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Comparison of Weberian ossicles. 3D-reconstruction based on serial semithin section photomicrographs (A, B) and based on an image stack from a mCT scan (C, D) showing isolated Weberian ossicles. (A) shows a lateral and (B) a ventral view of a specimen of 11.3 mm SL (group XS) and (C) lateral and (D) ventral view of a 85.5 mm SL specimen (group XL). Cl-Claustrum, Ic-Intercalarium, Sc-Scaphium, Tr-Tripus; scale bars in A, B = 300 mm and in C, D = 3 mm; anterior is to the left, posterior to the right, (A), (C): dorsal above, ventral below. doi:10.1371/journal.pone.0018511.g002
Source publication
The weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19(th) century. No studies, however, are available on the development of the weberian ossicles and its effect on the development of hearing in catfish...
Contexts in source publication
Context 1
... scaphium and claustrum were located anterior- dorsally to the tripus right below the first vertebra (Figure 1). The intercalarium as well as the interossicular ligaments were missing ( Figure 3) and thus no connection existed between the tripus and the scaphium at this stage (Figure 2 A, B, Figure 3). This not yet fully developed Weberian apparatus, the missing ossicles and interossicular ligaments had major impact on the hearing abilities of group XS. ...
Context 2
... contrast, specimens of size groups S to XL possessed a well- developed chain of Weberian ossicles consisting of the tripus, intercalarium, scaphium, claustrum and of interossicular ligaments ( Figure 5, Figure 2 C, D, Figure 6). The intercalarium of L. cyclurus showed only a slight indication of an ascending processus (an ascending processus of the intercalarium is a typical characteristic for the intercalaria of many basal otophysans). ...
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Citations
... The hearing capability of zebrafish has been evaluated at early developmental stages [6,7], entire life span [8][9][10][11], ageing [12] and comparisons of laboratory fish lines [13] using behavioural and electrophysiological auditory methods, which serve as fundamental baselines for further exploring of hearing mechanisms. It is widely accepted and demonstrated that Weberian apparatus of zebrafish, like any other otophysan fishes, contribute to their high hearing sensitivities and large frequency range compared to nonotophysan fishes [9,14,15]. However, the Weberian apparatus, the functional analogue of middle ear in human, has not been part of the equation in hearing loss, form-function correlation, nor biomechanical studies. ...
Zebrafish, an essential vertebrate model, has greatly expanded our understanding of hearing. However, one area that remains unexplored is the biomechanics of the Weberian apparatus, crucial for sound conduction and perception. Using micro-computed tomography (μCT) bioimaging, we created three-dimensional finite element models of the zebrafish Weberian ossicles. These models ranged from the exact size to scaled isometric versions with constrained geometry (1 to 10 mm in ossicular chain length). Harmonic finite element analysis of all 11 models revealed that the resonance frequency of the zebrafish's Weberian ossicular chain is approximately 900 Hz, matching their optimal hearing range. Interestingly, resonance frequency negatively correlated with size, while the ratio of peak displacement and difference of resonance frequency between tripus and scaphium remained constant. This suggests the transmission efficiency of the ossicular chain and the homogeneity of resonance frequency at both ends of the chain are not size-dependent. We conclude that the Weberian apparatus's resonance frequency can explain zebrafish's best hearing frequency, and their biomechanical characteristics are not influenced by isometric ontogeny. As the first biomechanical modelling of atympanic ear and among the few non-human ear modelling, this study provides a methodological framework for further investigations into hearing mechanisms and the hearing evolution of vertebrates.
... This serves to increase sensitivity to sound, thereby lowering hearing thresholds and broadening the bandwidth of hearing so that most otophysans, including zebrafish, can detect sound up to 3-4 kHz. 25,75,77 Hearing sensitivity ...
Zebrafish, like all fish species, use sound to learn about their environment. Thus, human-generated (anthropogenic) sound added to the environment has the potential to disrupt the detection of biologically relevant sounds, alter behavior, impact fitness, and produce stress and other effects that can alter the well-being of animals. This review considers the bioacoustics of zebrafish in the laboratory with two goals. First, we discuss zebrafish hearing and the problems and issues that must be considered in any studies to get a clear understanding of hearing capabilities. Second, we focus on the potential effects of sounds in the tank environment and its impact on zebrafish physiology and health. To do this, we discuss underwater acoustics and the very specialized acoustics of fish tanks, in which zebrafish live and are studied. We consider what is known about zebrafish hearing and what is known about the potential impacts of tank acoustics on zebrafish and their well-being. We conclude with suggestions regarding the major gaps in what is known about zebrafish hearing as well as questions that must be explored to better understand how well zebrafish tolerate and deal with the acoustic world they live in within laboratories.
... In juveniles and adult fish, the emergence of the Weberian ossicles enables the transmission of sound pressure detected by the swim bladder to the inner ear5. In some species, this structure decreases the detection threshold and increases the sensitivity for high frequencies [7]. However, they are capable of using auditory information to detect prey, avoid predators, or to eavesdrop on animals from the same or different species [8][9][10]. ...
