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Coordinated mechanics of feeding, swimming, and eye movements in Tautoga onitis, and implications for the evolution of trophic strategies in fishes

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Abstract

Fish feeding behavior results from successful coordination of the fins, jaws, and sensory systems, and the organization of this behavior may affect the fish’s foraging abilities and trophic ecology. Using quantitative kinematic methods, movements of the jaws, fins and eyes of Tautoga onitis (Teleostei: Labridae) were analyzed during feeding events. Tautog feeding events consisted of three phases: approach, strike, and recovery, each defined by a combination of kinematic events. The approach was characterized by changes in fin movements and in body position, with the eyes directed forward at the food item. The strike began with the onset of jaw opening and protrusion, then cranial elevation, with the eyes no longer looking at the food item. The end of the strike and the beginning of the recovery involved a braking maneuver with the pectoral fins; the fish turns and swims away from the original food location item after prey capture. The coordination performance variables of tautog were quantitatively compared to published data from closely related cheiline wrasses and parrotfishes, which represent different feeding ecologies within a monophyletic assemblage. Fishes feeding on molluscs and benthic invertebrates (Cheilinus fasciatus and Tautoga onitis) represented an intermediate coordination condition, with herbivores (the parrotfishes, Scarus quoyi and Sparisoma radians) at one extreme, and fishes feeding on elusive prey (Epibulus insidiator and Oxycheilinus digrammus) at the other extreme. The analysis suggests that the biomechanical demands of coordination for feeding on benthic invertebrates may represent a generalized, and perhaps ancestral behavior in the wrasses, whereas more specialized trophic niches have evolved divergent, more specialized demands. Examining the movement and coordination of the jaws, fins, and eyes during fish feeding provides a detailed mechanistic basis for behavior, and comparison of coordination patterns during feeding among different taxa can measure how these trophic strategies differ. Understanding the evolution of feeding ecologies in these demersal fishes may have implications for understanding their role within their shallow water reef community.

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References

  • Alfaro ME, Janovetz J, Westneat MW (2001) Motor control across trophic strategies: muscle activity of biting and suction feeding fishes. Am Zool 41:1266–1279

    Google Scholar 

  • Auster PJ (1987) The effect of current speed on the small scale spatial distribution of fishes. In: DeLuca M, Babb I (eds) Symposia series for undersea research, vol 2. NOAA Office of Undersea Research, Rockville, pp 7–16

    Google Scholar 

  • Auster PJ (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (North Atlantic and Mid-Atlantic)––tautog and cunner. US Fish Wildl Serv Biol Rep 82(11.105) TR EL-82-4:1–13

  • Bellwood DR (1988) Ontogenetic changes in the diet of early post-settlement Scarus species (Pisces: Scaridae). J Fish Biol 33:213–219

    Article  Google Scholar 

  • Bellwood DR (2003) Origins and escalation of herbivory in fishes: a functional perspective. Paleobiology 29:71–83

    Article  Google Scholar 

  • Bernstein NB (1967) The coordination and regulation of movements. Pergamon Press, London

    Google Scholar 

  • Choat JH (1982) Fish feeding and the structure of benthic communities in temperate waters. Annu Rev Ecol Syst 13:423–449

    Article  Google Scholar 

  • Collin SP, Pettigrew JD (1988a) Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269–282

    Article  CAS  Google Scholar 

  • Collin SP, Pettigrew JD (1988b) Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density areae. Brain Behav Evol 31:283–295

    Article  CAS  Google Scholar 

  • Collin SP, Shand J (2003) Retinal sampling and the visual field in fishes. In: Collin SP, Marshall NJ (eds) Sensory processing in the aquatic environment. Springer, New York, pp 139–169

    Chapter  Google Scholar 

  • Cyrus DP, Blaber SJM (1982) Mouthpart structure and function and the feeding mechanisms of Gerres (Teleostei). S Afr J Zool 17:117–121

    Article  Google Scholar 

  • Daffertshofer A, Lamoth CJC, Meijer OG, Beek PJ (2004) PCA in studying coordination and variability: a tutorial. Clin Biomech 19:415–428

    Article  Google Scholar 

  • Deacutis CF (1983) Feeding behavior of red hake and tautog, and responses to oil-tainted food. Ph.D. dissertation. Graduate School of Oceanography, University of Rhode Island

