Development of ultrasound detection in American shad (Alosa sapidissima)
1 Department of Biology, University of Windsor, Windsor, Ontario, N9B 3P4
Canada
2 Institut für Biologie II, RWTH Aachen, Germany
3 Department of Biology and Neuroscience and Cognitive Science Program,
University of Maryland, College Park, MD 20742, USA
4 Office of Naval Research, Arlington, VA 22217, USA
* Author for correspondence (e-mail: dhiggs{at}uwindsor.ca)
Accepted 30 September 2003
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Summary |
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Key words: ultrasound detection, bullae, utricle, American shad, Alosa sapidissima
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Introduction |
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While the mechanism used for high-frequency detection is understood in most
species that can detect frequencies higher than 1.5 kHz [e.g. the Weberian
ossicles of the Cyprinidae (von Frisch,
1938; Fay and Popper,
1974
) or the accessory air sac of the Mormyridae
(von Frisch, 1938
;
Yan and Curtsinger, 2000
;
Fletcher and Crawford, 2001
)],
the mechanistic basis for ultrasonic detection in clupeiform fishes remains
unclear. As in other teleosts, there are three auditory end organs in the
inner ear of clupeiform fish: the utricle, saccule and lagena. Fishes in the
order Clupeiformes, however, have a modified inner ear in which the utricular
epithelium is divided into anterior, middle and posterior maculae
(Tracy, 1920
;
O'Connell, 1955
;
Best and Gray, 1980
), as
opposed to the single utricular epithelium found in all other vertebrates
(e.g. Platt, 1984
). The
clupeiform ear is surrounded by one (in sprat, Sprattus sprattus) or
two (in most other clupeiformes) gas-filled bubbles, called the prootic and
pterotic bullae, which are themselves connected to the swim bladder
via a thin tube (O'Connell,
1955
; Allen et al.,
1976
; Blaxter and Hunter,
1982
). The prootic bulla is connected directly to the middle
utricular epithelium by a thin `elastic thread'
(Best and Gray, 1980
). Fluid
motion through the fenestra (a narrow opening at the bullautricle
interface) also physically couples the bulla and the middle utricular
epithelium. Pressure waves impinging upon a clupeiform fish cause the swim
bladder and auditory bullae to vibrate
(Denton and Blaxter, 1979
).
Vibrations of the bullae may induce movements of the middle utricular
epithelium (Denton and Gray,
1979
; Best and Gray,
1980
), thus forming an indirect pathway transferring pressure
information detected by the swim bladder or bullae to displacement information
detected by the inner ear. The indirect pathway allows the ear to respond to
higher frequencies than would be possible without this pathway
(Blaxter and Hoss, 1981
).
It was first hypothesized (Mann et al.,
1998) that the prootic bulla was responsible for ultrasound
detection in Clupeiformes via the indirect pathway described above.
While the bulla may be involved in ultrasound detection, it is now clear that
it is not solely responsible because, while all Clupeiformes have prootic
bullae connected to a tripartite utricle
(Blaxter and Hunter, 1982
), not
all of these species detect ultrasound
(Mann et al., 2001
). Thus,
there clearly must be an additional specialization in those clupeoids that
have been shown to detect ultrasonic frequencies.
One powerful technique for assessing the functional basis of auditory
abilities has been to examine the development of structural and functional
attributes together. In mammals and birds, development of the middle ear bones
coincides with an expansion of detectable frequencies
(Ehret and Romand, 1981;
Saunders et al., 1986
;
Geal-Dor et al., 1993
).
Similarly, zebrafish (Danio rerio; Cypriniformes) show an increase in
maximum detectable frequency coincident with development of the Weberian
ossicles (Higgs et al., 2003
).
