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First published online May 2, 2008
Journal of Experimental Biology 211, 1681-1689 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016436
Size matters: diversity in swimbladders and Weberian ossicles affects hearing in catfishes
Department of Behavioural Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
* Author for correspondence (e-mail: friedrich.ladich{at}univie.ac.at)
Accepted 4 March 2008
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Key words: auditory evoked potential (AEP), Weberian apparatus, Siluriformes
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INTRODUCTION |
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;
Hawkins and Myrberg, 1983;
Hawkins, 1993;
Popper and Fay, 1993;
Ladich and Popper, 2004).
Otophysans, a group of hearing specialists comprising Cypriniformes,
Siluriformes, Characiformes and Gymnotiformes, possess the Weberian apparatus.
This consists of fused anterior vertebrae, known as `complex vertebra'
(Wright, 1884), and a paired
chain of one to four ossicles and ligaments joining the swimbladder to the
inner ear (Weber, 1820). The
Weberian apparatus facilitates sound transmission to the inner ear and
generally improves the hearing sensitivity of otophysines
(Ladich, 1999;
Ladich and Wysocki, 2003). The
catfish order, currently consisting of approximately 3100 species within 36
families (Ferraris, 2007),
exhibits a huge variability in the morphology of the Weberian ossicles and the
gasbladder. Numerous catfish families have large single, free swimbladders. On
the other hand, many groups have highly reduced, tiny and paired swimbladders
located to the left and right of the vertebral column, directly behind the
cranium. Additionally, these tiny bladders are surrounded by bony capsules
formed by the skull and anterior vertebrae. These conspicuous structures
prompted Bridge and Haddon (Bridge and
Haddon, 1889; Bridge and
Haddon, 1892; Bridge and
Haddon, 1893) to split catfish into two groups, the `siluridae
normales' with well-developed bladders and the `siluridae abnormales' with
reduced bladders.
Several investigators have described the structures of the Weberian
apparatus in numerous species of catfishes (e.g.
Sörensen, 1895;
Chranilov, 1929;
Alexander, 1964;
Alexander, 1965;
Mahajan, 1967;
Chardon, 1968;
Coburn and Grubach, 1998;
Chardon et al., 2003), but its
function was debated in the 1800s. While Weber
(Weber, 1820) originally
assumed that ossicles facilitate hearing, Bridge and Haddon
(Bridge and Haddon, 1889;
Bridge and Haddon, 1892;
Bridge and Haddon, 1893) denied
this contention, which was then contradicted by Sörensen
(Sörensen, 1895). The
effect of reduced and encapsulated swimbladders continued to be discussed
ambivalently. Chranilov (Chranilov,
1929) assumed that swimbladder encapsulation and its reduction in
size as well as reduction in the number of ossicles improves the sensitivity
due to free, moveable ossicles. Ladich and Bass
(Ladich and Bass, 2003)
expected reduced hearing because a reduction in size of the swimbladder walls
reduces the ability of the swimbladder to oscillate.
Studies on hearing in catfishes are rather sparse and have been carried out
in only a few members of a few families (for a review, see
Ladich and Bass, 2003). Most
studies have been conducted in ictalurids
(von Frisch, 1923;
von Frisch, 1936;
von Frisch, 1938;
Stetter, 1929;
Poggendorf, 1952;
Kleerekoper and Roggenkamp,
1959; Weiss et al.,
1969; Fay and Popper,
1975; Moeng and Popper,
1984; Plassmann,
1985) and a few in ariids
(Tavolga, 1977;
Popper and Tavolga, 1981;
Tavolga, 1982). More recently,
doradids, pimelodids and callichthyids
(Ladich, 1999;
Ladich, 2000) have been
investigated. Among all the species tested, only the callichthyid
Corydoras paleatus possesses tiny, paired and bony encapsulated
bladders and a single Weberian ossicle
(Coburn and Grubach, 1998).
This species had the lowest hearing ability, and Ladich
(Ladich, 1999) assumed that
this was due to the small relative size of its swimbladder.
