Fishes, including elasmobranchs (sharks, rays, and skates), present an astonishing diversity in inner ear morphologies; however, the functional significance of these variations and how they confer auditory capacity is yet to be resolved. The relationship between inner ear structure and hearing performance is unclear, partly because most of the morphological and biomechanical mechanisms that underlie the hearing functions are complex and poorly known. Here, we present advanced opportunities to document discontinuities in the macroevolutionary trends of a complex biological form, like the inner ear, and test hypotheses regarding what factors may be driving morphological diversity. Three-dimensional (3D) bioimaging, geometric morphometrics, and finite element analysis are methods that can be combined to interrogate the structure-to-function links in elasmobranch fish inner ears. In addition, open-source 3D morphology datasets, advances in phylogenetic comparative methods, and methods for the analysis of highly multidimensional shape data have leveraged these opportunities. Questions that can be explored with this toolkit are identified, the different methods are justified, and remaining challenges are highlighted as avenues for future work.
REFERENCES
1.
Aguirre
,
H.
, and
Lombarte
,
A.
(1999
). “
Ecomorphological comparisons of sagittae in Mullus barbatus and M. surmuletus
,” J. Fish. Biol.
55
, 105
–114
.2.
Alcocer
,
I.
,
Lima
,
H.
,
Sugai
,
L. S. M.
, and
Llusia
,
D.
(2022
). “
Acoustic indices as proxies for biodiversity: A meta‐analysis
,” Biol. Rev.
97
, 2209
–2236
.3.
Aroyan
,
J. L.
(2001
). “
Three-dimensional modeling of hearing in Delphinus delphis
,” J. Acoust. Soc. Am.
110
, 3305
–3318
.4.
Berquist
,
R. M.
,
Gledhill
,
K. M.
,
Peterson
,
M. W.
,
Doan
,
A. H.
,
Baxter
,
G. T.
,
Yopak
,
K. E.
,
Kang
,
N.
,
Walker
, H. J.
,
Hastings
, P. A.
, and
Frank
,
L. R.
(2012
). “
The digital fish library: Using MRI to digitize, database, and document the morphological diversity of fish
,” PloS One
7
, e34499
.5.
Bhandiwad
,
A. A.
,
Whitchurch
,
E. A.
,
Colleye
,
O.
,
Zeddies
,
D. G.
, and
Sisneros
,
J. A.
(2017
). “
Seasonal plasticity of auditory saccular sensitivity in ‘sneaker’ type II male plainfin midshipman fish, Porichthys notatus
,” J. Comp. Physiol. A.
203
, 211
–222
.6.
Bregman
,
A. S.
(1990
). Auditory Scene Analysis: The Perceptual Organization of Sound
(
MIT Press
,
Cambridge, MA
).7.
Camilieri-Asch
,
V.
,
Shaw
,
J. A.
,
Mehnert
,
A.
,
Yopak
,
K. E.
,
Partridge
,
J. C.
, and
Collin
,
S. P.
(2020a
). “
diceCT: A valuable technique to study the nervous system of fish
,” eNeuro.
7
, ENEURO.0076-20.2020
.8.
Camilieri-Asch
,
V.
,
Shaw
,
J. A.
,
Yopak
,
K. E.
,
Chapuis
,
L.
,
Partridge
,
J. C.
, and
Collin
,
S. P.
(2020b
). “
Volumetric analysis and morphological assessment of the ascending olfactory pathway in an elasmobranch and a teleost using diceCT
,” Brain Struct. Funct.
225
, 2347
–2375
.9.
Chapuis
,
L.
(2022
). “Finite Element Analysis of the elasmobranch inner ear” (unpublished).10.
Chapuis
,
L.
, and
Collin
,
S. P.
(2022
). “
The auditory system of cartilaginous fishes
,” Rev. Fish. Biol. Fisheries
32
, 521
–554
.11.
Chollet-Villalpando
,
J. G.
,
García-Rodríguez
,
F. J.
,
Luna
,
E. D.
, and
Cruz-Agüero
,
J. D. L.
(2019
). “
Geometric morphometrics for the analysis of character variation in size and shape of the sulcus acusticus of sagittae otolith in species of Gerreidae (Teleostei: Perciformes)
,” Mar. Biodivers.
49
, 2323
–2332
.12.
Codarin
,
A.
,
Wysocki
,
L. E.
,
Ladich
,
F.
, and
Picciulin
,
M.
(2009
). “
Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy)
,” Mar. Pollut. Bull.
58
, 1880
–1887
.13.
Coffin
,
A. B.
,
Mohr
,
R. A.
, and
Sisneros
,
J. A.
(2012
). “
Saccular-specific hair cell addition correlates with reproductive state-dependent changes in the auditory saccular sensitivity of a vocal fish
,” J. Neurosci.
32
, 1366
–1376
.14.
Collin
,
S. P.
(1997
). “
Specialisations of the teleost visual system: Adaptive diversity from shallow-water to deep-sea
,” Acta Physiol. Scand. Suppl.
638
, 5
–24
.15.
Corn
,
K. A.
,
Martinez
,
C. M.
,
Burress
,
E. D.
, and
Wainwright
,
P. C.
(2021
). “
A multifunction trade-off has contrasting effects on the evolution of form and function
,” Syst. Biol.
