involved in foraging
behavior in bottlenose dolphins (Connor
and Smolker, 1996; Nowacek,
2005).
|
The playback treatment for all groups was divided into three periods: (1) vocal activity was recorded for 5 min prior to playback (`5 Pre'); (2) one of the four stimuli (see Table 1) was then presented for 5 min, in a looped-mode playback (`5 Stim'). (3) 5 min of post-playback activity was then recorded with no playback sound presented (`5 Post'). The number of individuals for each group was: whistles alone (N=5), dolphin pops alone (N=4), dolphin whistles and pops (N=9), snapping shrimp pops (N=7).
Toadfish vocal responses were recorded onto a Sony laptop computer
(digitized using Syrinx software, designed by John Burt, Cornell Lab of
Ornithology, Ithaca, NY, USA). Levels of stimuli were monitored in the center
of the calling population (see above) and are presented as sonograms in
Fig. 2. All recording data were
analyzed with CoolEdit Pro 1.2a software (Syntrillium, Phoenix, AZ, USA).
Recorded individuals were identified unambiguously based on call duration,
amplitude, and fundamental frequency (see
Edds-Walton et al., 2002;
Thorson and Fine, 2002a;
Remage-Healey and Bass, 2005;
Remage-Healey and Bass, 2006).
Two acoustic measurements were quantified for each individual: `call rate',
which is the number of boatwhistles per 5 min playback period, and `call
duration', which is the duration of the hoot portion of each boatwhistle
[Fig. 1, defined as the period
of the constant-frequency portion of the boatwhistle, after Tavolga
(Tavolga, 1958), Thorson and
Fine (Thorson and Fine, 2002a;
Thorson and Fine, 2002b) and
Remage-Healey and Bass (Remage-Healey and
Bass, 2005)].
Plasma sampling and analysis
Blood samples were taken from male toadfish following three playback
treatments: dolphin whistles and pops, dolphin pops alone and snapping shrimp
pops. Field conditions allowed sampling of plasma cortisol from animals in
these three groups only. The two groups that were exposed to stimuli
containing dolphin pops (dolphin whistles and pops, and dolphin pops alone)
were grouped together as `dolphin pops' for statistical purposes (see below).
Following the last playback period (5 Post), individual fish were immediately
brought to the surface and briefly anesthetized (<1 min; 0.025% benzocaine)
for blood sampling (see Remage-Healey and
Bass, 2005; Remage-Healey and
Bass, 2006). The operculum was drawn back and gill exposed, and
excess water from the gill slits was drawn into a transfer pipette to prevent
dilution of the blood sample. A 0.5 ml blood sample was then drawn from the
gill arch using a 1.0 c.c. heparinized syringe (26 gauge needle tip). No more
than four fish were sampled following any one playback stimulus, and the
length of time between the end of playback stimuli and collection of blood
sample for all fish ranged from 4.22 min to 18.12 min (mean interval=10.99
min). Only one fish was brought to the surface at a time after playback
stoppage, reducing disturbance effects on plasma cortisol levels. No
significant difference in plasma cortisol levels was found between early (4-6
min) and late (12-18 min) samples (U-test; P>0.05),
therefore samples were pooled by group (dolphin pops versus shrimp
pops) for analysis. Average sampling times did not differ between the two
groups (dolphin pops vs shrimp pops; t-test;
P>0.05). Whole blood was centrifuged at 400 g and
plasma was stored frozen until later analysis. Plasma was analyzed for
cortisol using radioimmunoassay (RIA) at the Diagnostic Laboratory, New York
State College of Veterinary Medicine at Cornell University.
|
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Hormonal responses
Cortisol levels in the fish exposed to dolphin pops were significantly
elevated compared to levels in fish exposed to snapping shrimp pops
(Fig. 4; Wilcoxon rank sum
test; 
2=5.16; d.f.=1; P<0.02). The dolphin pops
group includes all animals exposed to dolphin pops alone (N=4) and a
subset of animals exposed to dolphin whistles and pops (N=4); there
were no significant differences between the two groups in cortisol
responsiveness (U-test; P>0.05) and these groups were
combined to increase power (overall N=8). Field logistics
circumvented obtaining blood samples from all animals in the dolphin whistles
and pops group.
