Individual voices in a cluttered soundscape: acoustic ecology of the Bocon toadfish, Amphichthys cryptocentrus - Erica Staaterman
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Environ Biol Fish
https://doi.org/10.1007/s10641-018-0752-0
Individual voices in a cluttered soundscape: acoustic ecology
of the Bocon toadfish, Amphichthys cryptocentrus
Erica Staaterman & Simon J. Brandl & Michelle Hauer &
Jordan M. Casey & Austin J. Gallagher & Aaron N. Rice
Received: 21 July 2017 / Accepted: 20 March 2018
# Springer Science+Business Media B.V., part of Springer Nature 2018, corrected publication April/2018
Abstract Toadfishes (family Batrachoididae) are a well- recorded fourteen individuals in a seagrass habitat over
studied family of soniferous fishes, yet only a fraction of six nights in the Bocas del Toro Archipelago. Like other
species within the family have been recorded, and only toadfishes, A. cryptocentrus produces compound calls
few detailed descriptions of calls exist. Here, we present with broadband and tonal components; a typical call
the first description of the acoustic ecology of contains 1–2 grunts, followed by 1–2 boops (average
Amphyichtys cryptocentrus, a new-world toadfish species, fundamental frequency=112 Hz, average source level=
distributed across the southern Caribbean Sea. We 138 dB re:1 μPa RMS). While we observed relatively low
between-individual variation in frequency components,
our results show that individuals can be readily identified
E. Staaterman (*) : S. J. Brandl : M. Hauer based on their call composition and call rate. This sug-
Tennenbaum Marine Observatories Network, Smithsonian gests that each toadfish has an individual Bvoice,^ which
Environmental Research Center, Edgewater, MD 21037, USA may transmit selection-linked information to females
e-mail: staatermane@si.edu
about body condition, status, or motivation to mate. We
J. M. Casey also observed that toadfish produced grunts during neigh-
Department of Invertebrate Zoology, National Museum of Natural bors’ calls, a previously-described aggressive behavior
History, Smithsonian Institution, Washington, DC 20560, USA called Bacoustic tagging^, which can intercept a potential
E. Staaterman : A. J. Gallagher rival’s mating advertisement. Our findings suggest that
Beneath the Waves, Inc., Herndon, VA 20172, USA A. cryptocentrus (and its population in Bocas del Toro, in
particular) represents a useful system for the study of fish
E. Staaterman : S. J. Brandl : A. J. Gallagher bioacoustics and behavioral ecology, and we demonstrate
Smithsonian Tropical Research Institute, Bocas del Toro, Panama
that acoustic communication represents a major aspect of
A. N. Rice social behavior in coral reef fishes.
Bioacoustics Research Program, Cornell Laboratory of
Ornithology, Cornell University, Ithaca, NY 14850-1999, USA
Keywords Toadfish . Batrachoididae . Acoustic
communication . Sound propagation . Individual
Present Address: recognition
E. Staaterman
Bureau of Ocean Energy Management, Sterling, VA 20166,
USA
Introduction
Present Address:
S. J. Brandl
Earth to Ocean Research Group, Department of Biological Fishes of the family Batrachoididae (toadfish and mid-
Sciences, Simon Fraser University, Burnaby, BC, Canada shipman) have been well studied due to their specialized
Environ Biol Fish
vocal organ and their prolific and complex acoustic be- (O. beta and O. tau), males deliberately produce grunts
haviors (e.g., Brantley and Bass 1994; dos Santos et al. during other males’ harmonic advertisement calls, a
2000; Mosharo and Lobel 2012; Rice and Bass 2009; phenomenon called Bacoustic tagging^ (Mensinger
Tavolga 1958). Although there are over 70 species within 2014; Thorson and Fine 2002a). These agonistic acous-
the family (Greenfield et al. 2008), sounds from only five tic interactions may be used to assert dominance, to
genera and eight species have been described in detail interrupt neighbors’ signals, or to redirect the attention
(reviewed in Mosharo and Lobel 2012; Rice and Bass of a nearby female. It is unclear how widespread acous-
2009). While it is likely that sound production is wide- tic tagging behaviors are for other species within
spread, if not universal, among toadfishes, our capacity to Batrachoididae.