Atlantic herring (Clupea harengus; Clupeiformes) larvae show a steep
increase in behavioural responsiveness to an acoustic stimulus coincident with
bulla inflation (Blaxter and Batty,
1985
) and also an increase in responsiveness to predatory attack
as the bulla fills (Fuiman,
1989
; Blaxter and Fuiman,
1990
). Interestingly, there is no change in behavioural
responsiveness coincident with bulla inflation in Atlantic menhaden
(Brevoortia tyrannus; Clupeiformes) and bay anchovy (Anchoa
mitchilli; Clupeiformes) when using a mechanical stimulus (Higgs and
Fuiman, 1996
,
1998
), suggesting that changes
seen in clupeoid predator studies were due to detection of auditory
(pressure), rather than mechanosensory (displacement), information.
The purpose of the current study was to investigate the development of hearing and auditory morphology in the American shad, particularly with regard to the onset of ultrasound detection. We used a combination of behavioural, physiological and morphological techniques to show how the onset of ultrasound detection coincides with the development of apparent specializations in the utricle of American shad. We also compare the utricle of adult shad with the utricle in three other clupeoid species, one that can detect ultrasound and two that cannot, to show that the observed utricular specialization may be restricted to ultrasound-detecting species.
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Materials and methods |
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Behaviour
Fish were filmed approximately once per week from 2 July to 3 September
2002 (Table 1). All fish in the
tank were exposed to the sound, but only those fish that were in the field of
view at stimulus onset were recorded and used for data analysis. Thus, there
is no way of knowing if fish were tested more than once, but, due to the
apparently random distribution of fish in the tank, we do not feel this biased
our results. Fish were recorded for approximately 3 s before sound
presentation, 3 s during sound presentation and 3 s after sound was stopped.
Images were recorded through a digital video camera (512 pixelsx492
pixels, 30 frames s1; Sanyo Corp., San Diego, CA, USA)
connected to a frame grabber (Pinnacle DC 10+) using MGI Videoware software on
a PC. Video files were compressed with VirtualDub software (1:50, Intel Indeo
5.1® Codec) to reduce file size. Response was scored as positive if fish
made an obvious C-start (Eaton et al.,
1977) at the onset of sound presentation. A response was labelled
a C-start if the flexion was faster than one video frame (33.3 ms). As the
C-start is a fixed action pattern initiated by Mauthner cells
(Eaton et al., 1977
), the
degree of body flexion does not change developmentally
(Kimmel et al., 1974
;
Taylor and McPhail, 1985
;
Eaton and DiDomenico, 1986
),
providing an objective measure for the onset of startle responses. The
proportion of fish responding in each experiment was recorded. To obtain the
daily mean size of fish in the tank for each set of experiments, all fish in
the field of view were measured before the first experiment of the day
commenced.
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Auditory brainstem response (ABR) recording
Due to the extreme fragility of American shad larvae, we were not able to
obtain auditory brainstem recordings (ABRs) from any animals smaller than 30
mm TL. Thus, we cannot ascertain when ABR first occurs in response to
ultrasound. We were able to determine, however, how the response changes with
later development. Following the protocols of Higgs et al.
(2002a,
2003
), fish were held in place
with a small piece of netting wrapped around the trunk. A tube with flowing
water was placed into the fish's mouth to hold the head stable and to irrigate
the gills. This arrangement held the fish securely in place so no muscle
relaxants or anaesthetics were necessary. Fish were lowered underwater so that
the top of the head was at least 5 cm under the water surface. Tone bursts of
frequency 0.1 kHz, 0.2 kHz, 0.4 kHz, 0.6 kHz, 0.8 kHz, 1 kHz, 2 kHz and 4 kHz
were presented via a UW-30 (University Sound Inc., Buchanan, MI, USA)
underwater speaker placed 25 cm below the fish. Tone bursts of 40 kHz, 60 kHz,
80 kHz and 90 kHz were presented via an ITC-1042 underwater
transducer. All tone bursts had a 10 ms duration and were gated through a
Hanning window with a 2 ms rise/fall time. Tone bursts were presented at
alternating starting phases of 90° and 270° to cancel stimulus
artifacts in the response recordings. The speakers were connected to a
McIntosh amplifier, which was in turn connected to a Tucker-Davis Technologies
(TDT, Alachula, FL, USA) physiology apparatus. Tone bursts were generated
using TDT SigGen software and played from the computer through the TDT system.
