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Hearing Sensitivity of the Painted Goby, Pomatoschistus pictus

  • Ocean Science Consulting

Abstract and Figures

Pomatoschistus pictus is a coastal and estuarine species that inhabits shallow gravel and sand ­substrate areas of the eastern Atlantic Ocean and Mediterranean Sea (Miller 1986). Studies on P. pictus show that, like in other species of this genus (Malavasi et al. 2008), males produce sounds during courtship and agonistic contexts (Amorim and Neves 2007, 2008).
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A.N. Popper and A. Hawkins (eds.), The Effects of Noise on Aquatic Life,
Advances in Experimental Medicine and Biology 730, DOI 10.1007/978-1-4419-7311-5_24,
© Springer Science+Business Media, LLC 2012
M. Bolgan ()
Facoltà di Scienze Matematiche, Fisiche e Naturali, Dipartimento di Scienze della Vita-CSEE ,
University of Trieste , 34127 Trieste , Italy
S. S. Pedroso M. C. P. Amorim
Instituto Superior de Psicologia Aplicada , Unidade de Investigação em Eco-Etologia , 1149–041 Lisbon , Portugal
R. O. Vasconcelos J. M. Jordão P. J. Fonseca
Centro de Biologia Ambiental, Departamento de Biologia Animal ,
Faculdade de Ciências da Universidade de Lisboa , 1749–016 Lisbon , Portugal
1 Introduction
Pomatoschistus pictus is a coastal and estuarine species that inhabits shallow gravel and sand
substrate areas of the eastern Atlantic Ocean and Mediterranean Sea (Miller 1986 ) . Studies on
P. pictus show that, like in other species of this genus (Malavasi et al. 2008 ) , males produce sounds
during courtship and agonistic contexts (Amorim and Neves 2007, 2008 ) .
The amount of anthropogenic noise pollution has been increasing significantly in the last decades
in coastal environments (Codarin et al. 2009 ; Ross 2005 ) . A noisy coastal environment may strongly
impact the ability of such a vocal species to communicate and, ultimately, reproduce. A first step in
understanding the impact of anthropogenic noise is to describe this species’ hearing sensitivity.
However, nothing has been described in terms of the auditory abilities of this genus to date. This
study presents the first data on the hearing sensitivity of P. pictus .
2 Materials and Methods
Six adult P. pictus were caught in April 2010 at Parede (38°41 ¢ N, 009°21 ¢ W), Portugal. The fish
were maintained in aquaria at 18 ± 1°C.
Hearing thresholds were estimated using the auditory evoked potential (AEP) recording technique.
Test subjects were mildly immobilized with 47.9 mg/g of pancuronium bromide diluted in teleost
saline solution. The subjects were placed just below the water surface of a plastic tank (diameter
36 cm, water depth 13 cm), 7 cm above the center of the underwater speaker disk. Fish respiration
was secured through a temperature-controlled (20 ± 1°C) gravity-fed seawater circulation system
Hearing Sensitivity of the Painted Goby,
Pomatoschistus pictus
Marta Bolgan, Silvia S. Pedroso, Raquel O. Vasconcelos,
Joana M. Jordão, M. Clara P. Amorim, and Paulo J. Fonseca
110 M. Bolgan et al.
using a micropipette tip inserted in the subject’s mouth. The experimental tank was positioned on a
vibration-insulated table surrounded by a Faraday cage.
The AEPs were recorded using platinum electrodes (diameter 1 mm). The recording electrode
was placed above the brain stem and the reference electrode was close to the nares. Electrode leads
were connected to a differential AC amplifier (CP 511, Grass Technologies). The AEP signal was
monitored with an oscilloscope and digitized using an analog-to-digital (A/D) converter (Edirol
UA25, Roland) connected to a personal computer running Adobe Audition 3.0 (Adobe Systems).
Sound stimuli were created with Adobe Audition 3.0 and consisted of tone pulses presented
1,000 times at opposite polarities. Hearing thresholds were estimated at 15 Hz with a repetition rate
of 5 s
-1 , 30 and 60 Hz with a repetition rate of 10 s
-1 , and 100, 200, 300, 400, 500, 800, and 1,000 Hz
with a repetition rate of 20 s
-1 , randomly presented. Sound stimuli ranged from 2 (15–100 Hz) to 5
complete cycles. Stimuli, presented in 4-dB steps from 92 to 136 dB re 1 mPa, were fed to a home-
made underwater speaker device and amplifier (P. J. Fonseca) using the laptop and an A/D converter
(Edirol UA 25). Before each experiment, the sound stimuli were calibrated with a hydrophone
(Brüel and Kjaer 8103) connected to a sound level meter (Brüel and Kjaer Mediator 2238) placed
in the same position as the fish. AEPs were averaged to minimize stimulus artifacts using home-
made software (P. J. Fonseca).
