Available online at www.sciencedirect.com ScienceDirect
Fish bioacoustics
Friedrich Ladich
Bony fishes have evolved a diversity of sound generating structures and to determine which selective forces acted
mechanisms and produce a variety of sounds. By contrast to during the evolution of these structures. How did life
sound generating mechanisms, which are lacking in several history traits and ecoacoustical conditions interact with
taxa, all fish species possess inner ears for sound detection. each other? Here, I review the diversity in vocal organs,
Fishes may also have various accessory structures such as sounds generated, hearing organs, hearing sensitivities and
auditory ossicles to improve hearing. The distribution of sound how and if the evolution of sound generating and detecting
generating mechanisms and accessory hearing structures structures are linked to each other.
among fishes indicates that acoustic communication was not
the driving force in their evolution. It is proposed here that Sound generating mechanisms
different constraints influenced hearing and sound production The first observation when studying sound production in
during fish evolution, namely certain life history traits fishes is the incredible diversity in sound generating
(territoriality, mate attraction) in the case of sound generating mechanisms [4–7]. This diversity is unique among
mechanisms, and adaptation to different soundscapes vertebrates and it is no exaggeration to call fishes the
(ambient noise conditions) in accessory hearing structures ‘insects’ among vertebrates (this also holds for the hearing
(Ecoacoustical constraints hypothesis). organs). Terrestrial vertebrates have a main vocal
Addresses organ — the larynx in anurans, reptiles and mammals
Department of Behavioural Biology, University of Vienna, Althanstrasse and the syrinx in birds [8] — but no main vocal organ
14, 1090 Vienna, Austria
exists in fishes. How widespread is sound production in
fishes from a systematic point of view? Our knowledge of
Corresponding author: Ladich, Friedrich ([email protected])
their sound production stems entirely from modern ray-
finned bony fishes (class Actinopterygii). Little is known
Current Opinion in Neurobiology 2014, 28:121–127 from the more primitive jawless fishes (e.g. lampreys),
cartilaginous fishes (e.g. sharks) or lobe-finned bony fishes
This review comes from a themed issue on Communication and
language (e.g. lungfishes) even though the latter are the closest
relatives to tetrapods [7,9]. Thus, sound production in
Edited by Michael Brainard and Tecumseh Fitch
fishes and tetrapods is apparently the outcome of con-
vergent evolutionary processes despite some similarity in
neuronal vocal pathways (see [10], and Bass, this volume).
http://dx.doi.org/10.1016/j.conb.2014.06.013
0959-4388/ # 2014 Published by Elsevier Ltd. All right reserved. The occurrence of vocal organs in different species of fish
does not follow any systematic pattern. Moreover, we do
not know how many species in families known to be vocal
(e.g. polypterids, gobiids, damselfish) generate sounds.
Due to the enormous structural diversity it is difficult to
categorize vocal organs in fishes.
Introduction
Fish bioacoustics comprises sound production, sound The most important mechanism comprises structures
detection and the functional significance of both, namely solely devoted to sound production such as sonic (drum-
acoustic communication and orientation. Although all will ming) muscles for swim bladder vibration. The drum-
agree that the evolution of sound generating mechanisms ming muscles can be directly attached to the bladder wall
(often termed sonic or vocal organs) serves acoustic com- (intrinsic type, e.g. toadfishes; Figure 1a), or they
munication (be it with conspecifics or heterospecifics), we originate on a structure outside the swim bladder and
know little about what fishes listen to besides conspecific inserting on its wall (extrinsic direct type, e.g. pimelodid
vocalizations. Although the capacity for sound reception, catfish). Finally, they can vibrate the bladder indirectly
based on hair cells, is a shared derived trait of all via broad tendons or bony plates without any attachment
vertebrates, hearing enhancing structures and sound pro- to its wall (e.g. doradid catfishes and piranhas) (extrinsic
ducing mechanisms appear to have evolved indepen- indirect type; Figure 1b) [3 ,7,11].