Output levels were calibrated with a precalibrated hydrophone (InterOcean
Systems, San Diego, CA, USA) for sonic frequencies and an LC-10 hydrophone for
ultrasonic frequencies.
Recording of auditory responses was also accomplished through the TDT
system, running TDT BioSig software and a 50 ms recording duration. A
recording electrode was placed just under the skin of the fish, along the
midline just dorsal to the opercular edge. A reference electrode was placed
under the skin along the midline, posterior to the eyes. A ground electrode
was placed in the water near the body of the fish. All electrodes (Rochester
Electromedical Inc., Tampa, FL, USA) had stainless steel tips coated with
fingernail polish as insulation, with the tip of the electrode remaining
uninsulated. The remainder of the electrode was covered in waterproof
insulation so recording underwater was not a problem. Electrode leads were
connected to a TDT HS4 head stage, which was integrated into the rest of the
physiological apparatus. Responses to stimulation were sent through a 60 Hz
notch filter to reduce electrical artifact. For each frequency and intensity,
400 responses were averaged together. Threshold responses were defined for
each frequency as the sound level at which stereotypical ABR responses were
first observed (see Fig. 2A).
This visual inspection method is common in ABR studies across vertebrates
(Walsh et al., 1986;
Hall, 1992
) and gives
comparable results to more statistical approaches
(Mann et al., 2001
;
Brittan-Powell et al., 2002
).
For statistical comparison of threshold over development, fish were lumped
into one of four size classes; 3039 mm TL (N=6),
4055 mm TL (N=3), 7590 mm TL
(N=10) and >100 mm TL (N=2). No fish were tested
more than once. Thresholds were compared across size classes with two-way
analysis of variance (ANOVA; Zar,
1984
). Because of a change in calibration procedures in our
laboratory, care must be taken when comparing current thresholds with those in
our previous work (Mann et al.,
1997
,
1998
,
2001
). The current technique
results in thresholds approximately 2030 dB re 1 µPa lower than our
previous reports. While we feel our new calibration technique may be more
accurate (Higgs et al.,
2002b
), it does not change the conclusions of our previous work,
just the threshold numbers.
|
Morphology
For the first 100 days posthatch (100 dph; mean TL=32 mm),
45 larvae were removed from the tank every 47 days. Animals were
anaesthetized with MS-222 (tricaine methanesulfonate; Sigma) and immediately
examined under a dissecting microscope. TL was measured and the
inflation of the auditory bulla (visible as a silver bubble when inflated) and
the number and position of otoliths present were recorded. Both bulla
inflation and otolith number were easily visible through the skin of larvae
until at least 20 mm TL. After recording external development, larvae
were killed with an overdose of MS-222 and immediately placed into 4%
paraformaldehyde until sectioned.
After at least 24 h of fixation, animals were embedded in Immunobed (Polysciences Corp., Warrington, PA, USA) plastic resin and sectioned at 10 µm. For all size classes, sections were made in both sagittal and frontal planes. Sections were mounted on slides, dried for at least 24 h on a 40°C slide warmer, cleared, stained with cresyl violet and coverslipped with Permount (Sigma). Sections were examined and the state of utricular development was recorded. Images were captured with a digital camera (Magnafire, Optronics Inc., Goleta, CA, USA) directly connected to the microscope.
For comparative purposes, the utricles of at least three adults of American shad, gulf menhaden (Brevoortia patronus; Clupeiformes), bay anchovy and scaled sardine (Harengula jaguana; Clupeiformes) were fixed in 4% paraformaldehyde, embedded and sectioned in Immunobed and mounted onto slides. Menhaden and scaled sardine were collected from the field at Mote Marine Laboratory (Sarasota, FL, USA), and bay anchovies were collected from the field in Chesapeake Bay, MD, USA. Field-collected animals were immediately killed in MS-222 and fixed in 4% paraformaldehyde. American shad adults were obtained from our lab stock.
