Sound Generation

  

Fishes have evolved the highest diversity of sound-generating organs found among vertebrates. They range from rapidly contracting muscles to vibrate the swim bladder and pectoral girdle to bony elements, which produce sound by stridulation or plucking tendons (Fine and Ladich 2003, Ladich and Fine 2006, Ladich and Bass 2011, Ladich 2014).

For example the sonic (drumming) muscles in piranhas insert on a broad tendon that surrounds the swim bladder ventrally (Ladich and Bass 2005). Swim bladder muscles of fishes can contract at frequencies up to 250 Hz, making them the fastest muscles in the animal kingdom.

Piranha sound sample

To operate at such high frequencies fish have developed sonic muscles fibres containing thin myofibrils surrounded by a well-developed sarcoplasmic reticulum (SR). Catfishes exhibit a large diversity in the fine structure of these muscles and they even possess muscles protecting the inner ear during drumming (Ladich 2001).

 

The diversity of sonic/vocal organs is not only found between different orders but is also expressed in varying degrees within orders. The degree to which this diversity is paralleled by CNS development and the possible homologies among the sound-generating mechanisms has been investigated in five collaboration with research laboratories in the USA.

The sonic motor nuclei (SMNs) innervating the sound-producing organs are always found in the brainstem and spinal cord. The results suggest several patterns of organization for sound-producing systems in teleost fishes. Pectoral fin/girdle-associated muscles are innervated by SMNs positioned within the ventral motor column, and non-pectoral associated muscles are innervated by SMNs located on or close to the midline ventrally or laterally of the central canal (Ladich & Bass 1998, 2005, 2011).

 

Acoustic Communication

Fishes utter sounds in a variety of behavioural contexts, like agonistic interactions, courtship, spawning and competitive feeding. The functional significance of sounds has seldom been investigated despite the enormous amount of behavioural studies that have addressed the phenomenon (Ladich 2004, Ladich and Myrberg 2006). This can be partly explained by methodological problems (difficulties in creating adequate acoustic conditions underwater) but there are also biological reasons for the lack of functional analyses.

Croaking sounds of gouramis

The majority of sounds appear to be relevant at close distance so playback-experiments rarely elicit unambiguos behaviour without additional visual stimuli. In the croaking gourami Trichopsis vittata differences in dominant frequencies and intensities of sounds suggest that they serve to assess the fighting ability in opponents (Ladich 1998).

The croaking gourami is the only fish species in which females are known to initiate spawning acoustically. Females produce courtship sounds which are shorter in duration and lower in sound levels than agonistic sounds (Ladich 2007).

Sex-specific differences in sounds produced during agonistic interactions have been studied in the croaking gourami and the callichthyid armoured catfish Megalechis thoracata and in courtship sounds in the longsnout seahorse Hippocampus reidi (Ladich 2007, Oliviera et al. 2014, Hadjiaghai and Ladich 2015; reviewed in Ladich 2015b).

The development of acoustic signals and of hearing was investigated in representatives on three nonrelated taxa, the croaking gourami, the Lusitanian toadfish Halobatrachus didactylus and the squeaker catfish Synodontis schoutedeni (Henglmüller and Ladich 1999, Wysocki and Ladich 2001, Vasconcelos and Ladich 2008, Lechner et al. 2010; reviewed in Ladich 2015a).

 

Sound Detection

Fish ears

Fishes have evolved an astonishing diversity of inner ears and peripheral structures facilitating sound transmission to the inner ears. The functional significance of this morphological diversity in ear structure is widely unknown (Ladich and Popper 2004, Schulz-Mirbach and Ladich 2016, Ladich and Schulz-Mirbach 2016).

 

The role of acoustic communication as a driving force for this diversity is being investigated. Comparison of the ear structures among sound-producing and non-vocal labyrinth fishes has revealed no obvious differences in either the inner ear anatomy, or the auditory sensitivity or sensory epithelia (Ladich and Popper 2001).

Several fish taxa possess peripheral structures, which conduct sound vibration to the inner ears to enhance their hearing sensitivity. Otophysines (carps, minnow, catfishes, piranhas), the most successful freshwater fish group, developed "middle ear'-like ossicles (Weberian ossicles) to transmit vibrations of the swim bladder, which functions as a tympanum, to the inner ear. The functional significance of these ossicles was examined in the goldfish. It was shown that Weberian ossicles enhance hearing by up to 30 dB depending on frequency (Ladich and Wysocki 2003, Ladich 2016).

The effects of the ontogenetic development of Weberian ossicles on hearing sensitivities have been studies in the African bullhead catfish (Lechner et al. 2011).

Catfishes reveal a high diversity in the morphology of the swimbladder and Weberian ossicles. Some possess large unpaired bladders whereas others have small, paired, encapsulated bladders. Catfishes with free bladders hear significantly better above 1 kHz than those having encapsulated bladders (Lechner and Ladich 2008). However, in thorny catfishes smaller swimbladders resulted in relatively better hearing (Zebedin and Ladich 2013; for a review see Ladich 2016).

Cichlids provide a good example to investigate effects of swim bladder morphology on hearing abilities because this species-rich family displays a high diversity in their swimbladder morphology ranging from tiny reduced bladders, to species possessing large swim bladders without extensions, to species in which the swim bladder contacts the inner ears via anterior projections. Our results indicate that anterior swim bladder extensions improve auditory sensitivities. Besides anterior extensions, the size of the swim bladder appears to be an important factor for extending the detectable frequency range (Schulz-Mirbach et al. 2012, 2013, Ladich and Schulz-Mirbach 2016).