70
, 681
–693
.16.
Corwin
,
J. T.
(1981
). “
Peripheral auditory physiology in the lemon shark: Evidence of parallel otolithic and non-otolithic sound detection
,” J. Comp. Physiol.
142
, 379
–390
.17.
Corwin
,
J. T.
(1989
). “
Functional anatomy of the auditory system in sharks and rays
,” J. Exp. Zool.
252
, 62
–74
.18.
Cranford
,
T. W.
, and
Krysl
,
P.
(2015
). “
Fin whale sound reception mechanisms: Skull vibration enables low-frequency hearing
,” PLoS One
10
, e0116222
.19.
Dawood
,
Y.
,
Hagoort
,
J.
,
Siadari
,
B. A.
,
Ruijter
,
J. M.
,
Gunst
,
Q. D.
,
Lobe
,
N. H. J.
,
Strijkers
,
G. J.
,
de Bakker
, B. S.
, and
van den Hoff
,
M. J. B.
(2021
). “
Reducing soft-tissue shrinkage artefacts caused by staining with Lugol's solution
,” Sci. Rep.
11
, 19781
.20.
Deng
,
X.
,
Wagner
,
H.-J.
, and
Popper
,
A. N.
(2013
). “
Interspecific variations of inner ear structure in the deep-sea fish family melamphaidae: Inner ear of melamphaid deep-sea fish
,” Anat. Rec.
296
, 1064
–1082
.21.
Deng
,
X.
,
Wagner
,
H.-J.
, and
Popper
,
A. N.
(2017
). “
Comparison of the Saccules and Lagenae in six macrourid fishes from different deep-sea habitats
,” J. Acoust. Soc. Am.
141
, 3860
–3861
.22.
Duarte
,
C. M.
,
Chapuis
,
L.
,
Collin
,
S. P.
,
Costa
,
D. P.
,
Devassy
,
R. P.
,
Eguiluz
,
V. M.
,
Erbe
,
C.
,
Gordon
,
T. A. C.
,
Halpern
,
B. S.
,
Harding
,
H. R.
,
Havlik
,
M. N.
,
Meekan
,
M.
,
Merchant
,
N. D.
,
Miksis-Olds
,
J. L.
,
Parsons
,
M.
,
Predragovic
,
M.
,
Radford
,
A. N.
,
Radford
,
C. A.
,
Simpson
,
S. D.
,
Slabbekoorn
,
H.
,
Staaterman
,
E.
,
Van Opzeeland
,
I. C.
,
Winderen
,
J.
,
Zhang
,
X.
, and
Juanes
,
F.
(2021
). “
The soundscape of the Anthropocene ocean
,” Science
371
(6529), eaba4658
.23.
Endler
,
J. A.
(1992
). “
Signals, signal conditions, and the direction of evolution
,” Am. Nat.
139
, S125
–S153
.24.
Endler
,
J. A.
(1993
). “
Some general comments on the evolution and design of animal communication systems
,” Philos. Trans. R. Soc. London, Ser. B: Biol. Sci.
340
, 215
–225
.25.
Endler
,
J. A.
, and
McLellan
,
T.
(1988
). “
The processes of evolution: Toward a newer synthesis
,” Annu. Rev. Ecol. Syst.
19
, 395
–421
.26.
Erbe
,
C.
,
McCauley
,
R.
, and
Gavrilov
,
A.
(2016
). “
Characterizing marine soundscapes
,” in The Effects of Noise on Aquatic Life II
, edited by
A. N.
Popper
and
A.
Hawkins
(Springer, New York), Vol. 75, pp. 265
–271
.27.
Evangelista
,
C.
,
Mills
,
M.
,
Siebeck
,
U. E.
, and
Collin
,
S. P.
(2010
). “
A comparison of the external morphology of the membranous inner ear in elasmobranchs
,” J. Morphol.
271
, 483
–495
.28.
Evers
,
S. W.
,
Joyce
,
W. G.
,
Choiniere
,
J. N.
,
Ferreira
,
G. S.
,
Foth
,
C.
,
Hermanson
,
G.
,
Yi
,
H.
,
Johnson
,
C. M.
,
Werneburg
,
I.
, and
Benson
, R. B. J.
(2022
). “
Independent origin of large labyrinth size in turtles
,” Nat. Commun.
13
, 5807
.29.
Farina
,
S. C.
,
Kane
,
E. A.
, and
Hernandez
,
L. P.
(2019
). “
Multifunctional structures and multistructural functions: Integration in the evolution of biomechanical systems
,” Integr. Comp. Biol.
59
, 338
–345
.30.
Fay
,
R.
(2009
). “
Soundscapes and the sense of hearing of fishes
,” Integr. Zool.
4
, 26
–32
.31.
Fay
,
R. R.
, and
Edds-Walton
,
P. L.
(1997
). “
Diversity in frequency response properties of saccular afferents of the toadfish, Opsanus tau
,” Hear. Res.
113
, 235
–246
.32.