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Results |
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Physiology
By 30 mm TL, the smallest size that we were able to test with ABR,
all fish responded behaviourally to 90 kHz. We also found that all fish 30
mm TL responded to ultrasound at the level of ABR
(Fig. 2B). There was no
significant difference in auditory threshold (P=0.5, N=21
for size class main effect) for fish from 30 mm to >100 mm TL. In
the 3039 mm size class, all fish responded to tone bursts from 0.1 kHz
to 90 kHz. From 0.1 kHz to 4 kHz, the threshold was in the range of
101122 dB re 1 µPa, while in the ultrasonic frequencies,
(4090 kHz) threshold for 3039 mm fish was in the range of
112145 dB re 1 µPa. This was similar to the values for the larger
fish (>75 mm TL), who had a range of sonic (0.14 kHz)
thresholds of 92115 dB re 1 µPa and ultrasonic thresholds of
102135 dB re 1 µPa (Fig.
2B).
Auditory structure
In adult American shad, the prootic bulla sits directly in front of the
utricle (Fig. 4A). The bulla is
subdivided into a gas-filled and a fluid-filled portion by a flexible bulla
membrane (Fig. 4B,C). The bulla
membrane is directly connected to the anterior portion of the middle macula of
the utricle by an `elastic thread' (sensu
Denton and Gray, 1979;
Fig. 4B,C). The utricular
middle macula in adults is suspended from the rest of the utricle by a thin
connection approximately one cell layer thick
(Fig. 4B,C,G).
|
The utricular epithelium of newly hatched shad larvae is continuous, with no division into anterior, posterior and middle maculae, a situation that continued until at least 12.5 mm TL (Fig. 4D). By 16 mm TL, the utricle first shows division into a tripartite structure (Fig. 4E). At 16 mm TL, the three portions of the utricular maculae could be differentiated from one another but the three components were still well connected (Fig. 4E). The connection between the middle macula and the rest of the ear continued to thin so that by 26 mm TL the middle macula was connected to the anterior and posterior portions of the utricle by a sheet of cells approximately one cell layer thick (Fig. 4F) and looked similar to the utricular suspension seen in adults (Fig. 4G).
Shad larvae hatch with no evidence of an auditory bulla and never show
bulla inflation up to 11 mm TL
(Fig. 5). By 12 mm TL,
the prootic bulla begins to inflate and at 13 mm, all larvae examined had
inflated prootic bullae (Fig.
5).
|
At hatching, shad larvae have two otoliths in each ear, the lapillus and
sagitta, which overlay the utricular and saccular epithelia, respectively
(Fig. 5). There is no sign of
an asteriscus (lagenar otolith) until 15 mm, at which point 30% of the
larvae examined had asteriscus (Fig.
5). By 18 mm, all larvae had asteriscus
(Fig. 5) overlying a small
lagenar epithelium.
On a comparative level, the utricle of adult American shad is similar to that of gulf menhaden but different from those of bay anchovy or scaled sardine (Fig. 6). The middle macula of both shad and menhaden is very loosely attached to the rest of the utricle, connected only by tissue approximately one cell layer thick (Fig. 6A,B). By contrast, both anchovy and sardine middle maculae have a firmer base of attachment to the rest of the utricle (Fig. 6C,D) and resemble the situation seen in shad larvae (Fig. 4E) more than in adult shad (Fig. 6A).
|
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Discussion |
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It has been previously hypothesized (Mann et al.,
1998,
2001
;
Astrup, 1999
) that the response
of American shad to ultrasonic frequencies is an adaptation for avoiding
predation by echolocating odontocetes. The current results add some support to
this hypothesis, although the role of odontocete clicks in shad escape
behaviour has yet to be explicitly tested. Pacific herring (Clupea
pallasi) show evasive responses to a simulated echolocation click
(Wilson and Dill, 2002
),
although due to the broadband nature of the stimulus used it is not clear
whether or not they respond to ultrasonic frequencies. While there are
species- and habitat-specific differences in frequencies used in echolocation
signals, many odontocetes emit echolocation clicks with a peak frequency of
90100 kHz (Au, 2000
). It
may be this component of echolocation signals that has driven the evolution of
shad ultrasound detection, although more experiments must be conducted before
this can be determined.