Organisms use their sensory systems to acquire information from their environment and integrate this information to produce relevant behaviors. Nevertheless, how sensory information is converted into adequate motor patterns in the brain remains an open question. Here, we addressed this question using two-photon and light-sheet calcium imaging in intact, behaving zebrafish larvae. We monitored neural activity elicited by auditory stimuli while simultaneously recording tail movements. We observed a spatial organization of neural activity according to four different response profiles (frequency tuning curves), suggesting a low-dimensional representation of frequency information, maintained throughout the development of the larvae. Low frequencies (150-450 Hz) were locally processed in the hindbrain and elicited motor behaviors. In contrast, higher frequencies (900-1,000 Hz) rarely induced motor behaviors and were also represented in the midbrain. Finally, we found that the sensorimotor transformations in the zebrafish auditory system are a continuous and gradual process that involves the temporal integration of the sensory response in order to generate a motor behavior.
... The Weberian apparatus is well-known to improve hearing abilities of otophysan fishes, in terms of both hearing bandwidth and hearing sensitivity 20,21 . The eight serrasalmid species investigated in our study were able to detect frequencies up to at least 3000 Hz which is common to Otophysi 19,22,33,34 . ...
... The size ranges of the different species indicate that the majority of specimens were juveniles or subadults. Hearing range and auditory sensitivity are known to increase along with the development of the auditory structures 20,21 . In the goldfish Carassius auratus, the Weberian apparatus reaches the adult condition at 25 mm length 46 . ...
Like all otophysan fishes, serrasalmids (piranhas and relatives) possess a Weberian apparatus that improves their hearing capacities. We compared the hearing abilities among eight species of serrasalmids having different life-history traits: herbivorous vs. carnivorous and vocal vs. mute species. We also made 3D reconstructions of the auditory system to detect potential morphological variations associated with hearing ability. The hearing structures were similar in overall shape and position. All the species hear in the same frequency range and only slight differences were found in hearing thresholds. The eight species have their range of best hearing in the lower frequencies (50-900 Hz). In vocal serrasalmids, the range of best hearing covers the frequency spectrum of their sounds. However, the broad overlap in hearing thresholds among species having different life-history traits (herbivorous vs. carnivorous and vocal vs. non-vocal species) suggests that hearing ability is likely not related to the capacity to emit acoustic signals or to the diet, i.e. the ability to detect sounds is not associated with a given kind of food. The inner ear appears to be highly conservative in this group suggesting that it is shaped by phylogenetic history or by other kinds of constraints such as predator avoidance.
... Additionally, electrophysiological data are not appropriate for longitudinal comparison. For instance, AEP data obtained from zebrafish showed conflicting relationship between hearing sensitivity and age/size of subjects [21][22][23][24][25]. This phenomenon occurs because of the Weberian ossicles connecting the inner ear to the swim bladder, which play a facilitative role in enhancing hearing sensitivity and extending the upper frequency limit [26]. ...
Zebrafish is an emerging animal model for studies on auditory system. This model presents high comparability with humans, good accessibility to the hearing organ, and high throughput capacity. To better utilize this animal model, methodologies need to be used to quantify the hearing function of the zebrafish. Zebrafish displays a series of innate and robust behavior related to its auditory function. Here, we reviewed the advantage of using zebrafish in auditory research and then introduced three behavioral tests, as follows: the startle response, the vestibular-ocular reflex, and rheotaxis. These tests are discussed in terms of their physiological characteristics, up-to-date technical development, and apparatus description. Test limitation and areas to improve are also introduced. Finally, we revealed the feasibility of these applications in zebrafish behavioral assessment and their potential in the high-throughput screening on hearing-related genes and drugs.
... Ladich (1999) studied species from four ostariophysan orders (Cypriniformes, Characiformes, Siluriformes, and Gymnotiformes) and elicited auditory brainstem responses up to at least 5 kHz in all species. Furthermore, brown bullhead (10-13 kHz; Ameirus nebulosus; Poggendorf, 1952) and neotropical catfish (6 kHz; Lophiobagrus cyclurus; Lechner et al., 2011) have frequency sensitivity beyond 5 kHz. Therefore, it is possible that bighead carp can detect higher frequencies than those previously reported by Lovell et al. (2006). ...
Recent studies have shown the potential of acoustic deterrents against invasive silver carp (Hypophthalmichthys molitrix). This study examined the phonotaxic response of the bighead carp (H. nobilis) to pure tones (500–2000 Hz) and playbacks of broadband sound from an underwater recording of a 100 hp outboard motor (0.06–10 kHz) in an outdoor concrete pond (10 × 5 × 1.2 m) at the U.S. Geological Survey Upper Midwest Environmental Science Center in La Crosse, WI. The number of consecutive times the fish reacted to sound from alternating locations at each end of the pond was assessed. Bighead carp were relatively indifferent to the pure tones with median consecutive responses ranging from 0 to 2 reactions away from the sound source. However, fish consistently exhibited significantly (P < 0.001) greater negative phonotaxis to the broadband sound (outboard motor recording) with an overall median response of 20 consecutive reactions during the 10 min trials. In over 50% of broadband sound tests, carp were still reacting to the stimulus at the end of the trial, implying that fish were not habituating to the sound. This study suggests that broadband sound may be an effective deterrent to bighead carp and provides a basis for conducting studies with wild fish.