  • Drucker EG, Walker JA, Westneat MW (2006) Mechanics of pectoral fin swimming in fishes. In: Shadwick RE, Lauder GV (eds) Fish biomechanics. Elsevier Academic Press, San Diego, pp 369–423

    Google Scholar 

  • Ferry-Graham LA, Wainwright PC, Westneat MW, Bellwood DR (2001) Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus digrammus (Teleostei: Labridae). J Exp Zool 290:88–100

    Article  CAS  Google Scholar 

  • Ferry-Graham LA, Bolnick DI, Wainwright PC (2002a) Using functional morphology to examine the ecology and evolution of specialization. Integr Comp Biol 42:265–277

    Article  Google Scholar 

  • Ferry-Graham LA, Wainwright PC, Westneat MW, Bellwood DR (2002b) Mechanisms of benthic prey capture in wrasses (Labridae). Mar Biol 141:819–830

    Article  Google Scholar 

  • Fineran BA, Nicol JAC (1974) Studies on the eyes of New Zealand parrot-fishes (Labridae). Proc R Soc B 186:217–247

    Article  CAS  Google Scholar 

  • Forner-Cordero A, Levin O, Li Y, Swinnen SP (2005) Principal component analysis of complex multijoint coordinative movements. Biol Cybern 93:63–78

    Article  CAS  Google Scholar 

  • Freadman MA (1979) Energetics of pectoral fin locomotion of cunners (Tautogolabrus adspersus) and tautogs (Tautoga onitis). Am Zool 19:897

    Google Scholar 

  • Freadman MA (1980) Acceleration patterns during pectoral fin locomotion of two wrasses. Am Zool 20:910

    Google Scholar 

  • Fulton CJ, Bellwood DR (2002) Patterns of foraging in labrid fishes. Mar Ecol Prog Ser 226:135–142

    Article  Google Scholar 

  • Fulton CJ, Bellwood DR (2004) Wave exposure, swimming performance, and the structure of tropical and temperate reef fish assemblages. Mar Biol 144:429–437

    Article  Google Scholar 

  • Gosline WA (1987) Jaw structures and movements in higher teleostean fishes. Jap J Ichthyol 34:21–32

    Google Scholar 

  • Green JM, Martel G, Martin DW (1984) Comparisons of the feeding activity and diets of male and female cunners Tautogolabrus adspersus (Pisces: Labridae). Mar Biol 84:7–11

    Article  Google Scholar 

  • Grubich JR (2001) Prey capture in Actinopterygian fishes: a review of suction feeding motor patterns with new evidence from an elopomorph fish, Megalops atlanticus. Am Zool 41:1258–1265

    Google Scholar 

  • Hanel R, Westneat MW, Sturmbauer C (2002) Phylogenetic relationships, evolution of broodcare behavior, and geographic speciation in the wrasse tribe Labrini. J Mol Evol 55:776–789

    Article  CAS  Google Scholar 

  • Higham TE (2007a) Feeding, fins and braking maneuvers: locomotion during prey capture in centrarchid fishes. J Exp Biol 210:107–117

    Article  Google Scholar 

  • Higham TE (2007b) The integration of locomotion and prey capture in vertebrates: morphology, behavior, and performance. Integr Comp Biol 47:82–95

    Article  Google Scholar 

  • Higham TE, Malas B, Jayne BC, Lauder GV (2005) Constraints on starting and stopping: behavior compensates for reduced pectoral fin area during braking of the bluegill sunfish Lepomis macrochirus. J Exp Biol 208:4735–4746

    Article  Google Scholar 

  • Janssen J (1997) Comparison of response distance to prey via the lateral line in the ruffe and yellow perch. J Fish Biol 51:921–930

    Article  Google Scholar 

  • Janssen J, Corcoran J (1993) Lateral line stimuli can override vision to determine sunfish strike trajectory. J Exp Biol 176:299–305

    CAS  PubMed  Google Scholar 

  • Konow N, Bellwood DR (2005) Prey-capture in Pomacanthus semicirculatus (Teleostei, Pomacanthidae): functional implications of intramandibular joints in marine angelfishes. J Exp Biol 208:1421–1433

    Article  Google Scholar 

  • Kotrschal K (1988) Evolutionary patterns in tropical marine reef fish feeding. Z Zool Syst Evolut Forsch 26:51–64

