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Ultrasound Detection in Fishes and Frogs:
Discovery and Mechanisms
Peter M. Narins, Maria Wilson, and David A. Mann
Keywords Alosinae • Amphibian papilla • Anti-predator response • Basilar papilla
• Clupeids • Echolocation • Environmental constraints on hearing • Huia
cavitympanum • Hair cells • Inner ear • Lateral line • Odorrana graminea
•Odorrana tormota • Toothed whales • Torus semicircularis
1 Introduction
The frequency range of hearing in fishes and frogs historically has been thought to
be confined to relatively low frequencies in comparison to mammals (Hawkins,
1981; Fay, 1988). The fishes with the greatest sensitivity and frequency bandwidth,
such as the otophysans, a group of species that have a mechanical coupling between
the swim bladder and inner ear, have upper frequency sensitivities below 5 kHz
(Fay, 1988). Similarly for frogs, audiogram studies typically have tested only up to
4–5 kHz (Fay, 1988).
However, there have been hints of higher frequency sensitivity in some fishes and
frogs. In 1982 Boyd Kynard discovered that ultrasonic sonar (about 160 kHz) caused
behavioral responses in migrating Alosa sapidissima (Kynard & O’Leary, 1990).
P.M. Narins (*)
Departments of Integrative Biology & Physiology, and Ecology & Evolutionary Biology,
University of California Los Angeles, 621 Charles E. Young Drive S., Los Angeles,
CA 90095-1606, USA
e-mail: pnarins@ucla.edu
M. Wilson
Department of Bioscience, The Faculty of Mathematics and Natural Sciences, University of
Oslo, Oslo, Norway
e-mail: maria.wilson@biology.au.dk
D.A. Mann
Loggerhead Instruments, 6576 Palmer Park Circle, Sarasota, FL 34238, USA
e-mail: dmann@loggerheadinstruments.com
C. Ko
¨ppl et al. (eds.), Insights from Comparative Hearing Research,
Springer Handbook of Auditory Research 49, DOI 10.1007/2506_2013_29,
©Springer Science+Business Media New York 2013
This eventually led Mann et al. (1997) to measure the audiogram of Alosa
sapidissima and indeed confirmed that the species could detect ultrasound (US).
More recently, studies of anurans with a unique canal ear morphology showed that
there were ultrasonic components in their vocalizations, and that they could detect
these ultrasonic call components (Narins et al., 2004; Feng et al., 2006).
This chapter reviews US detection in fishes and frogs and ultrasonic acoustic
communication in frogs. Ultrasonic acoustic communication has not been found in
any soniferous fish species to date. Although the evolution of US detection in these
species is still a topic of study, both fishes and frogs have faced the challenge of
producing very high frequency responses from systems that evolved with
low-frequency sensitivity.
2 US Detection in Fish
2.1 Historical Overview of US Detection in Fish
In the early 1990s, several papers were published showing that pulsed high-
frequency sounds at 110–140 kHz and with high intensities (180 dB re 1 μPa)
were effective in deterring at least two fish species belonging to the subfamily of
Alosine (shad and menhaden) from power plant intakes: Alosa aestivalis (Nestler
et al., 1992) and Alosa pseudoharengus (Dunning et al., 1992). It was unclear
whether the fishes detected the ultrasonic component of the emitted signals or
low-frequency byproducts, but still these observations mark the beginning of the
study of US detection in fish.
The first audiogram of a member of the Alosinae, the Alosa sapidissima, was
measured using classical conditioning of heartbeat by Mann et al. (1997), who
showed that this species could detect sound in the ultrasonic frequency range up to
180 kHz. The detection threshold was high in comparison to low-frequency
thresholds, as the most sensitive ultrasonic frequency of 38 kHz had a threshold
of 137 dB re 1 μPa (rms) (Mann et al., 1997,1998) (Fig. 1).
Later behavioral and physiological studies showed that additional species
belonging to the Alosinae can detect and respond to US. These include Brevoortia
patronus (Mann et al., 2001) and two species of European shad, Alosa fallax fallax
(Gregory et al., 2007) and Alosa alosa (Wilson et al., 2008). The ability to detect US
appears to be limited to the subfamily of Alosinae, as it has not been found in other
clupeiforme fish species in the subfamily Clupeinae, including Clupea pallasii,
Anchoa mitchilli,Harengula Jaguana (Mann et al., 2001,2005), Clupea harengus
(Wilson, unpublished data), or in the subfamily Dorosomatinae, including
Dorosoma petense (Casper and Mann, unpublished data).
It also does not appear that other fishes are able to detect US, although very
few hearing studies have tested for this ability. One study conditioned Gadus
morhua to ultrasonic pulses at 38 kHz with a threshold for detection of 204 dB
P.M. Narins et al.
re 1 μPa (pp) (Astrup & Møhl, 1993). However, because of the very high thresholds,
the authors suggested that the response might be caused by stimulation of cutaneous
or other somatosensory receptors. A follow-up study by Schack et al. (2008) found
that unconditioned Gadus morhua did not show any behavioral or physiological
response when exposed to the same type of stimulus generated with the same
equipment as used in the study performed by Astrup and Møhl (1993). Thus,
there appears to be little evidence favoring US detection by Gadus morhua.