understand the evolution and diversity of acoustic com- In the present study, we provide the first descriptions
munication in this family, and for teleost fishes in general, of acoustic behaviors of the Bocon toadfish,
requires detailed descriptions of acoustic behaviors in Amphichthys cryptocentrus (Valenciennes), a species
many species and in various habitats. that is distributed across the southern Caribbean and
Sounds from four toadfish species have been exten- northern part of South America (Hoffman and
sively studied: the Lusitanian toadfish (Halobatrachus Robertson 1983; Collette 2002). A high-density popu-
didactylus), the oyster toadfish (Opsanus tau), the Gulf lation of nesting males adjacent to the dock of the
toadfish (O. beta), and the plainfin midshipman Smithsonian Tropical Research Institute in Bocas del
(Porichthys notatus) (e.g., Brantley and Bass 1994; dos Toro, Panamá provided a unique opportunity to describe
Santos et al. 2000; Gray and Winn 1961; Tavolga 1958; the calling behavior through in situ recordings of multi-
Vasconcelos et al. 2012). For these species, investigators ple individuals over several days. Since this species
found that male toadfishes establish nests under hard reproduces year-round (Granado and Gonzalez 1988),
substrates at the beginning of the breeding season, where we were able to evaluate acoustic behaviors associated
they typically produce low-frequency harmonic calls to with courtship advertisements. Our goals were to (1)
attract females (Gray and Winn 1961; Tavolga 1958; describe the acoustic behavior of this species, (2) to
Winn 1972). These sounds are produced by sonic muscles compare this species’ acoustic parameters to other toad-
that surround the swim bladder. The fundamental frequen- fish genera, and (3) to determine the individuality of
cy is determined by the muscle contraction rate; therefore, calls produced by different males based on a range of
these Bboat whistle^ vocalizations vary for each species call parameters. We hypothesized that due to the rela-
and at different temperatures (e.g., Bass and Rice 2010; tively dense occurrence of A. cryptocentrus individuals
Fine 1978; Fine et al. 2001; McKibben and Bass in this location, their acoustic signals contain sufficient
1998).The sonic muscles are driven by evolutionarily- information to be individually distinct, thus creating an
conserved vocal motor neurons in the hindbrain (Bass acoustic landscape that female toadfishes can navigate
et al. 1994, 2008; Bass and McKibben 2003; Chagnaud based on mate choice.
and Bass 2014). Due to considerable knowledge of the
behavior and physiology of their communication, toadfish
have served as a model system for understanding acoustic Materials and methods
communication and the underlying physiological mecha-
nisms in fishes and vertebrates more broadly. Data collection
While male advertisement calls have received the
most attention from researchers, acoustic signals are also All recordings took place near the Smithsonian Tropical
used in aggressive and territorial contexts. For many Research Institute’s field station in the Bocas del Toro
years it was assumed that the sole function of the boat archipelago on the Caribbean side of Panamá (Fig. 1a).
whistles was to attract females, but Vasconcelos et al. The research station is located on the edge of a bay
(2010) showed that boat whistles were also produced in (water depth: 0.5–10 m) lined with mangroves and
response to intruders, suggesting that they may mediate covered in seagrass beds, which gradually progresses
both inter- and intrasexual interactions (Bass and into coral reef habitat. Two parallel intake pipes from the
McKibben 2003). In addition, both males and females aquarium system run perpendicular from shore into the
are known to produce short broadband Bgrunts^ that bay for a distance of 98 m (Fig. 1b). Each pipe is
may be agonistic in nature. In two Opsanus species supported by cinder blocks positioned approximately
Environ Biol Fish
A) C)
5 km
Isla Colón
STRI
PANAMÁ
Isla
Bastimentos
D)
Isla
Cristóbal
1 cm
B) LEGEND
2m
E)
sampled
occupied N
unoccupied
E
D
F
G
H
SEAGRASS BED
98 m
K
A
STRI DOCK
L
J
23 m N
B
C
I
1m
M MANGROVE
Fig. 1 a Map of the study area at the Smithsonian Tropical recordings, grey burrows denote those that were occupied by
Research Institute (STRI) station in Bocas del Toro, Panamá toadfish but not recorded, and white boxes mark empty burrows.
(Caribbean Sea), where two parallel intake pipes b run from the c Adult Amphichthys cryptocentrus pictured next to one of the
research station into a shallow bay, spanning a water depth of intake pipes. d Juvenile A. cryptocentrus collected during a con-
0.5 m – 4 m. Each square on the figure represents a cinder block, current research project. e Habitat surrounding the two parallel
thus representing a potential toadfish burrow. Red, labeled bur- intake pipes
rows correspond to burrows at which we made acoustic
2–4 m apart, which provide habitat for a large popula- avoid repeated sampling. Recorders were anchored
tion of the Bocon toadfish (Fig. 1c–e). To establish on cinder blocks and positioned 1 m from the focal
baseline information about the toadfish distribution, burrow and 20 cm off the sand, and water depth
we snorkeled along the pipes over several sequential varied from 1.0–4.0 m along the pipeline. The snor-
days, noting which cinder blocks harbored individuals. kelers left the area as soon as the hydrophones were
We used four passive acoustic recorders (DSG, deployed. Recordings lasted between 12 and 20 h.
