Ear Morphology of Butterflyfishes: evolution for specialization of generalization?

The article I chose to summarize discusses the evolution of complex ear morphology of fish who possess an otophysic connection between the inner ear and swim bladder used for communication . The article particularly tries to determine if the complex ear morphology also evolved in fish who used communication with the swimbladder but did not have an otophysic connection, specifically the Butterflyfish.

The coral reefs serve as a very noisy habitat, with sounds produced by many biotic and abiotic factors (Webb et al. 2010). This vast amount of background noise might make it hard for a fish to communicate acoustically with its swimbladder if the other fish cannot pick up on its vibrations. Fortunately, many fish have adapted to these conditions with specialized hearing mechanisms. The common specialization is an otophysic connection to the swim bladder (a connection of the swimbladder to inner ear) and large dense otoliths within their inner ear (Webb et al. 2010). This allows for lower thresholds for hearing and the ability to hear a broader frequency range (Coombs & Popper, 1979). The butterflyfishes are also known to communicate acoustically but are not known to possess the otophysic connection or specialized inner ear structure commonly associated with hearing specialists. J.F. Webb, J.L. Herman, C.F. Woods, and D.R. Ketten conducted an experiment which attempts to reveal whether Chaetodon

(butterflyfishes) species are likely to have enhanced auditory capabilities like fish with an otophysic connection.

It is typical that the presence of an otophysic connection is correlated with both enhanced hearing and modified ear morphology (Popper, 1977). The otophysic connection is an anterodorsal diverticula, or `horns’, of the swimbladder that approach or come in direct contact with the region of the skull containing the inner ear (Webb et al. 2006). Basically, the swimbladder amplifies the sound like a drum and is able to transfer these vibrations to the inner ear. The inner ear is composed of 3 dense calcium carbonate structures known as otoliths. The solid structure vibrates in response to sound pressure waves. Otoliths sit on sensory hairs (sensory macula) that have a connection to nerve cells which then can relay the detection of sound to the brain (Webb et al. 2006). To have specialized hearing associated with an otophysic connection it would be important for the otoliths, which respond well to sound, to be specialized and/or modified as well. The correlation between modified ear morphology, the presence of an otophysic connection, and advanced hearing capabilities among taxa can suggest that knowledge of the morphology of the ear and swimbladder can be used to predict whether a fish has enhanced auditory capabilities (Webb et al. 2010).

Butterflyfishes do not fit into that predictive ideal quite as easily as most fish. The butterflyfish (family Chaetodontidae) have a laterophysic connection (LC), which interact with the swimbladder horns differently and appear to have a connection to the lateral line canals. This method is believed to enhance sound detection using a combination of acoustic inputs to both the lateral line and inner ear (Webb et al. 2010).

The question that Webb et al (2010) proposes is if butterflyfish may also have a modified ear structure like the otophysic hearing specialists. Popper (1977) examined the otoliths of the millet butterflyfish (Chaetodon miliaris) and reported that it has an unmodified ear similar to other percomorph fishes that lack an otophysic connection. But, this particular species' behavior is not similar to other butterflyfish behaviors, who are monogomous, pair-forming coral-eaters. Instead, C. miliaris eats plankton and spawn in groups. Webb et al. (2010) discusses that this difference is likely to influence the ways in which C. miliaris uses sound. He discusses that it is also possible that variation in ear morphology and hearing capabilities exists among Chaetodon species with different LC variants (e.g.direct vs. indirect LC, long wide swimbladder horns vs. long thin horns vs. short horns). If this hypothesis is true, then C. miliari may not be representative of the genus. This discrepancy warranted further study of the ear among Chaetodon species to see if there is a possibility that butterflyfishes may have a more complex ear structure then the morphology described by Popper (1977).

The study was performed by J.F. Webb, J.L. Herman, C.F. Woods, and D.R. Ketten compared the ear morphology of three representative Chaetodon species and one species of Forcipigier (which lacks swimbladder horns). Scanning electron microscopes and computed tomographic imaging was used to analyze ear morphology and spatial relationship of the ear and swimbladder. The fish were collected in the waters around Oahu, Hawaii, dissected and then imaged. The sizes and shapes were then recorded for further analysis (Webb et al. 2010).

The morphology of the three otolithic organs (sacculus, lagena and utriculus) and the hair cell orientation patterns in their sensory maculae were found to be similar among the three Chaetodon and one Forcipiger species examined (Webb et al. 2010). These aspects of ear morphology are similar to those reported by Popper (1977) for C. miliaris, despite the fact that its feeding and reproductive habits are different from that of the majority of Chaetodon species. Thus, it is expected that ear morphology is indeed the same among all members of the genus and perhaps among all members of the Chaetodontidae (Webb et al. 2010).