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Interspecific eavesdropping, e.g. between predators and
prey, could also exert strong selection on the evolution of acoustic
communication when both predators and prey vocalize. This study now shows that
the intermittent predation risk posed by dolphin predators has both behavioral
and physiological consequences for one of their prey, male Gulf toadfish. Our
experiments show that toadfish have adopted behavioral strategies to reduce
the risk of predation during the protracted breeding season (May-September)
when dolphin predators forage on near-shore grass beds. Reduction in call rate
by male toadfish during dolphin foraging bouts probably reflects an
evolutionary tradeoff between the fitness benefits of mate-advertisement and
the high risk of predation. Recent experimental data demonstrate that
bottlenose dolphins orient toward toadfish vocalizations
(Gannon et al., 2005), and
emit pops during foraging bouts (see below). Taken together, these results
suggest that a dynamic, co-evolutionary relationship exists between acoustic
communication systems of both members of a predator-prey interaction. Acoustic
eavesdropping between predators and prey is very likely to be a widespread
phenomenon among vertebrates and invertebrates (e.g.
Tuttle and Ryan, 1981;
Ryan, 1985;
Belwood and Morris, 1987), and
this report demonstrates such an interaction between a teleost species and a
mammal (see also Luczkovich et al.,
2000).
Detection of dolphin sounds
Bottlenose dolphins, as well as other toothed whales, use sound pulses
during prey searching, and echolocation clicks are emitted during foraging
dives (Johnson et al., 2004;
Miller et al., 2004). In
particular, bottlenose dolphins use echolocation clicks and low-frequency pops
when prey are in seagrass beds, at seagrass edges and over open sand
(Tyack and Clark, 2000;
Nowacek, 2005), and these are
the primary habitats for breeding (vocalizing) Gulf toadfish
(Sogard et al., 1989;
McMichael, 2002). The current
results indicate that male Gulf toadfish can detect low-frequency pops
employed by foraging dolphins and not high-frequency vocalizations, such as
whistles. Some teleost prey species can detect ultrasonic frequencies produced
by whales and dolphins (Mann et al.,
1997; Mann et al.,
1998; Mann et al.,
2001; Higgs et al.,
2004). However, the auditory frequency encoding of toadfishes is
most robust for 
1 kHz (see Introduction), which is consistent with the
utilization of low-frequency sounds in intra-specific communication in
toadfish. Our data indicate that toadfish detect the lowest-frequency
components of the pops produced by bottlenose dolphins and that they can use
this information to adjust advertisement calling.
Perception of dolphin sounds
Categorical perception has been defined as the "behavioral
segmentation of a stimulus that varies continuously along some physical
parameter" (Hoy,
1989). The current results suggest that Gulf toadfish employ
categorical perception of auditory cues, in which the valence of sounds is
encoded by a combination of frequency, repetition rate and pulse duration.
Field playback experiments with toadfish together demonstrate that acoustic
cues are divided into at least two categories: (1) stimulatory, such as the
advertisement boatwhistles of conspecific males
(Fish, 1972;
Remage-Healey and Bass, 2005),
and (2) suppressive, such as the foraging pops of bottlenose dolphins (current
study). This study also used a third playback stimulus, snapping shrimp pops,
which did not produce changes in toadfish vocal advertisement calls, despite
the fact that snapping shrimp pops and dolphin pops share a common frequency
range, peak intensity and pulse duration
(Table 1). It is important to
note that male toadfish emit individual grunts (30-75 ms duration) during
vocal advertisement bouts, and that grunts can be used to interrupt the
calling of neighbors in the closely-related O. tau
(Winn, 1972). The possibility
exists, therefore, that dolphin pops were perceived as acoustic signals of
competing male toadfish, which then resulted in reduced calling of focal
individuals in the current study. However, the temporal acoustic parameters of
grunts (30-75 ms duration, <1 Hz repetition rate) differ widely from
dolphin pops (Table 1).
