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Feeding Mechanism and Functional Morphology of the Jaws of the Lemon Shark Negaprion Brevirostris (Chondrichthyes, Carcharhinidae) Philip J

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Feeding Mechanism and Functional Morphology of the Jaws of the Lemon Shark Negaprion Brevirostris (Chondrichthyes, Carcharhinidae) Philip J University of South Florida Scholar Commons Integrative Biology Faculty and Staff ubP lications Integrative Biology 1997 Feeding Mechanism and Functional Morphology of the Jaws of the Lemon Shark Negaprion Brevirostris (Chondrichthyes, Carcharhinidae) Philip J. Motta University of South Florida, [email protected] Timothy C. Tricas Florida Institute of Technology Robert E. Hueter Mote Marine Laboratory Adam P. Summers University of Massachusetts Follow this and additional works at: https://scholarcommons.usf.edu/bin_facpub Scholar Commons Citation Motta, Philip J.; Tricas, Timothy C.; Hueter, Robert E.; and Summers, Adam P., "Feeding Mechanism and Functional Morphology of the Jaws of the Lemon Shark Negaprion Brevirostris (Chondrichthyes, Carcharhinidae)" (1997). Integrative Biology Faculty and Staff Publications. 307. https://scholarcommons.usf.edu/bin_facpub/307 This Article is brought to you for free and open access by the Integrative Biology at Scholar Commons. It has been accepted for inclusion in Integrative Biology Faculty and Staff ubP lications by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. The Journal of Experimental Biology 200, 2765–2780 (1997) 2765 Printed in Great Britain © The Company of Biologists Limited 1997 JEB1095 FEEDING MECHANISM AND FUNCTIONAL MORPHOLOGY OF THE JAWS OF THE LEMON SHARK NEGAPRION BREVIROSTRIS (CHONDRICHTHYES, CARCHARHINIDAE) PHILIP J. MOTTA1,*, TIMOTHY C. TRICAS2, ROBERT E. HUETER3 AND ADAM P. SUMMERS4 1Department of Biology, University of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620, USA, 2Department of Biological Sciences, Florida Institute of Technology, 150 West University Boulevard, Melbourne, FL 32901, USA, 3Center for Shark Research, Mote Marine Laboratory, 1600 Thompson Parkway, Sarasota, FL 34236, USA and 4Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003-5810, USA Accepted 7 August 1997 Summary This study tests the hypothesis that preparatory, distance during jaw closure and is concurrent with muscle expansive, compressive and recovery phases of biting activity in the dorsal and ventral preorbitalis and the behavior known for aquatically feeding anamniotes are levator palatoquadrati. Hydraulic transport events are conserved among extant elasmobranch fishes. The feeding shorter in duration than ram ingestion bites. Prey mechanism of the lemon shark Negaprion brevirostris is ingestion, manipulation and hydraulic transport events are examined by anatomical dissection, electromyography and all found to have a common series of kinematic and motor high-speed video analysis. Three types of feeding events are components. Individual sharks are capable of varying the differentiated during feeding: (1) food ingestion primarily duration and to a lesser extent the onset of muscle activity by ram feeding; (2) food manipulation; and (3) hydraulic and, consequently, can vary their biting behavior. We transport of the food by suction. All feeding events are propose a model for the feeding mechanism in composed of the expansive, compressive and recovery carcharhinid sharks, including upper jaw protrusion. This phases common to aquatically feeding teleost fishes, study represents the first electromyographic and kinematic salamanders and turtles. A preparatory phase is analysis of the feeding mechanism and behavior of an occasionally observed during ingestion bites, and there is elasmobranch. no fast opening phase characteristic of some aquatically feeding vertebrates. During the compressive phase, Key words: elasmobranch, electromyography, kinematics, variability, palatoquadrate protrusion accounts for 26 % of the gape jaw protrusion, feeding, lemon shark, Negaprion brevirostris. Introduction To understand the function and evolution of feeding Orectolobiformes and Heterodontiformes, the dominant mechanisms in vertebrates, we must have a thorough predaceous sharks of modern seas (Compagno, 1988; Shirai, understanding of the anatomy and functional morphology of 1996). From the earliest cladodont ancestor that grasped and the feeding apparatus of fishes. Our knowledge of the evolution possibly swallowed its prey whole or tore pieces from it of aquatic feeding mechanisms, however, is limited by a lack (Schaeffer, 1967; Moy-Thomas and Miles, 1971), sharks have of studies on cartilaginous fishes. The Chondrichthyes radiated to cover a variety of prey ingestion mechanisms diverged from a common ancestor with the Teleostomi before including biting, gouging and biting, ram-feeding, suction- the Devonian period and have retained the same major skeletal feeding and