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Lusitanian toadfish males that provide parental care rely on acoustic signals (the boatwhistle) to attract females to their nest. We test the hypothesis that male quality, namely male size and condition that are relevant for parental success, is reflected in vocal activity and boatwhistle characteristics and thus advertised to females. We recorded 22 males over a week during the peak of the breeding season. Calling rate and calling effort (percentage of time spent calling) strongly reflected male condition (lipid content of somatic muscles) and to a smaller extent sonic muscle hypertrophy and larger gonads. Males in better condition (increased body lipid and relative higher liver mass) also contracted the sonic muscles at faster rate as shown by the shorter boatwhistle pulse periods. Amplitude modulation reflected the degree of sonic muscle hypertrophy. None of the measured male quality parameters were good predictors of boatwhistle duration and dominant frequency. Altogether this study strongly suggests that Lusitanian toadfish males advertise their quality to females primarily with boatwhistle calling rate and calling effort, which mainly reflect male condition. Because pulse period had low variability, consistent with the existence of a vocal central pattern generator, we suggest that males that sustain sonic muscles contraction at a very fast rate close to their physiological limit may be honestly advertising their quality (condition). Similarly, males that produce boatwhistles with higher amplitude modulation, a feature that seems dependent on sonic muscle hypertrophy, could be more attractive to females.
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Females are often the choosy sex and select mates based on direct
benefits such as food, parental care or a good territory, or on indirect
benefits such as genetic quality (Andersson, 1994). Males advertise
their attributes through courtship displays, which inform their mates
about their quality. Signals can evolve to be reliable or honest if
they bear a cost to the sender either because of production costs or
through increased vulnerability of attack by heterospecific or
conspecific receivers (Zahavi, 1975). Alternatively, index signals
are reliable because they cannot be faked due to physical or
physiological constraints that force the signal to reveal honest
information (Vehrencamp, 2000; Maynard Smith and Harper,
2003). Honest signals can also be relatively cost-free if signallers
and receivers share a common interest or when there is a threat of
retaliation by the receiver (Vehrencamp, 2000).
Acoustic signals are good examples of sexually selected traits
predominantly used by females of several taxa to identify, locate
and choose between potential mates (Andersson, 1994; Bradbury
and Vehrencamp, 1998). Different components of vocalisations
seem to convey honest messages that are relevant for mate choice
but may also be maladaptive for females if female preference has
evolved, for example, by male sensory exploitation (Ryan et al.,
1990). Examples of honest acoustic signal components are high
calling rates that are energetically costly to maintain or may attract
predators or parasites, and the fundamental frequency of
advertisement calls that may be dependent on the vocal apparatus
size and thus on the sender size (Maynard Smith and Harper, 2003).
Fish probably represent the largest group of sound-producing
vertebrates and often emit acoustic signals during courtship (Ladich,
2004). However, there are few studies that relate calling rate and
call characteristics with male quality and even fewer that show the
role of acoustic signals in mate choice. This is probably due to
technical limitations related to underwater recordings (in natural
contexts) and playbacks, rather than to the lack of a role of fish
calls on mate choice (Ladich, 2004). For example, female of the
bicolour damselfish Stegastus partitus (Pomacentridae) prefer
courtship chirps of lower frequency that indicate a larger male body
size (Myrberg et al., 1986). Females of the same species also favour
males with high courtship rates who have better body condition and
are less prone to cannibalise their eggs (Knapp and Kovach, 1991).
Although it has not been tested, the studies by Myrberg et al.
(Myrberg et al., 1986) and Knapp and Kovach (Knapp and Kovach,
1991) both suggest that S. partitus females could be also selecting
males with a high courtship chirping rate, which could be indicative
of a better male condition and parental ability. McKibben and Bass
have also shown that females of the midshipman Porichthys notatus
(Batrachoididae) prefer the more intense of two hums, the male
mating signals (McKibben and Bass, 1998). In addition, the
percentage of females responding to sound playback increased as
duration of calls increased and the pauses between calls decreased,
indicating that longer continuous calls resembling natural hums are
more attractive to females (McKibben and Bass, 1998).
Breeding males from the family Batrachoididae (toadfishes and
midshipmen) nest under rocks and produce advertisement calls
The Journal of Experimental Biology 213, 2997-3004
© 2010. Published by The Company of Biologists Ltd
Lusitanian toadfish song reflects male quality
M. Clara P. Amorim1,*, J. Miguel Simões1, Nuno Mendonça2, Narcisa M. Bandarra2, Vitor C. Almada1and
Paulo J. Fonseca3
1Unidade de Investigação em Eco-Etologia, Instituto Superior de Psicologia Aplicada, Rua Jardim do Tabaco 34, 1149-041 Lisboa,
Portugal, 2Unidade de Valorização dos Produtos da Pesca e Aquicultura (U-VPPA), Instituto de Investigação das Pescas e do Mar
(IPIMAR), Instituto Nacional de Recursos Biológicos (INRB), Avenida de Brasília, 1449-006 Lisboa, Portugal and 3Departamento de
Biologia Animal e Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa. Bloco C2, Campo Grande,
1749-016 Lisboa, Portugal
*Author for correspondence (
Accepted 18 May 2010
Lusitanian toadfish males that provide parental care rely on acoustic signals (the boatwhistle) to attract females to their nest. We
test the hypothesis that male quality, namely male size and condition that are relevant for parental success, is reflected in vocal
activity and boatwhistle characteristics and thus advertised to females. We recorded 22 males over a week during the peak of the
breeding season. Calling rate and calling effort (percentage of time spent calling) strongly reflected male condition (lipid content
of somatic muscles) and to a smaller extent sonic muscle hypertrophy and larger gonads. Males in better condition (increased
body lipid and relative higher liver mass) also contracted the sonic muscles at faster rate as shown by the shorter boatwhistle
pulse periods. Amplitude modulation reflected the degree of sonic muscle hypertrophy. None of the measured male quality
parameters were good predictors of boatwhistle duration and dominant frequency. Altogether this study strongly suggests that
Lusitanian toadfish males advertise their quality to females primarily with boatwhistle calling rate and calling effort, which mainly
reflect male condition. Because pulse period had low variability, consistent with the existence of a vocal central pattern generator,
we suggest that males that sustain sonic muscles contraction at a very fast rate close to their physiological limit may be honestly
advertising their quality (condition). Similarly, males that produce boatwhistles with higher amplitude modulation, a feature that
seems dependent on sonic muscle hypertrophy, could be more attractive to females.
Key words: fish, Batrachoididae,
Halobatrachus didactylus
, acoustic communication, mate choice, male condition, muscle lipid content.