Moreover, acoustic playbacks of synthesized grunt-like calls at a natural
repetition rate (1 grunt/3 s) to this same population of male toadfish did not
cause reductions in call rate or changes in plasma cortisol levels
(Remage-Healey and Bass,
2005). In addition, Winn
(Winn, 1972) observed that
calling was not significantly inhibited by grunt stimuli presented at
supra-normal rates (>1 Hz) in a field population of the closely-related
Opsanus tau. The importance of both pulse duration and inter-pulse
gaps for signal recognition is shown by playback studies with the
closely-related midshipman fish, Porichthys notatus
(McKibben and Bass, 1998;
McKibben and Bass, 2001). We
suggest, therefore, that Gulf toadfish are able to differentiate conspecific
grunts from dolphin foraging pops by temporal acoustic cues, including
duration and repetition rate.
Since repetition rate also differs between snapping shrimp pops and dolphin
pops in this study (Table 1),
repetition rate may be a critical parameter employed by toadfish to
distinguish harmless background noise from predator sounds. A critical test of
the above `categorical perception' hypothesis would be to present advertising
toadfish with synthesized dolphin pops at the elevated repetition rate
(
200 Hz) observed here for snapping shrimp sounds. Alternatively, the
critical parameter that distinguishes dolphin sounds from snapping shrimp pops
may be variability in repetition rate, as dolphin vocalizations occur at
highly variable rates during foraging bouts
(Cranford, 2000). The
repetition rate for snapping shrimp pops emitted by individuals is not well
understood (see Au and Banks,
1998), however, it is evident that the rate of pops emitted by
shrimp populations constitute a uniform background rate with little
fluctuation on a minute-by-minute time scale (see
Fig. 2)
Stress hormones and anti-predatory behavior
In principle, acute elevation in stress steroid hormones (glucocorticoids)
could be a proximate mechanism leading to the adjustment of advertisement
signals during predator encounters in male Gulf toadfish [for similar results
in roughskin newts see Orchinik et al.
(Orchinik et al., 2002)]. Both
stress hormones (cortisol) and androgens exert rapid and dramatic effects on
vocal patterning via actions on the central nervous system in
toadfishes (Remage-Healey and Bass,
2004; Remage-Healey and Bass,
2006). In addition, prior field work with Gulf toadfish has shown
that rapid (within minutes) elevations in male advertisement calling during
territorial challenges are due to similarly rapid actions of androgens on the
central nervous system (Remage-Healey and
Bass, 2005; Remage-Healey and
Bass, 2006). Glucocorticoids and androgens may function
differently to mediate the cost/benefit tradeoff between predation risk and
mate advertisement, respectively, in Gulf toadfish.
The current results do not indicate whether acute elevations in plasma
cortisol are directly responsible for reductions in calling behavior in male
toadfish. Indeed, non-invasive treatment with cortisol does not produce
significant changes in calling behavior in nesting males in the field
(Remage-Healey and Bass,
2006). However, the transition from a non-calling to a calling
state is accompanied by a several-fold increase in baseline cortisol levels
(Remage-Healey and Bass,
2005), although these levels do not reach the stress-induced
levels observed here. We previously hypothesized that this behavioral
state-dependent elevation in baseline cortisol levels would aid the
mobilization of energy reserves to support the physiological demands of high
calling rates (but see Amorim et al.,
2002), consistent with the stimulatory effects of cortisol on
fictive calls in the laboratory
(Remage-Healey and Bass, 2005;
Remage-Healey and Bass, 2006).
The results of the current study now suggest an inverted U-shaped function
between cortisol levels and calling behavior in toadfish, whereby only
mid-range, rather than sub-threshold and elevated levels of cortisol, can
facilitate calling [for comparable glucocorticoid effects in other systems see
Sapolsky et al. (Sapolsky et al.,
2000), Breuner and Wingfield
(Breuner and Wingfield, 2000)
and Clement et al. (Clement et al.,
2005)]. In addition, the current data emphasize the importance of
the auditory environment, together with hormone levels, in determining changes
in calling behavior. As observed with androgens and male-male aggressive
calling in this same species
(Remage-Healey and Bass,
2006), cortisol may not be sufficient for the suppression of
calling behavior in the absence of auditory stimuli, in this case predator
vocalizations.
As shown here for toadfish, experimental presentation of predators and
predator stimuli causes significant glucocorticoid elevation in other systems
(Blanchard et al., 1998;
Kagawa and Mugiya, 2000;
Plata-Salaman et al., 2000;
Kavaliers et al., 2001;
Canoine et al., 2002;
Cockrem and Silverin, 2002).