Once developing shad could detect sounds, their sensitivity to these sounds
as measured by ABR did not change developmentally. There have been only a few
studies on the development of auditory sensitivity in fish, with the results
varying between species. In rays (Raja clavata;
Corwin, 1983) and damselfish
(Pomacentrus partitus; Kenyon,
1996
), auditory sensitivity (as measured by auditory nerve
recordings) improves (threshold decreases) with development, perhaps due to
increases in the number of sensory hair cells in the ear. In gouramis
(Trichopsis vittata; Wysocki and
Ladich, 2001
) and red sea bream (Pagrus major;
Iwashita et al., 1999
), small
changes in sensitivity are seen for some frequencies, although the changes are
not consistent developmentally. In goldfish (Carassius auratus;
Popper, 1971
) and zebrafish
(Higgs et al., 2002a
,
2003
), there is no change in
auditory sensitivity with development, even though there are significant
increases in hair cell number (Higgs et al.,
2002a
,
2003
).
We have previously hypothesized (Higgs
et al., 2003) that in those species possessing an indirect pathway
for pressure information to reach the ear, functional auditory development may
be more constrained by the conductive pathway of sound to the ear than by the
sensorineural pathway of hair cell addition. The results of the current study
lend support to this hypothesis. Once the bullae are filled in American shad,
there is no change in auditory sensitivity. In Atlantic herring, the pressure
sensitivity of bullar movements does not change once the bulla is filled
(Blaxter et al., 1981
), thus
delivering the same amount of stimulation to the utricular maculae for a given
pressure regardless of fish size. The same mechanism should also be working in
American shad. A given sound pressure should move the bulla the same amount,
regardless of fish size. If this is the mechanism of higher frequency sound
detection in shad, as has been shown for other Clupeiformes
(Blaxter and Hoss, 1981
), then
one should expect no change in auditory sensitivity with shad development once
the bullae are filled, as was shown by our ABR results.
Bulla inflation was complete by 14 mm, much before the size at which
animals responded to ultrasound (26 mm). This strongly suggests that an
inflated bulla is not sufficient itself for ultrasound detection. Also, other
clupeoid fishes with prootic bullae [bay anchovy, scaled sardine and Spanish
sardine (Sardinella aurita); Clupeiformes] do not detect ultrasound
(Mann et al., 2001) so the
presence of an inflated bulla is not sufficient for ultrasound detection. This
does not mean that the auditory bullae play no role in ultrasound detection.
Indeed, we suspect the bullae are an important part of the ultrasonic pathway
but the results do lead us to suggest that more than just an auditory bulla is
necessary to allow detection of ultrasonic frequencies.
While we did not expect the lagena to play a role in ultrasound detection, the frequency responses of the individual auditory end organs of fish are still too poorly understood to rule this out a priori. The shad lagenae first develop at 18 mm, but ultrasound detection did not begin until 26 mm. Thus, the lagena is not a limiting factor in ultrasound detection and it is doubtful that lagenar specializations play a role in this ability.
While still not definitive proof, development of utricular specializations
was coincident with the onset of behavioural responsiveness to 90 kHz
stimulation. The connection between the middle macula and the rest of the
utricle gradually thinned so that by 2635 mm the connection became as
thin as that seen in the adult. It was during this size range that
responsiveness to 90 kHz first began. Examination of this utricular
specialization in adults of other species in Clupeiformes lends further
support to this hypothesis. The two species (shad and menhaden) that have been
shown in previous studies to respond to ultrasound
(Mann et al., 2001) have a
very thin connection between the middle macula and the rest of the epithelium,
while those two species that are not responsive to ultrasound (bay anchovy and
scaled sardine) have a much more robust utricular suspension. Before the role
of the utricular suspension in shad ultrasound detection can be definitively
proven, single- or at least multi-unit recordings must be made from the
different utricular epithelia of clupeoid fishes. Despite this caveat, we
would argue that the correlation between utricular structure and response to
ultrasound is highly supportive of this hypothesis.