(boatwhistles or hums) from their nests to attract females by
contracting a pair of sonic muscles embedded in the sides of the
swimbladder (Fish, 1972; Brantley and Bass, 1994; dos Santos et
al., 2000). Batrachoidid males provide uniparental care until the
young are free-swimming and call to attract females until the nest’s
ceiling is fully covered with eggs and embryos (Brantley and Bass,
1994). Batrachoidids have become a model group in the study of
acoustic communication in teleosts (Bass and McKibben, 2003;
Sisneros, 2009) but little is known on the role of acoustic signals
in mate choice and reproductive success. The Lusitanian toadfish
Halobatrachus didactylus (Bloch and Schneider 1801) produces a
long (about 1s) tonal low-frequency advertisement sound, the
boatwhistle, which is highly stereotyped and shows considerable
inter-individual differences during short periods of time (<10min)
(Amorim and Vasconcelos, 2008). A recent study has shown that
the male’s sound-producing muscles are highly variable (c.v.40%)
and that its mass depends mostly on male length and condition,
suggesting that sounds could advertise male quality in this species
(Amorim et al., 2009). Because the boatwhistle seems to be the only
courtship signal in this species (M.C.P.A., P.J.F. and J.M.S.,
personal observation) [see also Brantley and Bass (Brantley and
Bass, 1994) for a detailed description of the mating behaviour of
P. notatus] we have hypothesised that it should contain information
relevant to the female for mate choice. In the present study, we test
the hypothesis that calling activity (calling rate and calling effort –
percentage of time calling) and boatwhistle characteristics (duration,
pulse period, dominant frequency and amplitude modulation) reflect
male quality. For that purpose we recorded 22 males, each over a
week during the peak of the breeding season, and measured their
body condition, body size, sonic muscle hypertrophy and
reproductive condition (gonad and accessory gland mass). Because
Lusitanian toadfish females seem to produce only one clutch of a
few large eggs per reproductive season (Modesto and Canário,
2003a; Costa, 2004) and have to probably rely on the parental ability
of one single male for their reproductive success, we predict that
boatwhistles should inform females of male size and condition,
which are relevant for nest defence and parental care.
Study species
Breeding males of the Lusitanian toadfish, H. didactylus, form
conspicuous choruses from May to July (in Portugal) and defend
nests in estuarine shallow waters that can contain clutches from
different females (Amorim et al., 2006). Parental care is provided
until the young are free-swimming. Besides the nest-guarding male
(‘type I’) morphotype, there are sneaker males (‘type II’) that have
larger testis (sevenfold), smaller accessory glands (threefold; the
accessory glands are part of the male reproductive apparatus, secrete
mucosubstances and are connected to the spermatic duct) and lower
(sixfold) 11-ketotestosterone levels than nesting males (Modesto and
Canário, 2003a; Modesto and Canário, 2003b). Only type I males
produce boatwhistles during the breeding season. Sonic muscles of
type I males but not of type II males or of females suffer hypertrophy
during the breeding season (Modesto and Canário, 2003a),
concurrent with an increase in vocal activity (Amorim et al., 2006).
Sound recording
Sixty artificial hemicylinder-shaped concrete shelters capped at one
end were deployed 1.5m apart in an intertidal area of the Tagus
estuary (Portugal, Montijo, Air-Force Base 6; 38°42N, 8°58W)
that was only exposed to air during spring low tides. Water level
varied between 0m and 2.8m in the study area. The shelters were
large enough (internal dimensions: 50cm long30cm wide20cm
high) to house a large male and several females and were readily
used as nests during the breeding season (Amorim et al., 2010).
Three groups of 6–8 males (N22) that spontaneously occupied these
artificial concrete shelters were recorded over a period of eight days
in June and July in 2006 and 2007, during the peak of the
reproductive season (May to July in Portugal) (Modesto and
Canário, 2003a). Shelters (6–8) containing subject males were placed
1.5m apart in two rows and were at least 15m apart from the
remaining shelters. The entrance of the subject males’ shelters were
closed with a plastic mesh preventing fish from abandoning the nest
during recordings but allowing prey items to enter and possible
visual interactions with conspecifics.
One hydrophone (High Tech 94 SSQ hydrophone, High Tech
Inc., Gulfport, MS, USA; sensitivity –165dB re. 1V/Pa, frequency
response within ±1dB from 30Hz to 6KHz) was firmly attached
to an iron rod partially buried in the sand substrate, placed ~10cm
from each shelter entrance and from the substrate. Simultaneous
multi-channel recordings were made to a laptop connected to USB
audio capture devices (Edirol UA25, Roland, Osaka, Japan; 16bit,
6kHz acquisition rate per channel) controlled by Adobe Audition
2.0 (Adobe Systems Inc., Mountain View, CA, USA). Recorded
sounds could be attributed to each male due to the high acoustic
attenuation observed in shallow water (Fine and Lenhardt, 1983).
Sounds from a neighbouring male were ~27dB lower than of a
subject male. Water temperature was measured every 3h during
recording periods and averaged 23°C (range: 19.5–28°C). All
subject fish experienced similar water temperature variability during
recordings; hence, the effect of temperature on call parameters
should be similar for all fish. Each male was recorded for an average
of 35h (range: 11–56h).
Sound analysis
Boatwhistles have been described in detail in Amorim and
Vasconcelos (Amorim and Vasconcelos, 2008) and, as in other
batrachoidids (e.g. Thorson and Fine, 2002), are characterised by
an initial shorter pulsed part followed by a longer tonal segment
(dos Santos et al., 2000; Amorim and Vasconcelos, 2008). We
analysed boatwhistles for total sound duration (ms, measured from
the start of the first pulse to the end of the last pulse), pulse period
of the tonal segment (ms, average peak-to-peak interval of six
consecutive pulses in the middle of this segment), dominant
frequency of the tonal segment (Hz, the frequency with maximum
energy in this part of the sound), and amplitude modulation [the
ratio between the mean amplitude (root mean square, r.m.s.) of the
initial and of the tonal segments; r.m.s. amplitude is a measurement
native to Raven software, Cornell Laboratory of Ornithology,
Ithaca, NY, USA]. Temporal variables and amplitude modulation
were measured from oscillograms, and dominant frequency from
power spectra computed with a 2048 points FFT conditioned by a
Hamming window, with a time overlap of 50.0% and a 10Hz filter
bandwidth. These acoustic parameters are depicted in Fig.1. Calling
rate (number of boatwhistles emitted per hour) was tallied for each
fish. Calling effort (number of hours calling / number of hours
recorded 100) was also calculated per fish. Sound analysis was
carried out with Adobe Audition 2.0 and Raven 1.2.1 for Windows.
Morphometric analysis
At the end of recordings subject males were killed with an excessive
dosage of MS 222 (tricaine methane sulphonate; Pharmaq, Skøyen,
Oslo, Norway). In the laboratory, each subject male was measured
to the nearest mm for total length (TL), and to the nearest g for
M. C. P. Amorim and others
2999Toadfish song reflects male quality
eviscerated body mass (ME). Males (N22) used in this study
averaged 42.9cm (range: 37.9–47.7cm) in total length and 1207g
(range: 857–1612g) in eviscerated mass. The gonads (MG), the
accessory glands (MAG) and the liver (ML) mass were tallied to the
nearest mg. Sonic muscles, which are embedded in the sides of the
swimbladder, were gently cut from the swimbladder wall with a
pair of fine dissection scissors and were also weighed to the nearest
mg (MSM). The mass of the accessory glands was included in the
measurements as they are part of the male reproductive apparatus
and increase in mass during the breeding season in nesting males
(Modesto and Canário, 2003a).
A sample of body muscles was taken (hypaxial muscle fibres)
and the lipid fraction of both somatic and sonic muscles was
quantified as an additional measurement of body and sonic muscle
condition. Lipids are an important source of energy in fish and are
often used as a direct measure of body condition (Chellapa et al.,
1995). Lipids are also one of the major metabolic substrates of sonic
muscles during prolonged aerobic activity (Fine et al., 1986).
All experimental procedures comply with Portuguese animal
welfare laws, guidelines and policies.