Three-dimensional reconstructions of the swimbladder and otoliths (Fig. 1) illustrate the relationships of the swimbladder horns to the ears. The minimum distance from the swimbladder or horns to the inner ear appeared to be smaller for Chaetodon than for Forcipiger (Webb et al. 2010). The distance is similar to that of an otophysic connection but figure 1 shows that the simple anterior swimbladder horns in Chaetodon spp. (Fig. 1(a),(b)) sit dorsal and lateral to the otoliths, unlike the swimbladder horns in Myripristis (which has a well developed otophysic connection) that wrap around and come into contact with the otic capsule (Fig. 1(d),(e)), which characterize the otophysic connection in this genus (Webb et al. 2010). The swimbladder horns of Chaetodon spp. (which define the laterophysic connection) do not have an intimate association with the otic capsule as in fishes with an otophysic connection. Rather, the swimbladder horns only approach the ears (within 1–2 mm), but in doing so, may enhance pressure sensitivity (Webb et al. 2010).

Figure 1. Three-dimensional reconstruction of computed tomographic imaging slices demonstrating the relationship of otoliths (red) to the volume of air within the swimbladder. Reprinted from Webb et al. 2010

The anatomical data that Webb et al (2010) presents, which suggest that Chaetodon and Forcipiger have unremarkable hearing capabilities (with regard to threshold and frequency range), are supported by preliminary physiological studies on the hearing capabilities of chaetodontids (Smith et al. 2006). Juvenile spotfin butterflyfish Chaetodon ocellatus (a Caribbean species with the same swimbladder horn and LC morphology as C. miliaris and C. multicinctus) have a relatively narrow audiogram with best frequency at 100–200 Hz (Smith et al. 2006), which is not unusual for teleosts lacking an otophysic connection. The best sensitivity for adult C. multicinctus, C. auriga and F. flavissimus is 200–600 Hz (Webb et al. 2010). This is a bit higher than that reported for C. ocellatus juveniles and a broader range that is typical for a laterophysic connection. Webb et al. (2010) suggest that this difference may be accounted for by some combination of methodological differences, species differences and ontogenetic effects.

The evidence supports that butterflyfish do not have modified inner ears, but referring to them as hearing generalists may not be correct. Fishes with otophysic connections have been considered to be ‘hearing specialists'. In contrast, fishes that lack an otophysic connection (and those that lack a swimbladder entirely) tend to have unremarkable auditory capabilities and have been considered to be ‘hearing generalists' (Poper & Fay 2010). Popper and Fay, (2010) however, have recently proposed that this dichotomous description be abandoned and suggest that variation in the auditory capabilities of fishes lie along a wide spectrum. Popper and Fay relate to the instance of the butterflyfish who use sound communication, have a laterophysic connection, and no specialized ear morphology as an example of why the dichotomous description of hearing is outdated.

Webb et al. (2010) findings concluded that the origin and diversification of the laterophysic connection in Chaetodon occurred in the absence of modifications in ear morphology and evidence for the enhancements of auditory capabilities like those in species with otophysic connections. Nevertheless, the fact that these fishes produce sound demonstrates that acoustic communication is important. The dependence on auditory communication probably favored the evolution of pairing behavior, a strategy that would increase the efficiency of communication in noisy coral reef environments (Webb et al. 2010). Such behavior is likely to exploit sensitivity to both particle displacement (hearing with the ears, given the short distances between animals) and pressure reception (via the swimbladder horns which amplifies sound to ears). Whatever the mechanism or mechanisms of acoustic detection in these fishes, the question of how fishes respond to increasing levels of sound on naturally noisy coral reefs is raised. There is possibility of affecting the social and reproductive behaviors of these important coral reef fish.

Literature Cited

Coombs, S. and A.N. Popper. 1979. Hearing differences among Hawaiian squirrelfishes(family Holocentridae) related to differences in the peripheral auditory anatomy.Journal of Comparative Physiology 132:203–207

Popper, A. N. 1977. A scanning electron microscopic study of the sacculus and lagena inthe ears of fifteen species of teleost fishes. Journal of Morphology 153:497–418

Popper, A. N. and R.R. Fay. 2010. Rethinking sound detection by fishes. Hearing Research doi: 10.1016/j.heares.2009.12.023 (in press).

Smith, W. L., Webb, J. F. and S.D. Blum. 2003. The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes. Cladistics 19: 287–306.

Webb, J.F., Herman, J.L., Woods, C.f. and D.R. Ketten. 2010. The ears of butterflyfish (Chaetodontidae): 'hearing generalists' on noisy coral reefs? Journal of Fish Biology 77: 1406-1423

We

Webb, J. F., Smith, W. L. and D. R. Ketten. 2006. The laterophysic connection and swimbladder in butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae). Journal of Morphology 267:1338–1355.