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FUNCTIONAL EVOLUTIONOF THE LATERAL LINESYSTEM: IMPLICATIONSFOR FISH BIOACOUSTICSJACQUELINE F. WEBB aa Department of Biology , VillanovaUniversity , Villanova , PA , 19085 , USA E-mail:Published online: 13 Apr 2012.

To cite this article: JACQUELINE F. WEBB (2002) FUNCTIONAL EVOLUTIONOF THE LATERAL LINE SYSTEM: IMPLICATIONS FOR FISH BIOACOUSTICS,Bioacoustics: The International Journal of Animal Sound and its Recording,12:2-3, 144-147, DOI: 10.1080/09524622.2002.9753676

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Bioacoustics The International Journal of Animal Sound and Its Recording, 2002, Vol. 12, pp. 143-163 0952-4622/02 $10 © 2002 AB Academic Publishers

SECTION III

BIOACOUSTICS AND THE LATERAL LINE SYSTEM

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FUNCTIONAL EVOLUTION OF THE LATERAL LINE SYSTEM: IMPLICATIONS FOR FISH BIOACOUSTICS

JACQUELINE F. WEBB1

1Department of Biology, Villanova University, Villanova, PA 19085 USA. jacqueline. webb@villanova.edu

FUNCTIONS OF THE MECHANOSENSORY LATERAL LINE SYSTEM

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The general ability of the lateral line system to respond to hydrodynamic flow (near-field acoustic stimuli) allows it to function in a variety of behavioural contexts including prey localisation, predator avoidance, communication during spawning, and navigation around environmental obstacles (Coombs and Montgomery 1999). In the past 15 years or so, physiological and modelling studies in a small number of species (e.g., herring, goldfish, mottled sculpin and ruffe) have provided a great deal of information about the functional attributes of the lateral line system in teleost fishes (reviewed by Coombs et al. 1992, Coombs and Montgomery 1999, Webb 2000). When information on the structural and functional attributes of lateral line systems is considered in the context of hypotheses of phylogenetic relationships, trends in the morphological and functional evolution of the lateral line system can be recognised.

PATTERNS OF EVOLUTIONARY CHANGE IN THE LATERAL LINE SYSTEM

The evolution of the lateral line system in teleost fishes is characterised by patterns of morphological change in canals and superficial neuromasts and the evolution of novel peripheral linkages of the lateral line system to the swim bladder. Evolutionary transitions in canal morphology, among the four types of head canal systems found in teleosts, for example (Webb 1989), is reflected by changes in the response properties of the system. A transition from a narrow to a widened canal system (with correlated changes in neuromast morphology (Webb 2000)) results in an increase in sensitivity but a slower response to near-field stimuli (Denton and Gray 1989). A shift from a narrow canal pattern to a reduced canal pattern represents a shift from a predominance of canal neuromasts, which respond to acceleration of water flow, to a predominance of superficial neuromasts, which respond to velocity (Kalmijn 1989). The evolutionary proliferation of superficial neuromasts which often

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accompanies the evolution of a reduced canal pattern (Webb 1989) represents the proliferation of velocity detectors.

In contrast, the evolution of peripheral linkages of the lateral line system with the swimbladder may broaden the functional repertoire of the system to include response to sound pressure (generally the realm of the inner ear) in addition to hydrodynamic flow. There are three examples of such linkages: the recessus lateralis of clupeiform fishes is known to make the lateral line system pressure sensitive (Denton and Blaxter 1976); the linkage in Ancistrus, a loricariid catfish (Bleckmann et al. 1991), whose contribution to lateral line function is unknown; and the laterophysic connection in butterflyfishes (Webb 1998).

All members of the butterflyfish genus Chaetodon (Family Chaetodontidae, Order Perciformes) have long or short bilateral anterior diverticula of the swimbladder ("horns") associated with a medial opening in the supracleithral lateral line canal, which defines a laterophysic connection (LC; Webb 1998). Well-defined interspecific variation in LC morphology is found among Chaetodon species. Two LC types are based on the proximity of horns to the medial opening in the supracleithrum: 1) a "direct LC", where horns make direct contact with a laterophysic "tympanum," which fills the medial opening in the supracleithrum, forming a barrier between the air-filled swimbladder horns and the fluid-filled lateral line canal; and 2) an indirect LC, where horns approach but do not make direct contact with the medial opening in the supracleithrum due to the presence of intervening muscle and/or kidney tissue. Six variants on LC types are defined by horn morphology and the presence/absence of mucoid connective tissue in the tympanum (Webb and Smith 2000, Smith et al. submitted).