dently many times among the roughly 30,000 species
of living fish [1,2,3 ]. A second group of mechanisms uses pectoral fins and
girdles for sound production. Structures (muscles) involved
Central goals of fish bioacoustic research therefore are to in these mechanisms have additional functions besides
investigate the diversity in sound generating and detecting sound production, namely swimming. Representatives of
www.sciencedirect.com Current Opinion in Neurobiology 2014, 28:121–127
122 Communication and language
Figure 1
2.0 1.0 1.5 0.8 1.0 0.6 0.4 0.5 0.2 Frequency (kHz) Frequency Frequency (kHz) Frequency
0 0
0 0.2 0.4 0.6 0.8 1 0 40 80 120160 Time (s) Time (ms)
(a) SL (b)
SMe VC SB
BT
SMi SM 2R
(e)
PT PG
PG
DP PM ET
PS (c) (d)
4 3 3 2 2 1 1 Frequency (kHz) Frequency Frequency (kHz) Frequency
0 0
0 40 80 120 160 0 40 80 120160200 Time (ms) Time (ms)
Current Opinion in Neurobiology
Diversity of sound generating mechanisms in fishes and sonagrams of sounds produced by these mechanisms. (a) Intrinsic sonic muscles (SMi)
attached to both swim bladder lobes (SL) in the Lusitanian toadfish Halobatrachus didactylus, (b) extrinsic sonic muscles (SMe) originating at the
second rib (2R) and inserting on a broad tendon (BT) ventrally of the swim bladder in the black piranha Serrasalmus rhombeus, (c) in the stridulatory
mechanism in catfish a ridged dorsal process (DP) of the pectoral spine (PS) rubs in a groove of the shoulder girdle (SG), (d) enhanced pectoral fin
tendons (ETs) are plucked similar to guitar strings in the croaking gourami Trichopsis vittata, (e) Pharyngeal teeth (PT) stridulation in damselfish,
sunfish, among others, and pectoral girdle vibration in sculpins by a sonic muscle (SM) originating at the skull and inserting at the dorsal part of the
pectoral girdle. 2R: second rib, BT: broad tendon, DP: dorsal process of pectoral spine, ET: enhanced tendons, PG: pectoral girdle, PM: pectoral
adductor muscle, PT: pharyngeal teeth, PS: pectoral spine, SL: swim bladder lobes, SM: sonic muscle, VC: vertebral column. All sonagrams show
sounds produced in agonistic contexts. Note different x-axes and y-axes ranges. Modified partly after [3 ,7,63]. With permission from Elsevier.
several catfish families have an enhanced first pectoral fin body axis [7,11] (Figure 1c). In croaking gouramis (genus
ray (pectoral spine) that can generate stridulatory sounds Trichopsis) two enhanced pectoral fin tendons are stretched
when rubbed against a groove of the shoulder girdle. The and plucked similar to guitar strings during rapid fin beat-
pectoral spine can furthermore be used as a predator ing (Figure 1d). In sculpins the entire pectoral girdle is
defense mechanism when locked in a right angle to the vibrated by a sonic muscle [12] (Figure 1e). Note that there
Current Opinion in Neurobiology 2014, 28:121–127 www.sciencedirect.com
Fish bioacoustics Ladich 123
is no clear separation between swim bladder and pectoral create a deflection of hair cell ciliary bundles. This process
girdle mechanisms because intermediate forms exist [13]. enables fish to detect particle motion at low frequency (up
to a few hundred hertz) [22 ,23]. Close to a sound source
Finally, there are mechanisms completely different from (nearfield) the ear’s ability to detect sound may overlap
the organs mentioned above and not known well enough with the ability of the lateral line to detect fluid flow near a
to be categorized clearly. Pharyngeal structures including sound source [24]. The lateral line is a mechanosensory
teeth may be moved against each other to produce system consisting of sensory cells termed neuromasts
sounds. Such mechanisms were suggested for sunfishes which are found in subdermal lateral line canals was well
and cichlids (Figure 1e) and described in more detail in as directly on the skin [25]. Its main task is the detection of
clownfish [14]. A simple organ homologous to the larynx is water movement generated by conspecifics, heterospeci-
present in lungfish [15]. The distribution of the mech- fics such as prey or inanimate sources (ocean currents, river
anisms across taxa is quite diverse. The tendon-plucking flows, among others).