The aim of this study was to demonstrate that the morphology of the Weberian apparatus (swimbladder size, size and number of Weberian ossicles) affects the hearing sensitivity in catfishes. Eleven species were chosen based on the size of their swimbladders. Six species belonging to the families Ariidae, Auchenipteridae, Heptapteridae, Malapteruridae, Mochokidae and Pseudopimelodidae have well-developed, free bladders, whereas five species belonging to the callichthyid subfamilies Callichthyinae and Corydoradinae, and to the loricariid subfamilies Hypoptopomatinae, Hypostominae and Loricariinae have reduced, paired and bony encapsulated bladders. Dissections along with clearing and staining techniques were used to examine and measure swimbladders and ossicles. Hearing thresholds between 50 Hz and 5 kHz were determined in all species using the auditory evoked potential (AEP) recording method.
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MATERIALS AND METHODS |
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Fish were obtained from tropical fish suppliers: Batrochoglanis raninus from Ruinemans Aquarium, Montfoort, Netherlands; Pimelodella sp. from Amazon Exotic Import, Rosenheim, Germany; all other species from Transfish, Munich, Germany. Specimens of Hemiodontichthys acipenserinus were aquarium reared; all other species were wild caught. Fish were kept in planted aquaria with a sand bottom, equipped with roots and clay or bamboo tubes as shelters. Only external filters were used. In order to provide a quiet environment we did not use any internal filters or air stones. Temperature was kept at 26±1°C and a 12 h:12 h L:D cycle was maintained. Depending on their specific requirements, fish were fed frozen chironomid larvae and artificial food (granulate and tablets) daily. All hearing experiments were performed with the permission of the Austrian Commission on Experiments in Animals (GZ 66.006/2-BrGT/2006).
Morphological measurements
Fish and swimbladder sizes were measured to the nearest 0.1 mm using
digital callipers. Standard length (SL) was measured as `standard
length 2' following Holcik et al. (Holcik
et al., 1989). A standardized swimbladder length (SBL)
was determined following the formula
SBL=(l+w+h)/3, where l is length,
w is width and h is height. For morphological measurements,
fish were killed using an overdose of tricaine methanesulphonate (MS-222);
measurements were taken either immediately or after preserving the fish in
alcohol (70%). Dissecting microscopes (Wild M7 and Wild M5, Wild Heerbrugg
Ltd, Heerbrugg, Switzerland) equipped with a camera lucida were used for these
measurements and morphological drawings. For investigation of the Weberian
ossicles and swimbladder capsules, additional specimens were trypsin cleared
and alizarin stained following Potthoff's method
(Potthoff, 1984). Ossicles of
Corydoras sodalis were additionally examined with a scanning electron
microscope (SEM Philips XL 20, software: Microscope Control, Philips,
Eindhoven, The Netherlands). Assuming these structures grow linearly with fish
growth (Fine, 1975;
Fine et al., 2007), `relative
swimbladder length' (rSBL) and `relative length of the ossicular chain' (rCL)
were calculated following the formulas rSBL=SBL/SL and
rCL=CL/SL, where CL is the ossicular chain length
and SL is the standard length.
In Malapterurus beninensis, only the dimensions of the anterior chamber of the bladder (camera aerea Weberiana) were used for calculations and comparisons.
Auditory sensitivity measurements
Hearing thresholds were determined using the AEP recording technique
following the protocol developed by Kenyon et al.
(Kenyon et al., 1998) and
modified by Wysocki and Ladich (Wysocki
and Ladich, 2005a; Wysocki and
Ladich, 2005b).