Interestingly, the way in which swimbladder horns either approach or directly contact the fluid-filled lateral line canals in the supracliethra in Chaetodon is analogous to the way in which swimbladder horns approach or contact the otic capsules in holocentrids (an otophysic connection). Coombs and Popper (1979) showed that a holocentrid species in which the horns directly contact the otic capsule has lower hearing thresholds and broader frequency responses than a species in which the horns approach, but do not contact, the otic capsule. Thus, it is suggested that in Chaetodon sound pressure will be transmitted through the laterophysic connection more effectively in species with a direct LC, resulting in lower thresholds (and possibly a broader frequency response), than species with an indirect LC, in which intervening tissues probably dampen the transmission of stimuli into the lateral line canal.

Hydrodynamic flows (near-field stimuli) can stimulate both the lateral line and the inner ear via "direct stimulation" caused by whole body acceleration, without any structural specialisations of either the ear or lateral line system. However, functional overlap of the two

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systems in the far field appears to require the evolution of a peripheral linkage between the swimbladder and the lateral line system. Hypotheses to explain the functional basis for the evolution of the laterophysic connection, the most recently described swimbladder­lateral line linkage, await experimental confirmation.

ACKNOWLEDGEMENTS

Supported by NSF grant IBN 9603896 and Villanova University.

REFERENCES

Coombs, S. & Montgomery, J.C. (1999) The enigmatic lateral line system. In Comparative Hearing: Fish and Amphibians (R.R. Fay and A.N. Popper, eds). Springer-Verlag; New York, pp. 319-362.

Coombs, S. & Popper, A.N. (1979) Hearing differences among Hawaiian squirrelfishes (Family Holocentridae) related to differences in the peripheral auditory system. J. Comp. Physiol. 132, 203-207.

Coombs, S., Janssen, J. & Montgomery, J. (1992) Functional and evolutionary implications of peripheral diversity in lateral line systems. In The Evolutionary Biology of Hearing (D.B. Webster, R.R. Fay and A.N. Popper, eds). Springer-Verlag; New York, pp. 267-294,

Denton, E.J. & Blaxter, J.H.S. (1976) The mechanical relationships between the clupeid swimbladder, inner ear and lateral line. J. Mar. Biol. Assoc. U.K. 56, 787-807.

Denton, E.J. & Gray, J.A.B. (1989) Some observations on the forces acting on neuromasts in fish lateral line canals. In The Mechanosensory Lateral Line: Neurobiology and Evolution (S. Coombs, P. Gi:irner and H. Miinz, eds). Springer­Verlag; New York, pp. 229-246.

Kalmijn, A.J. (1989) Functional evolution of lateral line and inner ear sensory systems. In The Mechanosensory Lateral Line: Neurobiology and Evolution (S. Coombs, P. Gi:irner, and H. Miinz, eds). Springer-Verlag; New York, pp. 187-216.

Smith, W.L., Webb, J.F. & Blum, S.D. The phylogeny and classification of butterflyfishes (Perciformes, Chaetodontidae) and the evolution of the laterophysic connection. Submitted to Systematic Biology.

Webb, J.F. (1989) Gross morphology and evolution of the mechanoreceptive lateral line system in teleost fishes. Brain Behav. Evol. 33, 34-53.

Webb, J.F. (1998) Laterophysic connection: A unique link between the swimbladder and the lateral-line system in Chaetodon (Perciformes: Chaetodontidae). Copeia 1998, 1032-1036.

Webb, J.F. (2000). Mechanosensory Lateral Line: Functional Morphology and Neuroanatomy. In Handbook of Experimental Animals - The Laboratory Fish (G. Ostrander, ed) Academic Press; London, pp. 236-244.

Webb, J.F. & 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.

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