Loggerhead Instruments, Sarasota FL, equipped On the following day, we retrieved the hydrophones,
with an HTI-96-min hydrophone, sample rate: off-loaded the data, and moved them to new bur-
5 kHz, sensitivity: −150 dBV/μPa) to record the rows. During retrieval, we verified that the fish were
toadfish in their habitat over six nights. Within an still present in their burrows, which was always the
hour of sunset, a team of snorkelers identified occu- case. Recordings took place between 20 February
pied burrows for sampling and marked them to and 3 March 2016, and water temperature rangedEnviron Biol Fish from 27.2–29.2 °C (Bocas del Toro meteorological for tonal sounds represents the first harmonic, while station: http://biogeodb.stri.si.edu/physical_ peak frequency is the frequency containing the greatest monitoring/research/bocas). acoustic energy; these two measurements are not always We time-synchronized the four recordings from equal. By zooming into the waveform of the middle- each night by matching sounds from external boop section, we counted the number of cycles within sources (e.g., human voices prior to deployment) this short time interval to calculate fundamental frequen- and importing them into Matlab (The Mathworks, cy (FF=# cycles/time) in a way that was not sensitive to Inc., Natick, MA) to create synchronous four- changes in FFT size in the spectrographic representation channel recordings. Using Raven Pro 1.4 Sound of the sounds. In a similar manner, we manually counted Analysis Software (Bioacoustics Research Program the number of cycles within each preceding grunt to 2012), we visualized each four-channel recording to obtain its fundamental frequency, although due to the identify calls from individual fish. We assumed that broadband nature of the grunts, this metric was less the calls with the highest received level recorded on precise (Fig. 2d). Using the characterized sensitivity of each hydrophone were produced by the individual in the recorders, calibrated measurements for Root-Mean- the focal burrow (typically 140–150 dB re:1 μPa Square (RMS) and maximum amplitude were converted RMS). However, in some cases, calls had lower into dB re:1 μPa. For the eight individuals that produced sound levels (
Environ Biol Fish
Table 1 Meta-data for each of the 14 toadfish individuals included in this study
Burrow Recording date Distance from shore (m) In focal burrow? # of calls measured Call rate measured? Comments
A Feb 27–28 43.7 No 17 No Offspring present
B Feb 27–28 ~15.9 No 21 No
C Feb 27–28 11.5 Yes 17 No
D Feb 28–29 76.6 No 18 Yes
E Feb 28–29 78.8 Yes 19 Yes Offspring present
F Feb 29-Mar 1 70.5 Yes 18 Yes
G Feb 29-Mar 1 67.8 Yes 20 Yes
H Feb 29-Mar 1 61.6 Yes 18 Yes
I Mar 1–2 8.0 Yes 18 Yes
J Feb 20–21 ~15.0 Yes 12 Yes Not in pipes area
K Feb 21–22 ~46.5 No 14 No
L Feb 21–22 ~25.8 Yes 15 No
M Feb 27–28 0.0 No 14 No
N Mar 1–2 20.0 No 12 Yes
The letters for burrows match those in Fig. 1 and refer to the burrows where hydrophones were placed. Reliable assignment of the recorded
calls to focal animals within the monitored burrows was possible in eight out of 14 cases, but this was not possible in the other six cases. We
only measured call rates when hydrophones were deployed before the start of the evening chorus
We used the coefficient of variation (CV; the dimen- calling vigorously and repetitively just after sunset and
sionless ratio of the standard deviation to the mean), to continued calling for several hours (~18:45–21:00 local
understand which components of the calls had the time), which was consistent with patterns from other
greatest variability within and between individuals. Fol- marine soundscapes in the region (Staaterman et al.
lowing Amorim and Vasconcelos (2008), we calculated 2017). To observe the rate at which individuals pro-
the CV for each call parameter for each individual, duced complete calls (preceding grunts plus boops),
which represents the within-individual variation isolated grunts, and tagging grunts throughout this
(CVW). We also calculated the CV of all calls by divid- nightly chorus, we collected additional data from eight
ing the standard deviation by the global mean, which individuals whose recording window began before the
represents the between-individual variation (CVB). chorus started. From 18:00–22:00 local time, we count-
When the ratio of CVB:CVW is large, it suggests that ed the number of boops and grunts (isolated and tagging
the acoustic parameter may be used for individual rec- grunts, but excluding preceding grunts) per minute in
ognition (Bee and Gerhardt 2001). Finally, to determine 10-min intervals. In addition, due to the close proximity
whether there were any differences between parameters of individuals F-H, we were able to observe acoustic
for different parts of a call (i.e., boop 1 and boop 2), we tagging behavior on a fine scale by counting how many
used paired sample t-tests. times each of these three individuals tagged his imme-
diate neighbors. We also calculated the received level of
Quantifying acoustic behaviors boops and grunts at these three burrows to measure the
transmission loss associated with the two sound types.
Throughout our analyses, we observed that toadfish To visualize the typical acoustic patterns observed
occasionally produced grunts that did not always pre- throughout the night in this toadfish habitat, we created
cede boops (Fine and Thorson 2008; Fine and a ~20 h spectrogram. This spectrogram includes data from
Waybright 2015). These grunts either occurred in isola- a recording made in the middle of the intake pipe area, but
tion or directly overlapping with neighbors’ boops, a one in which only distant individuals were audible (i.e.,
phenomenon called Bacoustic tagging,^ which has been this data is not included elsewhere in the manuscript). We
observed in Opsanus beta and O. tau (Thorson and Fine calculated Power Spectral Density in 1-Hz bins and plot-
2002a). We also observed that the toadfish started ted it over the ~20 h time window (Fig. 8).Environ Biol Fish
boop 1
A grunts boop 2
M.B. M.B.
amplitude
Relative swoop
B I.G.I. G.B.I. B.I.