The catfish were mildly immobilized with Flaxedil (gallamine triethiodide;
Sigma Aldrich Handels GmbH, Vienna, Austria) during these experiments. The
dosage used was 2.9–3.5 µg g–1 for Ancistrus
ranunculus, 2.13–2.95 µg g–1 for Ariopsis
seemanni, 39.6–45.3 µg g–1 for
Batrochoglanis raninus, 0.62–0.74 µg g–1
for Corydoras sodalis, 1.20–1.85 µg g–1 for
Dianema urostriatum, 1.13–3.27 µg g–1 for
Hemiodontichtys acipenserinus, 1.21–1.43 µg
g–1 for Hypoptopoma thoracatum, 6.17–7.7 µg
g–1 for Malapterurus beninensis, 1.61–1.96
µg g–1 for Pimelodella sp., 3.57–10.81
µg g–1 for Synodontis schoutedeni and
20.40–37.53 µg g–1 for Trachelyopterichthys
taeniatus. The lowest dosage that immobilized fish while enabling slight
movement of the opercula during the experiments was applied. All auditory
measurements were carried out in a bowl-shaped plastic tub (diameter 33 cm,
water depth 13 cm, 1 cm layer of gravel), which was lined inside with
acoustically absorbent material (air-filled packing wrap) to decrease
resonances and reflections. For a more detailed description see Wysocki and
Ladich (Wysocki and Ladich,
2002). The tub was positioned on an air table (TMC Micro-g 63-540,
Technical Manufacturing Corporation, Peabody, MA, USA), which rested on a
vibration-isolated plate of concrete. A sound-proof chamber, constructed as a
Faraday cage (interior dimensions: 3.2 mx3.2 mx2.4 m), enclosed
the whole setup.
Test subjects were positioned in the centre of the tub, so that the nape of the head was just above the water surface. For respiration a pipette was inserted into the fish's mouth and respiration was effected by a simple, temperature-controlled (25±1°C), gravity-fed water circulation system. The area of the head above the water surface was covered with a small piece of Kimwipes® tissue paper to keep it moist. Silver wire electrodes (diameter 0.38 mm) were used for recording AEPs. The recording electrode was placed in the midline of the skull over the region of the medulla, the reference electrode cranially between the nares. Both electrodes were pressed firmly against the skin.
Both presentation of sound stimuli and AEP waveform recording were achieved using a modular rack-mount system [Tucker-Davis Technologies (TDT) System 3, Gainesville, FL, USA] controlled by a PC containing a TDT digital signal processing board and running TDT BioSig RP software.
Sound stimuli
Hearing thresholds were determined at the following frequencies: 0.05, 0.1,
0.3, 0.5, 0.8, 1, 2, 3, 4 and 5 kHz. Ariopsis seemanni was
additionally tested at 0.2 kHz. Sound stimuli waveforms were created using TDT
SigGen RP software and fed through a power amplifier (Alesis RA 300, Alesis
Corporation, Los Angeles, CA, USA). For presentation of stimuli during
testing, a dual-cone speaker (Warfedale Pro Twin 8, Huntingdon, UK), installed
0.5 m above the test subjects, was used. The different frequencies were
presented in random order. A hydrophone (Brüel and Kjaer 8101, Naerum,
Denmark; frequency range 1 Hz to 80 kHz ±2 dB; voltage sensitivity
–184 dB re 1 V µPa–1) was placed 2 cm from the right
side of the animal to determine absolute sound pressure levels (SPLs) under
water in the immediate vicinity of the test subjects. A second, custom-built
preamplifier was used to boost the hydrophone signal. Sound stimuli consisted
of tone bursts played at a repetition rate of 21 s–1 and at
opposite polarities (90° and 270°). One-thousand stimuli of each
polarity were presented and the corresponding AEPs averaged by BioSig RP
software to eliminate stimulus artefacts. The SPL was reduced in 4-dB steps
until the AEP waveform was no longer identifiable. By overlaying replicate
traces, the lowest SPL yielding a repeatable AEP trace was determined and
regarded as threshold.
Data analysis
All data were tested for normal distribution utilizing Shapiro–Wilk's
test. When data were normally distributed, parametric statistical tests were
applied. The Mann–Whitney U-test was used to test for
differences in the relative length of the ossicular chain between species with
free and encapsulated bladders. Mean hearing thresholds were determined for
each species and at each frequency. A mean threshold curve for each frequency
was calculated for both types of species. The Mann–Whitney
U-test was used to analyse differences in the number of ossicles and
mean hearing thresholds at each frequency of all species with free bladders
from those of all species with bony encapsulated bladders. Pearson's
correlation was calculated for comparing mean hearing thresholds to
morphological measurements (rSBL, rCL, number of Weberian ossicles) of each
species. SPSS 15.0 (SPSS Inc., Chicago, IL, USA) was used to run statistical
tests.
