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Functional Morphology of the Feeding Apparatus, Feeding Constraints, and Suction Performance in the Nurse Shark Ginglymostoma Cirratum

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Functional Morphology of the Feeding Apparatus, Feeding Constraints, and Suction Performance in the Nurse Shark Ginglymostoma Cirratum JOURNAL OF MORPHOLOGY 269:1041–1055 (2008) Functional Morphology of the Feeding Apparatus, Feeding Constraints, and Suction Performance in the Nurse Shark Ginglymostoma cirratum Philip J. Motta,1* Robert E. Hueter,2 Timothy C. Tricas,3 Adam P. Summers,4 Daniel R. Huber,5 Dayv Lowry,6 Kyle R. Mara,1 Michael P. Matott,7 Lisa B. Whitenack,1 and Alpa P. Wintzer8 1Department of Biology, University of South Florida, Tampa, Florida 33620 2Center for Shark Research, Mote Marine Laboratory, Sarasota, Florida 34236 3Department of Zoology and Hawaii Institute of Marine Biology, University of Hawaii at Manoa, Honolulu, Hawaii 96822 4Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, California 92697 5Department of Biology, University of Tampa, Tampa, Florida 33606 6Washington Department of Fish and Wildlife, Point Whitney Shellfish Laboratory, Brinnon, Washington 98320 7Department of Molecular Pharmacology and Physiology, University of South Florida, Tampa, Florida 33620 8Department of Wildlife, Fish and Conservation Biology, University of California Davis, Davis, California 95616 ABSTRACT The nurse shark, Ginglymostoma cirratum, or attached to the substrate, elusive or stationary, is an obligate suction feeder that preys on benthic inverte- and even hidden within crevices. Inertial suction- brates and fish. Its cranial morphology exhibits a suite of feeding is the primary method by which aquatic structural and functional modifications that facilitate this vertebrates capture this prey and it is the primi- mode of prey capture. During suction-feeding, subambient tive method for bony fishes (Lauder, 1985). In con- pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in trast, based on the anatomy of the jaws, teeth, and suction-feeding bony fishes, the nurse shark exhibits ex- suspensory mechanism, ram feeding and biting pansive, compressive, and recovery kinematic phases that appear to be the predominant and ancestral mode produce posterior-directed water flow through the bucco- of prey capture in elasmobranchs, with suction pharyngeal cavity. However, there is generally neither a feeding evolving in numerous lineages of benthic preparatory phase nor cranial elevation. Suction is gener- sharks and rays, including the Heterodontiformes ated by the rapid depression of the buccopharyngeal floor (horn sharks), Orectolobiformes (carpet sharks), by the coracoarcualis, coracohyoideus, and coracobran- Carcharhiniformes (ground sharks), Squaliformes chiales muscles. Because the hyoid arch of G. cirratum is (dogfish sharks), and batoids (rays). The former loosely connected to the mandible, contraction of the rectus two groups include some of the most specialized cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, obligate suction feeders (Motta et al., 2002; Wilga resulting in large volumetric expansion. Suction pressures et al., 2007). in the nurse shark vary greatly, but include the greatest The bony fish feeding mechanism differs from subambient pressures reported for an aquatic-feeding ver- that of sharks by having a greater number of tebrate. Maximum suction pressure does not appear to be moveable elements, greater lateral expansion dur- related to shark size, but is correlated with the rate of buc- ing suction generation, a bony operculum and a bi- copharyngeal expansion. As in suction-feeding bony fishes, partite upper jaw comprising a premaxilla and suction in the nurse shark is only effective within approxi- maxilla as opposed to the single palatoquadrate mately 3 cm in front of the mouth. The foraging behavior cartilage (Motta, 2004; Westneat, 2006; Wilga, of this shark is most likely constrained to ambushing or 2008). In bony fishes, suction-feeding is dependent stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by for- on a rapid series of kinematic events that include aging within reef confines and close to the substrate, which cranial elevation, abduction of the operculum and can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Mor- Contract grant sponsor: National Science Foundation; Contract phol. 269:1041–1055, 2008. Ó 2008 Wiley-Liss, Inc. grant numbers: DEB 9117371, IBN 9807863; Contract grant spon- sor: The Porter Family Foundation. KEY WORDS: Elasmobranchii; muscles; jaw; biomechanics; anatomy; suction feeding *Correspondence to: Philip J. Motta, Department of Biology, Uni- versity of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620. E-mail: [email protected] Aquatic vertebrates are challenged with captur- Published