© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Response of clupeid fish to ultrasound: a review
a Department of Biology and Neuroscience and Cognitive Science Program, University of Maryland College Park, MD 20742, USA
b Institut für Biologie II, RWTH Aachen Kopernikusstr. 16, 52074 Aachen, Germany
c College of Marine Science, University of South Florida St. Petersburg, FL 33701, USA
d Department of Biology, University of Windsor Windsor, Ontario, Canada N9B 3P4
*Correspondence to A. N. Popper: tel: +1 301 460 5599; fax: +1 301 314 9358. e-mail: apopper{at}umd.edu.
A number of species of clupeid fish, including blueback herring, American shad, and gulf menhaden, can detect and respond to ultrasonic sounds up to at least 180 kHz, whereas other clupeids, including bay anchovies and Spanish sardines, do not appear to detect sounds above about 4 kHz. Although the location for ultrasound detection has not been proven conclusively, there is a growing body of physiological, developmental, and anatomical evidence suggesting that one end organ of the inner ear, the utricle, is likely to be the detector. The utricle is a region of the inner ear that is very similar in all vertebrates studied to date, except for clupeid fish, where it is highly specialized. Behavioural studies of the responses of American shad to ultrasound demonstrate that they show a graded series of responses depending on the sound level and, to a lesser degree, on the frequency of the stimulus. Low-intensity stimuli elicit a non-directional movement of the fish, whereas somewhat higher sound levels elicit a directional movement away from the sound source. Still higher level sounds produce a "wild" chaotic movement of the fish. These responses do not occur until shad have developed the adult utricle that has a three-part sensory epithelium. We speculate that the response of the American shad (and, presumably, other clupeids that can detect ultrasound) to ultrasound evolved to help these species detect and avoid a major predator – echolocating cetaceans. As dolphins echolocate, the fish are able to hear the sound at over 100 m. If the dolphins detect the fish and come closer, the nature of the behavioural response of the fish changes in order to exploit different avoidance strategies and lower the chance of being eaten by the predators.
Keywords: ear, fish, hearing, threshold, ultrasound, utricle
Received 18 March 2003; accepted 1 April 2004.
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Introduction |
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 Top Introduction Auditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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A number of studies have demonstrated that fish can be "classified" as hearing specialists or hearing non-specialists (or generalists) (Popper et al., 2003). Hearing non-specialists may detect sounds of 250–1500 Hz depending on the particular species, whereas hearing specialists are able to detect sounds of 3000 Hz or above, again depending on the specific species. All hearing specialists generally have better sensitivity (lower thresholds) than non-specialists. Until recently, it was generally assumed that even the best hearing species of fish could detect sounds to no more than about 5000 Hz (see Fay, 1988). This hearing limit was questioned with the discovery that ultrasonic signals at around 129 kHz could be used to keep certain clupeid species from entering the water intakes of power plants (e.g. Nestler et al., 1992; Ross et al., 1993, 1996). However, these results did not give any real indication of the hearing capabilities of clupeid fish, nor did they show how the fish detected such sounds. These studies did, however, lead to a number of behavioural and physiological investigations that are reviewed in this paper.
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Auditory sensitivity of clupeid fish |
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TopIntroductionAuditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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All fish in the order Clupeiformes have swimbladder and inner ear structures that have led to the suggestion that these fish have special hearing capabilities (e.g. O'Connell, 1955; Denton and Blaxter, 1979; Denton and Gray, 1979; Best and Gray, 1980; Blaxter et al., 1981; Astrup, 1999). These structural specializations include an extension of the swimbladder that terminates within the inner ear and a high degree of specialization within one end organ of the inner ear, the utricle, that makes the clupeiform utricle different from that found in all other vertebrates. The utricular specialization involves the sensory epithelium (or macula), which is a single sheet of tissue in most vertebrates but is divided into three distinct parts in the clupeiforms. The middle epithelium in clupeiforms has a thin connection that ties it to a membrane that lies between air-filled and fluid-filled bullae that are closely associated with the ear (e.g. Denton and Blaxter, 1979; Denton and Gray, 1979). It is thus possible that movements of this membrane as a result of motions of the air-filled chamber associated with the ear are directly imposed on the middle epithelium, causing it to move in response to the sound stimulus.
Early work suggested that the swimbladder and ear specializations in clupeids were related to detection of low frequencies and perhaps to pressure changes as fish moved through the water column (e.g. Denton and Gray, 1979). More recent behavioural and physiological work, however, suggests that the specializations in the ear and swimbladder are associated with ultrasound detection in some, but not all, clupeid species.
The first behavioural studies on hearing in clupeids to demonstrate ultrasound detection showed that the American shad (Alosa sapidissima) is able to detect sounds to at least 180 kHz (Mann et al., 1997). These studies, which were done with animals trained to respond when they detected a sound, showed that the American shad has good detection from 100 to 5000 Hz and from about 30 to 120 kHz, with a "notch" of relatively poor hearing sensitivity from 5 to 20 kHz (Figure 1). Although the American shad does not hear as well at low frequencies as other hearing specialists such as the goldfish (Carassius auratus) or other otophysan fish (e.g. Fay, 1988), its hearing range exceeds that of all other ultrasound-detecting vertebrates including dolphins and bats.