Lipid analysis
The fish somatic and sonic muscle homogenates (10g) were
extracted using 30ml of chloroform: methanol (1:2vol./vol.) with
a polytron system. In addition, a saturated sodium chloride solution
(4ml), chloroform containing 50p.p.m. (parts per million) of
butylhydroxytoluene (10ml) and water (10ml) were added to split
the system into an aqueous and an organic phase (Bligh and Dyer,
1959). The mixture was sonicated during 15min. Complete
separation of the two phases was obtained by adding isopropanol;
the total mixture was centrifuged and the chloroform phase
transferred to a weighed tube. The chloroform was evaporated under
nitrogen prior to gravimetrical determination of total lipids.
Statistical analysis
We examined eight potential predictors of call parameters. We
included total length (log10TL) as a metric of body size. We used
residuals of the simple linear regression of sonic muscle mass on
eviscerated body mass (RMSM) as a metric of sonic muscle
hypertrophy. This metric gives a measure of an observed sonic
muscle mass relative to a mean expected value (given by the
regression model) for a given body size. In other words, a male
with a high positive residual of RMSM will have heavier than average
sonic muscles for his size. Likewise we used the residuals of the
simple linear regressions of gonads, accessory glands and liver mass
on eviscerated body mass (RMG, RMAG, RML, respectively) as
metrics of these parameters controlled for the influence of body
size. In addition, we used the residuals of MEon TL (COND) as a
metric of body condition. We log10-transformed TL and mass data
to meet the assumptions of normality and to linearise allometric
relationships. We further considered the lipid content of somatic
and sonic muscles (LipidM and LipidSM, respectively) as possible
predictors of call parameters.
We first generated a correlation matrix of the six measured
call parameters (calling rate and effort, and boatwhistle
characteristics) and morphological traits to examine general
relationships among the variables across all individuals. We then
used multiple regression analysis to assess the statistical
significance of each physical parameter as a predictor of male
mating call parameters with a stepwise selection procedure
(P0.05 to add and P0.10 to remove).
Because three of our dependent variables, calling rate, calling
effort and pulse period, were highly correlated (Table1), we
included these variables in a factor analysis to generate a single
factor that would combine and explain most of the variance in this
group of variables. Pulse rate (the inverse of pulse period and
equivalent to sonic muscle contraction rate) was used instead of
pulse period because the former had a positive loading in the first
principle component, similar to the other two variables. The scores
of the first factor can be viewed as an index of ‘vocal performance’,
i.e. of length and rate of calling and of muscle contraction rate during
sound production. The first factor explained 75% of the total data
variance with call rate, effort and pulse rate presenting a factor-
loading score of 0.90, 0.89 and 0.81, respectively. We used this first
factor (hereafter called vocal performance) in a multiple regression
analysis with the same eight aforementioned predictors to further
analyse data.
Our final regression models complied with all assumptions of
multiple linear regression. All model residuals were normally
distributed. Further residual analysis was performed using
0.30.5 0.7 0.90.1
0.5 1.0 1.5 2.00
Frequency (kHz)
PP 10 ms
0.30.5 0.7 0.90.1
Sound duration
Time (s)
Frequency (kHz) Relative amplitude
Relative amplitude (dB)
Fig.1. Oscillogram (A), sonogram (B) and
power spectrum (D) of a boatwhistle. Sound
duration, the initial (fine continuous line) and
the tonal (fine dashed line) phases of the
boatwhistle are depicted in the oscillogram.
In the sonogram and in the power spectrum
the dominant frequency (DF) of the sound is
shown. (C)Detail of the boatwhistle tonal
phase waveform depicting the pulse period
(PP). Note that the pulse period is inversely
related to the fundamental frequency and not
to the dominant frequency of the boatwhistle.
Durbin–Watson statistics, residual plots as well as multicollinearity
tests (variance inflation factors, VIF).
All statistical analyses were performed using SPSS for Windows
(16.0, SPSS Inc., Chicago, IL, USA).
Acoustic activity
Acoustic activity varied greatly among subject males. All males
produced boatwhistles (BW) during the study period but calling rate
varied markedly among males and within males. The average calling
rate varied from 0.1 to 361.7BWh–1 per male (overall mean calling
rate39.9BWh–1; Table2). Only seven out of the 22 recorded males
exhibited average calling rates higher than 10BWh–1 during the
study period, and the maximum calling rate observed for each male
varied between 2 and 1071BWh–1 (mean244.5BWh–1). Males
vocalised for a different number of days [mean (range)5 (2–8)]
and for a different number of hours (calling effort, Table2) but
remained in silence most of the time.
Boatwhistle characteristics were consistent with previous
descriptions (e.g. Vasconcelos et al., 2010) and showed a large
between-individual variation (Table2).
Predictors of male acoustic characteristics and activity
Correlation analysis showed that both calling rate and calling effort
were significantly positively related with lipid content of the
somatic muscles, relative gonad mass and relative sonic muscle mass
(Table3). Boatwhistle duration was positively correlated with body
condition (Table3). Pulse period was negatively correlated with lipid
content of the somatic muscles and relative sonic muscle mass
(Table3), indicating that males that exhibited an average faster sonic
muscle contraction rate (i.e. shorter pulse period) had larger sonic
muscles and higher lipid levels in the body.
The best regression models for each dependent variable showed
that calling rate, calling effort and pulse period strongly reflect male
condition measured by the lipid content in the somatic muscles
(Table4). Body lipid showed high partial correlations with calling
rate, calling effort and pulse period (r0.89, 0.94 and –0.61,
respectively, Table4) and accounted for most of the variation
explained by each regression model (Table4). Lipid content of the
somatic muscles explained 77% (out of 82% explained by the full
model, Table4), 88% (out of 94%) and 31% (out of 46%) of calling
rate, calling effort and pulse period variability, respectively. Males
with higher body lipid content showed a significantly higher calling
rate, called for more hours and contracted the sonic muscles faster
during sound production, exhibiting shorter pulse periods in a
boatwhistle (Fig.2). Calling rate was further predicted by relative
sonic muscle mass, which explained a further 5% of its variability.
Males with heavier-than-average sonic muscles called at a higher
rate (Fig.2). Gonad mass also explained 3% of calling effort
variability, and males with relatively larger gonads spent longer
periods calling (Fig.2). Liver mass accounted for an additional 15%
of pulse period variation, and males with heavier livers for a given
size tended to contract the sonic muscles faster during sound
production as observed by their shorter pulse periods (Fig.2).
Consistently, vocal performance, a new variable that combined the
former dependent variables was only predicted by the lipid content
of the somatic muscles, the strongest predictor for these three
acoustic parameters (Table4).
Additionally, relative sonic muscle mass showed a weaker but
significant positive effect on amplitude modulation explaining 22%
of its variation (Table4; Fig.2). Both boatwhistle duration and
dominant frequency were not predicted by any of the independent
variables as regression models were not significant (P>0.05).
The boatwhistle produced by Lusitanian toadfish nesting males is
the major mate attraction signal and therefore essential for male
reproductive success (dos Santos et al., 2000) [see Bass and
McKibben (Bass and McKibben, 2003) for other batrachoidids].
This call shows a large inter-individual variation (Amorim and
Vasconcelos, 2008) (present work) and could thus be used to
discriminate among males. But can females use acoustic cues to
choose a mate? Our work shows that male vocal activity and mating
call characteristics reflect several aspects of male quality.
Calling rate and calling effort
High calling rate and increased calling effort strongly reflected good
male body condition measured by the lipid content of the somatic
muscles. The lipid fraction of the body
muscles explained 77% and 88% of the
variability of calling rate and effort observed
over a week in our focal males. In animals
where males provide parental care,
indicators of male parental ability such as
body condition are expected to play a
substantial role in intersexual
communication and be under strong mate
selection by females (Andersson, 1994).