mechanism occurs in only three species of the genus
Trichopsis (Anabantoidei), whereas intrinsic swim bladder Interestingly, numerous taxa among ray-finned bony fishes
muscles are found in all genera within the toadfish family connect their inner ears to gas-filled chambers, which allow
(Batrachoididae) and in a few more species of other them to detect sound pressure [1]. Walls of these chambers
families. The pectoral spine stridulatory mechanism is vibrate in a sound field. These vibrating walls function as
found in hundreds of species of several catfish families. internal ear drums (tympana) which transmit these oscil-
Sonic organs are lacking in numerous fishes, whereas lations in various ways to the inner ears. This enables these
some species may even possess two different mechanisms species to detect sound at lower levels and higher frequen-
(doradid or pimelodid catfishes) [11]. cies (up to a few kilohertz) (for reviews see [26 ,27 ]). The
diversity in inner ears and in accessory hearing structures is
Fish vocalizations generally consist of pulse series whose astonishing, as is the diversity in vocal organs [1,23,28 ].
main energies depend on the mechanisms involved Sound pressure fluctuations of the swim bladder can be
[16,17]. Swim bladder drumming sounds have mostly a transmitted via an ossicular chain to the inner ear (‘Weber-
harmonic structure and main energies below 500 Hz. ian ossicles’), very similar to mammals [29], or swim
Unlike periodic vocalizations in most tetrapods, the funda- bladder extensions can contact the inner ear directly, or
mental frequency is determined directly by the contraction the inner ears may contact the air-breathing organs [28 ].
rate of swim bladder drumming muscles and ranges from 50 Even in fish that lack a direct connection between inner ear
to 200 Hz (Figure 1a,b). Drumming sounds can last from a and gas-filled chambers, a possible function of the swim
few milliseconds up to several minutes in the Californian bladder in sound pressure detection cannot be ruled out
midshipman Porichthys notatus. Pectoral stridulatory without complicated experiments [30,31].
sounds, in contrast, consist of pulses whose energies are
concentrated at higher frequencies than those of swim One major shortcoming in analysing the functional sig-
bladder sounds. Energies extend up to several kilohertz nificance of fish hearing abilities is the scarcity of knowl-
with main energies at a few hundred hertz or even above 1 edge — except for a few indications — about what fishes
kilohertz, such as in the croaking gourami (Figure 1c,d). are listening to beyond conspecific vocalizations. The
Low-frequency pulsed sounds are also observed in species general assumption is that fishes ‘glean’ acoustic infor-
emitting pharyngeal or pectoral girdle vibration sounds mation from their environment (also termed auditory
[12,14]. Fishes often emit different sounds types in differ- scene, soundscape, ‘acoustic daylight’) [32–34]. It is
ent behavioural contexts by modifying the duration, assumed that fishes gain advantages from listening to
temporal pulse patterns or amplitudes [18–20]. abiotic (e.g. coastal surf, coral reefs) and biotic sound/
noise sources (conspecifics and heterospecifics, predators,
Sound detecting mechanisms prey), independent of vocalizations. Various soundscapes
Sound detecting organs are present in all vertebrates may help larvae and adults to find suitable habitats
including all fish species, in contrast to sound generating [33,35,36] or help to avoid danger. One example for
organs [21]. The hearing organs can be divided morpho- the interception of predator sounds is the detection of
logically into those consisting solely of the inner ears and toothed whales by some herrings and toadfish: the former
those utilizing additional peripheral structures to improve exhibit an evasive response during playbacks of echolo-
hearing. Inner ears consist of three semicircular canals and cation clicks, the latter suppress calling behaviour [37–
three otolithic end organs (utricle, saccule, lagena), each 40]. Important biotic sound or noise sources in the intras-
one consisting of a calcareous otolith overlying a sensory pecific context may include feeding, digging or swimming
field of hair cells. Because fish have the same density as the noise of conspecifics or heterospecifics (prey). This list of
surrounding medium (in contrast to terrestrial animals) incomplete observations and assumptions points to a large
they move back and forth with the sound wave excluding gap in our knowledge on the importance of hearing in fish,
any net movement between the animal and the water. Only calling for phonotaxis experiment using sounds other than
the heavier otoliths lag behind these movements and (conspecific or heterospecific) vocalizations as stimuli.