Predator exposure also causes behavioral responses that are similar to
behavioral changes observed during stress in lizards
(Van Damme and Quick, 2001)
and manted howler monkeys (Gil-da-Costa et
al., 2003). Furthermore, risk-taking behavior in mice is shifted
in the presence of predator odors, and this was accompanied by increases in
circulating corticosterone and decreases in circulating testosterone
(Kavaliers et al., 2001).
The well-documented acoustic startle response in flying insects is mediated
by auditory detection of predator cues by prey
(Hoy, 1989). Similarly, the
low-frequency, high-energy `pops' documented recently in foraging bottlenose
dolphins may be used to startle or flush fish prey species from nests or
hiding refuges (Nowacek,
2005). However, the current data suggest that dolphin foraging
pops also have consequences for detection by at least one prey species, male
Gulf toadfish. Lowfrequency dolphin foraging pops may be particularly
effective for use in habitats that scatter high-frequency echolocation clicks
such as seagrass and seagrass/sand edges
(Nowacek, 2005), but this
benefit is balanced against the potential costs of increased detection by
low-frequency `specialists' such as toadfish.
Startle behaviors generally occur in response to specific, noxious stimuli
and achieve fast reduction in conspicuousness, and the rapidity of these
responses depends on how fast prey must react to predators
(Bullock, 1984). The
stereotyped reduction in advertisement calling has been documented in katydids
as part of the acoustic startle response to bat echolocation signals
(Faure and Hoy, 2000).
Moreover, acute stress and the accompanying increases in plasma
glucocorticoids are associated with the acoustic startle response in rats
(Pryce et al., 2001).
Therefore, the current data are consistent with the hypothesis that some forms
of antipredator behavior have adapted existing neural mechanisms that link
startle responses with fast activation of `fight-or-flight' mechanisms,
including elevation in plasma glucocorticoids.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Amorim, M. C. P., McCracken, M. L. and Fine, M. L. (2002). Metabolic costs of sound production in the oyster toadfish, Opsanus tau. Can. J. Zool. - Rev. Can. Zool. 80,830 -838.
Au, W. W. L. (1993). The Sonar of Dolphins. New York, NY: Springer-Verlag.
Au, W. W. L. and Banks, K. (1998). The acoustics of the snapping shrimp Synalpheus parneomeris in Kaneohe Bay. J. Acoust. Soc. Am. 103,41 -47.[CrossRef]
Barros, N. B. (1993). Feeding Ecology and Foraging Strategies of Bottlenose Dolphins on the Central East Coast of Florida. PhD Thesis, University of Miami, Miami, USA.
Bass, A. H., Bodnar, D. A. and Marchaterre, M. A. (2001). Acoustic nuclei in the medulla and midbrain of the vocalizing gulf toadfish (Opsanus beta). Brain Behav. Evol. 57,63 -79.[CrossRef][Medline]
Belwood, J. J. and Morris, G. K. (1987). Bat
predation and its influence on calling behavior in neotropical katydids.
Science 238,64
-67.
Blanchard, R. J., Nikulina, J. N., Sakai, R. R., McKittrick, C., McEwen, B. and Blanchard, D. C. (1998). Behavioral and endocrine change following chronic predatory stress. Physiol. Behav. 63,561 -569.[CrossRef][Medline]
Bradbury, J. W. and Vehrencamp, S. L. (1998). Principles of Animal Communication. Sunderland, MA: Sinauer Associates.
Breuner, C. W. and Wingfield, J. C. (2000). Rapid behavioral response to corticosterone varies with photoperiod and dose. Horm. Behav. 37,23 -30.[CrossRef][Medline]
Bullock, T. H. (1984). Comparative neuroethology of startle, rapid escape, and giant-fiber mediated responses. In Neural Mechanisms of Startle Behavior (ed. R. C. Eaton), pp. 1-11. New York: Plenum.