    Article  Google Scholar 

  • Lara MR (2001) Morphology of the eye and visual acuities in the settlement-intervals of some coral reef fishes (Labridae, Scaridae). Environ Biol Fishes 62:365–378

    Article  Google Scholar 

  • Liem KF, Sanderson SL (1986) The pharyngeal jaw apparatus of labrid fishes: a functional morphological perspective. J Morphol 187:143–158

    Article  Google Scholar 

  • Lobel PS, Ogden JC (1981) Foraging by the herbivorous parrotfish Sparisoma radians. Mar Biol 64:173–183

    Article  Google Scholar 

  • McFarland WN (1991) The visual world of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 16–38

    Chapter  Google Scholar 

  • Monroe TA (2002) Wrasses. Family Labridae. In: Collette BB, Klein-MacPhee G (eds) Bigelow and Schroeder’s fishes of the Gulf of Maine, 3rd edn. Smithsonian Institution Press, Washington, pp 448–466

    Google Scholar 

  • Munz FW (1958) Retinal pigments of a labrid fish. Nature 181:1012–1013

    Article  Google Scholar 

  • Munz FW, McFarland WN (1975) Part I: presumptive cone pigments extracted from tropical marine fishes. Vision Res 15:1045–1062

    Article  CAS  Google Scholar 

  • Myrberg AA Jr, Fuiman LA (2002) The sensory world of coral reef fishes. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, New York, pp 123–148

    Chapter  Google Scholar 

  • New JG (2002) Multimodal integration in the feeding behaviors of predatory teleost fishes. Brain Behav Evol 59:177–189

    Article  Google Scholar 

  • Olla BL, Bejda AJ, Martin AD (1974) Daily activity, movements, feeding, and seasonal occurrence in tautog, Tautoga onitis. Fish Bull 72:27–35

    Google Scholar 

  • Olla BL, Bejda AJ, Martin AD (1975) Activity, movements, and feeding behavior of cunner, Tautogolabrus adspersus, and comparison of food habits with young tautog, Tautoga onitis, off Long Island, New York. Fish Bull 73:895–900

    Google Scholar 

  • Rand DM, Lauder GV (1981) Prey capture in the chain pickerel, Esox niger: correlations between feeding and locomotor behavior. Can J Zool 59:1072–1078

    Article  Google Scholar 

  • Rice AN, Westneat MW (2005) Coordination of feeding, locomotor, and visual systems in parrotfishes (Teleostei: Labridae). J Exp Biol 208:3503–3518

    Article  Google Scholar 

  • Rice AN, Cooper WJ, Westneat MW (2008) Diversification of coordination patterns during feeding behaviour in cheiline wrasses. Biol J Linn Soc 93:289–308

    Article  Google Scholar 

  • Siebeck UE, Marshall NJ (2000) Transmission of ocular media in labrid fishes. Phil Trans R Soc B 355:1257–1261

    Article  CAS  Google Scholar 

  • Steimle FW, Shaheen PA (1999) Tautog (Tautoga onitis) life history and habitat requirements. NOAA Tech Mem NMFS NE 118:1–23

    Google Scholar 

  • Tauber ES, Weitzman ED (1969) Eye movements during behavioral inactivity in certain Bermuda reef fish. Commun Behav Biol A 3:131–135

    Google Scholar 

  • Thorsen DH, Westneat MW (2005) Diversity of pectoral fin structure and function in fishes with labriform propulsion. J Morphol 263:133–150

    Article  Google Scholar 

  • Turvey MT (1990) Coordination. Am Psychol 45:938–953

    Article  CAS  Google Scholar 

  • Utne-Palm AC (2002) Visual feeding of fish in a turbid environment: physical and behavioural aspects. Mar Freshw Behav Physiol 35:111–128

    Article  Google Scholar 

  • von Holst E (1973) On the nature of order in the central nervous system. The behavioural physiology of animals and man: the collected papers of Erich von Holst. University of Miami Press, Coral Gables, pp 3–32

    Google Scholar 

  • Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 42–59

    Google Scholar 

  • Wainwright PC (1996) Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77:1336–1343

    Article  Google Scholar 

  • Wainwright PC, Shaw SS (1999) Morphological basis of kinematic diversity in feeding sunfishes. J Exp Biol 202:3101–3110