Fay
,
R. R.
, and
Popper
,
A. N.
(2000
). “
Evolution of hearing in vertebrates: The inner ears and processing
,” Hear. Res.
149
, 1
–10
.33.
Fetterplace
,
L. C.
,
Esteban
,
J. J. D.
,
Pini‐Fitzsimmons
,
J.
,
Gaskell
,
J.
, and
Wueringer
,
B. E.
(2022
). “
Evidence of sound production in wild stingrays
,” Ecology
103
, e3812
.34.
Fleming
,
R. C.
(2021
). “Three-dimensional reconstruction and finite element modeling of anuran middle ear biomechanics,” Masters thesis (
Colorado State University
).35.
Gignac
,
P. M.
,
Kley
,
N. J.
,
Clarke
,
J. A.
,
Colbert
,
M. W.
,
Morhardt
,
A. C.
,
Cerio
,
D.
,
Cost
,
I. N.
,
Cox
,
P. G.
,
Daza
,
J. D.
,
Early
,
C. M.
,
Scott Echols
,
M.
,
Henkelman
,
R. M.
,
Herdina
,
A. N.
,
Holliday
,
C. M.
,
Li
,
Z.
,
Mahlow
,
K.
,
Merchant
S.
,
Müller
,
J.
,
Orsbon
,
C. P.
,
Paluh
D. J.
,
Thies
M. L.
,
Tsai
,
H. P.
,
Lawrence
M.
, and
Witmer
L. M.
(2016
). “
Diffusible iodine‐based contrast‐enhanced computed tomography (diceCT): An emerging tool for rapid, high‐resolution, 3‐D imaging of metazoan soft tissues
,” J. Anat.
228
, 889
–909
.
[PubMed]
36.
Greef
,
D. D.
,
Buytaert
,
J. A. N.
,
Aerts
,
J. R. M.
,
Hoorebeke
,
L. V.
,
Dierick
,
M.
, and
Dirckx
,
J.
(2015
). “
Details of human middle ear morphology based on micro-CT imaging of phosphotungstic acid stained samples: Human middle ear morphology through micro-CT
,” J. Morphol.
276
, 1025
–1046
.37.
Hanson
,
M.
,
Hoffman
,
E. A.
,
Norell
,
M. A.
, and
Bhullar
,
B.-A. S.
(2021
). “
The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization
,” Science
372
, 601
–609
.38.
Hawkins
,
A. D.
, and
Popper
,
A. N.
(2018
). “
Directional hearing and sound source localization by fishes
,” J. Acoust. Soc. Am.
144
, 3329
–3350
.39.
Heffner
,
H. E.
, and
Heffner
,
R. S.
(2016
). “
The evolution of mammalian sound localization
,” Acoust. Today
12
, 20
–27, 35
.40.
Holmes
,
L. J.
,
McWilliam
,
J.
,
Ferrari
,
M. C. O.
, and
McCormick
,
M. I.
(2017
). “
Juvenile damselfish are affected but desensitize to small motor boat noise
,” J. Exp. Mar. Biol. Ecol.
494
, 63
–68
.41.
Iyer
,
J. S.
,
Zhu
,
N.
,
Gasilov
,
S.
,
Ladak
,
H. M.
,
Agrawal
,
S. K.
, and
Stankovic
,
K. M.
(2018
). “
Visualizing the 3D cytoarchitecture of the human cochlea in an intact temporal bone using synchrotron radiation phase contrast imaging
,” Biomed. Opt. Express
9
, 3757
–3767
.42.
Johansson
,
K.
,
Sigray
,
P.
,
Backström
,
T.
, and
Magnhagen
,
C.
(2015
). “
Stress response and habituation to motorboat noise in two coastal fish species in the Bothnian Sea
,” Adv. Exp. Med. Biol.
875
, 513
–521
.43.
Kasumyan
,
A. O.
(2004
). “
The vestibular system and sense of equilibrium in fish
,” J. Ichthyol.
44
, S224
–S268
.44.
Kenyon
,
T.
,
Ladich
,
F.
, and
Yan
,
H.
(1998
). “
A comparative study of hearing ability in fishes: The auditory brainstem response approach
,” J. Comp. Physiol. A.
182
, 307
–318
.45.
Kolston
,
P. J.
(2000
). “
Finite-element modelling: A new tool for the biologist
,” Philos. Trans. R. Soc. A.
358
, 611
–631
.46.
Koyabu
,
D.
,
Hosojima
,
M.
, and
Endo
,
H.
(2017
). “
Into the dark: Patterns of middle ear adaptations in subterranean eulipotyphlan mammals
,” R. Soc. Open Sci.
4
, 170608
.47.
Krysl
,
P.
,
Cranford
,
T. W.
, and
Hildebrand
,
J. A.
(2008
). “
Lagrangian finite element treatment of transient vibration/acoustics of biosolids immersed in fluids
,” Int. J. Numer. Methods Eng.
74
, 754
–775
.48.
Krysl
,
P.
,
Hawkins
,
A. D.
,
Schilt
,
C.
, and
Cranford
,
T. W.
(2012
). “
Angular oscillation of solid scatterers in response to progressive planar acoustic waves: Do fish otoliths rock?
,” PloS One
7
, e42591
.49.