online 12 May 2008 in ing prey under a myriad of circumstances. Prey Wiley InterScience (www.interscience.wiley.com) may be suspended in the water column, buried in DOI: 10.1002/jmor.10626 Ó 2008 WILEY-LISS, INC. 1042 P.J. MOTTA ET AL. suspensorium, mandible depression, upper jaw Matott et al., 2005). Preliminary performance protrusion, and hyoid depression (Lauder, 1985; measurements indicate that suction pressure gen- Westneat, 2006). The velocity of water flow into erated during feeding by G. cirratum approaches 1 the mouth is related to the rate of buccal expan- atm or 294 kPa (Tanaka, 1973). sion and diminishes rapidly with distance from the There is an extensive literature on the biome- mouth. Consequently, the maximum distance chanics, kinematics and performance of suction water may be sucked in by bony fish is approxi- feeding in bony fishes. However, studies of suction- mately one mouth width or 3 cm (Muller et al., feeding in elasmobranchs are confined principally 1982; Van Leeuwen and Muller, 1984; Svanback to kinematics of select species including Gingly- et al., 2002). In suction-feeding sharks, anatomical mostoma cirratum (Wu, 1994; Motta et al., 2002; differences in the feeding apparatus result in func- Matott et al., 2005), spotted wobbegong Orectolo- tional differences. Rapid buccopharyngeal expan- bus maculatus (Wu, 1994), horn shark Heterodon- sion results from depression of the mandible, tus francisci (Edmonds et al., 2001), whitespotted hyoid, and branchial arches. Cranial elevation and bambooshark Chiloscyllium plagiosum (Nauwe- upper jaw protrusion play little or no role in vol- laerts et al., 2006; Lowry and Motta, 2007a; Wilga ume expansion. In contrast to bony fishes where et al., 2007; Ramsay and Wilga, 2008), spiny dog- the hyoid cavity expands ventrally and laterally fish Squalus acanthias (Wilga and Motta, 1998), during suction feeding, the hyoid arch of sharks leopard shark Triakis semifasciata (Ferry-Graham, expands ventrally but compresses laterally during 1998; Lowry et al., 2007), lesser electric ray Nar- suction feeding. In addition, the lack of an opercu- cine brasiliensis (Dean and Motta, 2004a,b), and lum in sharks should preclude any significant gen- cownose ray Rhinoptera bonasus (Sasko et al., eration of suction pressure by lateral expansion of 2006). Suction performance and its ecological sig- the pharyngeal chamber, although slight subam- nificance has only been investigated in a few of bient pressure has been recorded in the parabran- these elasmobranchs (Sasko et al., 2006; Lowry chial chamber during respiration (Ferry-Graham, and Motta, 2007b; Wilga et al., 2007; Ramsay and 1999; Edmonds et al., 2001; Motta et al., 2002; Wilga, 2008; Wilga, 2008). Therefore, the goals of Matott et al., 2005; Huber et al., 2006; Lowry and this study were to: 1) investigate the functional Motta, 2007a; Wilga et al., 2007; Wilga, 2008). For morphology of suction-feeding in G. cirratum using small sharks at least, it appears that effective suc- anatomy, electromyography, and high-speed video; tion distance is similarly restricted to distances of 2) quantify suction performance at two locations in approximately 3 cm because of hydrodynamic con- the buccopharyngeal cavity; 3) determine the scal- straints (Wilga et al., 2007). ing of suction performance across a range of shark The orectolobiform sharks, which include the sizes; and 4) relate cranial morphology and suction carpet, blind, nurse, wobbegong, bamboo, zebra, performance of the nurse shark to feeding ecology and whale sharks (Shirai, 1996), include many and diet. specialized suction feeders as evidenced by their anatomy and feeding kinematics (Moss, 1977; Wu, 1994; Motta et al., 2002; Lowry and Motta, 2007a). MATERIALS AND METHODS The nurse shark, Ginglymostoma cirratum is an Anatomy obligate suction-feeding shark that grows to 300 To complement the anatomical descriptions of Motta and cm TL (Compagno et al., 2005). During suction Wilga (1999), three partially dissected Ginglymostoma cirratum capture this shark displays little modulation in its (101, 103, and 172 cm TL) specimens were manually manipu- prey capture kinematics or motor pattern (Motta lated to try and relate the electromyographic (EMG) motor pat- terns to kinesis of the feeding apparatus. Position of the ele- et al., 2002; Robinson and Motta, 2002; Matott ments during manipulation was based on the kinematic analy- et al., 2005). This species is common in shallow sis of G. cirratum (Motta et al., 2002). All animals in this study tropical and subtropical waters throughout the were collected in Florida Bay north of the Florida Keys and northwest Atlantic Ocean including the West In- treated in accordance with University of South Florida and dies and south Florida, where it feeds on small Mote Marine
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