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Subsequent physiological studies (Mann et al., 1998, 2001) showed that at least one other clupeid, the gulf menhaden (Brevoortia patronus), is able to detect ultrasound, whereas species such as the bay anchovy (Anchoa mitchilli), scaled sardine (Harengula jaguana), and Spanish sardine (Sardinella aurita) are only able to detect sounds to about 4 kHz (Figure 1). Other evidence in the literature from intake studies at power plants suggests that blueback herring (Alosa aestivalis) and a number of other species in the genus Alosa are able to detect ultrasound (e.g. Nestler et al., 1992; Ross et al., 1993, 1996). Although behavioural results are limited to just a few species, it is clear that not all clupeids are able to detect ultrasound, although all can detect sounds up to 4 kHz and thus are classified as hearing specialists. The results also support the argument that clupeid species in the subfamily Alosinae have evolved the ability to detect ultrasound, although it is possible that the same ability occurs in other clupeid groups that have yet to be investigated.
Of course, one must ask why clupeids detect ultrasound. The most logical argument for detection of ultrasound is that clupeids are listening to something in their environment that produces such sounds. The only natural sources of such sounds in water are echolocating dolphins and other odontocetes that may emit sonar signals to well over 120 kHz, with the specific frequencies a function of the species and the acoustic environment (Au, 2000). It is widely known that a number of clupeid species are a major food source of dolphins in some parts of the world (e.g. Domenici et al., 2000), and it has been suggested that detection of ultrasound serves as a mechanism protecting clupeids from a major predator (Mann et al., 1997, 1998, 2001; Astrup, 1999).
Clearly, there are a number of important questions to be asked regarding ultrasound detection. First, why do some clupeids detect ultrasound and others not? Related to this is why a number of land-locked species such as the blueback herring detect ultrasound, whereas a number of marine species, such as the sardine and anchovy, do not detect such signals. And how did ultrasound detection evolve? Second, is there any evidence that clupeids actually hear and respond to dolphin echolocation signals? Third, what is the mechanism by which ultrasound is detected?
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Why do some clupeids detect ultrasound? |
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TopIntroductionAuditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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The specializations of the swimbladder and the utricle of the ear are found in all clupeid fish. Thus, one might argue that if these specializations are involved in ultrasound detection, all clupeids should detect ultrasound. Indeed, the results from the physiological studies suggest that all clupeids are hearing specialists and able to detect sounds to 4 kHz or higher (Mann et al., 2001). However, detailed examinations of the ear of different clupeid species suggest that although all have the same basic specializations (Denton and Blaxter, 1979; Denton and Gray, 1979), there is a striking structural difference in the suspension of the middle utricular epithelium between ultrasound-detecting and non-detecting species (Higgs et al., 2004). Although direct investigations of this ear region are exceptionally hard to perform, the available evidence supports the hypothesis that the utricle in ultrasound-detecting species has evolved a small but significant difference from other members of this group.
Related to this is the question as to why some species of clupeids can detect ultrasound and why some species that are clearly dolphin prey cannot. One way to consider this question is first to attempt to understand where clupeids may have evolved. There is evidence that clupeids evolved in freshwater rather than in the oceans. It is also becoming clear that there are strong selective pressures for fish living in shallow water to evolve higher frequency hearing than fish living in deeper water because there is poor propagation of low-frequency sounds in shallow waters (Rogers and Cox, 1988). If one assumes that hearing the sounds in the environment, beyond those used just for communication, is important for survival of a fish (Fay and Popper, 2000), then there is a selective advantage for a fish in shallow waters to hear higher frequencies (the specific frequency depends on water depth).
Indeed, there is evidence that a number of different, taxonomically unrelated fish groups that live in shallow waters have evolved structures to enhance their hearing range. These include the otophysans, all species of which have Weberian ossicles to acoustically couple the swimbladder to the inner ear (Popper et al., 2003); the mormyrids, which have a bubble of air tightly attached to the inner ear (Fletcher and Crawford, 2001); and some anabantoids, which have a bubble of air in the pharyngeal cavity (Saidel and Popper, 1987; Ladich and Yan, 1998). Although there is no fossil evidence that we know of to support the argument, one may speculate that the high-frequency hearing capabilities of clupeids (up to 4 or 5 kHz) could have evolved in shallow water.
Asking why some marine clupeids, all of which must have evolved from freshwater species, are able to detect ultrasound is difficult to say. The only suggestion to be made at this point is that at sometime early in the marine experience of ancestral Alosinae, the selection pressures imposed by echolocating dolphins resulted in changes in the ear that allowed for detection of ultrasonic frequencies. Other clupeid groups either did not encounter the same selective pressures at the same time or did not respond to the pressures in the same way as the Alosinae.