Ladich
,
F.
(2013
). “
Diversity in hearing in fishes: Ecoacoustical, communicative, and developmental constraints
,” in Insights from Comparative Hearing Research
, edited by
C.
Köppl
,
G.
Manley
,
A.
Popper
, and
R.
Fay
(
Springer
,
New York
), Vol. 49, pp. 289
–321
.50.
Ladich
,
F.
, and
Fay
,
R. R.
(2013
). “
Auditory evoked potential audiometry in fish
,” Rev. Fish. Biol. Fish.
23
, 317
–364
.51.
Ladich
,
F.
, and
Schulz-Mirbach
,
T.
(2016
). “
Diversity in fish auditory systems: One of the riddles of sensory biology
,” Front. Ecol. Evol.
4
, 28
.52.
Lamont
,
T. A. C.
,
Chapuis
,
L.
,
Williams
,
B.
,
Dines
,
S.
,
Gridley
,
T.
,
Frainer
,
G.
,
Fearey
,
J.
,
Maulana
,
P. B.
,
Prasetya
,
M. E.
,
Jompa
,
J.
,
Smith
,
D. J.
, and
Simpson
,
S. D.
(2022
). “
HydroMoth: Testing a prototype low‐cost acoustic recorder for aquatic environments
,” Remote Sens. Ecol. Conserv.
8
, 362
–378
.53.
Livens
,
P.
,
Muyshondt
,
P. G. G.
, and
Dirckx
,
J. J. J.
(2019
). “
Sound localization in the lizard using internally coupled ears: A finite-element approach
,” Hear. Res.
378
, 23
–32
.54.
Lombarte
,
A.
, and
Popper
,
A.
(2004
). “
Quantitative changes in the otolithic organs of the inner ear during the settlement period in European hake Merluccius merluccius
,” Mar. Ecol. Prog. Ser.
267
, 233
–240
.55.
Lu
,
Z.
, and
Xu
,
Z.
(2002
). “
Effects of saccular otolith removal on hearing sensitivity of the sleeper goby (Dormitator latifrons)
,” J. Comp. Physiol.
188
, 595
–602
.56.
Lu
,
Z.
,
Xu
,
Z.
, and
Stadler
,
J. H.
(2002
). “
Roles of the saccule in directional hearing
,” Bioacoustics
12
, 205
–207
.57.
Macho
,
G. A.
,
Shimizu
,
D.
,
Jiang
,
Y.
, and
Spears
,
I. R.
(2005
). “
Australopithecus anamensis: A finite‐element approach to studying the functional adaptations of extinct hominins
,” Anat. Rec.
283A
, 310
–318
.58.
Maftoon
,
N.
,
Funnell
,
W. R. J.
,
Daniel
,
S. J.
, and
Decraemer
,
W. F.
(2015
). “
Finite-element modelling of the response of the gerbil middle ear to sound
,” J. Assoc. Res. Otolaryngol.
16
, 547
–567
.59.
Maiditsch
,
I. P.
,
Ladich
,
F.
,
Heß
,
M.
,
Schlepütz
,
C. M.
, and
Schulz-Mirbach
,
T.
(2022
). “
Revealing sound-induced motion patterns in fish hearing structures in 4D: A standing wave tube-like setup designed for high-resolution time-resolved tomography
,” J. Exp. Biol.
225
, jeb243614
.60.
Maisey
,
J. G.
(2001
). “
Remarks on the inner ear of elasmobranchs and its interpretation from skeletal labyrinth morphology
,” J. Morphol.
250
, 236
–264
.61.
Maisey
,
J. G.
, and
Lane
,
J. A.
(2010
). “
Labyrinth morphology and the evolution of low-frequency phonoreception in elasmobranchs
,” C. R. Palevol.
9
, 289
–309
.62.
Marcé-Nogué
,
J.
, and
Liu
,
J.
(2020
). “
Evaluating fidelity of CT based 3D models for Zebrafish conductive hearing system
,” Micron
135
, 102874
.63.
Masterton
,
R. B.
(1974
). “
Adaptation for sound localization in the ear and brainstem of mammals
,” Fed. Proc.
33
, 1904
–1910
.64.
Monteiro
,
L. R.
,
Beneditto
,
A. P. M. D.
,
Guillermo
,
L. H.
, and
Rivera
,
L. A.
(2005
). “
Allometric changes and shape differentiation of sagitta otoliths in sciaenid fishes
,” Fish. Res.
74
, 288
–299
.65.
Muñoz
,
M. M.
, and
Price
,
S. A.
(2019
). “
The future is bright for evolutionary morphology and biomechanics in the era of big data
,” Integr. Comp. Biol.
59
, 599
–603
.66.
Naylor
,
G. J. P.
,
Caira
,
J. N.
,
Jensen
,
K.
,
Rosana
,
K. A. M.
,
Straube
,
N.
, and
Lakner
,
C.
(2012
). “
Elasmobranch phylogeny: A mitochondrial estimate based on 595 species
,” in Biology of Sharks and Their Relatives
, 2nd ed
., edited by
J. C.
Carrier
,
J. A.
Musick
, and
M. R.
Heithaus
(
CRC Press
,
Boca Raton, FL
), pp. 31
–56
.67.