2.2 Why Detect US?
No fish species are known to produce communication sounds with ultrasonic
frequency components (Bass & Ladich, 2008). Although several clupeid species
have been reported to produce sound associated with gas release from the swim
bladder (Wahlberg & Westerberg, 2003; Wilson et al., 2004), the frequencies
produced are below 20 kHz. One of the obvious questions to ask is, then, why do
Alosinae detect ultrasonic signals at all?
One of the natural ultrasonic sound sources in the aquatic environment is the top
predatory toothed whales (Odontoceti) that target a broad range of both cephalopod
and fish species (Clarke, 1977; Santos et al., 2001). Toothed whales use echoloca-
tion to locate and catch prey and to seek information about their surroundings
102103104105106
100
110
120
130
140
150
160
170
Frequency (Hz)
Threshold (dB re 1 µPa)
Fig. 1 Audiogram from (Alosa sapidissima) obtained by classical conditioning of heartbeat.
Means SEM from five American shad. (Modified after Mann et al., 1997,1998.)
Ultrasound Detection in Fishes and Frogs
(Au, 1993; Madsen et al., 2005). The source levels of the emitted echolocation
clicks can be up to 228 dB re 1 μPa (pp) (Au, 1993) and in the case of Physeter
macrocephalus even up to 240 dB re 1 μPa (pp) (Møhl et al., 2003). These clicks
travel through the water and reflect off targets, and then are detected by toothed
whales (Au, 1993). Because of the very high source levels, the toothed whales
loudly announce their presence for a prey that is capable of detecting US. The
frequency span with the main energy of the toothed whale echolocation signals
coincides with the frequency span within which the Alosinae are sensitive in the
ultrasonic frequency range.
The behavioral threshold sensitivity of Alosa sapidissima to a simulated dolphin
click was 171 dB re 1 μPa (pp) (Mann et al., 1998). Assuming spherical spreading
and an absorption coefficient of 0.02 dB/m, the predicted detection range is 187 m
for a 220 dB re 1 μPa (pp) dolphin click (Mann et al., 1998). It is therefore tempting
to envision that Alosinae can detect US to potentially avoid or reduce predation by
echolocating toothed whales.
This is analogous to a similar acoustic predator–prey interaction between bats
and some nocturnal insects (Nestler et al., 1992; Mann et al., 1997; Astrup, 1999).
Like toothed whales, the much smaller bats emit intense ultrasonic cries and use the
echoes reflected off objects during search and capture of their prey (Griffin, 1958).
The heavy predation pressure from echolocating bats is believed to be the main
driving force of the parallel evolution of ultrasonic sensitive ears in several dis-
tantly related families of moths (Miller & Surlykke, 2001) and in a number of other
nocturnal insects (Yack & Fullard, 1993; Hoy & Robert, 1996). When certain moths
are exposed to low-intensity ultrasonic bat cries, they turn directly away from the
sound source, increasing the distance to the bat (Roeder, 1962). If the bat is close,
the moth will exhibit a much stronger and unpredictable flight response pattern that
often ends in a power dive or passive fall toward the ground (Roeder, 1998). The
different response patterns exhibited by moths indicate that they detect the direction
and proximity of the predatory bat by listening to the ultrasonic bat cries.
If US sensitivity of Alosinae is used to serve as a way of detecting and avoiding
echolocating toothed whales, one would expect the fish to show behaviors that
might resemble those exhibited by moths when exposed to bat cries. This is indeed
what playback studies conducted on Alosa sapidissima and Alosa alosa have
shown. When shad are exposed to pure ultrasonic tones played at varying sound
pressure levels, they exhibit a graded directional response pattern. If the sound is
very intense, the fish exhibit a very strong and panic-like response, but as the sound
pressure level is reduced, the response gets weaker (Plachta & Popper, 2003;
Wilson et al., 2008). In a following study, Alosa alosa were exposed to ultrasonic
clicks played at varying repetition rates mimicking toothed whales in different
phases of prey capture. Toothed whales generally produce echolocation clicks at a
higher repetition rate as they approach prey, and most prey capture attempts are
terminated with a buzz phase where the repetition rate can be up to several hundred
clicks per second (Madsen et al., 2002,2005). When the energy for a given time is
increased based on a faster click rate (but with a constant sound pressure level), the
Alosa alosa exhibited an increase in swimming speed and decrease in reaction time.
P.M. Narins et al.
It was also found that the response is consistent with a predator avoidance response
in that the fish turn away from the sound source (Wilson et al., 2011). Based on
these playback studies, it can be concluded that Alosinae behave as if the response
to US is used as an antipredatory response against echolocating toothed whales.
2.3 On the Mechanism of US Detection in Alosinae
During the past 15 years, the mechanism of US detection in Alosinae has been a
mystery and there are different hypotheses on how they detect US. It has been
suggested that the inner ear is key to US detection (Mann et al., 1998; Higgs et al.,
2004; Popper et al., 2004); however, another hypothesis suggests that US detection
involves the lateral line (Wilson et al., 2009).