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Evidence for behavioural responses to ultrasound |
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TopIntroductionAuditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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During initial studies of ultrasound detection, Mann et al. (1997) showed that presentation of a high-frequency pure tone elicited strong behavioural responses from American shad. They also demonstrated that the sensitivity of the American shad to ultrasound was sufficient for detection of echolocating dolphins at more than 100 m.
More recent studies have shown that the responses are frequency selective and graded and strongly suggest that American shad show a variety of behavioural responses to ultrasound that is related to the distance between the dolphin and the fish (Plachta and Popper, 2003). In this study, schools of American shad were presented with pure tone pulses at different frequencies and amplitudes, and the behavioural responses were recorded on videotape for later analysis (see http://www.lfsc.umd.edu/biology/popperlab/shadavi for videos of the behavioural responses). American shad showed little response to sounds below 160 dB re 1 µPa at any frequency, but at 175 dB re 1 µPa at 30–120 kHz using stimuli of at least 1-s duration, the fish would show a mild reaction to the onset of sounds. Between 175 and 184 dB re 1 µPa at stimulus frequencies between 70 and 110 kHz, the fish showed a very rapid and directional response directly away from the sound source, whereas above 185 dB re 1 µPa, the fish would show a very rapid and random pattern of behaviours that resulted in some animals attempting to jump out of the test tank.
Although this study was done in the laboratory and needs replication in the field, a study with Pacific herring (Clupea pallasii) (Wilson and Dill, 2002) showed a reaction to ultrasound in a field situation. These results are similar to the laboratory results from Plachta and Popper (2003) suggesting that the different behaviours seen are likely to be accurate representations of the behaviour of fish in the field. Interestingly, Clupea is not a member of the Alosinae and the only data on hearing in a member of the genus Clupea suggests hearing only up to about 4 kHz (Enger, 1967; although it should be noted that Enger probably did not test hearing to ultrasonic frequencies).
This leads to the observation that there are several degrees of response of ultrasound-detecting clupeids depending on the level of the echolocation signal and, presumably, on the calculated distance of the predator. If the sound is of low amplitude, the fish do not respond in any particular way. However, when the echolocation sound gets more intense, the fish show an agitated response that leads to movement away from the sound source when it gets louder. Presumably, this would result in the fish increasing their distance from the dolphin. Finally, if the sound is sufficiently loud, presumably meaning that the predator is nearby, the school of fish goes into a chaotic pattern. Under such a circumstance, an echolocating dolphin would "see" not a single fish or a few fish with its sonar but, instead, a wildly random pattern that would make it hard for the predator to home in on a single fish or identify the position of any prey object.
It is worth noting that the responses to ultrasound described for American shad are reminiscent of the responses of moths and other ultrasound-detecting insects to the sounds of echolocating bats (e.g. Roeder, 1975; Yager et al., 1990). Like American shad, moths show a variety of behavioural responses to ultrasound depending on the distance between the moth and the bat. And the ultimate response, when the bat sound is loudest, is a random "dive" of the moth into the substrate, making it more difficult for the bat to find its prey.
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Mechanism of ultrasound detection |
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TopIntroductionAuditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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The mechanism by which clupeids detect ultrasound is still not clear. The parsimonious argument is that the inner ear must be involved because it is the detector in virtually all other vertebrates that are known to detect ultrasound. Moreover, there are no other structures known in clupeids that could potentially detect ultrasound (including the lateral line). Finally, the specializations in the swimbladder and ear and the differences between the ultrasound-detecting and the non-detecting species support an argument that the ear is the ultrasound detector.
Due to difficulties in actually getting to the ear for physiological recording or surgical manipulation in clupeids, there have yet to be direct studies of inner ear function other than one study of Clupea harengus (Enger, 1967). However, recent analysis of the response of the auditory portion of the brain in the American shad provides compelling evidence that ultrasound is detected via the ear (Plachta and Popper, 2002; Plachta et al., unpublished data). These studies involved direct recording of the physiological responses of neurons in the brain. Results showed that the majority of neurons that respond to ultrasonic stimuli did not respond to sonic range stimuli, whereas other nearby neurons only respond to lower frequency (sonic) sounds. Interestingly, the responses of the ultrasound neurons recorded in one brain area are similar to the responses of ultrasound-detecting neurons in the brains of bats (Grinnell, 1995), suggesting that similar ultrasound-processing mechanisms may have evolved several times over the course of vertebrate evolution.
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Acknowledgements |
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Portions of the work reported here were supported by NIH Grant DC-03936 from the National Institute of Deafness and Other Communication Disorders (NIDCD) to ANP, NIH Grant DC-04502 from the NIDCD to DMH, and NIDCD Training Grant DC-00046 to DAM and DH. We thank Helen Popper for editing the manuscript.
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References |
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TopIntroductionAuditory sensitivity of clupeid...Why do some clupeids...Evidence for behavioural...Mechanism of ultrasound...References |
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