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RESULTS |
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Swimbladders
Free swimbladders were ellipsoid or slightly heart shaped, whereas the
shapes of encapsulated bladders varied from conical in A. ranunculus
to nearly spherical in H. thoracatum (Figs
1 and
2). Mean swimbladder length
ranged from 7.84 to 14.39 mm in the first group and from 1.09 to 4.68 mm in
the second group. Free bladders were absolutely and relatively larger than
encapsulated ones (rSBL: Student's t-test: t=–11.51,
N=36, P<0.001). None of the species with paired bladders
had a connection between the two lateral compartments.
Ossicles
Species with free bladders had generally four Weberian ossicles –
tripus, intercalarium, scaphium and claustrum, except for S.
schoutedeni, which lacked the latter. Interestingly, the auchenipterid
T. taeniatus had just one well-developed ossicle
(Fig. 1). The tripus was the
largest ossicle in all species, whereas the intercalarium usually was the
smallest one, mainly consisting of a thin plate. In species with free bladders
the scaphium had a typically patelliform concha. The scaphium in all species
showed a well-developed processus ascendens, except in S.
schoutedeni, where it was degenerated and only rudimentarily present. In
species with encapsulated bladders the scaphium, when present, showed no
processus and was reduced to the concha scaphii, which was bowl shaped as in
the group with free bladders (Fig.
2). Claustra, when present, were thin sticks with no connection to
the rest of the chain. They were positioned opposite the scaphium towards the
midline in B. raninus and M. beninensis, towards the caudal
end in A. seemanni and towards the rostral end in
Pimelodella sp. Representatives with encapsulated bladders had fewer
ossicles, usually one or two (Mann–Whitney U-test,
U=4, N1=6, N2=5, d.f.=9,
P<0.02). Ancistrus ranunculus, H. acipenserinus and
H. thoracatum exhibited a tripus and scaphium whereas C.
sodalis and D. urostriatum had only a single ossicle
(Fig. 3). SEM photographs of
the ossicle of C. sodalis (Fig.
4) revealed no sutures that would indicate a possible fusion of
several ossicles. Dianema urostriatum had a single bipartite ossicle.
These two parts were fused with a connecting shaft, which was still surrounded
by a ligament.
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Auditory sensitivities
All catfish examined showed AEPs in response to tone bursts from 50 Hz to 5
kHz. Only in three out of four larger individuals of Ancistrus
ranunculus did we fail to get any response at 5 kHz (possibly because our
equipment could not deliver SPLs beyond 129 dB re 1 µPa). (A conservative
calculation approach was used; accordingly, the data from these three
specimens were omitted in calculations at 5 kHz, and so the average
underestimates the threshold of A. ranunculus at this frequency.) The
lowest absolute auditory threshold was found in the sea catfish Ariopsis
seemanni at 3 kHz with a mean threshold of 67 dB, whereas in A.
ranunculus and Corydoras sodalis the highest thresholds were 117
and 121 dB at 4 and 5 kHz (Table
3A,B; Fig. 5).
Differences in hearing threshold increased rapidly at higher frequencies.
While thresholds varied maximally by 18 to 24 dB from 50 to 1000 Hz among all
species, at higher frequencies the differences ranged from 29 to 51 dB. The
largest difference (51 dB) was found between A. seemanni and A.
ranunculus at 4 kHz (Table
3A,B; Fig. 5).
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Hearing thresholds differed significantly between the group with free and the group with encapsulated bladders between 1 and 5 kHz, but not at lower frequencies (Fig. 6) (Mann–Whitney U-test, 1 kHz: U=494.5, P=0.028; 2 kHz: U=83, P<0.001; 3 kHz: U=25.5, P<0.001; 4 kHz: U=29, P<0.001; 5 kHz: U=34, P<0.001; N1=6, N2=5, d.f.=9).
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DISCUSSION |
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). Furthermore, in those groups that possess aerial
respiratory organs (Clariidae, Loricariidae and Callichthyidae) a reduced size
might compensate for the hydrostatic effect of an accessory air-filled
respiratory cavity (Alexander,
1964). Nevertheless, contrary to many other bottom-dwelling bony
fishes such as sculpins and some gobies, otophysines in general and catfishes
in particular never completely lose their swimbladders and Weberian ossicles.
At the same time they reduce swimbladder and ossicle size and ossicle number.