Fish unguarded eggs are quickly eaten by
M. C. P. Amorim and others
Table1. Correlations between the six acoustic variables showing the strong relations between calling rate, calling effort and pulse period
Calling rate Calling effort Duration Pulse period Dominant frequency Amplitude modulation
Calling rate 0.76*** 0.00 –0.67*** 0.27 0.41
Calling effort –0.06 –0.55* 0.20 0.33
Duration – –0.31 0.00 0.00
Pulse period – –0.12 –0.52*
Dominant frequency – –0.07
Amplitude modulation
Values shown are Spearman rank correlation coefficients. Significant differences are indicated by asterisks, i.e. *
<0.05; ***
-values are uncorrected
for multiple tests.
21 except for the correlation between calling rate and calling endurance where
Table 2. Descriptive statistics for the dependent acoustic variables
Mean s.d. Range c.v.
Calling rate 22 39.9 87.7 0.1–361.7 2.19
Calling effort 22 30.7 20.1 2.4–67.7 0.66
Boatwhistle duration (ms) 21 681.9 154.4 383.2–1049.7 0.23
Pulse period (ms) 21 19.2 1.1 17.4–22.4 0.06
Dominant frequency (Hz) 21 117.9 35.0 52.7–181.1 0.30
Amplitude modulation 21 0.7 0.2 0.5–1.3 0.26
Coefficient of variation (c.v.)s.d./mean.
3001Toadfish song reflects male quality
predators and females must rely on male brood protection for the
survival of their offspring (Sargent and Gross, 1993). Consequently,
females benefit from choosing good fathers, and more so if they
are single spawners such as batrachoidids (Brantley and Bass, 1994;
Modesto and Canário, 2003a). Parental care in the Lusitanian
toadfish is costly because type I males experience reduced feeding,
fan the eggs and defend their nest vigorously for at least 30 days
(till the fry becomes free swimming) (Modesto and Canário, 2003a;
Vasconcelos et al., 2010), consistent with the marked decrease in
the male’s condition (hepatossomatic index and the Fulton’s
condition factor, K) during the spawning season (Modesto and
Canário, 2003a). Our results suggest that Lusitanian toadfish females
should favour males that call at a higher rate and for prolonged
periods, as they would be in better condition and could provide better
parental care. Consistently, larger nesting males of the batrachoidid
P. notatus sampled at the end of the breeding season presented higher
body condition (K) and a larger number of viable late-stage embryos
in the nest (Sisneros et al., 2009), suggesting that body condition
is an honest indicator of parental ability in batrachoidids. Similarly,
in the sand goby (Pomatoschistus minutus), another teleost with
prolonged male parental care, only males with adequate body
condition initiate nest building and breeding (Lindström, 1998a),
and food supplemented males stay longer at the nest, mate sooner
and manage to get more eggs than non-fed males with lower
condition (Lindström, 1998b). Parental common goby
(Pomatoschistus microps) males with higher energy reserves are
also probably less likely of filial cannibalism than males with lower
condition, as observed in other fish (Kvarnemo et al., 1998). Future
work will need to address whether calling rate and effort reflect
male parental ability in the Lusitanian toadfish. In birds, call rate
and other song features may be reliable indicators of parental quality
(Dolby et al., 2005).
In our study species, the ability to call at higher rates and to sustain
calling for longer periods also reveal, although to a much smaller
Table 3. Relationship between male physical and acoustic characteristics (Spearman rank correlation)
Calling rate Calling effort Duration Pulse period Dominant frequency Amplitude modulation
0.51* 0.61** 0.03 –0.60** –0.05 0.50*
20 20 20 20 20 20
–0.06 –0.09 –0.25 0.39 0.33 –0.37
22 22 21 21 21 21
TL r
–0.27 –0.18 –0.02 0.30 –0.15 –0.21
22 22 21 21 21 21
0.49* 0.63** 0.05 –0.31 0.07 0.14
22 22 21 21 21 21
0.36 0.42 0.28 –0.29 –0.08 0.41
22 22 21 21 21 21
0.12 –0.09 0.15 –0.30 –0.19 0.09
22 22 21 21 21 21
0.58** 0.47* 0.21 –0.53* 0.13 0.41
22 22 21 21 21 21
0.04 0.08 0.51* –0.35 –0.35 0.07
22 22 21 21 21 21
Significant differences are indicated by asterisks, i.e. *
<0.05; **
-values are uncorrected for multiple tests. LipidM – total lipid content of somatic
muscles; LipidSM – total lipid content of sonic muscles.
– total length;
G– residuals of gonad mass;
AG – residuals of accessory gland mass;
L– residuals of liver mass;
SM – residuals of sonic muscle mass; COND – body condition.
Table4. Table for predictors of male call parameters (calling rate, calling effort and boatwhistle characteristics)
Included Model
Dependent variable predictor
tPr F
Calling performance Intercept –1.50 0.36 –4.19 0.001
LipidM 3.65 0.78 4.68 <0.001 0.74
<0.001 0.55 1.7 1.00
Calling rate LipidM 2.11 0.26 8.18 <0.001 0.89 1.04
SM 0.27 0.12 2.38 0.03 0.49
<0.001 0.82 1.8 1.04
Calling effort LipidM 73.69 6.11 12.06 <0.001 0.94 1.05
G6.46 2.68 2.41 0.03 0.49
<0.001 0.91 1.3 1.05
Pulse period Intercept 20.49 0.44 46.22 <0.001
LipidM –3.03 0.96 –3.14 0.006 –0.61 1.00
L–0.44 0.21 –2.15 0.046 –0.46
0.006 0.46 2.0 1.00
Amplitude modulation Intercept 0.736 0.039 18.69 <0.001
SM 0.086 0.038 2.27 0.036 0.47
0.04 0.22 1.9 1.00
Calling rate was log10 (
+1)-transformed to meet the linear regression model assumptions.
– partial correlation between the dependent variable and the
predictor, controlling for the effects of the other predictors in the model. LipidM – total lipid content in the somatic muscles.
SM – residuals of sonic
muscle mass.
G– residuals of gonad mass.
L– residuals of liver mass. Results are from multiple regression analysis (stepwise procedure).
Regression models for boatwhistle duration and dominant frequency were not significant.
extent, a higher degree of sonic muscle hypertrophy and relative
larger gonad mass. Muscle hypertrophy has been generally
associated with a higher capacity for calling (e.g. Connaughton et
al., 1997). The sonic muscle hypertrophy in H. didactylus males
observed in association to the reproductive season is accompanied
by an increase of total myofibril and sarcoplasm area and breeding
males show a larger sarcoplasm/myofibril area ratio than females
(Modesto and Canário, 2003b). A higher sarcoplasm/myofibril area
ratio has been interpreted as an adaptation to the increased speed
and fatigue resistance needed for boatwhistle production in the oyster
toadfish, Opsanus tau (Fine et al., 1990) and an increased
myofibrillar area should allow for more forceful contractions
resulting in higher amplitude calls (Connaughton et al., 1997).
Hence, Lusitanian toadfish males with larger sonic muscles should
M. C. P. Amorim and others
00 0.2 0.4 0.6 0.8 1.0
0 0.2 0.4 0.6 0.8 1.0
0 0.2 0.4 0.6 0.8 1.0
3 –2 –1 0 1 2 3
3 –2 –1 0 1 2 3
3 –2 –1 0 1 2 3
3 –2 –1 0 1 2 3
Calling rate (BW h–1)
Calling effort
Pulse period (ms)
Amplitude modulation
Fig.2. Relationship between
predictor variables of male
quality and call parameters.
