Comparative Anatomy, Development, and Systematic Significance of the Laterophysic Connection of Butterflyfishes and its Implications for Communication and Social Behavior

(Funded by NSF grants IBN 9603896 and IBN 0132607 to JFW)

Fishes that produce sounds in the context of social interactions must identify biologically relevant acoustic stimuli in the midst of the complex “soundscapes” that characterize coral reef ecosystems.  In 1998, we described the laterophysic connection (LC), a novel association of anterior swim bladder extensions and the lateral line system, which is found only in butterflyfishes of the genus Chaetodon (Webb, 1998). The morphological configuration of the LC suggests that it allows the lateral line system to be sensitive to sound pressure, WSKFigure3which is normally the realm of the inner ear.  We defined variation in the morphology of the LC among Chaetodon species (Webb 1998; Webb and Smith 2000), revised Chaetodon phylogeny, and revealed patterns of LC evolution (Smith et al. 2003). We used CT of live, anesthetized fishes to quantify the morphology of the swim bladder and swim bladder horns and their relationship to other tissues (Webb et al., 2006), and demonstrated that the ear of Chaetodon is unremarkable and lacks the features of the ears of hearing specialists (Webb, et al, 2010). We described the ontogenetic changes in the shape of the sensory maculae of the ear in C. ocellatus, demonstrating that that LC development occurs just after the transformation from the tholichthys stage to the juvenile stage in C. ocellatus, and showed that the hearing capabilities in this species are better than in damselfishes of the same size (Webb et al., 2012), suggesting a role for the swim bladder horns (and potentially the LC) in enhancement of hearing. Finally, we described the morphology of the swim bladder (using CT imaging) and the gas exchange epithelia (rete mirabile/red gland and oval) in several butterflyfishes in order to explore the morphological basis for the acoustic role of the swim bladder in these fishes  (Woods, MS Thesis 2006).

Cm11LMedialSacculusLagena copyCollaborator Tim Tricas (U. Hawaii) and his PhD student Kelly Boyle then documented the wide diversity of sounds produced by butterflyfishes including Chaetodon, and the challenges that these fishes face on acoustically noisy coral reefs. They experimentally demonstrated the contribution of the swim bladder horns associated with the laterophysic connection in Chaetodon to enhanced sensitivity to the hydrodynamic flow and pressure components of acoustic stimuli.  In doing so they provided the first evidence of acoustic communication in butterflyfishes, and the importance of acoustic communication in the social behavior in these prominent coral reef fishes. Tricas and Webb (2016) synthesized their work on sound production and sound reception in butterflyfishes that was stimulated by the discovery of the laterophysic connection, and investigations of its development, morphology, and evolution within the genus Chaetodon.

Publications from the Webb Lab

  1. Webb, JF. 1998.  Laterophysic Connection:  A unique link between the swim bladder and the lateral-line system in Chaetodon (Perciformes: Chaetodontidae).  Copeia 1998(4): 1032-1036.
  2. Webb, JF and Smith, W.L. 2000.  The laterophysic connection in chaetodontid butterflyfish:  Morphological variation and speculations on sensory function.  Phil. Trans. Roy. Soc. Lond. B 355: 1125-1129
  3. Smith, WL, Webb, JF, and Blum, SD. 2003.  The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes (Teleostei: Chaetodontidae). Cladistics.  19: 287-306.
  4. Webb, JF, Smith, WL, Ketten, DR. 2006. The laterophysic connection and swim bladder in butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae). J. Morphology. 267:1338–1355.
  5. Webb, JF, Herman, JL, Woods, CF and Ketten, DR.  2010. The ears of butterflyfishes: “Hearing generalists” on noisy coral reefs?  J. Fish Biol. 77: 1434-1451.
  6. Webb, JF, Walsh, RM, Casper, B and Mann, DA, Kelly, N, Cicchino, N. 2012. Ontogeny of the ear, hearing capabilities, and laterophysic connection in the Spotfin Butterflyfish (Chaetodon ocellatus). Environmental Biology of Fishes. 95: 275-290.
  7. Tricas, TC and Webb, JF. 2016. Acoustic communication in butterflyfishes: Anatomical novelties, physiology, and behavior. pp. 57-92. In: Sisneros, J. (ed.). Fish Hearing and Bioacoustics: An anthology in honor of Arthur N. Popper and Richard R. Fay. Advances in Experimental Medicine and Biology. Vol. 877. Springer Verlag. INVITED.