www.sciencedirect.com Current Opinion in Neurobiology 2014, 28:121–127
124 Communication and language
Figure 2
SB IE
140
Pa) H. gu ttatus μ
120 S. tinanti 100 E. macula tus
80
Hearing threshold (dB Hearing re 1 60
0.1 0.2 0.3 0.5 0.7 1 2 3 4
Frequen cy (kHz)
Current Opinion in Neurobiology
Relationship between peripheral hearing structures and auditory sensitivity in fishes illustrated in three representatives of the family Cichlidae. Lateral
view of the swim bladder (SB) and the inner ears (IE) including otoliths (lapillus: red, sagitta: pink, asteriscus: yellow). Note differences in swim bladder
(SB) sizes, distances to the inner ears (IE) and hearing thresholds. Etroplus maculatus has the largest swim bladder, the shortest distance to the inner
ear and the highest auditory sensitivity. Steatocranus tinanti has the smallest bladder and the lowest hearing sensitivity. Hemichromis guttatus is
intermediate in swim bladder size and sensitivity. Modified from [43 ].
The distribution of morphological specialization for hear- The answer to the first question may lie in the life
ing improvement across taxa does not reveal any clear histories of vocalizing species. In general, vocal species
pattern. Weberian ossicles are present in all otophysines produce sounds when defending limited resources
(four orders, 8000+ species); other specializations may be (mainly territories) against opponents, for example, ter-
present in one suborder such as the suprabranchial ritorial intruders, or when trying to attract mates (females)
chamber in Anabantoidei, and some may not even be to nest sites and during mating [45 ,46 ]. These life
present in all representatives within a single family, such history traits explain the absence of sonic organs in
as in holocentrids, sciaenids or cichlids [22 ,41,42 ]. The pelagic species such as sharks, but they do not provide
perciform family Cichlidae illustrates this diversity and the an explanation for the large diversity in sonic mechanisms
effects on auditory sensitivity within a single family among vocal fishes.
(Figure 2). In the Indian species Etroplus maculatus a huge
swim bladder extends rostrally up to the inner ear, whereas Which selective forces resulted in the evolution of hear-
in the African species Hemichromis guttatus and Steatocranus ing specializations, their large diversity and the systema-
tinanti the swim bladder does not contact the inner ears at tic distribution among fishes? One potential answer is that
all; the latter two species, however, differ considerably in they are evolved to facilitate acoustic communication
swim bladder size. These differences in size and distances [8,47]. Nonetheless, a more detailed analysis of the pre-
to the inner ears are reflected in their hearing abilities, with sence of both vocal and hearing organs across taxa does
E. maculatus having the highest and S. tinanti the lowest not support this hypothesis [2]. Well-known vocalizing
sensitivity (Figure 2) [43 ]; see also [44] for the effects of taxa such as toadfishes and gobies lack any specialization
bladder size on hearing in catfishes. Rostral swim bladder for hearing, whereas cypriniforms are hearing specialists
extensions and auditory ossicles certainly serve only in but rarely signal acoustically (and no vocal organs are
hearing, but swim bladders are primarily organs for buoy- known). Rather than acoustic signaling, hearing in many
ancy and suprabranchial chambers serve in air-breathing. species seems to be adapted to the ambient noise in a
fish’s habitat. The ‘ecoacoustical constraints hypothesis’
Evolutionary considerations postulates that species living in quiet waters should have
Why did sound generating mechanisms evolve in certain high auditory sensitivities, whereas the opposite should
taxa and not in other taxa, and why are they so diverse? be the case in species living in noisy environments where
Current Opinion in Neurobiology 2014, 28:121–127 www.sciencedirect.com
Fish bioacoustics Ladich 125
Figure 3
Sound generating Sound detecting mechanisms mechanisms Functional significance
No mechanisms Amient noise levels + spectra Baseline hearing Interception Inner ears Sonic muscles
Biotic + abiotic Constraints Swim bladder vibration sources Improved hearing Spezializations Pectoral mechanisms Additional functions Communication
Constraints Intra + interspecific Improved hearing Mechanisms? Various mechanisms Additional functions? Territoriality + mate attraction Territoriality
Current Opinion in Neurobiology
Diversity in sound generating and detecting structures in fishes, their functional significance and potential constraints during their evolution. Sound
generating mechanisms are divided into mechanisms with sonic muscles exclusively devoted to sound production and into pectoral mechanisms/
muscles that serve additional functions (swimming, predator defense). The third group comprises mechanisms not known well enough to be
categorized definitively, such as pharyngeal or neck mechanisms (clownfish, seahorses). Sound detecting mechanisms are divided into those
consisting merely of the inner ears (tiny or no swim bladders), those having well-developed peripheral structures for hearing (e.g. Weberian auditory
ossicles) and those in which the mechanism for improved hearing (sound pressure detection) is unknown (e.g. damselfish). Sonic/vocal organs always
serve acoustic communication, whereas hearing organs primarily serve interception of acoustic information emanating from various biotic sources
(conspecifics and heterospecifics, predators, prey) and abiotic sources (coral reefs, coastal surf, among others). Thus, different constraints have
apparently acted during the evolution of sound generating and detecting mechanisms. It is proposed here that vocal organs are linked to particular life
history traits (territory defense and mate attraction), whereas the diversity in hearing organs is due to different ambient noise conditions (soundscapes; ecoacoustical constraints hypothesis).