2.3.1 The Fish Lateral Line
Fishes have a lateral line that allows them to detect weak water motions (for
reviews see Coombs & Montgomery 1999; Sand & Bleckmann 2008). The sensory
receptors are hair cells clustered in groups of varying numbers forming a
neuromast. There are two types of neuromasts: superficial neuromasts found on
the skin surface and canal neuromasts embedded in canals (Webb et al., 2008). The
lateral line can be found on the head, trunk, or tail in varying patterns depending on
the species. In Clupeidae, canal neuromasts are restricted to the head (Hoss &
Blaxter, 1982; Blaxter et al., 1983) (Fig. 2), whereas the superficial neuromasts are
found on the entire body (Higgs & Fuiman, 1996).
Fig. 2 The canal lateral
line (Brevoortia tyrannus)
is restricted to the
head. N, neuromasts.
(From Hoss & Blaxter,
1982. Reproduced with
permission.)
Ultrasound Detection in Fishes and Frogs
The neuromasts are detectors of fluid flow and detect movements between
the fish and the surrounding water (Harris & van Bergeijk, 1962; Kalmijn, 1989).
The apical parts of the hair cells are embedded in a gelatinous cupula. Stimulation
of the neuromasts is by fluid motion that will make the cupula slide over the sensory
epithelium, causing a deflection of the hair cell (Kroese & van Netten, 1989). The
lateral line is a close-range system sensitive to low-frequency hydrodynamic
motion (Sand, 1981; Kalmijn, 1989; Bleckmann, 2008) and is involved in detection
of many stimuli, such as larger scale water motions, but also play an important role
on a smaller scale, including self-induced motions, swimming motions created by
a neighbor in schooling fish species, and predator–prey interactions (Coombs &
Montgomery, 1999).
2.3.2 The Fish Inner Ear
Fish have bilateral inner ears (Retzius, 1881). Each ear consists of three semicircu-
lar canals and three otolith organs (for a detailed review see Popper et al., 2003).
At the base of each canal there is a swelling, the ampulla, containing sensory hair
cells on a transverse ridge (crista ampullaris). Ventral to the canals are three fluid-
filled otolith organs, the utricle, saccule, and lagena. Each otolith organ contains a
dense calcified ear stone, the otolith, located on a gelatinous matrix overlying the
sensory epithelium (the macula) containing the hair cells (Fig. 3).
Fig. 3 The inner ear
(Clupea harengus).
(From Retzius, 1881.)
ca, cp; anterior, and
posterior semicircular
canals (not shown,
horizontal semicircular
canal), aa, ap; anterior, and
posterior cristae of
semicircular canals (not
shown; horizontal crista),
pl, and ms; lagenar
epithelium, and saccular
epithelium (not shown;
utriclar epithelium),
s; saccule
P.M. Narins et al.
The otolith organs can be modeled as accelerometers with decreasing sensitivity
above the resonance frequency of the system (Kalmijn, 1989; Sand & Karlsen,
2000). The fish body itself has almost the same acoustic impedance as water.
Thus, fish are effectively acoustically transparent and move with the same phase
as the surrounding water particles. However, when a fish is accelerated, hair cells
are deflected because of the inertial difference between the denser otolith
and the sensory epithelium in the inner ear (De Vries, 1950; Krysl et al., 2012).
An unspecialized fish ear is therefore stimulated by the particle motion component
of a sound field and is limited to frequencies below a few hundred Hz (Hawkins,
1981). Fish with only this direct pathway of stimulation include those without a
swim bladder, such as bottom-dwelling flatfish (Chapman & Sand, 1974), or fish
with a swim bladder but without a special connection between the inner ear and the
swim bladder, such as salmonids (Hawkins & Johnstone, 1978).
Some fish species have developed more sensitive hearing by mechanically
connecting the inner ear and the swim bladder or other gas-filled structures.
These specializations make the fish sensitive to the traveling sound pressure wave
of a sound field, and fish with this type of specialization can detect sound of
frequencies up to 3–5 kHz and with higher sensitivity (Popper et al., 2003).
2.3.3 The Ear of Clupeids
Clupeids have a unique anatomy in which the inner ear, lateral line, and swim
bladder are mechanically connected to one another via a hydrodynamic coupling.
In all clupeids (both US detecting and non-US detection species), gas-filled tubes on
each side of the head extend from the swim bladder and expand to gas-filled bullae
that are encapsulated in bone (O’Connell, 1955).
Computed tomography (CT) scans reveal rather elaborate structures of the
paired bullae (Wilson et al., 2009) (Fig. 4). All clupeids have one set of paired
bullae, the prootic bullae (named after the bone structure surrounding the bullae),
which is believed to be an auditory specialization (O’Connell, 1955) because it
is connected to the utricle of the inner ear (Fig. 5). The utricle is highly modified
in clupeids, unlike in non-clupeid fish, because it is divided into three parts:
anterior, middle, and posterior (Fig. 5) (O’Connell, 1955; Popper & Platt, 1979).