1600
Frequency (Hz)
1200
800
400
F0
0
0 0.4 0.8 1.2 1.6 2.0 2.4 2.8 3.2 3.6
Time (sec)
C grunt
D
amplitude
Relative
0.00 0.05 0 0.5 1.0 1.5 2.0 2.5
0.01 0.02 0.03 0.04 0.06 0.07
E boop F
amplitude
Relative
0 0.5 1.0 1.5 2.0 2.5
0.00 0.01 0.02 0.03 0.04 0.05
Time (sec) Frequency (kHz)
Fig. 2 A typical advertisement call from Amphichthys absolute, amplitude. F0 =Fundamental frequency of the boop (the
cryptocentrus. a: waveform; b: spectrogram; c: zoomed-in wave- first harmonic); I.G.I=inter-grunt interval; G.B.I. = grunt-boop
form of a grunt; d: power spectrum of the grunt; e: zoomed-in interval; B.I. = boop interval; M.B. = middle section of the boop,
waveform of a 50 ms middle-boop (M.B.) portion of call; f: power from which we obtained frequency and amplitude measurements
spectrum of the middle-boop. Y-axes are given in relative, not
Results due to their broadband nature, this metric was difficult to
quantify and is not as meaningful. Peak frequency of the
Call characteristics grunts was higher than the boops (paired t-test, t=7.5,
df=232, pEnviron Biol Fish
Table 2 Parameters of toadfish calls that were measured, including the global average and global standard deviation for all calls (n=233)
Call parameter Units Meaning Average S.D.
Number of preceding grunts Count # of grunts that occurred before the first boop 1.22 0.45
Number of boops Count # of boops in the Bcall^ 1.38 0.59
Grunt duration ms Duration of grunt 50.91 9.14
Grunt peak frequency Hz Frequency with the most energy 165.5 46.5
Grunt fundamental frequency Hz Lowest frequency 124.65 23.24
Grunt maximum amplitude dB (re: 1 μPa) Maximum amplitude 149.55 1.12
(source level)
Grunt RMS amplitude dB (re: 1 μPa) Average amplitude 138.26 14.64
(source level)
Inter-grunt interval ms Time between grunts (if applicable) 608.10 48.84
Grunt-boop interval ms Time between last grunt and first boop 289.72 198.42
Boop duration ms Duration of entire boop 1327.10 341.65
Boop peak frequency Hz Frequency with the most energy (measured 140.9 47.66
from middle portion of boop)
Boop fundamental frequency Hz Lowest frequency=frequency of first harmonic 112.43 3.90
(measured from middle portion of boop)
Boop maximum amplitude dB (re: 1 μPa) Maximum amplitude (measured from middle 147.49 2.41
(source level) portion of boop)
Boop RMS amplitude dB (re: 1 μPa) Average amplitude (measured from middle 138.03 14.71
(source level) portion of boop)
Boop interval ms Time between boops (if applicable) 282.10 157.6
Here, we only report values for the first grunts and first boops of the calls. Seventy-eight percent of the calls had only one preceding grunt,
and 67% of the calls had only one boop. Amplitude measurements reported here can be classified as Bsource level^, as we only included
amplitude data from the eight individuals that were calling at 1 m distance from the hydrophone (n=138 calls)
When individuals produced a second or third boop, Specifically, there was clear separation of individuals on
they were always shorter in duration than the first (first the nMDS ordination that focused on boop parameters
boop mean: 1327.1±314.6 ms, second boop mean: 514.9 only, with individual ID explaining 79% of the variance
±102.5 ms, third boop mean: 363.4±25.0 ms). The first (Fig. 4a, PERMANOVA: F=63.56; R2 =0.791; pEnviron Biol Fish
A D 1.0 m from source
Boop 1 Peak Frequency (Hz)
2000
200 1000
0
0 0.5 1.0
150
2.7 m from source
2000
100
Frequency (Hz)
1000
95 100 105 110 115 120
0
Boop 1 Fundamental Frequency (Hz) 0 0.5 1.0
3.0 m from source
B Nearby fish (F) C Distant fish (M) 2000
2400 2400 1000
Frequency (Hz)
Frequency (Hz)
2000 2000 0
1600 1600 0 0.5 1.0
1200 1200 8.9 m from source
800 2000
800
400 400 1000
0 0
0 1.0 2.0 0 1.0 0
Time (sec) Time (sec) 0 0.5 1.0
Time (sec)
Fig. 3 Effects of distance on spectral composition of toadfish environment and distance of certain individuals to the hydro-
calls. Panel a: For most of the calls measured, the fundamental phones, as very shallow water limits the transmission of the lowest
frequency and peak frequency of the boops were equal, which frequencies (Urick 1983). Panel d illustrates this phenomenon for
means that the first harmonic had the most energy (red arrow in a single toadfish call that was received on four hydrophones: with
panel b). For more distant individuals (Panel c), the second har- increasing distance from the fish, less energy is present in the
monic (red arrow) had more energy than the first, so peak frequen- lowest harmonic as well as the higher harmonics. In panel
cy was equal to twice the fundamental frequency. This result can d, Broadband tags from neighbors are also evident between 0.3–
be explained by the interaction between the physics of the 0.6 s
preceding grunts had higher variation in spectral param- Some individuals (G, H, J) produced nearly equal num-
eters both within and between individuals. CVw for peak bers of boops and tagging grunts over the course of four
frequency was 18.8%, and for fundamental frequency it hours, while others produced almost three times as
was 14.0%; CVB for peak frequency was 28.1%, and for many grunts as boops (F: 64 boops, 226 grunts; I: 24
fundamental frequency it was 18.7%. The traits with boops, 139 grunts). We calculated the percentage of total
the highest coefficients of variation related to call grunts used for tagging (# of tagging grunts/ (# of
composition: the number of boops, number of preced- preceding grunts + tagging grunts)) and found a range
ing grunts, inter-grunt interval, grunt-boop interval, across individuals, with a minimum of 50% of total
boop duration, and inter-boop interval (Fig. 5a). grunts used for tagging (D: 70%, E: 97%, F: 77%, G:
60%, H: 55%, I: 85%, J: 50%, N: 75%). Individual J,
Calling behaviors which was living in isolation at least 23 m from the other
burrows (Fig. 1), had the lowest call rate, with a total of
Call rates and usage of grunts by eight focal individuals 35 boops and 35 grunts.