Extreme reductions (or perhaps even absence) have been reported for
cave-dwelling troglomorphic North American ictalurids
(Hubbs and Bailey, 1947;
Lundberg, 1982;
Langecker and Longley, 1993).
Unfortunately none of these authors state clearly whether bladders are totally
absent or only extremely reduced and whether there are really catfish without
swimbladders.
The structures of the Weberian apparatus and the morphology of the
swimbladder in catfishes have been described by several authors since the late
19th century (Sagemehl, 1885;
Bridge and Haddon, 1889;
Bridge and Haddon, 1892;
Bridge and Haddon, 1893;
Sörensen, 1895;
Chranilov, 1929;
Alexander, 1964;
Alexander, 1965;
Mahajan, 1967;
Chardon, 1968;
Schaefer, 1987;
Aquino and Miquelarena, 2001;
Chardon et al., 2003). Our
morphological findings that free bladders are larger than encapsulated ones
and are accompanied by more ossicles are consistent with most of their
observations. We have shown that free single swimbladders are heart shaped or
ellipsoid, whereas paired bladders are tiny and in some species hardly
detectable, such as those in loricariids and callichthyids. Fish possessing
free single bladders had mostly four Weberian ossicles, and groups with small
encapsulated bladders had two ossicles in loricariids and a single one in
callichthyids. Ariids, heptapterids, malapterurids and pseudopimelodids are
regarded as basal catfish groups and we found a claustrum in all species of
the families examined, which corresponds to the report of Britz and Hoffmann
(Britz and Hoffmann, 2006).
While some authors could not detect an intercalarium in mochokids of the genus
Synodontis (Chranilov,
1929; Chardon,
1968) or stated that these fish possess only a highly reduced
intercalarium (Bridge and Haddon,
1893), we undoubtedly found this ossicle in Synodontis
schoutedeni. It is a very thin, small disc at which interossicular
ligaments insert, recognizable only after multiple alizarin stainings. We do
not know whether representatives of Synodontis exhibit a different
development of Weberian ossicles or whether prior investigators simply
overlooked the intercalarium.
Interestingly, the auchenipterid Trachelyopterichthys taeniatus
has a single free bladder but possesses just one ossicle, the tripus. The
tripus of T. taeniatus is, just like the tripus of
Pseudauchenipterus nodosus (Bridge
and Haddon, 1893), curled inward along the medial edge, but in
contrast to the tripus in P. nodosus does not form a thickened ridge
but remains hollow at this medial end. Bridge and Haddon did not mention
whether further ossicles are present or absent in this species
(Bridge and Haddon, 1893). A
description of the Weberian ossicles in the auchenipterid Centromochlus
albescens (probably Glanidium albescens in the current
nomenclature) given by Chranilov shows the presence of all four ossicles
(Chranilov, 1929), while the
respective description of Auchenipterus nigripinnis by Chardon lacks
any information on ossicle number
(Chardon, 1968). Based on the
present investigation of T. taeniatus, we assume that the
intercalarium, scaphium and claustrum are missing.
Catfishes with tiny paired bladders have reduced ossicle size and number.
The callichthyid catfishes Corydoras sodalis and Dianema
urostriatum have a single pair of ossicles. Coburn and Grubach state that
all ossicles except the tripus are reduced in C. paleatus
(Coburn and Grubach, 1998),
while other authors (e.g. Chranilov,
1929; Chardon,
1968) suppose the scaphium and tripus to be fused in
callichthyids. Comparing the shapes of these two parts in D.
urostriatum with those in the other groups indicates that the caudal part
was apparently a tripus and the cranial part resembled a scaphium (concha
scaphium). This supports the theory of Chranilov, Chardon and others that
scaphium and tripus fused into a single ossicle in callichthyid catfish.
However, three Weberian ossicles were found in some loricariids and
astroplebids according to Schaefer
(Schaefer, 1990) as well as in
certain sisorids (Mahajan,
1967).
As expected, H. acipenserinus had the smallest ossicles and bladders compared to body length, clearly due to the slender and elongate body shape of the loricariid subfamily Loricariinae.