Each prootic bulla (the auditory bulla) is divided into two halves separated by the
elastic prootic membrane (Fig. 5). The lower part is filled with gas from the swim
bladder. The upper part of the prootic bulla is filled with perilymph. A slit, the
fenestra, connects the upper part of the prootic bulla to the perilymph-filled space
under the utricular macula. A small elastic thread passes through the fenestra and
links the prootic bulla membrane to the middle part of the utricle (Popper & Platt,
1979; Best & Gray, 1980).
In many clupeids, a second pair of bullae can be found, the pterotic bullae, that
are connected to the prootic bullae. They are located within the loop of the
horizontal semicircular canal. The function of the pterotic bullae is not known
(O’Connell, 1955).
Ultrasound Detection in Fishes and Frogs
The bullae are also connected to the lateral line via the lateral recess membrane.
The lateral line system of clupeids is heavily branched, with primary branches
radiating from the lateral recess (O’Connell, 1955; Denton & Blaxter, 1976;
Hoss & Blaxter, 1982) (Fig 2). Sensory neuromasts are found only in the primary
lateral line branches. The branches are connected with the surrounding water via
numerous pores at the narrowing ends of the branches (Blaxter et al., 1981; Hoss &
Blaxter, 1982).
Enger (1967) suggested that each bulla acts as a pressure-to-displacement
converter that expands the hearing range, making clupeids able to detecting higher
frequencies. When a sound pressure wave impinges on a clupeid fish, the swim
bladder and the gas-filled parts of the bullae start to vibrate. Motion of the gas in the
bulla presumably generate vibrations of the bulla membrane, which will produce
motions of the perilymph and the elastic thread. In that way the sound pressure
Fig. 4 The bullae complex of (Brevoortia patronus) and (Harengula jaguana). (a,b) Sagittal
views of the 3D reconstructions of the bullae, bullae perilymph, and otoliths in the (a)Harengula
jaguana and (b) Brevoortia patronus. (c,d) Caudal views of the 3D reconstructions in the (c)
Harengula jaguana and (d) Brevoortia patronus with 2D images illustrating the positioning of the
bulla and lateral recess relative to the body surface. Bulla, yellow; perilymph of bulla, light blue;
utricle, red; saccule, green; lagena, dark blue; rostral body of bulla, white arrow; approximate
location of lateral recess membrane, pink arrow. (From Wilson et al., 2009. Reproduced with
permission.)
P.M. Narins et al.
wave will be transformed into a local particle motion in the perilymph. This fluid
motion and the movement of the elastic thread may stimulate the utricular macula,
creating deflection of the hair cells in the utricle (Denton & Blaxter, 1976;
Denton et al., 1979). However, the motion of the perilymph generated by the
oscillating bullae has been hypothesized to also generate fluid motions in the
cephalic lateral line canals because of the very compliant lateral recess membrane
(Denton & Blaxter, 1976; Denton & Gray, 1983; Gray, 1984). Clupeids live in
schools and the main function of the bullae complex is probably to detect pressure
and displacement fluctuations in the water created by the swimming movements of
neighboring fish. (Denton & Gray, 1983). It can also be reasonably hypothesized
that the US detector of the Alosinae may be associated with the bullae complex.
Fig. 5 Model of the prootic bulla and the coupling to the utricular macula (a). bm; bulla
membrane, et; elastic thread, P; perilymph, E; endolymph, m; macula. (b) The macula of the
utriculus, showing the division into two areas, where hair cells are orientated in opposite
directions. Arrows show the direction of the hair cells. (From Best & Grey 1980. Reproduced
with permission.)
Ultrasound Detection in Fishes and Frogs
2.3.4 The Utricle as the US Detector
The prootic bulla and its connection to the utricle has been suggested to be the
key to US detection in Alosinae (Mann et al., 1998). Higgs et al. (2004) suggested
that a specialization of the utricular macula could be the site for US detection. The
connection between the middle part of the utricular macula and the rest of the
epithelium differs between the clupeids that detect US and clupeids that do not.
In the Alosinae, the support for the middle section of the utricular macula is
particularly thin compared to that of other clupeids. Higgs et al. (2004) suggested
that the looser connection may allow a higher sensitivity to vibrations of the bullae,
leading to the suggestion that this part of the inner ear is the key to US detection
in Alosinae. Further, single-unit recordings of US-sensitive neurons were made in
regions of the brain typically associated with the auditory system (Plachta et al.,
2004). Many of the ultrasonically sensitive neurons did not respond to sonic
stimulation, which suggests that the Alosinae have a specialized processing path-
way for US detection (Plachta et al., 2004). However, the hypothesis that the utricle
mediates US detection has not been verified experimentally.
2.3.5 The Lateral Line as the US Detector
A recent experiment conducted on Brevoortia patronus revealed that the gas-filled
bullae and lateral line may be involved in US detection in Alosinae (Wilson et al.,
2009). Using a laser vibrometer, the authors showed that the gas-filled bulla
oscillates when placed in an ultrasonic sound field. They showed that the neural
response recorded as evoked potentials to US disappears when gas in the bullae was
replaced with a Ringer solution, suggesting that the gas-filled bullae are the
transducing element in US detection. Further, mechanical manipulation of a part
of the lateral line overlying the lateral recess eliminated the ability of Brevoortia
patronus to detect US, but did not affect detection of a 600 Hz low-frequency tone.