3 Preliminary Results
Some of the AEP waveforms obtained indicated a clear double-frequency effect, which was
further reassurance of a biological response. The audiogram showed that P. pictus sensitivity is
higher at low frequencies between 15 and 400 Hz, with the lowest hearing threshold of 105 dB re
1 mPa at 15 Hz (Fig. 1 ). This best hearing range matches the main sound energy of both courtship
(thump and drum) and agonistic (drum) calls, i.e., between ~83 and 297 Hz (Amorim and Neves
2007, 2008 ) .
Fig. 1 Hearing thresholds of Pomatoschistus pictus showing the range of the main sound energy of agonistic and
courtship calls. Values are averages ± SD
Hearing Sensitivity of the Painted Goby, Pomatoschistus pictus
4 Discussion
The hearing sensitivity of P. pictus seems adapted to detect conspecific sounds, indicating that
acoustic communication provides essential information during species-specific interactions. In
addition, we suggest that the enhanced low-frequency sensitivity (below 60 Hz) could be the result
of an evolutionary adaptation that, for a benthonic species, maximizes the ability to detect prey,
predators, and mates.
Noise pollution is a threat to marine gobies (Codarin et al. 2009 ) . Noise energy of man-made
activity is mainly concentrated below 1 kHz (Nakahara 1999 ) . Because P. pictus acoustic commu-
nication occurs within this frequency range, the concern is that anthropogenic noise might be
strongly masking their hearing and hence their ability to communicate and to react to relevant
acoustic stimuli. Future work is needed to test the masking effect of noise pollution on hearing in
P. pictus .
Amorim MCP, Neves ASM (2007) Acoustic signaling during courtship in the painted goby, Pomatoschistus pictus .
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Amorim MCP, Neves ASM (2008) Male painted gobies ( Pomatoschistus pictus ) vocalize to defend territories.
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tion in three fish species living in a protected area (Miramare, Italy). Mar Pollut Bull 58:1880–1087.
Malavasi S, Collatuzzo S, Torricelli P (2008) Interspecific variation of acoustic signal in Mediterranean gobies
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... Lowest thresholds occurred at 100-200 Hz at 65-80 dB re 1 μm/s 2 , which is comparable in both sensitivity and bandwidth to the AEP audiograms collected for another percid, Perca fl uviatilis (Amoser and Ladich 2005 ). In gobies, pressure audiograms have been collected from Padogobius bonelli and Padogobius nigricans , Neogobius melanostomus (Belanger et al. 2010 ;Zeyl et al. 2013 ), and Pomatoschistus pictus (Bolgan et al. 2012 ; Fig. 3c, d ). The particle motion audiograms available for Gobius cruentatus (Wysocki et al. 2009 ) and N. melanostomus found best sensitivities at 100-200 Hz at ~70 dB re 1 μm/s 2 . ...
... A goldfi sh ( Carassius auratus ) audiogram collected under the same experimental setup is shown for comparison ( n = 5). Goby audiogram sources include: Pomatoschitus pictus (Bolgan et al. 2012 ), Padogobius bonelli (formerly P. martensii ) and Padogobius nigricans , Gobius cruentatus (Wysocki et al. 2009 ), and Neogobius melanostomus (males and females averaged, Zeyl et al. 2013 ). Sculpin audiogram sources include: Cottus rhenanus and Cottus perifretum (Colleye et al. 2013 ), Cottus ricei (Mann et al. 2007 frequency of E. crossopterum , which resides in relatively quiet pools, but only about a 10 dB difference for E. fl abellare , which inhabits noisier riffl es. ...
Darters (Perciformes, Percidae), sculpins (Perciformes, Cottidae), and gobioids (Gobiiformes, Gobioidei) exhibit convergent life history traits, including a benthic lifestyle and a cavity nesting spawning mode. Soniferous species within these taxa produce pulsed and/or tonal sounds with peak frequencies below 200 Hz (with some exceptions), primarily in agonistic and/or reproductive contexts. The reduced or absent swim bladders found in these taxa limit or prevent both hearing enhancement via pressure sensitivity and acoustic amplification of the contracting sonic muscles, which are associated with the skull and pectoral girdle. While such anatomies constrain communication to low frequency channels, optimization of the S/N (signal-to-noise) ratio in low frequency channels is evident for some gobies, as measured by habitat soundscape frequency windows, nest cavity sound amplification, and audiograms. Similar S/N considerations are applicable to many darter and sculpin systems. This chapter reviews the currently documented diversity of sound production in darters, sculpins, and gobioids within a phylogenetic context, examines the efficacy of signal transmission from senders to receivers (sound production mechanisms, audiograms, and masking challenges), and evaluates the potential functional significance of sound attributes in relation to territorial and reproductive behaviours.