showed substantial variation (Fig. 6); they produced a Three closely neighboring toadfish provided addi-
range of 3 to 12 boops/min, and 5 to 27 grunts/min. tional insight into acoustic behaviors at a finer spatialEnviron Biol Fish
A. Boops only B. Boops and grunts
0.3
0.3
C N H E
F C
H D
B
I F
0.0
E
0.0
G A N
A L D J
M G K
J L
I
B K M
−0.3
−0.3
−0.5 0.0 0.5 −0.5 0.5
0.0
A B C D E F G H I J K L M N
Fig. 4 Non-metric multidimensional scaling ordinations (nMDS) parameters shows clear separation of individuals; a
of toadfish call parameters revealed clear clustering of calls. Note: PERMANOVA on the distance matrix underlying this ordination
This analysis included spectral and temporal parameters, but not explained 79% of the variance. b An ordination of boop and grunt
amplitude parameters, since amplitude depended on the distance parameters together; a PERMANOVA on this distance matrix
of each individual to the hydrophone and was not necessarily a explained only 54% of the variance, suggesting that boops contain
true indicator of animal behavior. a An ordination of boop more individual-specific traits
and temporal resolution, and an example of their Discussion
behaviors is shown in Fig. 7. Individuals F, G, and
H were spaced only a few meters apart, and while F Amphichthys cryptocentrus individuals recorded at our
and H shared many acoustic parameters (Fig. 4), G study site began calling en masse shortly after sunset
was more isolated in multi-dimensional space, likely and continued for several hours, substantially elevating
due to its exceptionally long boop interval (Fig. 5f). sound levels in the seagrass bed during their nightly
Individual G, whose burrow was in between F and H, chorus (Fig. 8). This pattern was repeated across all six
tagged F and H equally (five times each). Individual F nights of our study, and was consistent with soundscape
produced the most grunts (226 in total). Many of these patterns observed in other coastal habitats in the Bocas
grunts were tags on more distant neighbors, but 67 d e l To r o r e g i o n ( S t a a t e r m a n e t a l . 2 0 1 7 ) .
were tags on H, while only 16 tags were during calls A. cryptocentrus follow a pattern of acoustic signal
from individual G. Individual H tagged F 18 times, structures common among the Batrachoididae, with at
but only tagged G three times. The low overall call least two sound types: one with a broadband frequency
rate of individual G, as well as its distinct acoustic structure (grunts), and another with harmonic compo-
characteristics, may have reduced the tagging load it nents (boops). Rather than requiring an extensive vocal
received from its neighbors. repertoire, the temporal arrangement and combination of
The calls of these three individuals were detected these components (e.g., number of grunts, spacing be-
on several hydrophones, allowing us to measure the tween boops) may confer different behavioral information,
received levels of grunts and boops at each burrow as seen in Halobatrachus didactylus (Amorim et al. 2008).