Lines of univariate regressions
and 95% confidence interval
bands are shown. LipidM – lipid
content of body muscles;
– residuals of sonic muscle
G– residuals of gonad
L– residuals of liver
3003Toadfish song reflects male quality
sustain high calling rates and call at higher amplitudes, resulting in
a more conspicuous vocal output. The significant effect of relative
gonad mass suggests that calling rate and effort signal male mating
motivation as shown for fish and other vertebrates [e.g. fish (Fish,
1972); anurans (Burmeister and Wilczynski, 2001); mammals
(Vannoni and McElligott, 2009)]. Also, a higher than average calling
rate may signal other male traits such as a better immune system
[e.g. insects (Jacot et al., 2004)] or a higher fertilisation success
[e.g. anurans (Pfennig, 2000)].
Interestingly sonic muscle lipid content did not seem to predict
differences in the ability to sustain high calling rates over a week
but perhaps differences in lipid concentration would be visible in
the vocal performance of males in a longer time scale. For example,
Connaughton et al. (Connaughton et al., 1997) observed a
pronounced decrease in sonic muscle lipid in the weakfish
(Cynoscion regalis) during the peak of acoustic activity, which is
a month past the start of a high calling activity in this species.
Boatwhistle characteristics
Males in better condition (body lipid and higher liver mass) had shorter
pulse periods and hence contracted the sonic muscles faster during
sound production. However, we found a low between-male variability
for this parameter (c.v.6%), consistent with the existence of a vocal
central pattern generator in the hindbrain of batrachoidids that
establishes the patterned activity of the sonic muscles and hence the
pulse period of their calls (Bass and Baker, 1990). Consistently, O.
tau males also present a similar variability of fundamental frequency
of boatwhistles (c.v.6%) (Barimo and Fine, 1998), which is the
inverse of the pulse period. Lusitanian toadfish males that contract
the sonic muscles at a very fast rate could reliably be indicating to
females their better quality (condition) with the ability to sustain sonic
muscle contraction close to their physiological limit. Consistent with
this suggestion, males of the non-passerine bird brown skuas that
produce long difficult calls close to their performance limit are
honestly advertising their quality because they have a higher breeding
success and fledge more chicks (Janicke et al., 2008).
Relative sonic muscle mass showed a significant positive effect
on boatwhistles amplitude modulation. Amplitude modulation is an
important characteristic to distinguish boatwhistle emitted by nesting
males in different motivational contexts. Vasconcelos et al.
(Vasconcelos et al., 2010) have shown that the Lusitanian toadfish
also emits boatwhistles during territorial intrusions by other males
but these lack amplitude modulation, which seems characteristic of
a mating context. Consequently, it is possible that males can also
advertise their quality and motivation by increasing the amplitude
modulation of the mating boatwhistle, although this suggestion needs
to be tested.
Both boatwhistle duration and dominant frequency showed high
variability and were not predicted by any of the considered
independent variables. Boatwhistle duration was very variable
among males (see also Barimo and Fine, 1998; Amorim and
Vasconcelos, 2008). This parameter seems motivation dependent
in batrachoidids (M.C.P.A., P.J.F. and J.M.S., unpublished data)
(Thorson and Fine, 2002; Remage-Healey and Bass, 2005) and
probably translates the male’s physiological state (Remage-Healey
and Bass, 2005). Although pulse period (and hence the fundamental
frequency) showed little variability, the same was not true for the
dominant frequency because it may be represented by the
fundamental or by the first or the second harmonic (Amorim and
Vasconcelos, 2008).
Here, we have shown that calling rate, calling effort, pulse period
and amplitude modulation may honestly signal male quality, namely
male condition, spawning readiness and sonic muscle hypertrophy
in a batrachoidid. A recent study with P. notatus has shown that
females reveal best hearing sensitivity matching the higher harmonic
components of male advertisement calls during the breeding season
(Sisneros, 2009). This suggests the action of selective pressures for
these females to better detect and probably choose among different
males in dense breeding aggregations that are typical of
batrachoidids and other sound-producing teleosts. Although not
tested in fish, calling rate and time spent calling may influence
female choice in other species such as in insects and anurans
(reviewed in Gerhardt and Huber, 2002), in birds (e.g. Gentner and
Hulse, 2000) and in mammals (e.g. McComb, 1991). Calling
activity is also likely to be an important parameter for mate choice
in fish because sound duty cycle (the proportion of sound in a
stimulus) influences female preference (McKibben and Bass, 1998).
Whether females benefit from better brood care, better territories,
good genes or just ease of male location, remain still to be addressed
in fish.
BW boatwhistle
COND residuals of the simple linear regressions of eviscerated body
mass on total length
LipidM lipid content of somatic muscles
LipidSM lipid content of sonic muscles
MAG accessory glands’ mass
MEeviscerated body mass
MGgonads’ mass
MLliver mass
MSM sonic muscle mass
RMAG residuals of the simple linear regressions of accessory glands
on eviscerated body mass
RMGresiduals of the simple linear regressions of gonad on
eviscerated body mass
RMLresiduals of the simple linear regressions of liver on
eviscerated body mass
RMSM residuals of the simple linear regressions of sonic muscles on
eviscerated body mass
TL total length
We would like to thank the Air Force Base No. 6 of Montijo (Portugal) for allowing
this study in their military establishment. This research was funded by the Science
and Technology Foundation, Portugal (project PDCT/MAR/58071/2004,
pluriannual program UI&D 331/94 and UI&D 329, grants SFRH/BPD/14570/2003
and SFRH/BPD/41489/2007).
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M. C. P. Amorim and others
... The calling effort ( percentage of time spent calling relative to the total calling period) of acoustic advertisement calls is known to directly reflect a sender's energy expenditure in diverse taxa such as frogs (Bucher et al., 1982;Taigen and Wells, 1985), birds (Eberhardt, 1994) and insects (Nally and Young, 1981). Higher calling effort is associated with senders that are in better condition or have greater energy reserves in several vertebrate clades such as fishes (Amorim et al., 2010;Pedroso et al., 2013), birds (Reid, 1987) and frogs (Ziegler et al., 2016). Calling effort can be enhanced by increasing either calling rate, call duration, or both. ...
... Body condition was estimated using two indices, the residuals of the regression between the common logarithm (log) of body mass (in g) versus log of standard length (in cm) (COND), and Fulton's condition factor (K) which was computed using the formula 100×(body mass/standard length 3 ). Both COND and K are indirect measures of energy reserves in fish (Chellappa et al., 1995;Sutton et al., 2000) and have been used to assess body condition in the plainfin midshipman Sisneros et al., 2009) and related toadfish (Amorim et al., 2010(Amorim et al., , 2016. In 2020 (N=14 males), we measured the mass of the liver and used it to compute the hepatosomatic index, the ratio of liver mass to somatic mass expressed as a percentage computed by the formula 100×[mass of liver/(body mass−mass of gonads)]. ...
... Measures of vocal activity such as call duration, rate and effort did not correlate with the morphometrics of mass, standard length or body condition. This is in contrast to other studied fishes such as the painted goby where calling rate reflects body condition (amount of energy reserves) and the Lusitanian toadfish, where both calling rate and calling effort positively correlate with body condition (amount of energy reserves) (Amorim et al., 2010). In these species, the advertisement calls are quite short in duration being ∼0.05 s in the painted goby and ∼0.6 s in the Lusitanian toadfish and therefore it is likely that females can directly assess these quantities. ...