... Although few systematic comparisons of acoustic signals are available for closely-related fish species [21], temporal characteristics of sounds are thought to be important carriers of species-specific information in fish. In fact distinct temporal patterns, such as pulse number and rate, often differentiate sounds of closely-related sympatric species such as in the Pomacentridae, Cichlidae and Mormyridae [18,20,41,45] . Further, playback experiments testing male pomacentrids from the genus Stegastes provided evidence that fish can distinguish conspecific courtship sounds from those of closelyrelated congenerics, based on the number of pulses and pulse rate [17,45]. ...
... In fact distinct temporal patterns, such as pulse number and rate, often differentiate sounds of closely-related sympatric species such as in the Pomacentridae, Cichlidae and Mormyridae [18,20,41,45] . Further, playback experiments testing male pomacentrids from the genus Stegastes provided evidence that fish can distinguish conspecific courtship sounds from those of closelyrelated congenerics, based on the number of pulses and pulse rate [17,45]. Our results are consistent with the hypothesis that the pulse rate – and possibly also the pattern of sound emission (i.e. the sequence considering sound intervals) – contribute to the recognition of conspecific mates, although sound intervals show higher intra-specific variability than pulse rate (Table 2) and thus potentially provide less reliable species-specific acoustic cues. ...
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Acoustic signals can encode crucial information about species identity and individual quality. We recorded and compared male courtship drum sounds of the sand goby Pomatoschistus minutus and the painted goby P. pictus and examined if they can function in species recognition within sympatric populations. We also examined which acoustic features are related to male quality and the factors that affect female courtship in the sand goby, to determine whether vocalisations potentially play a role in mate assessment. Drums produced by the painted goby showed significantly higher dominant frequencies, higher sound pulse repetition rates and longer intervals between sounds than those of the sand goby. In the sand goby, male quality was predicted by visual and acoustic courtship signals. Regression analyses showed that sound amplitude was a good predictor of male length, whereas the duration of nest behaviour and active calling rate (i.e. excluding silent periods) were good predictors of male condition factor and fat reserves respectively. In addition, the level of female courtship was predicted by male nest behaviour. The results suggest that the frequency and temporal patterns of sounds can encode species identity, whereas sound amplitude and calling activity reflects male size and fat reserves. Visual courtship duration (nest-related behaviour) also seems relevant to mate choice, since it reflects male condition and is related to female courtship. Our work suggests that acoustic communication can contribute to mate choice in the sand goby group, and invites further study.
... Sound stimuli consisted of three reef and three offshore recordings, each cut to 3 min of duration. A low-pass filter of 3 kHz was applied to the recordings so that the frequency of sound stimuli was below the resonance frequency of the experimental tank [56] while matching the auditory ability of the species [57]. ...
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Atmospheric CO 2 levels have been increasing at an unprecedented rate due to anthropo-genic activity. Consequently, ocean pCO 2 is increasing and pH decreasing, affecting marine life, including fish. For many coastal marine fishes, selection of the adult habitat occurs at the end of the pelagic larval phase. Fish larvae use a range of sensory cues, including sound, for locating settlement habitat. This study tested the effect of elevated CO 2 on the ability of settlement-stage temperate fish to use auditory cues from adult coastal reef habitats. Wild late larval stages of painted goby (Pomatoschistus pictus) were exposed to control pCO 2 (532 μatm, pH 8.06) and high pCO 2 (1503 μatm, pH 7.66) conditions, likely to occur in nearshore regions subjected to upwelling events by the end of the century, and tested in an auditory choice chamber for their preference or avoidance to nighttime reef recordings. Fish reared in control pCO 2 conditions discriminated reef soundscapes and were attracted by reef recordings. This behaviour changed in fish reared in the high CO 2 conditions, with settlement stage larvae strongly avoiding reef recordings. This study provides evidence that ocean acidification might affect the auditory responses of larval stages of temperate reef fish species, with potentially significant impacts on their survival.
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Anthropogenic underwater noise is a global pollutant of increasing concern but its impact on reproduction in fish is largely unknown. Hence, a better understanding of its consequences for this important link to fitness is crucial. Working in aquaria, we experimentally tested the impact of broadband noise exposure (added either continuously or intermittently), compared to a control, on the behaviour and reproductive success of the common goby (Pomatoschistus microps), a vocal fish with exclusive paternal care. Compared to the intermittent noise and control treatments, the continuous noise treatment increased latency to female nest inspection and spawning and decreased spawning probability. In contrast, many other female and male pre-spawning behaviours, and female ventilation rate (proxies for stress levels) did not differ among treatments. Therefore, it is likely that female spawning decisions were delayed by a reduced ability to assess male acoustic signals, rather than due to stress per se and that the silent periods in the intermittent noise treatment provided a respite where the females could assess the males. Taken together, we show that noise (of similar frequency range as anthropogenic boat noise) negatively affects reproductive success, particularly under a continuous noise exposure.