(Fig. 7). We observed greater transmission loss (lower Compared to the properties of the harmonic seg-
received levels) for boops than for grunts. A boop ments of other toadfish calls (summarized in
produced by F experienced 10.3 dB transmission loss Table 1 in Mosharo and Lobel 2012), the peak
before arriving at G (2.7 m distance), and 22.8 dB of and fundamental frequencies for A. cryptocentrus
transmission loss before arriving at H (8.9 m dis- are considerably lower than those reported for other
tance). Likewise, a boop produced by H experienced toadfish. The fundamental frequency of toadfish
a 13.5 dB transmission loss before arriving at G, and calls is determined by the pacemaker neurons
24.5 dB before arriving at F. In contrast, grunts expe- (Chagnaud et al. 2011), which sets the firing rate
rienced far less transmission loss: a 4.6 dB loss from F of vocal motor neurons and the contraction speed
to G, and 12.3 dB from F to H (Fig. 7e). of the swimbladder muscle (Bass et al. 1994;Environ Biol Fish
A
0.9
pregrunt 1 pregrunt 2 boop 1 within individuals
0.8 between individuals
boop 2 boop 3
Coefficient of Variation
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Peak Freq
Peak Freq
# boops
Fund Freq
Fund Freq
# grunts
Peak Freq
Fund Freq
grunt-boop interval
inter-boop interval
inter-boop interval
boop 1 duration
Fund Freq
Fund Freq
inter-grunt interval
boop 2 duration
grunt 1 duration
Peak Freq
boop 3 duration
grunt 2 duration
Peak Freq
B 3.5
# boops C 1800 D 1800
inter-grunt interval (ms)
grunt-boop interval (ms)
# grunts
3 1600 1600
1400 1400
2.5
number
1200 1200
2 1000 1000
800 800
1.5
600 600
1 400 400
200 200
0.5
A B C D E F G H I J K L M N A B CD E FGH I J K L MN A B CD E FGH I J K L MN
E 1800 F 1800 G 1800
inter-boop interval (ms)
boop 1 duration (ms)
boop 2 duration (ms)
1600 1600 1600
1400 1400 1400
1200 1200 1200
1000 1000 1000
800 800 800
600 600 600
400 400 400
200 200 200
A B CD E FGH I J K L MN A B CD E FGH I J K L MN A B CD E FGH I J K L MN
Fig. 5 Intraspecific variation in call parameters. Panel a: Blue composition had the highest variance. Panels b–g: individual
dots: average values of within-individual Coefficient of Variation average±95% confidence intervals for the call parameters with
(CVw) across all individuals; Red triangles: between-individual the highest variance. b: number of boops (red) and number of
variation (CVB) which was calculated by dividing the standard grunts (blue); c: inter-grunt interval; d: grunt-boop interval; e:
deviation by the global mean. Call parameters that related to call boop 1 duration; f: inter-boop interval; g: boop 2 durationEnviron Biol Fish
30 # grunts =183 30 # grunts =112 30 # grunts =226 30 # grunts =27
D # boops =84 E # boops =38
F # boops =64 G # boops =23
number/minute
grunts
20 20 20 20 boops
10 10 10 10
0 0 0 0
18:00 20:00 22:00 18:00 20:00 22:00 18:00 20:00 22:00 18:00 20:00 22:00
30 30 # grunts =139 30 30
H # grunts =114
I # boops =24 J # grunts =35 N # grunts =141
# boops =35
# boops =92 # boops =35
number/minute
20 20 20 20
10 10 10 10
0 0 0 0
18:00 20:00 22:00 18:00 20:00 22:00 18:00 20:00 22:00 18:00 20:00 22:00
Fig. 6 Call rates (number/min) for eight individuals (lettered in written in the upper right corner. We also calculated the percentage
upper left) from 18:00–22:00, counted in 10-min intervals. Black of total grunts that were used for tagging (# of tagging grunts/ # of
lines depict the number of grunts that occurred in isolation or while preceding grunts + tagging grunts) and found a range across
tagging a neighbor’s call; preceding grunts are not shown here. individuals (d: 70%, e: 97%, f: 77%, g: 60%, h: 55%, i: 85%, j:
Red lines depict the number of boops. The total number of boops 50%, n: 75%). For all individuals, grunting and booping increased
and tagging grunts produced over the four-hour window (subsam- sharply at ~18:45, just 10 min after sunset (18:36 local time)
pled by counting calls in one minute out of every 10 min) are
Skoglund 1961), ultimately determining the funda- Do toadfishes have an individual Bvoice^?
mental frequency of the call. In contrast, vocal
prepacemaker neurons determine call duration Our multivariate analysis revealed separation of individ-
(Chagnaud et al. 2011). Species-specific differences uals based on spectral and temporal-based measure-
in anatomical structure and physiological properties ments of their calls. The separation of individuals ob-
of the vocal central pattern generator likely underlie served in the nMDS analysis (Fig. 4a), and the corre-
these species-specific differences among sponding PERMANOVA, showed that individual ID
batrachoidid vocalizations (Chagnaud and Bass explained 79% of the variance. This finding suggests
2014). There are also anatomical tradeoffs between that individual A. cryptocentrus do, in fact, possess their
call length and contraction speed (Mitchell et al own call signature and acoustic methods alone would
2008; Thorson and Fine 2002b), and the rather long allow female toadfishes (and researchers) to obtain in-
and complex call of A. cryptocentrus may impose formation on the positioning of individual males and an
an upper limit on the contraction speed. Increases approximate number of calling individuals within a
in water temperature are also associated with in- given population. When we included grunt parameters
creases in fundamental frequency within species in our nMDS analysis, the separation decreased. This
(Fine 1978; McKibben and Bass 1998), but it is suggests that the boop portion of the call contains more
unclear whether these temperature-related changes individual-specific traits, while the grunts are less dif-
are due to muscles contracting at a faster rate at ferentiated among individuals. In other words, it is likely
higher temperatures (Rome 2006), possible hor- that there is a selective advantage for male toadfishes to
monal influences (Fine 1978), temperature influ- encode individual information in their boops (as an
ences on the central pattern generator (Bass and advertisement or assertion of dominance), while there
Baker 1991), or some combination of the above. is likely less of a selective need for grunts to contain
The much lower fundamental frequency of A individual information when used agonistic contexts.