The plainfin midshipman fish (Porichthys notatus) has long served as a model organism for neuroethology research on acoustic communication and related social behaviors. Type I or “singing” males produce highly stereotyped, periodic advertisement calls that are the longest known uninterrupted vertebrate vocalizations, lasting up to two hours in duration. Despite the extensive literature on the acoustic behaviour of this species, it remains unclear whether reproductive males signal their quality via their highly energetic, multiharmonic advertisement calls. Here, we recorded the advertisement calls of 22 reproductive type I males at night in a controlled laboratory setting in which males were housed in artificial tanks maintained at a constant temperature (13.9+0.3°C). The duration of the advertisement calls from type I males was observed to increase from the first call of the night to the middle call after which call duration remained steady until the early morning hours and first light. A strong positive correlation was observed between loudness (SPL and maximum SPL) of the advertisement call and body size (mass and standard length; rs>0.8). In addition, an asymptotic relationship was observed between the harmonic frequencies (F0-F10) of the advertisement calls and male body condition, with harmonic frequencies initially increasing with body condition but then plateauing at higher body condition. Taken together, our results suggest that type I male advertisement calls provide reliable honest information about male quality regarding size and body condition. Such condition dependent information of calling males could potentially be used by receptive females to help facilitate mate choice decisions.
... However, some fish and invertebrate species are able to increase call rate [62][63][64] , which may improve the likelihood of being heard by conspecifics when listening space is restored between successive boat passages. Since the calls of fishes and invertebrates display wide inter-individual variation 17,65,66 , the ability to alter call rate is likely to be constrained by body size and condition 67 . Another coping strategy is to switch to predominantly visual displays 68 , a strategy used by some terrestrial species living in loud habitats 69 . ...
... Other species have been found to: reduce call rate in the presence of boat sound, possibly to avoid unnecessary energy expenditure 70,71 ; move away to quieter areas 45,72 ; and spend less time feeding 73 . Such masking release mechanisms may incur energetic and fitness costs as well as increased risk of predation 62,67 . For example, adjusting call rate may impact successful and efficient reproduction since females of some species rely on temporal variation of male calls to ...
Full-text available
Anthropogenic stressors, such as plastics and fishing, are putting coastal habitats under immense pressure. However, sound pollution from small boats has received little attention given the importance of sound in the various life history strategies of many marine animals. By combining passive acoustic monitoring, propagation modelling, and hearing threshold data, the impact of small-boat sound on the listening spaces of four coastal species was determined. Listening space reductions (LSR) were greater for fishes compared to crustaceans, for which LSR varied by day and night, due to their greater hearing abilities. Listening space also varied by sound modality for the two fish species, highlighting the importance of considering both sound pressure and particle motion. The theoretical results demonstrate that boat sound hinders the ability of fishes to perceive acoustic cues, advocating for future field-based research on acoustic cues, and highlighting the need for effective mitigation and management of small-boat sound within coastal areas worldwide.
... Because female Lusitanian toadfish are single spawners (Modesto and Canário, 2003), their reproductive success depends on a single mating decision and will profit not only from choosing a good quality male/good father but also a nest where offspring development will be maximised. In this species calling rate is associated with male quality, namely body energetic reserves that are key to parental care (Amorim et al., 2010b). In addition, nests exposed to noise will be disadvantageous for offspring growth as boat noise induces Fig. 3. Daily mean calling rate of 16 nesting males exposed to boat noise (N = 8) and control (N = 8) in two consecutive fortnights (data for 2016). ...
... In the present study, a continued lower calling activity was associated with higher cortisol levels, consistent with its regulatory role of reproductive functions, including sound production (Arterbery et al., 2010). Interestingly, males with a high mean calling rate had fewer dead eggs and elevated activity levels of the energy metabolism biomarker IDH (indicating increased aerobic metabolism) suggesting that calling rate could be advertising male quality and paternal abilities as suggested by previous studies (Amorim et al., 2010b(Amorim et al., , 2013. ...
Anthropogenic noise is a growing threat to marine organisms, including fish. Yet very few studies have addressed the impact of anthropogenic noise on fish reproduction, especially in situ. In this study, we investigated the impacts of boat noise exposure in the reproductive success of wild Lusitanian toadfish (Halobatrachus didactylus), a species that relies on advertisement calls for mate attraction, using behavioural, physiological and reproductive endpoints. Two sets of artificial nests were deployed in the Tagus estuary and exposed to either ambient sound or boat noise during their breeding season. Toadfish males spontaneously used these nests to breed. We inspected nests for occupation and the presence of eggs in six spring low tides (in two years) and assessed male vocal activity and stress responses. Boat noise did not affect nest occupation by males but impacted reproductive success by decreasing the likelihood of receiving eggs, decreasing the number of live eggs and increasing the number of dead eggs, compared to control males. Treatment males also showed depressed vocal activity and slightly higher cortisol levels. The assessment of oxidative stress and energy metabolism-related biomarkers revealed no oxidative damage in noise exposed males despite having lower antioxidant responses and pointed towards a decrease in the activity levels of energy metabolism-related biomarkers. These results suggest that males exposed to boat noise depressed their metabolism and their activity (such as parental care and mate attraction) to cope with an acoustic stressor, consistent with a freezing defensive response/behaviour. Together, our study demonstrates that boat noise has severe impacts on reproductive fitness in Lusitanian toadfish. We argue that, at least fishes that cannot easily avoid noise sources due to their dependence on specific spawning sites, may incur in significant direct fitness costs due to chronic noise exposure.
... Therefore, harmonic sounds with a series of units will increase signal distinctiveness and likely support signal discrimination (Parmentier and Frederich, 2016); the characteristics of the hoot call in F. variegata fit this explanation. For Lusitanian toadfish males, higher calling rate, calling effort, and amplitude modulation in their advertisement calls could be more attractive to females (Amorim et al., 2010); longer and more complex boatwhistles produced at a faster rate could be more attractive as well (Winn, 1967(Winn, , 1972Fish, 1972;Thorson and Fine, 2002). Similarly, longer hoots with more units could be more attractive to ripe females than the short sporadic agonistic grunts. ...
Full-text available
The variegated cardinalfish Fowleria variegata produces grunt and hoot calls during agonistic and courtship interactions. Both sounds are tonal and occur as single and multiunit calls. Grunts are of short duration with variable frequency spectra. Hoots are longer, have a higher fundamental frequency, and a more developed harmonic structure. Agonistic grunt calls and short hoot calls (1–2 hoots) are produced during chases and when striking an individual or a mirror. Grunts are produced primarily in male-female and mirror-image encounters, and short hoot calls are produced primarily in male-male interactions. During the reproductive period, long hoot calls (three and four hoots) are the main sound type in a mix-sexed tank and at Dongsha Atoll. These are likely produced by males because isolated females are silent, and isolated males emit long hoot calls. Courtship interactions are mostly silent, and males are silent after capturing eggs for oral brooding. Tank sounds peak at dusk to early evening with a smaller peak at noon, although there are dusk and dawn peaks at Dongsha Atoll. Tank sounds exhibit a semilunar rhythm with peaks at the new and full moon. Other cardinalfish species from the atoll produce grunts but not hoot calls.
... As for navigation and other nautical activities, they can generate considerable economic spin-offs with an influx of pleasure boaters (see Tables 8.2 and 8.4). However, these activities can also create problems such as bank erosion, destruction of seagrass beds through mooring, introduction of micropollutants into the sediment bed, physical disturbance of the environment by propellers, underwater noise pollution (Banner & Hyatt 1973, Herbert et al. 2009, Amorim et al. 2010, Holt & Johnston 2015, Lathrop et al. 2017, Glasby & West 2018, Smott et al. 2018). ...