This study showed that the lateral line is somehow involved in US detection, either
via the response of sensory cells to US or via its role as a mechanical connection to
the inner ear. These results add a new and surprising dimension to the role of the
lateral line and the bullae in Brevoortia patronus, as the lateral line of fish
previously has been believed to detect only low-frequency hydrodynamic stimuli
(<100 Hz). Future studies on US detection in Alosinae should focus on neuroanat-
omy and neural recordings from the lateral line and inner ear to elucidate details of
the mechanism of US detection.
P.M. Narins et al.
2.4 The Evolution of US Detection
Although it is generally accepted that heavy predation pressure from bats on
nocturnal insects has led to the evolution of ultrasonic sensitive ears in several
species of moths (Miller & Surlykke, 2001), it is less certain what has driven
the evolution of US sensitivity in Alosinae. It seems reasonable to assume that
the ability to detect US arose in the Alosinae in response to predation by
echolocating cetaceans. However, why has it not also arisen in other clupeid fishes
that share an evolutionary origin and many of the same specialized ear and lateral
line structures?
The Clupeiformes are an ancient lineage and fossils are known from the Lower
Cretaceous period (130 million years ago), a long time before the evolution of
odontocete cetaceans in the Oligocene (25–38 million years ago). All Clupeiformes
share the auditory bullae specializations of the inner ear. So, it is clear that
the specialized bullae evolved before the presence of echolocating cetaceans.
Because the ability to detect US has been found only in the Alosinae, and not in
the closely related Clupeinae, the question becomes: When did the Alosinae
evolve? Based on hypothesized phylogeny for Alosinae it was around the same
time as the evolution of the echolocating river dolphins (Hamilton et al., 2001;
Lavoue
´et al., 2007) (Fig. 6).
Fig. 6 Hypothesized phylogeny of the suborder Clupeiodei (A). (Modified from Whitehead et al.,
1985). Y ¼number of species with positive responses to US; N, number of species tested that
failed to respond to US
Ultrasound Detection in Fishes and Frogs
It is therefore tempting to envision that US detection arose in the Alosinae in
response to predation from echolocating river dolphins. This hypothesis is based on
the following line of reasoning:
• Most of the species in the Alosinae are found in freshwater for all of their lives
(e.g., Gadusia spp.) or during the freshwater phase of anadromous reproduction
(e.g., Alosa spp.). A few species, such as the menhaden (Brevoortia spp.), can
live their entire lives in the marine environment, although juveniles have been
found in rivers.
• The Alosinae are likely to be the most recently derived subfamily of the
Clupeidae (Lavoue
´et al., 2007). Given that US detection has been found in
every member of this subfamily that has been tested, it is possible that the ability
to detect US evolved only once.
• The Platanistidae, river dolphins, are among the oldest lineages of echolocating
odontocetes and are thought to have evolved in the early Miocene, about
23 million years ago (Hamilton et al., 2001). The extant members of the
Platanistidae are found in the Indus and Ganges River systems, which are also
regions of high diversity of Alosinae fishes.
• Rivers are confined areas, and river dolphins could thus present a much greater
selection pressure than odontocete cetaceans in the open ocean, where fishes
have many more predators that do not echolocate.
3 Ultrasonic Communication in Frogs
3.1 Historical Overview of the Discovery
of Ultra-high-Frequency Sensitivity of Frogs
Whereas the ability of fish to detect US was discovered by observations of
the behavioral responses of migrating American Shad (Alosa sapidissima)to
ensonification by ultrasonic sonar (Section 2.1), this same capability in frogs was
revealed in a completely different manner. It had been known that only two Old
World frog species (out of more than 6000 anuran amphibians) possess tympanic
membranes that are recessed from the head surface and form the terminus of a
chamber or a tube (ear canal) much like the human outer ear: Huia (Inger, 1966)
and Amolops (Zhou & Adler, 1993). It was this unusual ear morphology that
sparked a field study to record the vocalizations of Amolops tormotus [now
Odorrana tormota (Frost et al., 2006)] in the animals’ riverine habitat in Anhui
Province, China. Initial analysis of those vocalizations revealed an extremely high
degree of call diversity (Feng et al., 2002), with a call repertoire larger than that of
the Madagascar Rhacorphorid frog, Boophis madagascariensis, males of which
produce 28 different call types, more than any other frog known at the time (Narins
et al., 2000). In addition, although the vocalizations appeared to contain multiple
P.M. Narins et al.
Fig. 7 Sound spectrograms (top section in each panel), waveforms (bottom section in each panel),
and instantaneous amplitude spectra [insets taken at indicated points in time (arrowheads)] of
vocal signals of the frog, Odorrana tormota, in Huangshan Hot Springs, China. (a) Long call, and
(b, c) two short calls showing significant energy in the ultrasonic range and a spectral notch in the
range 32–45 kHz. For all plots, dynamic range: 90 dB; temperature range during recordings:
17–18C. (Permission has been obtained from JASA to reproduce this figure.)