cryptocentrus documented here, compared to other The occurrence of individually-distinct calls has pre-
toadfishes, opens an intriguing avenue for research viously been described for several species of toadfishes
integrating anatomical traits and individual behavior (Amorim and Vasconcelos 2006, 2008; Edds-Walton
in different lineages of toadfishes. et al. 2002; Fine and Thorson 2008; Thorson and FineEnviron Biol Fish Fig. 7 a–c: Waveforms of a three-channel sound recording from nest F. Animal G tags this boop at 0.6 s, and animal H tags it at three nearby nests of Amphichthys cryptocentrus. Recordings are 0.8 s. Panel d shows the distances between nests along the pipe- from nest F (Panel a), nest G (Panel b) and nest H (Panel c). Calls line. Panel e shows the transmission loss as a function of distance are designated with blue (F), red (G), and green (G) based on the from the fish (source=0 m) for several boops (circles) and grunts nest from which they originated, and calls not originating from (diamonds) originating at these three burrows. Boops experience either of these three nests are shaded in grey. Different call ele- greater transmission loss with distance than grunts. Note that while ments are labeled as boop (b), grunt (g) or tag (t). For example, a this example shows clipping of calls from individuals F and H, no call from animal F starts at 0.3 s, and is then received at nest G and clipped data were used in data analysis 2002b), as well as other fish species, such as damselfish there is behavioral evidence that fishes can make this (Myrberg and Riggio 1985). While researchers can use distinction as well (Myrberg and Riggio 1985), indicat- statistical analyses to distinguish between individuals ing that individual call properties are in fact behaviorally (Amorim and Vasconcelos 2008; Vieira et al. 2015), and socially relevant. Distinguishing between multiple
Environ Biol Fish
Power spectral density
110
(dB re: 1 µPa2/Hz)
100
90
80
1000 70
900
800
700
Fr
eq
600
ue
nc
500
y(
400
Hz
6:44) 12:00
se (0
Sunri
)
300 2F 09:00
0
06:00
200 F 03:00
0
100 et (18
:36) 00:00 m)
Suns
21:00 ay ( hh:m
0 18:00 Tim e of d
Fig. 8 Spectrogram from a ~20-h recording at the intake pipe is also evident during the peak chorusing hours (~18:45–21:00).
area, but not next to one of the focal burrows. The color bar Vocal activity from the Bocon toadfish makes a significant contri-
matches the vertical axes and shows the acoustic energy in each bution to the acoustic environment in this shallow bay in Bocas del
1-Hz band up to 1000 Hz. At sunset, acoustic energy at ~112 Hz Toro. This species is often overlooked in visual biodiversity sur-
(the average Fundamental Frequency of toadfish boops, labeled veys (true for many benthic and cryptic fishes), but is acoustically
F0) and at ~224 Hz (the second harmonic, labeled 2F0) increased dominant in several habitats around the archipelago (Staaterman
and lasted throughout the night. Some energy at higher harmonics et al. 2017)
calling individuals may have several important func- to distinguish between calling males, the critical next
tions. For example, females may assess the quality or step is to demonstrate that this information is received
status of advertising males, while territorial males in and processed by females or other males, thus leading to
nests may be able to distinguish between their neighbors behavioral decisions and the mediation of social inter-
and possible intruders (Myrberg and Riggio 1985). actions between individuals in this species.
Myrberg and Riggio (1985) suggested that both spectral Our analysis of the CV of different call parameters
content and temporal patterning were likely the salient yields insights about which elements of the calls contain
acoustic cues for the basis of individual recognition. the most variability. The CV for boop fundamental
Additionally, as evidenced by midshipman, female frequency, both within and between individuals, was
batrachoidids exhibit positive phonotaxis to male adver- extremely low, suggesting that this is a Bstatic trait^ (as
tisement calls (McKibben and Bass 2001), and they defined by Gerhardt 1991). This is not surprising, con-
have the ability to localize sound sources with relatively sidering that fundamental frequency is driven by phys-
high spatial precision (Zeddies et al. 2012). Thus, indi- iological or physical factors, as described above. These
vidual discrimination, combined with the ability to lo- constraints leave little room for individual control and
calize calling males, would allow females to identify active peripheral modulation of fundamental frequency.