 

 
Weberian ossicles: C - Claustrum, S - Scaphium, I - Intercalarium, T- Tripus

 

Correlation of Vocalization and Hearing in Fishes

Fishes have evolved a unique diversity of mechanisms for acoustical communication. This diversity is found both in sound-generating mechanisms and organs for acoustic perception. Fishes are able to produce different types of sounds and to perceive acoustic signals of different frequencies, temporal patterns and intensities. The aim of the comparative investigations is to show the degree of correlation between sound production and hearing in fishes .

Matched studies of intraspecific sound spectra and hearing thresholds have rarely been done in fish. There seems to be a rough correspondence in best hearing frequencies and main frequencies of sound, but mismatches have also been described (Ladich and Yan 1998, Ladich 1999, 2000, Ladich and Bass 2003b).

In order to determine whether fishes are able to utilize temporal characteristics of acoustic signals, time resolution was determined in otophysines and anabantoids by analyzing auditory evoked potentials (AEPs) to double-click stimuli with varying click periods (Wysocki and Ladich 2002). In a third step we investigated the ability of the auditory system to process fish's sounds (Wysocki and Ladich 2003, 2005b, Vasconcelos et al. 2011).

Both, sound production and hearing sensitivity are affected by the ambient temperature in ectothermic animals. The effects of temperature on sound characteristics (of stridulatory as well as drumming sounds) and on the hearing were shown in cyprinids, catfishes and croaking gouramis (Papes and Ladich 2011, Maiditsch and Ladich 2014, Ladich and Schleinzer 2015). Data in the neotropical Striped Raphael catfish Platydoras armatulus suggest that temperature affects acoustic communication in fishes (Papes and Ladich 2011).

 
Drumming and stridulation sounds of a pimelodid catfish
 

AEP recording technique

  

We have utilized the non-invasive auditory evoked potential (AEP) recording technique to measure auditory sensitivities in fishes (Kenyon et al. 1998, Ladich and Wysocki 2009, for a review see Ladich and Fay 2013). This allows us to assess the effect of long term noise exposure, the amount of masking by white noise, ambient noise, ship noise, the temporal resolution capacity of the auditory system, the detection of conspecific sounds and the functional significance of accessory hearing structures.

Hearing sensitivities were characterized in terms of sound pressure level and particle acceleration level in the three Cartesian directions using a miniature pressure-acceleration sensor (Wysocki et al. 2009, Schulz-Mirbach et al. 2010). The effects of speaker choice (underwater vs. air speaker) and fish position on hearing thresholds have been studied in the goldfish (Ladich and Wysocki 2009).

 

 

Noise, Stress and Communication

 

Over the past few years an increasing amount of man-made noise from shipping, power plants etc. has been added to the natural sound levels under water.
This noise pollution has various effects on the behaviour, physiology, communication and most likely the fitness of aquatic animals. While there is growing knowledge that anthropogenic noise has negative effects on the life of aquatic mammals, in particular of whales, much less is known about fish. Some data has shown that noise can affect hearing or even damage inner ear sensory cells, but almost nothing is known about its impact on acoustic communication or whether intense noise elicits stress responses.

Underwater ship sound

Several series of experiments are planned to address these questions. The first step involves investigating to what degree long term as well as simultaneous noise exposure can affect auditory sensitivity. For comparative purposes studies concentrate on sound-producing hearing specialists such as catfishes, cyprinids and labyrinth fishes, and on non-specialists such as sunfishes, cichlids and toadfishes.

The data show that long time noise exposure results in temporary threshold shifts (TTS) and diminishes the ability of fishes to resolve temporal patterns of sounds (Amoser and Ladich 2003, Wysocki and Ladich 2005b).

Besides TTS noise can also mask the detection of acoustic signals. We have measured ambient noise encountered in various habitats in Austria (lakes, streams, rivers, backwaters) and investigated the masking effect of continuous white noise and of ambient noise on the auditory sensitivity of hearing specialists and hearing generalists (Wysocki and Ladich 2005a, Amoser and Ladich 2005, Scholz and Ladich 2006, Wysocki et al. 2007, Amoser and Ladich 2010, Ladich and Schulz-Mirbach 2013).

In order to assess the effect of anthropogenic noise pollution we performed several studies. Noise levels measured during the first power boat race at the lake Traunsee in Upper Austria indicated that local cyprinids are able to detect the high-speed boat at distances up to 300 m (Amoser et al. 2004). Investigations of the coastal regions of Portugal and the Adriatic Sea revealed that the ship noise can mask sound detection and thus hinders acoustic communication in several fish families: toadfish, damselfish and croakers (Vasconcelos et al. 2007, Codarin et al. 2009).

 

 

Fishes are often kept for leisure and thus exposed to various noise types, in particular from equipment necessary to maintain optimal water conditions. We observed high noise levels and complex spectral distributions in the aquaria with different filtering techniques. Our results indicate that hearing specialists, and to a lesser degree hearing non-specialists, are considerably masked under holding conditions in aquaria (Gutscher et al. 2011).

Exposing fishes to ship noise increased their cortisol secretion, independently of their hearing abilities. This indicates that ship noise constitutes a potential stressor, contrary to continuous noise (Wysocki et al. 2006).