Ultrasound Detection in Fishes and Frogs
examples of unusually high-frequency call components, frequency response
limitations of the recording equipment precluded definitive identification of ultra-
sonic call components at that time. Subsequent workers, armed with ultrasonic
recording gear, were able to establish unambiguously the existence of clear ultra-
sonic components in Odorrana vocalizations as high as 128 kHz (Narins et al.,
2004) (Fig. 7).
Acoustic playback experiments in the animal’s natural habitat revealed that
calling males in the field would vigorously respond to playbacks of (a) their
complete advertisement calls, (b) a high-pass filtered version of their advertisement
call containing only ultrasonic call components, or (c) a low-pass filtered version
of the complete advertisement call containing only audible (to humans) call
components. These results, combined with auditory evoked potential (AEP) and
single-unit recordings from the torus semicircularis (the amphibian homolog of the
mammalian inferior colliculus in the midbrain) of anesthetized males of O. tormota,
demonstrated the existence of both overall midbrain sensitivity to US as well as the
existence of single cells in the inferior colliculus of males of O. tormota that
reliably and repeatedly increased their spike rate to ultrasonic stimuli (Feng et al.,
2006; Narins et al., 2007b). Moreover, the thickness of the tympanic membrane in
males of this species is about 3–4 μm, which is about an order of magnitude thinner
than that of the American bullfrog, Rana catesbeiana. This observation, coupled
with the fact that the eardrum is recessed, resulting in a shorter, less massive
ossicular chain, are now both viewed as adaptations favoring high-frequency
sensitivity (Feng et al., 2006; Narins & Feng, 2007; Narins et al.,2007b).
In a parallel electrophysiological study, males of the sympatric species, Odorrana
livida (now Odorrana graminea), also exhibited responses to US, although with an
upper limit of sensitivity of 22 kHz, whereas males of the dark-spotted frog
Pelophylax nigromaculata living in rice paddies were quite insensitive to frequencies
above 4 kHz (Feng et al., 2006).
Subsequent field and lab studies of the Bornean hole-in-the-head frog,
Huia cavitympanum, revealed that in addition to its recessed tympanic membranes,
these animals produce vocalizations containing fundamental frequencies that can
exceed the nominal upper limit of human hearing: 20 kHz (Arch et al., 2008,2009).
In other words, Huia cavitympanum represents the first known example of a
nonmammalian vertebrate that produces a call with frequencies restricted entirely
to the ultrasonic range.
3.2 Evolutionary and Environmental Constraints
and Selection Pressures on Ultrasonic Signaling
Measurements of the noise energy produced by rushing water in the Tau Hua Creek
in Anhui Province, PRC, revealed a high-intensity, broadband sound, with dominant
energy in the low frequencies (<5 kHz) and falling off with frequency. Thus, any
P.M. Narins et al.
frog attempting to communicate acoustically in this environment would gain an
advantage by calling using frequencies above 5 kHz. Observations that the torrent
frogs O. tormota and O. graminea are sensitive to US, whereas the P. nigromaculata
that live in relatively quiet rice paddies are not, gave rise to the idea that these species
have increased both their call frequencies and their upper limit of hearing as an
evolutionary response to the broadband, principally low-frequency ambient noise
(Feng et al., 2006; Gridi-Papp & Narins, 2009). A similar observation was reported
for urban populations of Great tits (Parus major), which have higher (although not
ultrasonic) minimum frequencies in their calls compared to rural populations of the
same bird (Slabbekoorn & Peet, 2003). The shifting of echolocation call frequencies
by big brown bats (Eptesicus fuscus) to avoid noisy echoes in cluttered environments
has also been recently reported (Hiryu et al., 2010).
O. tormota exhibits another novel middle ear mechanism that is, so far, unique to
this species of frog. Whereas most frogs are believed to have large, permanently
open Eustachian tubes (ETs) connecting the mouth cavity to the middle ear (Chung
et al., 1981; Jaslow et al., 1988; Jorgensen, 1991), O. tormota can actively close its
ETs, drastically reducing the volume of air behind the tympanic membranes (TMs;
Gridi-Papp et al., 2008). This volume reduction increases the TM stiffness and
hence the ear’s impedance and shifts the middle ear tuning toward high frequencies.
The result is an improvement in the ear’s sensitivity to high-frequency (including
ultrasonic) signals at the expense of low-frequency sensitivity (Gridi-Papp et al.,
2008). This remarkable mechanism is not present in Rana pipiens, a frog with
advertisement call frequencies confined to <4 kHz (Hall & Feng, 1988), suggesting
that it indeed functions as an adaptation for enhancing high-frequency communica-
tion (Gridi-Papp et al., 2008).
3.3 Case Studies
3.3.1 Odorrana tormota (formerly Rana tormota and Amolops tormotus)
This species has been the most extensively studied of all ultrasonically communi-
cating amphibians to date. It is an arboreal frog in the family Ranidae restricted in
its distribution to Anhui and Zhejiang provinces in central China (Fei et al., 2010).