    PubMed  Google Scholar 

  • Wainwright PC, Bellwood DR, Westneat MW (2002) Ecomorphology of locomotion in labrid fishes. Environ Biol Fish 65:47–62

    Article  Google Scholar 

  • Wainwright PC, Bellwood DR, Westneat MW, Grubich JR, Hoey AS (2004) A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biol J Linn Soc 82:1–25

    Article  Google Scholar 

  • Walker JA (1997) QuickSAND: quick smoothing and numerical differentiation for the Power Macintosh. Field Museum of Natural History, Chicago

    Google Scholar 

  • Walker JA (1998) Estimating velocities and accelerations of animal locomotion: a simulation experiment comparing numerical differentiation algorithms. J Exp Biol 201:981–995

    Google Scholar 

  • Walker JA, Westneat MW (2000) Mechanical performance of aquatic rowing and flying. Proc R Soc B 267:1875–1881

    Article  CAS  Google Scholar 

  • Walker JA, Westneat MW (2002) Performance limits of labriform propulsion and correlates with fin shape and motion. J Exp Biol 205:177–187

    PubMed  Google Scholar 

  • Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120

    Article  Google Scholar 

  • Westneat MW (1990) Feeding mechanics of teleost fishes (Labridae, Perciformes): a test of four-bar linkage models. J Morphol 205:269–295

    Article  Google Scholar 

  • Westneat MW (1994) Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 114:103–118

    Article  Google Scholar 

  • Westneat MW (1995a) Feeding, function, and phylogeny: analysis of historical biomechanics in labrid fishes using comparative methods. Syst Biol 44:361–383

    Article  Google Scholar 

  • Westneat MW (1995b) Phylogenetic systematics and biomechanics in ecomorphology. Environ Biol Fish 44:263–283

    Article  Google Scholar 

  • Westneat MW (2004) Evolution of levers and linkages in the feeding mechanisms of fishes. Integr Comp Biol 44:378–389

    Article  Google Scholar 

  • Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogenet Evol 36:370–390

    Article  Google Scholar 

  • Westneat MW, Alfaro ME, Wainwright PC, Bellwood DR, Grubich JR, Fessler JL, Clements KD, Smith LL (2005) Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae. Proc R Soc B 272:993–1000

    Article  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Acknowledgments

This study was funded by a University of Chicago Hinds Fund Grant, ASIH Raney Fund Award, and a SICB Grant in Aid of Research, and by grants NSF IBN-0235307 and ONR N000149910184 to M.W. Westneat. During the final stages of manuscript preparation, I was supported by NIMH training grant 5-T32-MH15793. Thanks to M.W. Westneat for collecting study specimens. W.J. Cooper, M.E. Hale, M. LaBarbera, J.L. Morano, J.G. New, and M.W. Westneat provided helpful discussion and comments. Experiments performed comply with U.S. Federal regulations, and those of the Field Museum of Natural History (Animal Care and Use Committee protocol number FMNH04-04).

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  1. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, 60637, USA

    Aaron N. Rice

  2. Department of Zoology, Field Museum of Natural History, Chicago, IL, 60605, USA

    Aaron N. Rice

  3. Department of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca, NY, 14853-2702, USA

    Aaron N. Rice

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Correspondence to Aaron N. Rice.

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Communicated by J.P. Grassle.

Appendix

Appendix

Tables 2 and 3.

Table 2 Eigenvector loadings for principal components analysis of coordination kinematics (movement of body, fins, jaws, head, and eyes) during feeding behaviors for Cheilinus fasciatus, Epibulus insidiator, Oxycheilinus digrammus, Scarus quoyi, Sparisoma radians, and Tautoga onitis
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Table 3 Eigenvector loadings for principal components analysis of feeding kinematics (movement of jaws and head only) during feeding behaviors for Cheilinus fasciatus, Epibulus insidiator, Oxycheilinus digrammus, Scarus quoyi, Sparisoma radians, and Tautoga onitis
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Rice, A.N. Coordinated mechanics of feeding, swimming, and eye movements in Tautoga onitis, and implications for the evolution of trophic strategies in fishes. Mar Biol 154, 255–267 (2008). https://doi.org/10.1007/s00227-008-0918-y

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