... Male condition has been shown to correlate with aspects of acoustic courtship (Amorim et al., 2013b;Pedroso et al., 2013). The best example may be female Lusitanian toadfish (Halobatrachus didactylus) that prefer males with a higher vocal activity, which also reflects body condition (Amorim et al., 2010;Vasconcelos et al., 2012). In addition, courtship sounds vary between species and are potentially used in species recognition (Amorim et al., 2004;Blom et al., 2016;Crawford et al., 1997;Pedroso et al., 2013;Verzijden et al., 2010). ...
Full-text available
Many teleost fishes use acoustic and visual signalling during courtship. Such displays may convey information about body condition. Here we experimentally altered body condition of sand goby (Pomatoschistus minutus) males to examine effects on acoustic and visual courtship and subsequent spawning decisions. Over two weeks, males fed in excess were fed daily, whereas food-deprived males were fed once a week. Females only spawned with males that produced courtship sound. However, there were no treatment effects on the occurrence of spawning and males fed in excess did not invest more in visual or acoustic courtship than food-deprived males. That said, males fed in excess built more well-covered nests, with more sand piled on top, compared to food-deprived males. Male condition measured as lipid content differed significantly between treatments. However, only males fed in excess differed in lipid content from wild caught males, indicating that in nature, males are of similar condition to males in the low condition treatment group. Apart from the importance of courtship sound, the only male or female behaviour predicting reproductive success was if male displayed in the nest opening. Males often produce courtship sounds together with a visual display in this position. A female dark-eye display did not associate with reproductive success which, together with previous results, suggest a non-ornamental function of this trait. We conclude that male courtship sounds appear to be crucial in female mate choice, but the information content of the courtship sounds and how it relates to male condition remains elusive.
... Regardless, it is typically males that vocalise to attract a mate and signify their fitness. For example, higher drumming activity in male painted gobies (Pomatoschistus pictus) is a good predictor of size, condition factor (Fulton's K) and fat reserves (Amorim et al., 2013), and calling rate and effort are good indicators of gonad size in the Lusitanian toadfish (Halobatrachus didactylus: Amorim et al., 2010). Males also produce sounds when defending territory (Myrberg, 1997;Bass and McKibben, 2003;Parmentier et al., 2010) and during competitive or aggressive interactions with hetero-or conspecifics (e.g. ...
Rising levels of anthropogenic underwater sound may have negative consequences on freshwater ecosystems. Additionally, the biological relevance of sound to fish and observed responses to human-generated noise promote the use of acoustics in behavioural guidance technologies that are deployed to control the movement of fish. For instance, acoustic stimuli may be used to prevent the spread of invasive fishes or facilitate the passage of vulnerable native species at man-made obstructions. However, a strong understanding of fish response to acoustics is needed for it to be effectively deployed as a fisheries management tool, but such information is lacking. Therefore, this thesis investigated the group behavioural responses of cyprinids to acoustic stimuli. A quantitative meta-analysis and experimental studies conducted in a small-tank or large open-channel flume were used to address key knowledge gaps that are necessary to improve the sustainability of acoustic deterrent technologies, and assist in conservation efforts to reduce the negative impacts of anthropogenic noise. Current understanding on the impact of anthropogenic noise on fishes (marine, freshwater and euryhaline species) was quantified. The impact of man-made sound is greatest for fish experiencing anatomical damage, for adult and juveniles compared to earlier life-stages, and for fish occupying freshwater environments. These findings suggest a review of the current legislation covering aquatic noise mitigation which commonly focus on marine-centric strategies, thereby undervaluing the susceptibility of freshwater fish to the rising levels of anthropogenic sound. Limitations and knowledge gaps within the literature were also identified, including: 1) group behavioural responses to sound, 2) the response of fish to different fundamental acoustic properties of sound, 3) system longevity (e.g. habituation to a repeated sound exposure), and 4) site-specific constraints. Fish movement and space use were quantified using fine-scale behavioural metrics (e.g. swimming speed, shoal distribution, cohesion, orientation, rate of tolerance and signal detection theory) and their collective response to acoustics assessed using two approaches. First, a still-water small tank set-up allowed for the careful control of confounding factors while investigating cyprinid group response to fundamental acoustic properties of sound (e.g. complexity, pulse repetition rate, signal-to-noise ratio). Second, a large open-channel flume enabled the ability of a shoal to detect and respond to acoustic signals to be quantified under different water velocities. Shoals of European minnow (Phoxinus phoxinus), common carp (Cyprinus carpio) and roach (Rutilus rutilus) altered their swimming behaviour (e.g. increased group cohesion) in response to a simple low frequency tonal stimulus. The pulse repetition rate of a signal was observed to influence the long-term behavioural recovery of minnow to an acoustic stimulus. Furthermore, signal detection theory was deployed to quantify the impact of background masking noise on the group behavioural response of carp to a tonal stimulus, and investigate how higher water velocities commonly experienced by fish in the wild may influence the response of roach to an acoustic stimulus. Fine-scale behavioural responses were observed the higher the signal-to-noise ratio, and discriminability of an acoustic signal and the efficacy at which fish were deterred from an insonified channel was greatest under higher water velocities. The information presented in this thesis significantly enhances our understanding of fish group responses to man-made underwater sound, and has direct applications in freshwater conservation, fish passage and invasive species management.<br/
... As for navigation and other nautical activities, they can generate considerable economic spin-offs with an influx of pleasure boaters (see Tables 8.2 and 8.4). However, these activities can also create problems such as bank erosion, destruction of seagrass beds through mooring, introduction of micropollutants into the sediment bed, physical disturbance of the environment by propellers, underwater noise pollution (Banner & Hyatt 1973, Herbert et al. 2009, Amorim et al. 2010, Holt & Johnston 2015, Lathrop et al. 2017, Glasby & West 2018, Smott et al. 2018). ...
This chapter presents the causes of physical and ecological degradation of estuaries in relation to human activities and climate change. The direct and indirect effects of degradation on ecosystem services and fish are listed, as well as the key questions that need to be answered in order to undertake rehabilitation and restoration actions. Ecohydrology and ecoengineering are indispensable tools to be mobilised alongside a variety of models to guide actions in favour of habitat and whole estuary functioning. Finally, several examples of restoration are presented to move from theory to practice. The restoration of estuaries has often become essential to ensure sustainable fish communities and requires a holistic view of the problems and a coordination of efforts to ensure the success of the actions undertaken.
Anthropogenic noise is considered a major underwater pollutant as increasing ocean background noise due to human activities is impacting aquatic organisms. One of the most prevalent anthropogenic sounds is boat noise. Although motorboat traffic has increased in the past few decades, its impact on the communication of fish is still poorly known. The highly vocal Lusitanian toadfish (Halobatrachus didactylus) is an excellent model to test the impact of this anthropogenic stressor as it relies on acoustic communication to attract mates. Here, we performed two experiments to test the impact of boat noise on the acoustic communication of the Lusitanian toadfish. Using the auditory evoked potential (AEP) technique, we first compared the maximum distance a fish can perceive a boatwhistle (BW), the mate attraction acoustic signal, before and after embedding it in boat noise. Noises from a small motorboat and from a ferryboat reduced the active space from a control value of 6.4–10.4 m to 1.7–2.5 m and 6.3–6.7 m, respectively. In the second experiment we monitored the acoustic behaviour of breeding males exposed to boat noise playbacks and we observed an increase in the inter-onset interval of BWs and a disruption of the usual vocal interactions between singing males. These results demonstrate that boat noise can severely reduce the acoustic active space and affect the chorusing behaviour in this species, which may have consequences in breeding success for individuals and could thus affect fitness.