improved hearing would be meaningless [42 ]. Several taxa. Sound communication is primarily linked to the mode
investigations and analyses show that most species with of reproduction namely territoriality and substrate breed-
improved hearing live in quiet stagnant freshwaters (at ing and seems to be unrelated to the evolution of hearing
least two thirds of freshwater fish possess specializations), enhancements.
whereas non-specialized species inhabit rather noisy mar-
ine habitats [48 ,49,50]. Studies indicate that fish are Conflict of interest statement
adapted to the ambient noise in their habitats and that There exists no conflict of interests.
artificial (anthropogenic) noise hinders acoustic communi-
cation and prey detection [51–53,54 ] (Figure 3). To test Acknowledgement
The author’s research was supported by the Austrian Science Fund (FWF
this ‘ecoacoustical constraints hypothesis’ many more
grants 15873, 17263, 22319).
ambient noise measurements and masking experiments
need to be carried out in fish species differing in their
References and recommended reading
hearing sensitivities [49,52,55–58]. Moreover, this hypoth-
Papers of particular interest, published within the period of review,
esis does not rule out that fish are well adapted to detect have been highlighted as:
conspecific or even heterospecific sounds as long as the
of special interest
sound levels are high and communication distances short of outstanding interest
enough to be detectable — also during different stages of
1. Ladich F, Popper AN: Parallel evolution in fish hearing organs.
ontogenetic development ([59–61]; but see [57,62]).
In Evolution of the Vertebrate Auditory System. Edited by Manley
G, Fay RR, Popper AN. Springer; 2004:95-127.
Conclusions
2. Ladich F: Acoustic communication and the evolution of hearing
Based on the phylogenetic distribution of sound generating in fishes. Phil Trans Roy Soc B: Biol Sci 2000, 355:1285-1288.
mechanisms and vocalizations it is concluded that acoustic
3. Ladich F, Bass AH: Vocal behavior of fishes: anatomy and
communication evolved multiple times in non-related fish physiology. In Encyclopedia of Fish Physiology: From Genome to
www.sciencedirect.com Current Opinion in Neurobiology 2014, 28:121–127
126 Communication and language
Environment. Edited by Farrell AP. San Diego: Academic Press; 24. Webb JF, Montgomery JC, Mogdans J: Bioacoustics and the
2011:321-329. lateral line system in fishes. In Fish Bioacoustics. Edited by
This review provides an overview of sound generating mechanisms and Webb JF, Popper AN, Fay RR. New York: Springer; 2008:145-182.
their neuronal control in fishes. The latter is best investigated in repre-
25. Bleckmann H: Role of the lateral line in fish behaviour. In
sentatives of the toadfish family.
Behaviour of Teleost Fishes. Edited by Pitcher TJ. London:
4. Tavolga WN: Sound production and underwater Chapman & Hall; 1993:201-246.
communication in fishes. In Animal Sounds and
26. Fay RR (Ed): Hearing in Vertebrates: A Psychophysics Databook.
Communication. Edited by Lanyon WE, Tavolga WN. Washington,
Hill-Fay Associates; 1988.
DC: American Institute of Biological Sciences; 1960:93-136.
5. Tavolga WN: Sonic characteristics and mechanisms in marine This book summarizes all available data on hearing in fishes (and other
fishes. In Marine Bio-Acoustics. Edited by Tavolga WN. Oxford: vertebrates) up to 1988. All auditory data were redrawn in standard
Pergamon Press; 1964:195-211. figures to make comparisons for readers easy. It has become a classic
in fish bioacoustics. It does not include AEP-data because the AEP-
6. Schneider H: Morphology and physiology of sound-producing
technique became popular several years later (see [27 ]).
mechanisms in teleost fishes. In Marine Bio-Acoustics, Vol. 2.