Additional Publications from the Tricas Lab

  1. Boyle, K.S., A.K. Dewan and T.C. Tricas. 2013. Fast Drum Strokes: Novel and convergent features of sonic muscle ultrastructure, innervation, and motor neuron organization in the pyramid butterflyfish (Hemitaurichthys polylepis). Journal of Morphology 274:377-394.
  2. Tricas, T.C. and K.S. Boyle. 2014. Acoustic behavior in Hawaiian coral reef fish communities. Marine Ecology Progress Series. 511:1-16
  3. Dewan, A.K. and T.C. Tricas. 2014. Cytoarchitecture of the telencephalon in the coral reef multiband butterflyfish (Chaetodon multicinctus: Perciformes). Brain Behavior and Evolution. 84:31-50
  4. Boyle, K.S and T.C. Tricas. 2014. Discrimination of mates and intruders: visual and olfactory cues for a monogamous territorial coral reef butterflyfish. Animal Behavior. 92:33-43
  5. Tricas, T.C. and K.S. Boyle. 2015a. Diversity and evolution of sound production in the social behavior of Chaetodon butterflyfishes. Journal of Experimental Biology 218:1572-1584
  6. Tricas, T.C. and K.S. Boyle. 2015b. Sound pressure enhances the hearing sensitivity of Chaetodon butterflyfishes on noisy coral reefs. Journal of Experimental Biology 218:1585-1595.

Press Coverage

Parks, N. 2006.  The Talk of the Sea.  ScienceNOW Daily News, Nov 30 2006.

Graduate and Undergraduate Students Trained in the Webb Lab

  1. Dr. William Leo Smith (BS, University of California, San Diego), Villanova MS 2001. Thesis – “Comparative morphology and evolution of the laterophysic connection in butterflyfishes” [Ph.D, 2005, Columbia Univ.; Asst. Curator of Fishes, Field Museum of Natural History, Chicago, now Associate Professor and Curator of Ichthyoloygy, U. Kansas]
  2. James Lucas Herman (BA, Franklin and Marshall College), Villanova MS 2005. Thesis – “The inner ear of chaetodontid butterflyfishes with a novel swim bladder-lateral line connection”  [now forensic scientist in NYC]
  3. Christopher Woods (BSc, University of Portsmouth, UK), Villanova MS 2006.  Thesis – “Function and bioacoustics of the swim bladder of butterflyfishes” [now biomedical lab tech in UK]
  4. Dr. Ryan M. Walsh (Undergraduate Honors Thesis), Villanova BS 2005 – Honors Thesis – “Development of the ear in the butterflyfish, Chaetodon ocellatus”. [MD, Eastern Virginia Medical School; Army physician in Washington State],
  5. Undergraduate Research Students – Natasha Kelly, Nicole Cicchino, Sandra Castelli, Erin Shearman

 

Conference Talks and Posters by the Webb Lab

  International Conferences/Symposia

  1. Webb, JF and Smith, WL. 1999.  Comparative morphology of the laterophysic connection, A unique swim bladder-lateral line connection in chaetodontid butterflyfishes.  First International Conference on Sensory Processing of the Aquatic Environment, Heron Island, Great Barrier Reef, Australia. INVITED.
  2. Webb, JF, Smith, WL and Ketten, DR. 2001.  The Laterophysic Connection, A Unique Swim Bladder-Lateral Line Connection in Butterflyfishes: An Evolutionary Novelty with Implications for Sensory Function.  International Congress of Vertebrate Morphology, Jena, Germany, July 2001.
  3. Webb, JF., Smith, WL and Ketten, DR. 2001. The Laterophysic Connection, A Unique Swim Bladder-Lateral Line Connection in Butterflyfishes: Morphological Variation and Putative Sensory Function.  International Congress of Neuroethology, Bonn, Germany.
  4. Webb, JF, Smith, WL, Tricas, TC, Ketten, DR. 2002. The laterophysic connection:  A novel specialization thought to enhance sound pressure sensitivity in butterflyfishes (Chaetodontidae, Chaetodon).  First Pan-American/Iberian Meeting on Acoustics, Symposium on Coral Reef Bioacoustics, at meeting of the Acoustical Society of America, Cancun, Mexico.  INVITED.