Auditory sensitivities
The sensitivities described in the present study differ only slightly from
the findings of Ladich, who detected sensitivity maxima between 300 and 1000
Hz in all catfish species tested and a flat curve in species with free
swimbladders (Ladich, 1999).
Four out of six species with free swimbladders tested in the present study
exhibited lowest hearing thresholds at higher frequencies, at 2 kHz (B.
raninus, 77.7 dB; M. beninensis, 79.8 dB; T. taeniatus,
68.33 dB). The lowest thresholds of A. seemanni occurred at 3 kHz (67
dB), which was the best value among all species we examined. Moreover,
catfishes with free bladders showed rather flat hearing curves, similar to
those in Pimelodus blochii, Pimelodus pictus and Platydoras
costatus tested previously (Ladich,
1999). Batrochoglanis raninus exhibited a difference of
only 7 dB across its hearing range from 500 to 5000 Hz.
The audiogram of the ariid catfish Ariopsis seemanni used in the
current study differs from that in the sea catfish Ariopsis (formerly
Arius) felis (Popper and
Tavolga, 1981). Although we also observed a large utricular
otolith as described previously in Ariopsis, the hearing curve
reveals no particularly well-developed low-frequency hearing ability. Popper
and Tavolga found lowest hearing thresholds at 200 Hz and no response above 1
kHz in behavioural tests (Popper and
Tavolga, 1981). Our data on A. seemanni show very good
hearing ability at several kilohertz. The well-developed low frequency
sensitivity in A. felis could be an adaptation for the primitive
echolocation abilities of this species
(Tavolga, 1976). Another
explanation might be that the previous study used behavioural techniques,
which occasionally yield lower thresholds at lower frequencies
(Kenyon et al., 1998).
Our results in catfish species with tiny and bony encapsulated bladders are
similar to those obtained previously
(Ladich, 1999). Both
Corydoras species tested showed a decreased sensitivity at higher
frequencies. On the other hand, the callichthyid Dianema urostriatum
(encapsulated bladder) and Synodontis schoutedeni (free bladder)
showed the best hearing ability of all species tested in the 50–300 Hz
range. Therefore, encapsulation of the swim bladder may not affect hearing at
lower frequencies. The loricariid Hypoptopoma thoracatum has the best
hearing ability of all species with reduced and bony encapsulated bladders at
the highest frequencies tested (4 and 5 kHz). In loricariids the capsules of
the swimbladders and the pterotic-supracleithrum have pores. These pores are
particularly large in the ear-grid plecos [subfamily Hypoptopomatinae
(Schaefer, 1987)] and they
probably facilitate sound transmission to the inner ear and might explain
their – compared with other loricariids – enhanced hearing
ability.
Relationship between accessory hearing structures and auditory sensitivity
As hearing specialists, otophysans exhibit a large diversity in hearing
sensitivity (Ladich, 1999;
Ladich and Bass, 2003). These
differences may be based on various reductions of the Weberian system and
swimbladders, but clear relationships had not been worked out. The present
study clearly shows that reducing the size of air-filled bladders and reduced
Weberian ossicles negatively affect hearing sensitivity, particularly at
higher frequencies.
This relationship between larger swimbladders and better hearing at higher
frequencies agrees with the work of Kleerekopper and Roggenkamp (Kleerekopper
and Roggenkamp, 1959) and with that of Ladich and Wysocki, whose elimination
studies showed that large swimbladders improve hearing especially at higher
frequencies in catfish and goldfish
(Ladich and Wysocki, 2003).
Bilateral extirpation of the tripus in goldfish caused an increasing hearing
loss at higher frequencies, ranging from 7 dB at 100 Hz to 33 dB at 2 kHz.
The basic factors improving hearing abilities at higher frequencies in
`free bladder' catfishes are mostly unknown. Alexander analysed the physics of
free swimbladders and concluded that amplitudes of wall movements increase
with swimbladder size (Alexander,
1966). Fay and Popper, recording microphonic potentials in a
standing wave tube, calculated that the auditory system of the goldfish gains
with increasing frequency due to the impedance transform characteristics of
the fish's accessory hearing structures
(Fay and Popper, 1974). This
agrees with our observation that the hearing sensitivity in catfishes with
free bladders increases at higher frequencies. Alexander furthermore assumed
that the encapsulation of the tiny bladders helps hold the surrounding tissue
clear of the moving part of the bladder wall. This would allow larger
oscillations of the wall because there is some free fluid-filled space between
the bladder and the bony capsule. Therefore, the bony encapsulation might
compensate for the loss in hearing sensitivity to some degree in groups with
tiny swimbladders.