Edited by Tavolga WN. Oxford: Pergamon Press; 1967:135-158. 27. Ladich F, Fay RR: Auditory evoked potential audiometry in fish.
Rev Fish Biol Fisher 2013, 23:317-364.
7. Ladich F, Fine ML: Sound-generating mechanisms in fishes: a
This review covers all 100+ papers on hearing in fish using the Auditory
unique diversity in vertebrates. In Communication in Fishes.
Evoked Potential (AEP) technique since 1998. Baseline hearing abilities
Edited by Ladich F, Collin SP, Moller P, Kapoor BG. Science were described and compared in 111 species from 51 families. In
Publishers Inc.; 2006:3-43.
addition, studies on the functional significance of accessory hearing
structures, on the ontogenetic development of hearing, and on the effects
8. Bradbury JW, Vehrencamp SL (Eds): Principles of Animal
of masking by and exposure to various noise types (white, ambient, ship
Communication. Sinauer Associates Inc. Publishers; 2011.
noise) were listed, along with the effects of various ecological, genetic,
methodological and behavioural factors on hearing.
9. Thomson KS: Lung ventilation in dipnoan fishes. Postilla 1968,
122:1-2.
28. Braun CB, Grande T: Evolution of peripheral mechanisms for
the enhancement of sound reception. In Fish Bioacoustics.
10. Bass AH, Chagnaud BP: Shared developmental and
Edited by Webb JF, Popper AN, Fay RR. Springer; 2008:99-144.
evolutionary origins for neural basis of vocal–acoustic and
This book chapter reviews the literature on peripheral mechanisms for
pectoral–gestural signaling. Proc Nat Acad Sci USA 2012,
enhanced hearing in fishes. It illustrates the morphology of accessory
109(Suppl 1):10677-10684.
hearing structures with a number of helpful drawings but does not give
11. Fine ML, Ladich F: Sound production, spine locking and related audiograms. The authors also mention that in numerous families we do
adaptations. In Catfishes, Vol. 1. Edited by Kapoor BG, Arratia G, not know whether specializations such as anterior swim bladder exten-
Chardon M, Diogo R. Science Publishers, Inc; 2006:249-290. sions improve hearing.
¨
12. Ladich F: Sound production by the river bullhead Cottus gobio 29. Weber EH: Vergleichende Anatomie der Gehorwerkzeuge.
L. (Cottidae, Teleostei). J Fish Biol 1989, 35:531-538. Deutsches Archiv fu¨r die Physiologie 1819, 5:323-332.
Hearing in damselfishes: an analysis of
13. Hallacher LE: The comparative morphology of extrinsic 30. Myrberg AA, Spires JY:
signal detection among closely related species. J Comp
gasbladder musculature in the scorpionfish genus Sebastes
140
(Pisces: Scorpaenidae). Proc Calif Acad Sci 1974, 40:59-86. Physiol 1980, :135-144.
31. Popper AN, Fay RR: Rethinking sound detection by fishes. Hear
14. Parmentier E, Colleye O, Fine ML, Frederich B, Vandewalle P et al.:
Res 2011, 273:25-36.
Sound production in the clownfish Amphiprion clarkii. Science
2007, 316:1006.
32. Bregman AS (Ed): Auditory Scene Analysis. The Perceptual
Organisation of Sound. MIT Press; 1990.
15. Kirchner JA: The vertebrate larynx: adaptations and
aberrations. Laryngoscope 1993, 103:1197-1201.
33. Slabbekoorn H, Bouton N: Soundscape orientation: a new field
in need of sound investigation. Anim Behav 2008, 76:e5-e8.
16. Fish MP, Mowbray WH: Sounds of Western North Atlantic Fishes.
Baltimore: John Hopkins Press; 1970, .
34. Fay RR: Soundscapes and the sense of hearing in fishes. Integr
Zool 2009, 4:26-32.