Males of this species call nightly from the low vegetation along the banks of rivers
and streams (Narins et al., 2004). Video recordings of vocalizing males in their
natural habitat revealed that two pairs of vocal sacs are inflated during calling: a
lateral pair and a subgular pair (Narins, personal observation). The inflation
dynamics for these two pairs of sacs are not known, nor are the delays (if any)
between inflations of the two pairs of vocal sacs. Given the extremely wide variety
of call notes produced by males of O. tormota (Feng et al., 2002; Feng & Narins,
2008), and the nearly ubiquitous presence of nonlinear call features and motifs in
this species’ calls (Narins et al., 2004; Suthers et al., 2006), we predict that the vocal
sac inflation system may exhibit some unusual features worth investigation.
Ultrasound Detection in Fishes and Frogs
Given the high-frequency call components, it follows that sound localization by
O. tormota should be highly developed. This is in fact the case—males are able to
locate the source of a sound to within 0.7, rivaling the accuracy of the vertebrates
with the highest localization acuity (Shen et al., 2008). In addition, males are able to
discriminate individuals by their calls (Feng et al., 2009a) or distinguish neighbors
from strangers (Feng et al., 2009b). Moreover, the deeply recessed eardrum is found
only in males of O. tormota; females exhibit eardrums only slightly recessed from
the head surface. Using acoustic playback experiments, AEP recordings from the
midbrain, and laser measurements of the TM, Shen and his colleagues recently
demonstrated that females of O. tormota are insensitive to US; the ultrasonic realm
is therefore reserved for males of this species (Shen et al., 2011b).
3.3.2 Odorrana graminea (formerly Odorrana livida)
O. graminea is a rather common species in the Tau Hua Creek; it is significantly
larger than the sympatric and congeneric O. tormota (mean SVL male O. tormota:
34 mm, female: 60 mm; mean SVL male O. graminea: 48 mm, female: 91 mm).
Electrophysiological experiments have shown that males of this species are sensi-
tive to tones as high as 22 kHz (Feng et al., 2006). Moreover, broadband recordings
of their calls have only recently revealed that the short tonal calls contain
frequencies up to 44.1 kHz (Shen et al., 2011a). In summary, males of this species
produce ultrasonic vocalizations, they are sensitive to ultrasonic signals (up to
22 kHz), and yet they do not possess a deeply recessed tympanic membrane.
The piebald odorous frog, Odorrana schmackeri, is another sympatric, congeneric
torrent frog that also inhabits the Tau Hua Creek. It too has nonrecessed tympanic
membranes but its auditory sensitivity measured with AEP recordings from the
inferior colliculus in the midbrain suggests a high-frequency detection limit of 8.5
kHz, well below US (Yu et al., 2006). Thus, although this species is sympatric with
O. tormota and O. graminea, its calls contain no US components. It appears that there
are many and varied responses to high levels of background noise, and future studies
will undoubtedly bring many more of these responses to light (Arch & Narins, 2008).
3.3.3 Huia cavitympanum
Of the more than 6000 known species of anuran amphibians, there are only two frog
species with recessed tympana: Odorrana tormota from China and Huia
cavitympanum from Borneo (Amphibia Web: http://amphibiaweb.org/, Inger,
1966). In 2007, an expedition was launched to Gunung Mulu National Park in
Sarawak, Malaysian Borneo for the purpose of (1) finding calling males of
H. cavitympanum, (2) recording their vocalizations in situ, (3) obtaining high-
quality recordings of the ambient noise in which calling males were found, and
(4) initiating the process of capturing and transporting live animals back to the
Unites States for physiological studies. During this first expedition, vocalizations
P.M. Narins et al.
were recorded from 10 males of H. cavitympanum. In addition to possessing the
recessed tympanic membranes, these animals are capable of producing two classes
of vocalizations: (1) those with fundamental frequencies below the nominal upper
limit of human hearing (20 kHz), and are therefore audible to humans, and (2) those
with fundamental frequencies that exceed the nominal upper limit of human hearing
(Arch et al., 2008,2009). This species represents the first known example of a
nonmammalian vertebrate that can produce calls with frequencies restricted
entirely to the ultrasonic range. Acoustic playback experiments in this animal’s
natural habitat showed that vocalizing males change their calling pattern in
response to playback of purely ultrasonic signals (Arch et al., 2009), and AEP
recordings from the midbrain show robust responses to tones of frequencies as high
as 39 kHz, with peak sensitivity above 20 kHz, making this amphibian an ultrasonic
specialist (Arch et al., 2009).
3.4 Mechanism of US Detection in Frogs—Still Unknown
In a study of the concave-eared torrent frog Odorrana tormota, the neural activity
patterns in the auditory brain stem were examined in response to a full-spectrum
conspecific call, a filtered US-only call, and a control (no sound) stimulus generated
by playing back a 30-minute file that does not contain any sound (Arch et al., 2011).
To gain insight into the structures responsible for US sensitivity in the frog’s brain,
brain neural activity was determined by measuring the expression of the immediate
Fig. 8 Schematic diagram of the frog ear. The amphibian papilla and the basilar papilla are the
two inner ear organs in the frog that are specialized for detecting airborne sounds. In some frogs,
the middle ear and the basilar papilla have undergone a series of morphological changes that
facilitate detection of high-frequency sound (see text). (Adapted from Wever, 1973.)