filter-feeding. features for over 400 million years (Schaeffer and Williams, The transition from an amphistylic jaw suspension in the 1977; Long, 1995). Elasmobranchs have undergone two major earliest sharks to hyostyly in modern sharks (galeoids and episodes of adaptive radiation, one of these being in the squaloids) (see Compagno, 1977; Maisey, 1980, regarding jaw ctenacanthid lineage that gave rise to neoselachians (modern suspension terminology) presumably resulted in the sharks, skates and rays) (Carroll, 1988). Within the exploitation of new feeding niches. Associated with this change neoselachians, the most speciose group is the Galeomorpha, in jaw suspension was a shortening of the jaws, palatoquadrate which includes the Lamniformes, Carcharhiniformes, or upper jaw protrusion, a dentition suited for shearing and *e-mail: [email protected] 2766 P. J. MOTTA AND OTHERS sawing, and presumably greater bite force (Schaeffer, 1967; 1993a,b; Cortés and Gruber, 1990), (3) preliminary functional Moy-Thomas and Miles, 1971). The evolution of a highly data exist on its biting behavior (Motta et al. 1991) and (4) it kinetic upper jaw and upper jaw protrusibility in elasmobranchs is readily available and thrives in captivity. is convergent with these same features in bony fishes (Schaeffer The goal of this study was to investigate the feeding and Rosen, 1961; Schaeffer, 1967). mechanism of a carcharhinid shark, N. brevirostris, under Compared with studies on teleosts, there have been fewer semi-natural conditions. We tested the following hypotheses: anatomical studies on elasmobranch feeding structures (1) the kinematic pattern of preparatory, expansive, (reviewed in Motta and Wilga, 1995). There are even fewer compressive and recovery phases common to other aquatically data on the natural feeding behavior of sharks (Springer, 1961; feeding vertebrates is conserved in N. brevirostris during the Gilbert, 1962; Tricas, 1985; Frazzetta, 1994), and the only three feeding events of prey ingestion, manipulation and studies on the functional morphology and kinematics of the hydraulic transport; (2) there is inter-individual variability of feeding apparatus have been based either on manual kinematic and motor patterns in the feeding events, such that manipulation of dead specimens or on cine analyses of live muscle activity and kinematic events vary only in duration, not feeding sharks (Moss, 1977; Tricas and McCosker, 1984; in relative timing; (3) the three feeding events have a common Tricas, 1985; Frazzetta and Prange, 1987; Wu, 1994). series of kinematic and motor patterns but are distinguishable In contrast to our relatively limited knowledge of feeding in by their duration and relative timing; and (4) upper jaw sharks, extensive studies on aquatic feeding in teleosts, protrusion is effected by contraction of the preorbitalis, salamanders and turtles have revealed common patterns. Four levator palatoquadrati, levator hyomandibuli and distinct phases occur during suction or ram prey capture: the quadratomandibularis muscles. From the analysis of our preparatory, expansive, compressive and recovery phases (Liem, results, we propose a quantitative functional model of the 1978; Lauder, 1985; Lauder and Shaffer, 1985; Lauder and feeding apparatus of N. brevirostris. Prendergast, 1992; Lauder and Reilly, 1994; Reilly, 1995). In bony fishes, the kinematic patterns involved in hydraulic prey Materials and methods transport towards the esophagus are very similar to those of initial prey capture by suction feeding (Lauder and Reilly, 1994). High-speed video recording There are many sources of intra- and inter-individual Specimens of juvenile Negaprion brevirostris (Poey, 1868) variation in muscle activity patterns during feeding in teleost were collected in Florida Bay north of the Florida Keys, USA, fishes. Most teleosts appear to be capable of modulating the and held in 5 m diameter circular holding tanks in natural sea timing and activity patterns of the jaw muscles in response to water at Mote Marine Laboratory, Sarasota, Florida. different prey (Liem, 1980; Lauder, 1981; Wainwright and Specimens ranged from 66.5 to 78 cm in total length, Lauder, 1986). By comparison, the feeding behavior of sharks corresponding to ages of approximately 1–2 years old (Brown has been considered to be a series of stereotyped movements and Gruber, 1988). Approximately 2 weeks prior to the (Gilbert, 1970; Tricas, 1985), although there is preliminary experiments, each animal was transferred to a 2.4 m diameter, evidence of inter-individual variation in prey capture 1400 l semicircular tank with a 0.5 m×1.7 m acrylic window kinematics and modulation of the biting behavior (Frazzetta and was fed cut pieces of fish three times a week. Pieces of and Prange, 1987; Motta et al. 1991). fillets of Atlantic thread herring (Opisthonema oglinum) and The elasmobranch mechanism of jaw protrusion
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