... Recently, the AEP method has been critiqued because it typically involves the use of small tanks, which produce complex acoustic environments and there are often discrepancies both among thresholds reported between AEP studies and with behaviorally derived thresholds for the same species (Ladich and Fay, 2013;Sisneros et al., 2016). Lovell et al. (2006) also did not test past 3000 Hz, so it is possible that silver carp are sensitive to a larger range of frequencies contained within the outboard motor sound, as other ostariophysans hear beyond 5000 Hz (Stetter, 1929;Poggendorf, 1952;Lechner et al., 2011). ...
Invasive silver carp (Hypophthalmichthys molitrix) are notorious for their prolific and unusual jumping behavior. Juvenile and adult (~25 kg) carp can jump up to 3 m above the water surface in response to moving watercraft; however, it is unclear what is the trigger that elicits jumping. Broadband sound (0.06 – 10 kHz) recorded from an outboard motor (100 hp at 32 km/hr), elicited jumping behavior in wild fish when played from speakers mounted on a slow moving (3 – 6 km/hr) boat in the Spoon River near Havana, Illinois. Fish jumped in 100% of the sound trials, implying that broadband sound elicits jumping. The findings suggest that anthropogenic sound can be used to alter the behavior of silver carp and has implications for deterrent barriers or herding fish for removal.
... These are a series of four bones forming a chain between the swim bladder and the spinal medulla, assisting in the transmission of oscillations. This structure can be found in carps, minnows, catfishes, electric eels and characins (all belonging to the Superorder Otophysi) (Diogo, 2009, Lechner et al., 2011, Popper and Fay, 2011. Another type of specialization is the air-filled suprabranchial chamber next to the inner ear, as can be found in labyrinth fishes (Anabantoids) (Wysocki et al., 2006). ...
... These structures allow the transmission of sound-induced vibrations from the swim bladder to the inner ear (Weber 1820 ). Although the Weberian apparatus is associated with more sensitive hearing and broader frequency detection (Higgs et al. 2003 ;Ladich and Wysocki 2003 ;Lechner et al. 2011 ), conductive hearing loss in fi shes has only been shown in a few studies. Bang et al. ( 2002 ) found that approximately 1 % of the zebrafi sh ( Danio rerio ) that were exposed to a 400 Hz tone did not exhibit an escape refl ex. ...
Sensory hair cells are the mechanotransductive receptors that detect gravity, sound, and vibration in all vertebrates. Damage to these sensitive receptors often results in deficits in vestibular function and hearing. There are currently two main reasons for studying the process of hair cell loss in fishes. First, fishes, like other non-mammalian vertebrates, have the ability to regenerate hair cells that have been damaged or lost via exposure to ototoxic chemicals or acoustic overstimulation. Thus, they are used as a biomedical model to understand the process of hair cell death and regeneration and find therapeutics that treat or prevent human hearing loss. Secondly, scientists and governmental natural resource managers are concerned about the potential effects of intense anthropogenic sounds on aquatic organisms, including fishes. Dr. Arthur N. Popper and his students, postdocs and research associates have performed pioneering experiments in both of these lines of fish hearing research. This review will discuss the current knowledge regarding the causes and consequences of both lateral line and inner ear hair cell damage in teleost fishes.
... These structures allow the transmission of sound-induced vibrations from the swim bladder to the inner ear (Weber 1820 ). Although the Weberian apparatus is associated with more sensitive hearing and broader frequency detection (Higgs et al. 2003 ;Ladich and Wysocki 2003 ;Lechner et al. 2011 ), conductive hearing loss in fi shes has only been shown in a few studies. Bang et al. ( 2002 ) found that approximately 1 % of the zebrafi sh ( Danio rerio ) that were exposed to a 400 Hz tone did not exhibit an escape refl ex. ...
Sensory hair cells are the mechanotransductive receptors that detect gravity, sound, and vibration in all vertebrates. Damage to these sensitive receptors often results in deficits in vestibular function and hearing. There are currently two main reasons for studying the process of hair cell loss in fishes. First, fishes, like other non-mammalian vertebrates, have the ability to regenerate hair cells that have been damaged or lost via exposure to ototoxic chemicals or acoustic overstimulation. Thus, they are used as a biomedical model to understand the process of hair cell death and regeneration and find therapeutics that treat or prevent human hearing loss. Secondly, scientists and governmental natural resource managers are concerned about the potential effects of intense anthropogenic sounds on aquatic organisms, including fishes. Dr. Arthur N. Popper and his students, postdocs and research associates have performed pioneering experiments in both of these lines of fish hearing research. This review will discuss the current knowledge regarding the causes and consequences of both lateral line and inner ear hair cell damage in teleost fishes.