Canoine, V., Hayden, T. J., Rowe, K. and Goymann, W. (2002). The stress response of European stonechats depends on the type of stressor. Behaviour 139,1303 -1311.[CrossRef]
Clement, T. S., Parikh, V., Schrumpf, M. and Fernald, R. D. (2005). Behavioral coping strategies in a cichlid fish: the role of social status and acute stress response in direct and displaced aggression. Horm. Behav. 47,336 -342.[CrossRef][Medline]
Clinchy, M., Zanette, L., Boonstra, R., Wingfield, J. C. and Smith, J. N. M. (2004). Balancing food and predator pressure induces chronic stress in songbirds. Proc. R. Soc. Lond. B Biol. Sci. 271,2473 -2479.[Medline]
Cockrem, J. F. and Silverin, B. (2002). Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen. Comp. Endocrinol. 125,248 -255.[CrossRef][Medline]
Connor, R. C. and Smolker, R. A. (1996). `Pop' goes the dolphin: a vocalization male bottlenose dolphins produce during consortships. Behaviour 133,643 -662.
Cranford, T. W. (2000). In search of impulse sound sources in odontocetes. In Hearing by Whales and Dolphins (ed. W. W. L. Au), pp. 109-155. New York: Springer.
Earley, R. L. and Dugatkin, L. A. (2002). Eavesdropping on visual cues in green swordtail (Xiphophorus helleri) fights: a case for networking. Proc. R. Soc. Lond. B Biol. Sci. 269,943 -952.[Medline]
Edds-Walton, P., Mangiamele, L. A. and Rome, L. C. (2002). Variations of pulse repetition rate in boatwhistle sounds from oyster toadfish Opsanus tau around Waquoit bay, Massachusetts. Bioacoustics 13,153 -173.
Endler, J. A. (1983). Natural and sexual selection on color patterns in Poeciliid fishes. Environ. Biol. Fishes 9,173 -190.
Endler, J. A. (1987). Predation, light-intensity and courtship behavior in Poecilia reticulata (Pisces, Poeciliidae). Anim. Behav. 35,1376 -1385.[CrossRef]
Endler, J. A. (1992). Signals, signal conditions, and the direction of evolution. Am. Nat. 139,S125 -S153.[CrossRef]
Evans, J. P., Kelley, J. L., Ramnarine, I. W. and Pilastro, A. (2002). Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 52,496 -502.[CrossRef]
Faure, P. A. and Hoy, R. R. (2000). The sounds of silence: cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae). J. Comp. Physiol. A Sens. Neural Behav. Physiol. 186,129 -142.[CrossRef][Medline]
Fay, R. R. and Edds-Walton, P. L. (2000). Frequency response of auditory brainstem units in toadfish (Opsanus tau). Biol. Bull. 199,173 -174.[Medline]
Fish, J. F. (1972). The effect of sound playback on the toadfish. In Behavior of Marine Animals. Vol. 2 (ed. H. E. Winn), pp.386 -434. New York: Plenum.
Fish, J. F. and Offutt, G. C. (1972). Hearing thresholds from toadfish, Opsanus tau, measured in laboratory and field. J. Acoust. Soc. Am. 51,1318 -1321.[CrossRef][Medline]
Forsgren, E. and Magnhagen, C. (1993). Conflicting demands in sand gobies - predators influence reproductive behavior. Behaviour 126,125 -135.
Gannon, D. P., Barros, N. B., Nowacek, D. P., Read, A. J., Waples, D. M. and Wells, R. S. (2005). Prey detection by bottlenose dolphins, Tursiops truncatus: an experimental test of the passive listening hypothesis. Anim. Behav. 69,709 -720.[CrossRef]
Gil-da-Costa, R., Palleroni, A., Hauser, M. D., Touchton, J. and Kelley, J. P. (2003). Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proc. R. Soc. Lond. B Biol. Sci. 270,605 -610.[Medline]
Gray, G. A. and Winn, H. E. (1961). Reproductive ecology and sound production of toadfish, Opsanus tau.Ecology 42,274 -282.[CrossRef]
Higgs, D. M., Plachta, D. T. T., Rollo, A. K., Singheiser, M.,
Hastings, M. C. and Popper, A. N. (2004). Development of
ultrasound detection in American shad (Alosa sapidissima).
J. Exp. Biol. 207,155
-163.