We posit the following hypothesis for ultrasound detection in American
shad. As sound waves impinge upon the air-filled bulla, the sound causes the
air-filled chambers to move. This results in vibration of the middle
epithelium due to the motion of the fluids in the chamber and the direct
connection to the bullar membrane via the elastic thread
(Denton and Gray 1979;
Denton et al., 1979
). While it
was previously thought that movement of the middle macula decreased rapidly
for frequencies greater than 1 kHz (Denton
et al., 1979
), recent data obtained using a noninvasive vibration
measurement technique originally developed by Rogers and Hastings
(1989
) show that movement of
the bulla, and therefore presumably of the middle macula, resumes at
frequencies above
40 kHz (M. C. Hastings, unpublished data). The looser
connection of the middle epithelium found in American shad and menhaden, as
compared with species that do not detect ultrasound, may allow higher
sensitivity to bullar vibrations due to its greater freedom of movement.
In effect, one can regard the connection between the middle epithelium and
the rest of the ear as a spring-like mechanism. Oscillations of the bullar
membrane would alternately pull the middle epithelium towards the auditory
bulla and then push it back toward the otolith via the elastic thread
connection and impinging oscillatory movement of the perilymph through the
fenestra at the bullautricle interface. The structure overlying the
epithelium should stay stable during these bullar vibrations, and the relative
movement between the otolith or cupula and the hair cell epithelium would
result in depolarizations of the hair cells. The extremely thin connection
between the middle epithelium and the rest of the utricle is essentially a
spring with miniscule mass that would require little energy to stretch, thus
making this epithelium more sensitive to vibrations at ultrasonic frequencies.
In essence, the system may resemble a very crude place-type mechanism, whereby
part or all of the middle epithelium in ultrasound-detecting Clupeiformes
responds to ultrasound due to possible changes in stiffness along its length
associated with the variations in thickness, just as part of the basilar
membrane responds to ultrasound in bats and dolphins
(Echteler et al., 1994). The
response of such a spring-controlled system would be `flat' over its frequency
bandwidth so that the sensitivity to ultrasound should be about the same at
all frequencies to which the bulla responds. Indeed, Mann et al.
(1997
,
2001
) demonstrated that
hearing sensitivity in ultrasound-detecting species is about the same from 40
kHz to >100 kHz. Our hypothesis leaves the enhanced sensitivity we found at
90 kHz unexplained (Mann et al.,
1997
,
2001
did not test 90 kHz tone
bursts), so finer scale analyses of bullar vibration need to be conducted to
determine if there is a bullar resonance around 90 kHz.
If our hypothesis for the mechanism of ultrasound detection is correct, one
can then suggest a relatively direct path to the evolution of ultrasound
detection. Many freshwater fishes show hearing specializations that are
thought to have arisen to enhance detection of higher frequencies in shallow
waters, where low frequencies propagate only very short distances
(Rogers and Cox, 1988). While
it is not known where clupeoid fishes arose, it is likely that they did evolve
in freshwater, and thus development of higher frequency hearing up to 4 kHz,
as found in all species in this group
(Mann et al., 2001
), may be
associated with hearing in shallow waters. Once these species invaded the
oceans and were subject to selective pressures imposed by echolocating
dolphins, some clupeoids may have evolved a simple change in the thickness of
the middle sensory epithelium in the utricle, thereby facilitating detection
of sounds at higher frequencies than in other related species. In effect, the
middle epithelium was `preadapted' for hearing higher and higher frequencies
needed for ultrasound detection.
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Acknowledgments |
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References |
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