Nedelec
,
S. L.
,
Mills
,
S. C.
,
Lecchini
,
D.
,
Nedelec
,
B.
,
Simpson
,
S. D.
, and
Radford
,
A. N.
(2016
). “
Repeated exposure to noise increases tolerance in a coral reef fish
,” Environ. Pollut.
216
, 428
–436
.68.
Neenan
,
J. M.
,
Reich
,
T.
,
Evers
,
S. W.
,
Druckenmiller
,
P. S.
,
Voeten
,
D. F. A. E.
,
Choiniere
,
J. N.
,
Barrett
,
P. M.
,
Pierce
, S. E.
, and
Benson
, R. B. J.
(2017
). “
Evolution of the sauropterygian labyrinth with increasingly pelagic lifestyles
,” Curr. Biol.
27
, 3852
–3858.e3
.69.
Nelson
,
E. M.
(1955
). “
The morphology of the swim bladder and auditory bulla in the Holocentridae
,” Fieldiana, Zool.
35
(5
), 121
–130
.70.
Nieder
,
C.
,
Rapson
,
J.
,
Holland
,
K.
,
Meyer
,
C.
,
Montgomery
,
J.
, and
Radford
,
C.
(2023
). “
Operant conditioning as a tool to assess hearing abilities in sharks
,” J. Fish. Biol.
103
, 411
–424
.71.
Norton
,
S. F.
,
Luczkovich
,
J. J.
, and
Motta
,
P. J.
(1995
). “
The role of ecomorphological studies in the comparative biology of fishes
,” Environ. Biol. Fish.
44
, 287
–304
.72.
O'Higgins
,
P.
,
Fitton
,
L. C.
, and
Godinho
,
R. M.
(2019
). “
Geometric morphometrics and finite elements analysis: Assessing the functional implications of differences in craniofacial form in the hominin fossil record
,” J. Archaeol. Sci.
101
, 159
–168
.73.
Oldfield
,
C. C.
,
McHenry
,
C. R.
,
Clausen
,
P. D.
,
Chamoli
,
U.
,
Parr
,
W. C. H.
,
Stynder
,
D. D.
, and
Wroe
,
S.
(2012
). “
Finite element analysis of ursid cranial mechanics and the prediction of feeding behaviour in the extinct giant Agriotherium africanum
,” J. Zool.
286
, 171
–171
.74.
Panagiotopoulou
,
O.
(2009
). “
Finite element analysis (FEA): Applying an engineering method to functional morphology in anthropology and human biology
,” Ann. Hum. Biol.
36
, 609
–623
.75.
Pfaff
,
C.
,
Kriwet
,
J.
,
Martin
,
K.
, and
Johanson
,
Z.
(2019a
). “
Ontogenetic development of the otic region in the new model organism, Leucoraja erinacea (Chondrichthyes; Rajidae
),” Earth Environ. Sci. Trans. R.
109
, 105
–114
.76.
Pfaff
,
C.
,
Schultz
,
J. A.
, and
Schellhorn
,
R.
(2019b
). “
The vertebrate middle and inner ear: A short overview
,” J. Morphol.
280
, 1098
–1105
.77.
Platt
,
C.
(1988
). “Equilibrium in the vertebrates: Signals, senses, and steering underwater,” in Sensory Biology of Aquiatic Animals, edited by J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (Springer, New York), pp. 783
–809
.78.
Platt
,
C.
, and
Popper
,
A. N.
(1981
). “
Structure and function in the ear
,” in Hearing and Sound Communication in Fishes
, edited by
W. N.
Tavolga
,
A. N.
Popper
, and
R. R.
Fay
(Springer, New York), pp. 3–38.79.
Polly
,
P. D.
,
Stayton
,
C. T.
,
Dumont
,
E. R.
,
Pierce
,
S. E.
,
Rayfield
,
E. J.
, and
Angielczyk
,
K. D.
(2016
). “
Combining geometric morphometrics and finite element analysis with evolutionary modeling: Towards a synthesis
,” J. Vertebr. Paleontol.
36
, e1111225
.80.
Ponton
,
D.
(2006
). “
Is geometric morphometrics efficient for comparing otolith shape of different fish species?
,” J. Morphol.
267
, 750
–757
.81.
Popper
,
A. N.
(1981
). “
Comparative scanning electron microscopic investigations of the sensory epithelia in the teleost sacculus and lagena
,” J. Comp. Neurol.
200
, 357
–374
.82.
Popper
,
A. N.
, and
Coombs
,
S.
(1982
). “
The morphology and evolution of the ear in actinopterygian fishes
,” Am. Zool.
22
, 311
–328
.83.
Popper
,
A. N.
, and
Hawkins
,
A. D.
(2019
). “
An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes
,” J. Fish. Biol.
94
, 692
–713
.84.
Popper
,
A. N.
,
Hawkins
,
A. D.
,
Sand
,
O.
, and
Sisneros
,
J. A.
(2019
). “
Examining the hearing abilities of fishes
,” J. Acoust. Soc. Am.
146
, 948
–955
.85.
