JOURNAL OF MORPHOLOGY 267:1338–1355 (2006) The Laterophysic Connection and Swim Bladder of Butterflyfishes in the Genus Chaetodon (Perciformes: Chaetodontidae) Jacqueline F. Webb,1* W. Leo Smith,1–3 and Darlene R. Ketten4,5 1Department of Biology, Villanova University, Villanova, Pennsylvania 19085 2Department of Ichthyology, American Museum of Natural History, New York, New York 10024 3Center for Environmental Research and Conservation, Columbia University, New York, New York 10027 4Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543 5Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts ABSTRACT The laterophysic connection (LC) is an standing of how fishes interpret sound. An acoustic association between bilaterally paired, anterior swim stimulus (e.g., modeled as a vibrating sphere, Kal- bladder extensions (horns) and medial openings in the mijn, 1989) has two components—hydrodynamic supracleithral lateral line canals that diagnoses butterfly- flow (the ‘‘near field’’) and a propagating sound pres- fishes in the genus Chaetodon. It has been hypothesized sure wave (the ‘‘far field’’). Hydrodynamic flow is that the LC makes the lateral line system sensitive to sound pressure stimuli that are transmitted by the swim generated by the movement of water near the bladder horns and converted to fluid flow into the lateral acoustic stimulus source and sound pressure waves line system via a laterophysic tympanum. The purpose of propagate from the acoustic source as a cyclic com- this study was to define variation in the morphology of pression and rarefaction of water molecules. The the LC, swim bladder and swim bladder horns among 41 mechanosensory lateral line is generally sensitive Chaetodon species from all 11 Chaetodon subgenera and a to hydrodynamic flow (local displacement) within 1– species from each of four non-Chaetodon genera using 2 body lengths from the source. The inner ear is also gross dissection, histological analysis as well as 2D or 3D sensitive to hydrodynamic flow as a result of whole CT (computed tomographic) imaging of live, anesthetized body acceleration, but sound pressure-induced oscil- fishes. Our results demonstrate that the lateral line sys- lations of the air volume within the swim bladder tem appears rather unspecialized with well-ossified nar- row canals in all species examined. Two LC types (direct generates a secondary local displacement field that and indirect), defined by whether or not the paired ante- is capable of stimulating the inner ear (reviewed by rior swim bladder horns are in direct contact with a Schellart and Popper, 1992; Popper and Fay, 1999; medial opening in the supracleithral lateral line canal, Popper et al., 2003). are found among species examined. Two variants on a The ability to detect sound pressure stimuli is direct LC and four variants of an indirect LC are defined enhanced by the presence of intimate associations by combinations of soft tissue anatomy (horn length [long/ of a volume of air (in the swim bladder, swim blad- short] and width [wide/narrow], number of swim bladder der horns or branchial diverticulae, reviewed by chambers [one/two], and presence/absence of mucoid con- Schellart and Popper, 1992) and the otic capsule, nective tissue in the medial opening in the supracleith- known as otophysic connections, which increase the rum). The combination of features defining each LC vari- ant is predicted to have functional consequences for the auditory sensitivity and frequency response of the bioacoustics of the system. These findings are consistent inner ear (Poggendorf, 1952; Coombs and Popper, with the recent discovery that Chaetodon produce sounds 1979) and the distance over which sound pressure during social interactions. The data presented here pro- stimuli can be detected (Coombs et al., 1992, Popper vide the comparative morphological context for the and Fay, 1993, Coombs and Montgomery, 1999). functional analysis of this novel swim bladder-lateral Otophysic connections occur in at least 50 fami- line connection. J. Morphol. 