Hoy, R. R. (1989). Startle, categorical response, and attention in acoustic behavior of insects. Annu. Rev. Neurosci. 12,355 -375.[CrossRef][Medline]
Janik, V. M. (2000). Source levels and the estimated active space of bottlenose dolphin (Tursiops truncatus) whistles in the Moray Firth, Scotland. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 186,673 -680.[CrossRef][Medline]
Janik, V. M., Sayigh, L. S. and Wells, R. S.
(2006). Signature whistle shape conveys identity information to
bottlenose dolphins. Proc. Natl. Acad. Sci. USA
103,8293
-8297.
Johnson, M., Madsen, P. T., Zimmer, W. M. X., de Soto, N. A. and Tyack, P. L. (2004). Beaked whales echolocate on prey. Proc. R. Soc. Lond. B Biol. Sci. 271,S383 -S386.
Kagawa, N. and Mugiya, Y. (2000). Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. Zool. Sci. 17,1061 -1066.[CrossRef]
Kavaliers, M., Choleris, E. and Colwell, D. D. (2001). Brief exposure to female odors `emboldens' male mice by reducing predator-induced behavioral and hormonal responses. Horm. Behav. 40,497 -509.[CrossRef][Medline]
Koga, T., Backwell, P. R. Y., Jennions, M. D. and Christy, J. H. (1998). Elevated predation risk changes mating behaviour and courtship in a fiddler crab. Proc. R. Soc. Lond. B Biol. Sci. 265,1385 -1390.[CrossRef]
Luczkovich, J. J., Daniel, H. J., Hutchinson, M., Jenkins, T., Johnson, S. E., Pullinger, R. C. and Sprague, M. W. (2000). Sounds of sex and death in the sea: bottlenose dolphin whistles suppress mating choruses of silver perch. Bioacoustics 10,323 -334.
Mann, D. A., Lu, Z. M. and Popper, A. N. (1997). A clupeid fish can detect ultrasound. Nature 389,341 .[CrossRef]
Mann, D. A., Lu, Z. M., Hastings, M. C. and Popper, A. N. (1998). Detection of ultrasonic tones and simulated dolphin echolocation clicks by a teleost fish, the American shad (Alosa sapidissima). J. Acoust. Soc. Am. 104,562 -568.[CrossRef][Medline]
Mann, D. A., Higgs, D. M., Tavolga, W. N., Souza, M. J. and Popper, A. N. (2001). Ultrasound detection by clupeiform fishes. J. Acoust. Soc. Am. 109,3048 -3054.[CrossRef][Medline]
McKibben, J. R. and Bass, A. H. (1998). Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. J. Acoust. Soc. Am. 104,3520 -3533.[CrossRef][Medline]
McKibben, J. R. and Bass, A. H. (2001). Effects of temporal envelope modulation on acoustic signal recognition in a vocal fish, the plainfin midshipman. J. Acoust. Soc. Am. 109,2934 -2943.[CrossRef][Medline]
McMichael, R. (2002). Fisheries-independent Monitoring Program 2002 Annual Data Summary Report, pp. A14-A30. St Petersburg, FL: Florida Marine Research Institute.
Miller, P. J. O., Johnson, M. P. and Tyack, P. L. (2004). Sperm whale behaviour indicates the use of echolocation click buzzes `creaks' in prey capture. Proc. R. Soc. Lond. B Biol. Sci. 271,2239 -2247.[Medline]
Mougeot, F. and Bretagnolle, V. (2000). Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals. Anim. Behav. 60,647 -656.[CrossRef][Medline]
Myrberg, A. A. (1981). Sound communication and interception in fishes. In Hearing and Sound Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay), pp.395 -426. New York: Springer-Verlag.
Nowacek, D. P. (2005). Acoustic ecology of foraging bottlenose dolphins (Tursiops truncatus), habitat-specific use of three sound types. Mar. Mamm. Sci. 21,587 -602.[CrossRef]
Orchinik, M., Gasser, P. and Breuner, C. (2002). Rapid corticosteroid actions on behavior: cellular mechansims and organismal consequences. In Hormones, Brain and Behavior. Vol. 3 (ed. D. W. Pfaff), pp.567 -600. San Diego: Elsevier.