Popper
,
A. N.
,
Hawkins
,
A. D.
, and
Sisneros
,
J. A.
(2022
). “
Fish hearing ‘specialization’ - a re-evaluation
,” Hear. Res.
425
, 108393
.86.
Popper
,
A. N.
, and
Tavolga
,
W. N.
(1981
). “
Structure and function of the ear in the marine catfish, Arius felis
,” J. Comp. Physiol.
144
, 27
–34
.87.
Rajabizadeh
,
M.
,
Wassenbergh
,
S. V.
,
Mallet
,
C.
,
Rücklin
,
M.
, and
Herrel
,
A.
(2021
). “
Tooth-shape adaptations in aglyphous colubrid snakes inferred from three-dimensional geometric morphometrics and finite element analysis
,” Zool. J. Linn. Soc.
191
, 454
–467
.88.
Ramprashad
,
F.
,
Landolt
,
J. P.
,
Money
,
K. E.
, and
Laufer
,
J.
(1986
). “
Comparative morphometric study of the vestibular system of the vertebrata: Reptilia, aves, amphibia, and pisces
,” Acta Oto-Laryngol., Suppl.
427
, 1
–42
.89.
Rayfield
,
E. J.
(2007
). “
Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms
,” Annu. Rev. Earth Planet. Sci.
35
, 541
–576
.90.
Retzius
,
G.
(1881
). Das GehöRorgan Der Wirbelthiere: Morphologisch-Histologische Studien
(The Auditory Organ of Vertebrates: Morphological-Histological Studies) (
Samson and Wallin
, Stockholm
).91.
Richmond
,
B. G.
,
Wright
,
B. W.
,
Grosse
,
L.
,
Dechow
,
P. C.
,
Ross
,
C. F.
,
Spencer
,
M. A.
, and
Strait
,
D. S.
(2005
). “
Finite element analysis in functional morphology
,” Anat. Rec.
283A
, 259
–274
.92.
Robins
,
H.
, and
Chapuis
,
L.
(2022
). “Hearing system of the Southern fiddler ray, Trygonorrhina dumerilii” (unpublished).93.
Rogers
,
L. S.
, and
Sisneros
,
J. A.
(2020
). “
Auditory evoked potentials of utricular hair cells in the plainfin midshipman, Porichthys notatus
,” J. Exp. Biol.
223
, jeb226464
.94.
Salas
,
A. K.
,
Wilson
,
P. S.
, and
Fuiman
,
L. A.
(2019a
). “
Predicting pressure sensitivity through ontogeny in larval red drum (Sciaenops ocellatus)
,” Proc. Mtgs. Acoust.
37
, 010006
.95.
Salas
,
A. K.
,
Wilson
,
P. S.
, and
Fuiman
,
L. A.
(2019b
). “
Ontogenetic change in predicted acoustic pressure sensitivity in larval red drum (Sciaenops ocellatus
),” J. Exp. Biol.
222
, jeb201962
.96.
Sauer
,
D. J.
,
Radford
,
C. A.
,
Mull
,
C. G.
, and
Yopak
,
K. E.
(2023
). “
Quantitative assessment of inner ear variation in elasmobranchs
,” Sci. Rep.
13
, 11939
.97.
Sauer
,
D. J.
,
Yopak
,
K. E.
, and
Radford
,
C. A.
(2022a
). “
Ontogenetic development of inner ear hair cell organization in the New Zealand carpet shark Cephaloscyllium isabellum
,” Front. Ecol. Evol.
10
, 1034891
.98.
Sauer
,
D. J.
,
Yopak
,
K. E.
, and
Radford
,
C. A.
(2022b
). “
Ontogeny of the inner ear maculae in school sharks (Galeorhinus galeus)
,” Hear. Res.
424
, 108600
.99.
Schilt
,
C. R.
,
Cranford
,
T. W.
,
Krysl
,
P.
, and
Hawkins
,
A. D.
(2011
). “
Vibration of otolithlike scatterers due to low frequency harmonic wave excitation in water
,” J. Acoust. Soc. Am.
129
, 2472
.100.
Schnetz
,
L.
,
Kriwet
,
J.
, and
Pfaff
,
C.
(2016
). “
Virtual reconstruction of the skeletal labyrinth of two lamnid sharks (Elasmobranchii, Lamniformes)
,” J. Fish. Biol.
90
, 1083
–1089
.101.
Schulz-Mirbach
,
T.
,
Heß
,
M.
, and
Metscher
,
B. D.
(2013
). “
Sensory epithelia of the fish inner ear in 3D: Studied with high-resolution contrast enhanced microCT
,” Front. Zool.
10
(1
), 63
.102.
Schulz-Mirbach
,
T.
, and
Ladich
,
F.
(2016
). “
Diversity of inner ears in fishes: Possible contribution towards hearing improvements and evolutionary considerations
,” Adv. Exp. Med. Biol.
877
, 341
–391
.103.
Schulz-Mirbach
,
T.
,
Ladich
,
F.
,
Mittone
,
A.
,
Olbinado
,
M.
,
Bravin
,
A.
,
Maiditsch
,
I. P.
,
Melzer
,
R. R.
,
Krysl
,
P.