US Conferences/Symposia

  1. Smith, WL and Webb, JF. 1998. Lateral line and swim bladder modifications associated with the laterophysic connection of chaetodontid butterflyfishes.  American Society of Ichthyologists and Herpetologists, Guelph, Ont. Canada, 1998.
  2. Webb, JF and Smith, WL. 1999.  Comparative morphology of the laterophysic connection in Chaetodon:  Ecomorphological or phylogenetic explanations?  Society for Integrative and Comparative Biology, Denver, CO. (Amer. Zool. 38:107A).
  3. Smith, WL and Webb, JF 1999.  Morphology of the laterophysic connection, a novel lateral-line connection may support Chaetodon relationships.  American Society of Ichthyologists and Herpetologists, Penn. State University, 1999.
  4. Webb, JF, Smith, WL and Ketten, DR. 2000.  CT (Computerized Tomography) provides new views of the swimbladder in butterflyfishes (Chaetodon) with a novel specialization of the mechanosensory lateral line system. Society for Integrative and Comparative Biology, Atlanta, GA (Amer. Zool. 39: 16A).
  5. Smith, WL and Webb, JF 2001.  Phylogenetic variation in the morphology of the laterophysic connection in butterflyfishes of the genus Chaetodon. Society for Integrative and Comparative Biology, Chicago, IL. (Amer. Zool. 40: 1615)
  6. Webb, JF, Kelly, N, and Cicchino, N. 2001. Ontogeny of the laterophysic connection, a novel swim bladder-lateral line connection, in larvae and juveniles of the Caribbean butterflyfish, Chaetodon ocellatus.  American Society of Ichthyologists and Herpetologists, Penn. State University, 2001
  7. Webb, JF, Tricas, TC, Shearman, E, Walsh, RM, Ketten, DR, and Herman, JL. 2004.   Ear and Swim Bladder Morphology in Chaetodontid Fishes:  Adaptations for Enhancement of Hearing?  International Congress of Vertebrate Morphology, Boca Raton, FLA, 2004.
  8. Webb, JF, Herman, JL and Ketten, DR. 2005.  Ear and otolith morphology in a prominent group of coral reef fishes with a putative specialization for enhanced hearing. Society for Integrative and Comparative Biology, San Diego, CA,2005.
  9. Woods, CF, Webb, JF and Ketten, DR.  2005. The physoclistous swim bladder of chaetodontid butterflyfishes: Implications for acoustic function.  American Society of Ichthyologists and Herpetologists, 2005
  10. Webb, JF, Herman, JL, Walsh, RM, Ketten, DR, Casper, BM, Mann, DA.  2005. The ear and auditory capabilities of butterflyfishes with a laterophysic connection (Family Chaetodontidae). American Society of Ichthyologists and Herpetologists.
  11. Webb, JF, Smith, WL, Herman, JL, Woods CF and Ketten, DR. 2005.  The laterophysic connection: Peripheral specialization for reception of acoustic stimuli in chaetodontid butterflyfishes?  J.B. Johnston Club (at Society for Neurosciences). 2005.
  12. Webb, JF.  2006.  Comparative development of the cranial sensory systems of fishes: Beyond Zebrafish.  For “ Zebrafish in Comparative Context” Symposium (co-organizer).  Society for Integrative and Comparative Biology.
  13. Woods, CF, Webb, JF and Ketten, DR. 2006. The physoclistous swim bladder of chaetodontid butterflyfishes: Implications for acoustic function.  Acoustical Society of America, Honolulu, 2006. (poster presented by DR Ketten).
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