Ultrasound Detection in Fishes and Frogs
early gene, egr-1.Egr-1 expression was measured in the superior olivary nucleus
(SON) in the hindbrain, which is a major source of afferents for the torus
semicircularis (TS) in the midbrain, and in the principal (Ptor) and laminar (Ltor)
nuclei of the TS. US-only calls elicited robust expression of egr-1 in the SON and
Ptor. Moreover, in the Ptor, egr-1 expression was greater in response to US-only
calls than to the full-spectrum calls, suggesting a pivotal role for this nucleus in US
detection in this species (Arch et al., 2011).
Anurans are unique among vertebrates in that their auditory periphery contains
two distinct auditory organs (Fig. 8), the amphibian papilla (AP) and basilar papilla
(BP) (Wever, 1973; Capranica, 1976; Lewis & Narins, 1999). In the American
bullfrog, Rana catesbeiana, the BP contains 50–90 hair cells, whereas the AP
contains roughly 10 times this number (Geisler et al., 1964; Lewis et al., 1982a).
The AP responds to low and middle frequencies and is tonotopically organized,
with low-frequency-sensitive hair cells located rostrally and mid-frequency
cells located caudally (Lewis et al., 1982a,b). The BP is a simpler organ that acts
as a mechanical resonator that responds to a restricted band of higher frequencies
(Feng et al., 1975; Ronken, 1990; van Dijk et al., 2011). The BPs of Rana
catesbeiana and its close relative Rana pipiens can detect sounds up to 2 and
4 kHz, respectively—frequencies near the upper frequencies in the species-specific
advertisement calls (Capranica, 1976).
The sensory epithelium of the basilar papilla is found at the base of a tubular
outpocket of the sacculus, an inner ear organ primarily responsible for detecting
substrate vibrations (Narins, 1990; Yu et al., 1991). The BP outpocket is terminated
by its contact membrane, which is tuned to the species’ BP frequency (Purgue &
Narins, 2000a,b). In addition, a tectorial membrane spans the lumen of the BP
recess, covering the sensory hair cells that are embedded in the cartilaginous wall of
this recess (Wever, 1985). Optical measurements of the mechanical response of the
BP tectorial membrane in R. pipiens have revealed that it is tuned to a frequency
of approximately 2 kHz, corresponding closely to the characteristic frequencies of
the species’ BP nerve fibers (Schoffelen et al., 2009). Thus, both BP membranes
are tuned to the frequency of the organ, consistent with the idea that the BP acts as a
mechanical resonator (Feng et al., 1975; Ronken, 1990; van Dijk et al., 2011).
In a recent comparative study, basilar papilla morphologies of six frog species,
three known to detect US (O. tormota,O. livida, and Huia cavitympanum), two
relatively unstudied frog species from Laos (O. chloronota and Amolops daorum),
and one non-US communicator (R. pipiens), were compared (Arch et al., 2012). In
this study, immunohistochemistry and confocal microscopy were used to examine
several anatomical features of the basilar papillae of the inner ears, including the
recess entrance area (REA), epithelium surface area (ESA), number of hair cells or
hair cell count (HCC), hair cell soma length (SL), and bundle height (BH). The
REA, ESA, and HCC values for all ultrasonic species (US) tested were significantly
smaller than those for R. pipiens. Moreover, the three US-detecting frogs had values
for these metrics that were statistically indistinguishable from one another and from
A. chloronota (Arch et al., 2012). These data also reveal that H. cavitympanum,
O. tormota,O. livida, and O. chloronota have significantly smaller BP organs and
P.M. Narins et al.
sensory epithelia than those of R. pipiens and A. daorum. In addition, basilar papilla
SL, BL, and BH values from the US-sensitive frogs and O. chloronota were not
significantly different and their SL values were significantly smaller than those of
R. pipiens and A. daorum. Together, these BP morphological data suggest that
O. chloronota from northeastern Laos be considered a putative US detector, and
that future physiological studies of the mechanisms underlying US detection should
include this species along with the three known US detectors.
4 Summary and Outlook: Comparative Insights
from the Study of High-Frequency Hearing
in Fishes and Frogs
The evolutions of US detection in fishes and frogs are clearly independent events
with different ecological drivers. These comparative evolutionary stories provide
some guide as to where to look for surprises in hearing and communication in fishes
and frogs. Frogs with ultrasonic hearing live in unusual environments with high
levels of low-frequency noise and also produce sounds at very high frequencies.
Thus, communication appears to have been the primary selective force for high-
frequency hearing in some frogs (Narins et al., 2007a). No fishes are known to
communicate with ultrasonic signals, but it could be interesting to study acoustic
communication in fishes with good hearing sensitivity that live in areas of high
background noise (see also the chapter by Ladich, this volume). US detection by the
Alosinae fishes appears to have resulted from selective pressure from echolocating
cetaceans. Some frogs fall prey to echolocating bats, and thus it would be interest-
ing to determine whether they, also, are capable of detecting echolocation signals to
avoid bat predation. Likewise, it would be interesting to learn if any of the
US-sensing frogs are able to use the ultrasonic components of insect stridulation
sounds to locate their prey.
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