, and
Heß
,
M.
(2020
). “
Auditory chain reaction: Effects of sound pressure and particle motion on auditory structures in fishes
,” PLoS One
15
, e0230578
.104.
Schulz-Mirbach
,
T.
,
Ladich
,
F.
,
Plath
,
M.
,
Metscher
,
B. D.
, and
Heß
,
M.
(2014
). “
Are accessory hearing structures linked to inner ear morphology? Insights from 3D orientation patterns of ciliary bundles in three cichlid species
,” Front. Zool.
11
, 25
.105.
Schulz-Mirbach
,
T.
,
Metscher
,
B.
, and
Ladich
,
F.
(2012
). “
Relationship between swim bladder morphology and hearing abilities–A case study on Asian and African cichlids
,” PloS One
7
, e42292
.106.
Schulz-Mirbach
,
T.
,
Olbinado
,
M.
,
Rack
,
A.
,
Mittone
,
A.
,
Bravin
,
A.
,
Melzer
,
R. R.
,
Ladich
,
F.
, and
Heß
,
M.
(2018
). “
In-situ visualization of sound-induced otolith motion using hard X-ray phase contrast imaging
,” Sci. Rep.
8
, 3121
.107.
Schwab
,
J. A.
,
Young
,
M. T.
,
Neenan
,
J. M.
,
Walsh
,
S. A.
,
Witmer
,
L. M.
,
Herrera
,
Y.
,
Allain
,
R.
,
Brochu
,
C. A.
,
Choiniere
,
J. N.
,
Clark
,
J. M.
,
Dollman
,
K. N.
,
Etches
,
S.
,
Fritsch
,
G.
,
Gignac
,
P. M.
,
Ruebenstahl
,
A.
,
Sachs
,
S.
,
Turner
,
A. H.
,
Vignaud
,
P.
,
Wilberg
,
E. W.
,
Xu
,
X
,
Zanno
,
L. E.
, and
Brusatte
, S. L.
(2020
). “
Inner ear sensory system changes as extinct crocodylomorphs transitioned from land to water
,” Proc. Natl. Acad. Sci. U.S.A.
117
, 10422
–10428
.108.
Seehausen
,
O.
,
Terai
,
Y.
,
Magalhaes
,
I. S.
,
Carleton
,
K. L.
,
Mrosso
,
H. D. J.
,
Miyagi
,
R.
,
van der Sluijs
,
I.
,
Schneider
,
M. V.
,
Maan
,
M. E.
,
Tachida
,
H.
,
Imai
,
H.
, and
Okada
,
N.
(2008
). “
Speciation through sensory drive in cichlid fish
,” Nature
455
, 620
–626
.109.
Sethi
,
S. S.
,
Jones
,
N. S.
,
Fulcher
,
B. D.
,
Picinali
,
L.
,
Clink
,
D. J.
,
Klinck
,
H.
,
Orme
,
C. D. L.
,
Wrege
,
P. H.
, and
Ewers
,
R. M.
(2020
). “
Characterizing soundscapes across diverse ecosystems using a universal acoustic feature set
,” Proc. Natl. Acad. Sci. U.S.A.
117
, 17049
–17055
.110.
Simões
,
J. M.
,
Teles
,
M. C.
,
Oliveira
,
R. F.
,
Van der Linden
,
A.
, and
Verhoye
,
M.
(2012
). “
A three-dimensional stereotaxic MRI brain atlas of the cichlid fish Oreochromis mossambicus
,” PloS One
7
, e44086
.111.
Sparks
,
J. S.
,
Schelly
,
R. C.
,
Smith
,
W. L.
,
Davis
,
M. P.
,
Tchernov
,
D.
,
Pieribone
,
V. A.
, and
Gruber
,
D. F.
(2014
). “
The covert world of fish biofluorescence: A phylogenetically widespread and phenotypically variable phenomenon
,” PLoS One
9
, e83259
.112.
Staggl
,
M. A.
,
Abed-Navandi
,
D.
, and
Kriwet
,
J.
(2022
). “
Cranial morphology of the orectolobiform shark, Chiloscyllium punctatum Müller & Henle, 1838
,” Vertebr. Zool.
72
, 311
–370
.113.
Stowell
,
D.
(2022
). “
Computational bioacoustics with deep learning: A review and roadmap
,” PeerJ.
10
, e13152
.114.
Tse
,
T. C. H.
,
Lo
,
H. C.
,
Montgomery
,
J.
, and
Anderson
,
I.
(2014
). “
Towards a fish-inspired underwater hearing device
,” Proc. SPIE
9055
, 90550E
.115.
Tubelli
,
A. A.
,
Zosuls
,
A.
,
Ketten
,
D. R.
, and
Mountain
,
D. C.
(2018
). “
A model and experimental approach to the middle ear transfer function related to hearing in the humpback whale (Megaptera novaeangliae
),” J. Acoust. Soc. Am.
144
, 525
–535
.116.
Tubelli
,
A. A.
,
Zosuls
,
A.
,
Ketten
,
D. R.
,
Yamato
,
M.
, and
Mountain
,
D. C.
(2012
). “
A prediction of the minke whale (Balaenoptera acutorostrata) middle-ear transfer function
,” J. Acoust. Soc. Am.