Plata-Salaman, C. R., Ilyin, S. E., Turrin, N. P., Gayle, D., Flynn, M. C., Bedard, T., Merali, Z. and Anisman, H. (2000). Neither acute nor chronic exposure to a naturalistic (predator) stressor influences the interleukin-1 beta system, tumor necrosis factor-alpha, transforming growth factor-beta 1, and neuropeptide mRNAs in specific brain regions. Brain Res. Bull. 51,187 -193.[CrossRef][Medline]
Pryce, C. R., Bettschen, D., Bahr, N. I. and Feldon, J. (2001). Comparison of the effects of infant handling, isolation, and nonhandling on acoustic startle, prepulse inhibition, locomotion, and HPA activity in the adult rat. Behav. Neurosci. 115, 71-83.[CrossRef][Medline]
Remage-Healey, L. and Bass, A. H. (2004).
Rapid, hierarchical modulation of vocal patterning by steroid hormones.
J. Neurosci. 24,5892
-5900.
Remage-Healey, L. and Bass, A. H. (2005). Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in Gulf toadfish. Horm. Behav. 47,297 -305.[CrossRef][Medline]
Remage-Healey, L. and Bass, A. H. (2006). From social behavior to neural circuitry: steroid hormones rapidly modulate advertisement calling via a vocal pattern generator. Horm. Behav. 50,432 -441.[CrossRef][Medline]
Rukstalis, M. and French, J. A. (2005). Vocal buffering of the stress response: exposure to conspecific vocalizations moderates, urinary cortisol excretion in isolated marmosets. Horm. Behav. 47,1 -7.[CrossRef][Medline]
Ryan, M. J. (1985). The Tungara Frog. A Study in Sexual Selection and Communication. Chicago, IL: University of Chicago Press.
Sapolsky, R. M., Romero, L. M. and Munck, A. U.
(2000). How do glucocorticoids influence stress responses?
Integrating permissive, suppressive, stimulatory, and preparative actions.
Endocr. Rev. 21,55
-89.
Sogard, S. M., Powell, G. V. N. and Holmquist, J. G. (1989). Utilization by fishes of shallow, seagrass-covered banks in Florida Bay. 1. Species composition and spatial heterogeneity. Environ. Biol. Fishes 24, 53-65.
Tavolga, W. N. (1958). Underwater sounds produced by two species of toadfish, Opsanus tau and Opsanus beta. Bull. Mar. Sci. Gulf Carrib. 8, 278-284.
Thorson, R. F. and Fine, M. L. (2002a). Acoustic competition in the gulf toadfish Opsanus beta: acoustic tagging. J. Acoust. Soc. Am. 111,2302 -2307.[CrossRef][Medline]
Thorson, R. F. and Fine, M. L. (2002b). Crepuscular changes in emission rate and parameters of the boatwhistle advertisement call of the gulf toadfish, Opsanus beta. Environ. Biol. Fishes 63,321 -331.[CrossRef]
Tuttle, M. D. and Ryan, M. J. (1981). Bat
predation and the evolution of frog vocalizations in the neotropics.
Science 214,677
-678.
Tyack, P. L. and Clark, C. W. (2000). Communication and acoustic behavior of dolphins and whales. In Hearing by Whales and Dolphins (ed. W. W. L. Au), pp.156 -224. New York: Springer.
Van Damme, R. and Quick, K. (2001). Use of predator chemical cues by three species of lacertid lizards (Lacerta bedriagae, Podarcis tiliguerta, and Podarcis sicula). J. Herpetol. 35,27 -36.
Versluis, M., Schmitz, B., von der Heydt, A. and Lohse, D.
(2000). How snapping shrimp snap: through cavitating bubbles.
Science 289,2114
-2117.
Winn, H. E. (1972). Acoustic discrimination by the toadfish with comments on signal systems. In Behavior of Marine Animals; Current Perspectives in Research (ed. H. E. Winn and B. L. Olla), pp. 361-385. New York: Plenum Press.
Yan, H. Y., Fine, M. L., Horn, N. S. and Colon, W. E. (2000). Variability in the role of the gasbladder in fish audition. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 186,435 -445.[CrossRef][Medline]
Zuk, M. and Kolluru, G. R. (1998). Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73,415 -438.[CrossRef]
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  Y. Hager EAVESDROPPING TO STAY ALIVE J. Exp. Biol., November 15, 2006; 209(22): i - ii. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