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Gobies emit sounds during different stages of reproduction, including courtship, pre-spawning events (in the nest) and spawning. The breeding sounds of the painted goby Pomatoschistus pictus and associated courtship behaviour were recorded in captivity and described for the first time. Males emitted thump-like sounds mainly when displaying alone in the nest and produced drumming sounds outside the nest. Thumps have never been reported for other species of the genus Pomatoschistus. Thumps were short (~80 ms) very-low frequency (below 100 Hz) non-pulsed sounds, whereas drums were longer (hundreds of ms) and consisted of low frequency (~300 Hz) pulse trains. Thump characteristics varied significantly among males but also showed high within-male variability. The frequency of thump emissions and courtship behaviour (total number of courtship displays, lead and nest display) were positively correlated with male size but not with male somatic condition. Thump bursts emitted during nest displays were significantly longer than when emitted with other behaviours. These results suggest that larger males courted females more intensively, both with visual and acoustic displays, than smaller ones.
Many fish species emit sounds in agonistic contexts. During direct confrontations sounds are typically produced during the display phase in conjunction with visual exhibitions. Here we studied sound production during territorial defence in captive painted gobies, Pomatoschistus pictus, and related acoustic parameters with male traits and the date of recording (Julian day, i.e., with the approach of the peak of the breeding season). Territorial males emitted drumming sounds during displays that involved darkening the chin and fins, spreading fins and quivering the body. Drums were trains of low frequency pulses (≈23 pulses) repeated every 27 ms and usually lasting under a second. Drums were produced in short sequences of sounds (bursts). All acoustic parameters differed significantly among males. Drum and burst duration, and drum number of pulses increased significantly with male size. Calling duration (including drum, burst duration and drum number of pulses) also increased significantly with Julian date and presented a high intra-male variability, suggesting that these parameters may also depend on the individual's motivation. We provide the first report for agonistic sound production in sand gobies and give evidence that sound parameters contain information that can be used during mutual assessment in contests over territories.
Sound production of 11 Mediterranean goby species, belonging to five different genera, have been comparatively analysed on the basis of the quantitative properties of the acoustic signal emitted by the male in both the reproductive and aggressive context. The results obtained showed that three groups of species can be recognized on the basis of signal similarity: the larger sized species (genus Padogobius and Gobius paganellus) producing tonal sounds, showing high values of pulse rate and low values of duration; the larger-sized species producing grunt sounds (genus Gobius and Zosterisessor) with low pulse rate and low duration; and the small-sized species producing grunt sounds (genus Pomatoschistus and Knipowitschia) with low pulse rate and high duration. The comparison between these results and those found in previous studies suggests congruence between the acoustic affinities among species and that obtained by means of morphological and genetic data. Furthermore, first hypotheses on the evolution of acoustic communication and the associated mechanisms in this fish group are suggested. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 763–778.
The WWF-Natural Marine Reserve of Miramare (Trieste, Italy) is located in a major industrial and vacation area in the Adriatic Sea. Consequently, noise emanating from boating and shipping is an inevitable factor for local fishes. This study investigates the effects of ambient and ship noise on representatives of three vocal fish families with different hearing abilities. Ambient and ship noise were recorded, their sound pressure levels measured and played back in the lab. Auditory sensitivity was determined in Chromis chromis, Sciaena umbra and Gobius cruentatus, utilizing the auditory evoked potential recording technique. Compared to lab conditions, hearing thresholds determined during ambient noise playbacks were barely masked. Contrary, the noise emanating from a cabin-cruiser substantially reduced auditory sensitivity relative to thresholds in ambient noise. This masking effect was most pronounced in the frequency range where acoustic communication takes place. Boat noise potentially affects acoustic communication in fishes inhabiting the reserve.
The rapid increase in world shipping results in an increase in low-frequency ambient noise at an average rate of about 1/2 dB per year. During the past 10 years there has been a virtual revolution in the sizes and speeds of merchant ships, resulting in significant increases in the noise radiated by the average ship. This trend is continuing. In this paper, the trends in world merchant shipping will be presented, including important changes in propulsion plants as well as in numbers and sizes of ships. The need for radiated noise measurements of these new ship types will be stressed. Ambient noise is also dependent on the geographical distribution of shipping. The LRAPP-sponsored program to establish standard shipping distributions for the Northern Hemisphere will be discussed, and the reliability of current information will be assessed.