Our results revealed that the size and number of Weberian ossicles further
influence hearing sensitivity. Obviously, larger and more ossicles transmit
vibrations from the swimbladder to the inner ear more efficiently and improve
hearing, in particular at higher frequencies. Improvement of the mechanical
linkages between ossicles, the moveabilities of ossicles, the linkages to the
swimbladder and leverages between ossicles might be responsible for this
enhanced sound transmission. This correlation seems to be analogous to that
found in terrestrial vertebrates. Mammals, which possess three middle ear
ossicles (which are phylogenetically not related to Weberian ossicles), can
detect much higher sound frequencies than frogs, reptiles and birds, which
have just one ossicle (Fay,
1988). These results do not support prior assumptions. Chranilov
(Chranilov, 1929) assumed that
modifications such as swimbladder encapsulation and a reduction in the number
of ossicles increase the general sensitivity of the Weberian apparatus.
Besides the size of the accessory hearing structures, a better linkage of
oscillating bladders to the ear (i.e. a shorter distance between the two) is
beneficial for hearing at higher frequencies. Examination of hearing
thresholds in non-related squirrelfish (family Holocentridae) showed that
hearing sensitivities varied between genera
(Coombs and Popper, 1979;
Hawkins, 1993). Squirrelfish
of the genus Myripristis have a long anterior extension of the
swimbladder that directly couples the swimbladder to the otic bulla.
Myripristis shows one of the best hearing abilities among fish,
similar to that of carp (Hawkins and
Myrberg, 1983). In contrast, the hearing sensitivity in
Adioryx is 50 dB lower because they have no bladder–skull
connection. Holocentrus, on the other hand, has an intermediate
status and an intermediate sensitivity
(Tavolga and Wodinsky, 1963).
Atlantic sciaenids have a large variation in swimbladders and their
relationship to the otic region
(Ramcharitar and Popper,
2004). In the black drum Pogonias chromis and the spot
Leiostomus xanthurus, the swimbladder is relatively far from the otic
capsule, while in the Atlantic croaker Micropogonias undulatus and
the weakfish Cynoscion regalis, anteriorly directed
bladder–diverticula end close to the otic capsule
(Ramcharitar and Popper, 2004;
Ramcharitar et al., 2006).
Nevertheless, the two groups show no significant difference in hearing
thresholds. Closer connection between swimbladders and the inner ear in the
weakfish and croaker, however, improved their ability to detect higher
frequency sound. Similarly, gouramis (Anabantoidei) and mormyrids show
enhanced hearing due to gas-filled chambers in close proximity to the inner
ear (Yan, 1998;
Yan and Curtsinger, 2000).
These observations support the general idea that a close connection of
gas-filled chambers to the inner ear improves hearing at higher frequencies
(Popper and Tavolga, 1981;
Fay, 1988;
Ladich and Popper, 2004).
Significance of swimbladder reductions
The fact that bottom-dwelling otophysines (Siluriformes as well as the
examined Cypriniformes) have variously reduced swimbladders but never lack
bladders indicates that this group of bony fishes has reached a compromise
between reducing the buoyancy of an air-filled cavity within the body and
keeping the auditory function of these air-filled cavities. The extremely
small, paired bubbles directly behind or even within the head of loricariids
and callichthyids have clearly lost most of their hydrostatic function and can
no longer be called `swimbladders'. Despite their tiny size and thus tiny
surface, the oscillations of the bladder walls in the sound field are still
sufficient to enhance the hearing of these species far beyond that of hearing
generalists. Retaining the auditory sensitivity for various purposes such as
analysing the auditory scene for predators, prey or communicating conspecifics
is the most likely explanation for why bottom-dwelling otophysans such as
catfishes, which evolved and live in low ambient noise environments, never
reduced their swimbladders, contrary to other bottom-dwelling teleosts
belonging to hearing generalists.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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