132
, 3263
–3272
.117.
Ullmann
,
J. F. P.
,
Cowin
,
G.
, and
Collin
,
S. P.
(2010a
). “
Magnetic resonance microscopy of the barramundi (Lates calcarifer) brain
,” J. Morphol.
271
, 1446
–1456
.118.
Ullmann
,
J. F. P.
,
Cowin
,
G.
, and
Collin
,
S. P.
(2011
). “
Quantitative assessment of brain volumes in fish: Comparison of methodologies
,” Brain. Behav. Evol.
76
, 261
–270
.119.
Ullmann
,
J. F. P.
,
Cowin
,
G.
,
Kurniawan
,
N. D.
, and
Collin
,
S. P.
(2010b
). “
A three-dimensional digital atlas of the zebrafish brain
,” NeuroImage
51
, 76
–82
.120.
v. Frisch
,
K.
, and
Stetter
,
H.
(1932
). “
Unterbuchungen über den Sitz des Géhörsinnes bei der Elritze
” (“Experiments on the localization of auditory sensitivity in the minnow”), Z. Vgl. Physiol.
17
, 686
–801
.121.
Vetter
,
B. J.
,
Seeley
,
L. H.
, and
Sisneros
,
J. A.
(2019
). “
Lagenar potentials of the vocal plainfin midshipman fish, Porichthys notatus
,” J. Comp. Physiol. A.
205
, 163
–175
.122.
Vickerton
,
P.
,
Jarvis
,
J.
, and
Jeffery
,
N.
(2013
). “
Concentration‐dependent specimen shrinkage in iodine‐enhanced microCT
,” J. Anat.
223
, 185
–193
.123.
Wainwright
,
P. C.
(2007
). “
Functional versus morphological diversity in macroevolution
,” Annu. Rev. Ecol. Evol. Syst.
38
, 381
–401
.124.
Weber
,
E. H.
(1819
). “
Vergleichende Anatomie der Gehörwerkzeuge
” (“Comparative anatomy of the hearing system”), Dtsch. Physiol.
5
, 323
–332
.125.
Weber
,
E. H.
(1820
). De Aure et Auditu Hominis et Animalium. Part I. De Aure Animalium Aquatilium
(Of the Ear and Hearing of Man and Animals. Part I. About Ears of Aquatic Animals) (
Apud Gerhardum Fleischerum
,
Lipsiae
).126.
Wei
,
C.
,
Au
,
W. W. L.
,
Ketten
,
D. R.
,
Song
,
Z.
, and
Zhang
,
Y.
(2017
). “
Biosonar signal propagation in the harbor porpoise's (Phocoena phocoena) head: The role of various structures in the formation of the vertical beam
,” J. Acoust. Soc. Am.
141
, 4179
–4187
.127.
Wei
,
C.
,
Au
,
W. W. L.
,
Ketten
,
D. R.
, and
Zhang
,
Y.
(2018
). “
Finite element simulation of broadband biosonar signal propagation in the near- and far-field of an echolocating Atlantic bottlenose dolphin (Tursiops truncates)
,” J. Acoust. Soc. Am.
143
, 2611
–2620
.128.
Wei
,
C.
, and
McCauley
,
R. D.
(2022
). “
Numerical modeling of the impacts of acoustic stimulus on fish otoliths from two directions
,” J. Acoust. Soc. Am.
152
, 3226
–3234
.129.
Wilkins
,
M. R.
,
Seddon
,
N.
, and
Safran
,
R. J.
(2013
). “
Evolutionary divergence in acoustic signals: Causes and consequences
,” Trends Ecol. Evol.
28
, 156
–166
.130.
Yopak
,
K. E.
,
Carrier
,
J. C.
, and
Summers
,
A. P.
(2018
). “
Imaging technologies in the field and laboratory
,” in Shark Research: Emerging Technologies and Applications for the Field and Laboratory
, edited by
C. A.
Simpfendorfer
,
J. C.
Carrier
, and
M. R.
Heithaus
(
CRC Press
,
New York
), pp. 157
–176
.131.
Yopak
,
K. E.
, and
Frank
,
L. R.
(2009
). “
Brain size and brain organization of the whale shark, rhincodon typus, using magnetic resonance imaging
,” Brain. Behav. Evol.
74
, 121
–142
.132.
Yopak
,
K. E.
,
Galinsky
,
V. L.
,
Berquist
,
R. M.
, and
Frank
,
L. R.
(2016
). “
Quantitative classification of cerebellar foliation in cartilaginous fishes (class: chondrichthyes) using three-dimensional shape analysis and its implications for evolutionary biology
,” Brain. Behav. Evol.
87
, 252
–264
.133.
Zhang
,
X.-H.
,
Tao
,
Y.
,
Zhou
,
Y.-L.
,
Tang
,
L.-G.
,
Liu
,
M.
, and
Xu
,
X.-M.
(2021
). “
Acoustic properties of the otolith of the large yellow croaker Larimichthys crocea (perciformes: sciaenidae)
,” Zool. Stud.
60
, e64
.© 2023 Acoustical Society of America.
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