17. Fine ML, Winn HE, Olla BL: Communication in fishes. In How
Animals Communicate. Edited by Sebeok TA. Bloomington:
35. Simpson SD, Meekan MG, Jeffs A, Montgomery JC,
Indiana University Press; 1977:472-518.
McCauley RD: Settlement-stage coral reef fish prefer the
higher frequency invertebrate-generated audible component
18. Myrberg AA: Ethology of the bicolor damselfish,
of reef noise. Anim Behav 2008, 75:1861-1868.
Eupomacentrus partitus (Pisces: Pomacentridae): a
comparative analysis of laboratory and field behaviour. Anim
36. Radford CA, Stanley JA, Simpson SD, Jeffs AG: Juvenile coral reef
Behav Monogr 1972, 5:197-283.
fish use sound to locate habitats. Coral Reefs 2011, 30:295-305.
19. Amorim MCP: Diversity in sound production in fish. In
37. Mann DA, Lu Z, Popper AN: A clupeid fish can detect
Communication in Fishes. Edited by Ladich F, Collin SP, Moller P,
ultrasound. Nature 1997, 389:341.
Kapoor BG. Science Publishers Inc.; 2006:71-105.
38. Plachta DTT, Popper AN: Evasive responses of American shad
20. Ladich F: Females whisper briefly during sex: context- and
(Alosa sapidissima) to ultrasonic stimuli. Acoust Res Lett Online
sex-specific differences in sounds made by croaking
2003, 4:25-30.
gouramis. Anim Behav 2007, 73:379-387.
39. Remage-Healey L, Nowacek DP, Bass AH: Dolphins foraging
21. Ladich F: Hearing: Vertebrates. In Encyclopedia of Animal
sounds suppress calling and elevate stress hormone levels in
Behaviour. Edited by Breed MD, Moore J. Oxford: Academic
prey species, the Gulf toadfish. J Exp Biol 2006, 209:4444-4451.
Press; 2010:54-60.
40. Wilson M, Acolas ML, Begout ML, Madsen PT, Wahlberg M: Allis
22. Hawkins AD: Underwater sound and fish behaviour. In
shad (Alosa alosa) exhibit an intensity-graded behavioural
Behaviour of Teleost Fishes. Edited by Pitcher TJ. Chapman and
response when exposed to ultrasound. J Acoust Soc Am 2008,
Hall; 1993:129-169. 124:EL243-EL247.
This book chapter gives a short introduction in fish bioacoustics including
the physics of underwater sound, sound production, vocal behaviour and 41. Ramcharitar JU, Higgs DM, Popper AN: Audition in sciaenid
hearing mechanism. fishes with different swim bladder-inner ear configurations. J
Acoust Soc Am 2006, 119:439-443.
23. Popper AN: Auditory system morphology. In Encyclopedia of
Fish Physiology: From Genome to Environment.. Edited by Farrel 42. Ladich F: Diversity in hearing in fishes: ecoacoustical,
AP. San Diego: Academic Press; 2011:252-261. communicative, and developmental constraints. In Insights
Current Opinion in Neurobiology 2014, 28:121–127 www.sciencedirect.com
Fish bioacoustics Ladich 127
from Comparative Hearing. Edited by Koeppl C, Manley GA, 51. Vasconcelos RO, Amorim MCP, Ladich F: Effects of ship noise
Popper AN, Fay RR. New York: Springer; 2014:289-321. on the detectability of communication signals in the
This book chapter reviews the literature on the diversity of hearing abilities Lusitanian toadfish. J Exp Biol 2007, 210:2104-2112.
in fishes and attempts to explain this diversity from an ecoacoustical,
communicative and ontogenetic point of view. Based on our current 52. Codarin A, Wysocki LE, Ladich F, Picciulin M: Effects of ambient
knowledge the review concludes that ecoacoustical constraints, namely and boat noise on hearing and communication in three fish
differences in noise levels and noise spectra, are the most likely explana- species living in a marine protected area (Miramare, Italy). Mar
tion for the diversity in hearing sensitivities. This notion is summarized in Poll Bull 2009, 58:1880-1887.
the ‘ecoacoustical constraints hypothesis’.
53. Purser J, Radford AN: Acoustic noise induces attention shifts
43. Schulz-Mirbach T, Metscher B, Ladich F: Relationship between and reduces foraging performances in threespined
swim bladder morphology and hearing abilities — a case sticklebacks (Gasterosteus aculeatus). PloS One 2011,
study on Asian and African cichlids. PloS One 2013, 7:e42292. 6:e17478.
