256
Popper and Fay 1973 , 1993 , 1999 ; Fay and Popper 2012 ). While this might be a
reasonable approach to take for terrestrial animals, we feel it is unjustifi ed for studying
responses of fi sh to sound due to the complexities of sound transmission underwater
(Parvulescu 1967 ; Akamatsu et al. 2002 ; Zeddies et al. 2010 ) as well as the short
distances over which fi sh “acoustic” communication typically occurs (reviewed in
Zelick et al. 1999 ; Ladich 2004 ). As early as 1967 Parvulescu argued that, especially in laboratory experiments, “animal behavior may be due to lateral-line
response rather than to auditory system response” (Parvulescu 1967 ) and yet many
researchers focus largely on the “auditory response” when examining responses of
fi sh after sound presentation in tanks. By focusing on hearing as the main mechanism of sound source detection in fi sh, not only are we missing valuable insights
into how fi sh respond to sound stimuli but we also may have diffi culty interpreting
evolutionary trends in sound detection. We argue here that detection of many sound
sources, although by no means all, is best examined as a multimodal response in
which fi sh use both the ear and lateral line, and associated structures (e.g. Weberian
ossicles and laterophysic connections), to form a full picture of sound stimuli, likely
incorporating all inputs into a sensory gestalt after integration by central neural
structures. While we of course do not advocate going back to the views of van
Bergeijk ( 1964 ) that the ear plays little role in localization or even detection, we do
argue that the pendulum has swung too far toward focus on the ear as the primary
detector of sound stimuli, especially in the highly artifi cial laboratory or nearfi eld
environment. The ear and lateral line are complementary, but not redundant, systems
and only by fully understanding their central integration will we have a true appreciation for the importance of sound to the sensory ecology of fi sh and how this may
have evolved across the Osteichthyes particularly and across the broader grouping
of animals considered “fi sh”.
2 Basic Concepts
An underwater acoustic stimulus has two components, the nearfi eld and farfi eld,
both of which provide important information to fi sh. The “nearfi eld” is dominated
by hydrodynamic fl ow and the “farfi eld” is dominated by a propagating pressure
wave (Fig. 1 ). Hydrodynamic fl ow is generated by the movement of water near the
acoustic stimulus source, while sound pressure waves propagate from the acoustic
source as a cyclic compression and rarefaction of the water (Rogers and Cox 1988 ;
Higgs et al. 2006 ). The fi sh mechanosensory lateral line is sensitive to hydrodynamic fl ow within one to two body lengths from the source (nearfi eld), and is not
generally sensitive to pressure (Montgomery et al. 1995 ; Sand and Bleckmann
2008 ). The lateral line has two types of receptors: superfi cial neuromasts (particle
velocity sensitive), which lie on the surface of the skin; and canal neuromasts (particle
acceleration sensitive), which are found in subdermal canals that open to the external environment via a series of pores. The inner ear is also sensitive to the particle
movement of an acoustic fi eld as a result of whole-body accelerations (Rogers and
D.M. Higgs and C.A. Radford
Popper and Fay 1973 , 1993 , 1999 ; Fay and Popper 2012 ). While this might be a
reasonable approach to take for terrestrial animals, we feel it is unjustifi ed for studying
responses of fi sh to sound due to the complexities of sound transmission underwater
(Parvulescu 1967 ; Akamatsu et al. 2002 ; Zeddies et al. 2010 ) as well as the short
distances over which fi sh “acoustic” communication typically occurs (reviewed in
Zelick et al. 1999 ; Ladich 2004 ). As early as 1967 Parvulescu argued that, especially in laboratory experiments, “animal behavior may be due to lateral-line
response rather than to auditory system response” (Parvulescu 1967 ) and yet many
researchers focus largely on the “auditory response” when examining responses of
fi sh after sound presentation in tanks. By focusing on hearing as the main mechanism of sound source detection in fi sh, not only are we missing valuable insights
into how fi sh respond to sound stimuli but we also may have diffi culty interpreting
evolutionary trends in sound detection. We argue here that detection of many sound
sources, although by no means all, is best examined as a multimodal response in
which fi sh use both the ear and lateral line, and associated structures (e.g. Weberian
ossicles and laterophysic connections), to form a full picture of sound stimuli, likely
incorporating all inputs into a sensory gestalt after integration by central neural
structures. While we of course do not advocate going back to the views of van
Bergeijk ( 1964 ) that the ear plays little role in localization or even detection, we do
argue that the pendulum has swung too far toward focus on the ear as the primary
detector of sound stimuli, especially in the highly artifi cial laboratory or nearfi eld
environment. The ear and lateral line are complementary, but not redundant, systems
and only by fully understanding their central integration will we have a true appreciation for the importance of sound to the sensory ecology of fi sh and how this may
have evolved across the Osteichthyes particularly and across the broader grouping
of animals considered “fi sh”.
2 Basic Concepts
An underwater acoustic stimulus has two components, the nearfi eld and farfi eld,
both of which provide important information to fi sh. The “nearfi eld” is dominated
by hydrodynamic fl ow and the “farfi eld” is dominated by a propagating pressure
wave (Fig. 1 ). Hydrodynamic fl ow is generated by the movement of water near the
acoustic stimulus source, while sound pressure waves propagate from the acoustic
source as a cyclic compression and rarefaction of the water (Rogers and Cox 1988 ;
Higgs et al. 2006 ). The fi sh mechanosensory lateral line is sensitive to hydrodynamic fl ow within one to two body lengths from the source (nearfi eld), and is not
generally sensitive to pressure (Montgomery et al. 1995 ; Sand and Bleckmann
2008 ). The lateral line has two types of receptors: superfi cial neuromasts (particle
velocity sensitive), which lie on the surface of the skin; and canal neuromasts (particle
acceleration sensitive), which are found in subdermal canals that open to the external environment via a series of pores. The inner ear is also sensitive to the particle
movement of an acoustic fi eld as a result of whole-body accelerations (Rogers and
D.M. Higgs and C.A. Radford