267:1338–1355, 2006. Ó 2006 lies in all major teleostean lineages (Schellart and Wiley-Liss, Inc. KEY WORDS: Chaetodon; lateral line; hearing; swim Contract grant sponsor: National Science Foundation; Contract bladder; laterophysic connection; CT imaging; butterflyfish grant numbers: IBN-9603896, IBN-0132607. *Correspondence to: Jacqueline F. Webb, Department of Biological Sound stimuli are important in the social behav- Sciences, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881. E-mail: [email protected] ior of a wide variety of fishes (Myrberg, 1981; Haw- kins, 1993; Ladich and Bass, 2003; Ladich and Pop- Published online 18 October 2006 in per, 2004), but the complex physical features of Wiley InterScience (www.interscience.wiley.com) underwater acoustics have confounded our under- DOI: 10.1002/jmor.10480 Ó 2006 WILEY-LISS, INC. CHAETODON LATEROPHYSIC CONNECTION 1339 TABLE 1. Acanthomorph families with representatives surfaces of the supracleithra’’ (Fig. 1). Webb and that have anterior swim bladder horns Blum (1990) and Webb (1998) further described this (modified from Smith, 2000) feature in Chaetodon using histological analysis, Family Reference calling it the ‘‘laterophysic connection’’ (LC) to draw attention to its apparent structural and putative Acropomatidae Katayama, 1959 Centropomidae Katayama, 1959 functional similarity to the simple otophysic connec- Chaetodontidae Gunther, 1860; Blum, 1988 tions in other fishes. Two LC types were described Cichlidae Dehadrai, 1959 (direct and indirect), based on whether or not the Ephippidae Herre and Montalban, 1927 swim bladder horns are in direct contact with the Gerreidae Green, 1971 Haemulidae Johnson, 1980 medial opening in the supracleithrum (Webb, 1998). Holocentridae Nelson, 1955 Among species with an indirect LC, most species Kuhliidae Gosline, 1966 have long horns, but a few species have short horns Lactariidae Leis, 1994 (Webb and Smith, 2000; Smith et al., 2003). Menidae Johnson, pers. commun. The two LC types found among Chaetodon species Moridae Parker, 1882 Moronidae Katayama, 1959 are analogous to the kind of variation found in the Nemastiidae Rosenblatt and Bell, 1976 simple otophysic connections among holocentrid Percichthyidae MacDonald, 1978 subfamilies (Nelson, 1955). Coombs and Popper Polyprionidae Katayama, 1959 (1979) demonstrated that Myripristis (subfamily Priacanthidae Starnes, 1988 Scombridae Collette and Nauen, 1983 Myripristinae), which has robust anterior swim Sciaenidae Sasaki, 1989; Chao, 1986, 1995 bladder horns that come into intimate contact with Sillaginidae McKay, 1985 the otic capsule (Nelson, 1955; unpub. data) and Sparidae Tavolga, 1974 modified inner ear morphology (Popper, 1977), dem- onstrates higher sensitivity to sound stimuli over a broader frequency range, when compared to Sargo- Popper, 1992). For instance, clupeiform fishes have centron (Adioryx, subfamily Holocentrinae), which complex otophysic connections in which anterior lacks swim bladder horns (Nelson, 1955; unpub. extensions of the swim bladder (otic bullae) invade observ.) and has unmodified inner ear morphology the otic capsule and directly contact thefluids of the (Popper, 1977). Ramcharitar et al. (2002, 2004) has inner ear and the cranial lateral line canals forming also demonstrated correlations among auditory the ‘‘recessus lateralis’’ (e.g., O’Connell, 1955; Best capabilities (thresholds and frequency response), and Gray, 1980). Otophysan fishes have modified and morphology of the swim bladder and ear among vertebral elements that form the Weberian appara- several genera of drums (family Sciaenidae). tus, which mechanically link the swim bladder with Webb (1998) suggested that the LC in Chaetodon the otic capsules (e.g., Alexander, 1962; Rosen and transmits pressure from the air-filled swim bladder Greenwood, 1970; Fink and Fink, 1996). to the fluid-filled lateral-line canal via the anterior Simple otophysic connections in which anterior swim bladder horns at the LC, initiating fluid move- swim bladder horns contact the otic capsule or invade ments in the lateral-line canal that are capable of the otic capsule (as bullae) are found in osteoglosso- stimulating canal neuromasts in the vicinity of the morphs and elopomorphs (Bridge, 1900; Greenwood, LC. She hypothesized that the presence of anterior 1970) and have been shown to enhance auditory capa- swim bladder extensions and a LC in Chaetodon bilities in mormyrids (Yan and Curtsinger, 2000; makes the lateral line sensitive to sound pressure. Fletcher and Crawford, 2001). Simple otophysic con- This would expand the functional repertoire of the nections have also been investigated experimentally lateral line system to include the reception of sound in a few acanthomorph taxa (holocentrids, Coombs pressure stimuli. The observation that swim bladder and Popper, 1979, and sciaenids, Ramcharitar et al., morphology is correlated with LC type (Webb and 2002, 2004). Interestingly, anterior swim bladder Smith, 2000) suggests that swim bladder bioacoustics horns are known in representatives of at least 21 play an important role in LC function, thus demand- other acanthomorph families (Table 1), suggesting ing a closer examination of the swim bladder itself. that modifications of the swim bladder that enhance hearing may be even more widespread among fishes. In butterflyfishes of the genus Chaetodon,swimblad- Visualization of Swim Bladder Morphology der horns form an association,