and choose mates. For females living in environments We also observed low within-individual variation for
with high male density or high noise levels, individual peak frequency but fairly high between-individual var-
discrimination of acoustic cues may confer a selective iation (33.8% and 32.4% for boop 1 and boop 2, respec-
advantage, particularly in cases where olfactory or visu- tively), but this finding is predominantly explained by
al cues are limited (Beecher 1989). Thus, while our the physics of sound transmission. Shallow water limits
nMDS analysis demonstrates that there is sufficient the propagation of the lowest frequencies (i.e., the Blow-
information contained within A. cryptocentrus signals frequency cutoff^; Bass and Clark 2003; Urick 1983),Environ Biol Fish
so at close distances, the fundamental frequency con- traits are known to send a message about individual
tains the most energy, but for individuals that were characteristics, and in other taxa, individuals with
farther away, the second harmonic had more energy than longer-duration calls or higher call rates tend to be the
the first (peak frequency=2× fundamental frequency; most attractive to females (treefrogs: Gerhardt 1991;
Fig. 3). Our results are consistent with those of Fine and crickets: Shaw and Herlihy 2000). Given the clear
Lenhardt (1983), who found that the fundamental fre- separation of animals based on call composition
quency of calls from O. tau were completely lost in (Figs. 4 and 5) and call rate (Fig. 6) revealed in the
background noise within just a few meters from the fish. present study, it appears likely that in A. cryptocentrus,
Their results varied across multiple recording locations, these parameters also reflect their readiness to mate or
which underscores the complexity of shallow-water body condition. Although we were not able to discern
sound propagation. We suggest that the presence of mul- a relationship between organismal traits and particular
tiple harmonics may be a form of redundancy to ensure call signatures, our results suggest that each toadfish
that the calls are successfully transmitted across differing does, in fact, have a distinct individual call. This
environmental conditions. We also found greater trans- finding poses questions for future work seeking to
mission loss with distance for the tonal boops compared disentangle the role of individual calls in the reproduc-
to the more broadband grunts, suggesting that the boops tive and social biology of A. cryptocentrus.
would function best as a short-distance signal, while the We also observed fairly high within-individual vari-
grunts may be more functional at larger distances. ation for duration-based parameters, suggesting that
These results suggest that call amplitude and frequen- individuals have control over the temporal axis of sound
cy are static parameters with little individual variation, production and may wait for quiet windows to produce
likely due to a combination of environmental and phys- multi-boop calls. Our results are consistent with Barimo
iological constraints. In experiments with both frogs and Fine (1998), who also found higher variation in
(Gerhardt 1991) and crickets (Shaw and Herlihy duration-based parameters. There also were instances
2000), females showed a unimodal preference for males when toadfish spontaneously grunted but did not follow
with frequency values closest to the mean of the popu- with a boop and did not directly tag a neighbor. It is
lation. The theory is that static call parameters may help unclear whether these spontaneous grunts represent calls
females determine species identity and avoid unfruitful that were aborted partway through, or whether they
mating attempts with other species. A. cryptocentrus co- serve a separate function, such as asserting presence to
occurs with another toadfish species, Sanopus astrifer neighbors or attracting females to the area where this
(Hoffman and Robertson 1983), which is also population resides.
soniferous and has an average fundamental frequency
of approximately 180 Hz (Mann et al. 2002; Mosharo Do toadfish individuals have a calling strategy?
and Lobel 2012). The ~65 Hz difference between the
calls of these two species would provide an important We observed high variability in calling rates and the
signal to females and allow them to correctly identify proportion of calling effort dedicated to each call type.
potential mates. Due to the importance of these static Some individuals produced nearly equal numbers of
traits, it is not surprising that toadfish will employ ‘tag- boops and grunts over a four-hour period, while others
ging’ as means for sexual selection, as described here produced three times as many grunts as boops. There
(Fig. 7) and by others (Fine and Thorson 2008; Mann did not seem to be any pattern related to location along
et al. 2002; Thorson and Fine 2002a). the pipeline or proximity to other burrows, although we
The traits with the highest between-individual varia- did observe that Individual J, who was living in isolation
tion related to call composition. BDynamic traits^ – away from the pipes, had the lowest call rate. This is
those which are easily modified and controlled by indi- consistent with Amorim et al. (2011), who observed that
viduals - typically have a CVB of at least 25% (Gerhardt males calling alone tended to call at lower rates. Three
1991). For the Bocon toadfish, the overall call rate, close neighbors within the present study exhibited very
number of boops and grunts per call, inter-grunt interval, different call rates and different grunt-to-boop ratios.
grunt-boop interval, boop duration, and boop interval The two individuals that tagged each other the most (F
had high between-individual variation (at least 36%), and H) had similar call qualities, while individual G,
suggesting that they are indeed dynamic traits. Dynamic who had the most distinctive call parameters (Fig. 3),Environ Biol Fish
received the lowest number of tags. Future work should Compliance with ethical standards
examine whether there is a relationship between call
similarity and tagging rates of close neighbors. When Ethical approval All applicable international, national, and/or
institutional guidelines for the care and use of animals were
living in an aggregation, there may be some degree of followed. All procedures performed in this study were in accor-
pressure to match or exceed the call rates of one’s dance with the ethical standards of the Smithsonian Tropical
neighbors in order to increase attractiveness to females Research Institute. This research was conducted under permit #
(Fish 1972). In addition, it would be interesting to SE/AP-2-16 and STRI IACUC approval 2016–0101-2019.
correlate reproductive output with tagging behaviors to
further examine the notion of a calling Bstrategy^ in
toadfish. Overall, both the individual voices and calling References
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