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We measured glycogen, lipid and water concentrations in toadfish (Opsanus tau) fast sonic muscle and white body muscle, and glycogen and lipid were localized histochemically in the sonic muscle. Sonic muscle had 5.05 μg of glycogen per mg wet weight, 15.64% fat and 81% water. These values were 2.2, 6.2 and 0.18 times higher than the corresponding concentrations in white body muscle. The presence of abundant glycogen and fat provides potential fuel for anaerobic and aerobic metabolism and agrees with the designation of sonic muscle as fast oxidative glycolytic. No sexual or ontogenetic differences were present in glycogen, fat or water concentrations in sonic or body muscle, and these molecules cannot be used to explain sexual differences in sound production. Glycogen is localized in sarcoplasm under the sarcolemma, in sarcoplasmic reticulum and throughout the sarcoplasmic core. Lipids have a similar distribution, except that their distribution in the core is restricted to the periphery. These findings are in accord with ultrastructure of sonic muscle fibers.
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We quantified crepuscular variation in the emission rate and call properties of the boatwhistle advertisement call of Gulf toadfish, Opsanus beta, from a field recording of a natural population of nesting males in the Florida Keys. Their calls are more variable and complex than previously reported. A call typically starts with a grunt followed by one to five tonal boop notes (typically two or three) and lasts for over a second. The first boop is considerably longer than later ones, and intervals between boops are relatively constant until the final interval, which approximately doubles in duration. Positions of fish are fixed and calls are sufficiently variable that we could discern individual callers in field recordings. Calling rate increases after sunset when males tend to produce shorter calls with fewer notes. Analysis by number of notes per call indicates some individuals decrease the number of initial grunts and the duration of the first note, but most of the decrease results from fewer notes. To our knowledge this sort of call plasticity has not been demonstrated before in fishes. We suggest that call shortening lowers the chances of overlapping calls of other males and that the small amount of time actually spent producing sound (total on time) is an adaptation to prevent fatigue in sonic muscles adapted for speed but not endurance.
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Several batrachoidids have been known to produce sounds associated with courtship and agonistic interactions, and their repertoires have been studied acoustically and behaviourally. In contrast, sound production of the Lusitanian toadfish Halobatrachus didactylus, although often noted, has not been acoustically studied.This sedentary predator of Northeastern Atlantic coastal waters is usually found in sandy and muddy substrates, under rocks or crevices. Sound recordings were made in Ria Formosa, a lagoon complex in southern Portugal. The sound producing apparatus was studied in adult individuals of both sexes captured by local fishermen.It is shown that this species produces acoustic emissions similar to other batrachoidids. It produces a long, rhythmical, tonal sound, often in choruses, which is comparable to the boatwhistle or hum signals of Opsanus and Porichthys, and a complex of signals that were classified as grunts, croaks, double croaks and mixed calls (‘grunt-croak’). As in other toadfishes, H. didactylus presents sonic muscles connected to a bi-lobed swimbladder. Asynchronous contractions of the sonic muscles were detected when massaging the ventral surface of the fish.
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Previous work has shown that neurons in the sonic motor nucleus of the oyster toadfish, Opsanus tau, grow larger in males than in females and increase in size and number for 7–8 years. In order to correlate postnatal motoneuron development with growth of target muscle fibers, we examined the ontogeny of sonic muscle growth. Both the swim bladder and attached sonic muscles increased in size for life and were, respectively, 20 and 44% larger in males than in females. The muscle and swim bladder grew at an equivalent rate in males, whereas in females, muscle growth did not keep up with bladder growth. The number of muscle fibers increased about 16-fold (31 000 to 488 000), and mean minimum fiber diameter increased almost 3-fold (11.5 to 28.6 μm) as fish grew. Fibers were 15.3% larger in females than in males (adjusted means of 21.9 and 19.0 μm, respectively), but males had 47% more fibers per muscle (adjusted means of 307 000 and 209 000). Muscle fibers also exhibited morphological changes. Most of the fibers in two juveniles had yet to differentiate the core of sarcoplasm characteristic of sonic muscle, whereas the largest cells in mature males and females tended to have multiple pockets of sarcoplasm and a contractile cylinder split into fragments. Multiple pockets in large fibers and the presence of smaller fibers in males than females are interpreted as adaptations for increased speed and fatigue resistance.
Sexual selection theory proposes that elaborate male secondary sexual characteristics, including complex song, may increase the attractiveness of males by honestly communicating to females their genetic quality or ability to provide material reproductive resources such as parental care. The Gray Catbird (Dumetella carolinensis) is sexually monochromatic, but males sing complex songs during the breeding season while females do not. We tested the hypotheses that song-phrase versatility and rate of song-phrase production are honest indicators of male parental effort. We predicted that both song-phrase versatility and rate of production would be positively correlated with paternal chick feeding rate. Paternal chick feeding rate was not significantly related to song-phrase versatility, but it was positively and significantly correlated with song-phrase production rate. Thus, song-phrase production rate may serve as a more reliable indicator of male parental quality than song versatility in the Gray Catbird.
Parental care may be defined as an association between parent and offspring after fertilisation that enhances offspring survivorship. This phenomenon has attracted the attention of evolutionary biologists since Darwin; however, it was not until the recent insurgence of behavioural ecology and sociobiology (e.g. Williams 1966a; Trivers 1972; Alexander 1974; Wilson 1975) that the variety of parental care patterns in animals has attracted such rigorous study. Perhaps because we ourselves are mammals, we tend to think of parental care as being the principal occupation of females, possibly with some help from males. A survey of the vertebrates, however, reveals that mammals are merely at one end of the spectrum, with predominantly female care, and fishes are at the other end, with predominantly male care (Table 11.1; see also Chapter 10 by Turner, this volume). Within teleost fishes with external fertilisation (about 85 per cent of all teleost families), one finds that the four states of parental care, ranked in descending order of their frequencies, are: no care, male care, biparental care, and female care. This seemingly peculiar trend has attracted considerable attention from evolutionary biologists, who have proposed several hypotheses about the origins of parental care in fishes (see reviews by Maynard Smith 1977; Blumer 1979; Perrone and Zaret 1979; Baylis 1981; Gross and Shine 1981; Gross and Sargent 1985).
Data from several field studies support the hypothesis that female European starlings, Sturnus vulgaris, attend to variation among the songs of conspecific males when making mate-choice decisions. However, for a variety of methodological reasons, direct evidence for female preferences based on song in starlings has been lacking. This study presents a novel technique for assaying directly female preference and choice in European starlings by using the presentation of conspecific male song as an operant reinforcer in a controlled environment. Using an apparatus in which the playback of songs from different nestboxes is under the operant control of the subject, we demonstrate how the reinforcing properties of conspecific song can be used to measure female preference and choice. The results of the study suggest three conclusions. First, female starlings prefer naturally ordered conspecific male songs over reversed songs. Second, female starlings display robust preferences for longer compared with shorter male song bouts. Behaviour in the operant apparatus varied directly with male song bout length. Third, preferences based on song bout length are sex specific. Male starlings failed to respond differentially to the same stimuli for which females showed strong preferences. These results suggest that male-male variation in song bout length is important for mate choice among starlings. In addition, we detail the use of a novel behavioural assay for measuring female preferences that can be applied to similar behaviours in other species of songbirds.