This is the most comprehensive study showing the effect of swim bladder
size and its distance to the inner ear on hearing sensitivity in closely 54. Ladich F: Effects of noise on sound detection and acoustic
related fishes belonging to the same family. communication in fishes. In Animal Communication and Noise.
Edited by Brumm H. Springer; 2013:65-90.
44. Lechner W, Ladich F: Size matters: diversity in swimbladders This book chapter summarizes our current knowledge on the effects of
and Weberian ossicles affects hearing in catfishes. J Exp Biol ambient as well as anthropogenic noise on hearing in general and on the
2008, 211:1681-1689. detection of communication sounds in particular.
45. Ladich F, Myrberg AA: Agonistic behaviour and acoustic
55. Chapman CJ, Hawkins AD: A field study of hearing in the cod,
communication. In Communication in Fishes. Edited by Ladich F,
Gadus morhua L.. J Comp Physiol A 1973, 85:147-167.
Collin SP, Moller P, Kapoor BG. Science Publishers Inc.; 2006:
122-148. 56. Wysocki LE, Ladich F: Hearing in fishes under noise conditions.
This is the first review summarizing all investigations on acoustic signal- J Assoc Res Otolaryngol 2005, 6:28-36.
ling during agonistic behaviour in fishes.
57. Lugli M: Sound of shallow water fishes pitch within the quiet
46. Myrberg AA, Lugli M: Reproductive behavior and acoustical
window of the habitat noise. J Comp Physiol A 2010, 196:439-451.
interactions. In Communication in Fishes. Edited by Ladich F,
Collin SP, Moller P, Kapoor BG. Science Publishers Inc.; 2006: 58. Ladich F, Schulz-Mirbach T: Hearing in cichlid fishes under
149-176. noise conditions. PloS One 2013, 8:e57588.
This is the first review summarizing all investigations on acoustic signal-
ling during reproductive behaviour in fishes. 59. Wysocki LE, Ladich F: The ontogenetic development of auditory
sensitivity, vocalization and acoustic communication in the
47. Fay RR, Popper AN: Hearing in fishes and amphibians: an
labyrinth fish Trichopsis vittata. J Comp Physiol A 2001,
introduction. In Comparative Hearing: Fish and Amphibians. 187:177-187.
Edited by Fay RR, Popper AN. Springer; 1999:1-14.
60. Maruska KP, Boyle KS, Dewan LR, Tricas TG: Sound production
48. Schellart NAM, Popper AN: Functional aspects of the evolution
and spectral hearing sensitivity in the Hawaiian sergeant
of the auditory system of actinopterygian fish. In The
damselfish, Abudefduf abdominalis. J Exp Biol 2007, 210:3990-
Evolutionary Biology of Hearing. Edited by Webster DE, Fay RR, 4000.
Popper AN. Springer; 1992:295-322.
This book chapter lists basic anatomical, auditory and habitat data and
61. Sisneros JA: Adaptive hearing in the vocal plainfin midshipman
feeding behaviour of representatives of 28 families out of 16 orders of
fish: getting in tune for the breeding season and implications
fishes and formulates general principles (hypotheses) on fish hearing. It is
for acoustic communication. Integr Zool 2009, 4:33-42.
highly interesting comparing these principles to the conclusions of the
present review. 62. Vasconcelos RO, Ladich F: Development of vocalization,
auditory sensitivity and acoustic communication in the
49. Amoser S, Ladich F: Are hearing sensitivities of freshwater fish
Lusitanian toadfish Halobatrachus didactylus. J Exp Biol 2008,
adapted to the ambient noise in their habitats? J Exp Biol 2005, 211:502-509.
208:3533-3542.
63. Bass AH, Ladich F: Vocal-acoustic communication: from
50. Wysocki LE, Amoser S, Ladich F: Diversity in ambient noise in
neurons to behavior. In Fish Bioacoustics. Edited by Webb JF,
European freshwater habitats: noise levels, spectral profiles
Fay RR, Popper AN. Springer; 2008:253-278.
and impact on fishes. J Acoust Soc Am 2007, 121:2559-2566.
www.sciencedirect.com Current Opinion in Neurobiology 2014, 28:121–127