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Kinematic Analysis of Suction Feeding in the Nurse Shark, Ginglymostoma Cirratum (Orectolobiformes, Ginglymostomatidae)

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Kinematic Analysis of Suction Feeding in the Nurse Shark, Ginglymostoma Cirratum (Orectolobiformes, Ginglymostomatidae) Copeia, 2002(1), pp. 24±38 Kinematic Analysis of Suction Feeding in the Nurse Shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae) PHILIP J. MOTTA,ROBERT E. HUETER,TIMOTHY C. TRICAS, AND ADAM P. SUMMERS Inertial suction feeding is known to occur in some sharks, but the sequence and temporal kinematics of head and jaw movements have not been de®ned. We inves- tigated the feeding kinematics of a suction feeding shark, the nurse shark Gingly- mostoma cirratum, to test for differences in the timing and magnitude of feeding components with other shark taxa when sharks were fed pieces of bony ®sh. Thir- teen kinematic variables were measured from high-speed video recordings. Food capture in this species consists of expansive, compressive, and recovery phases, as in most other sharks, but there is little or no cranial elevation. Mean time to maxi- mum gape (32 msec) is the fastest recorded for an elasmobranch ®sh. Other rela- tively rapid events include mandibular depression (26 msec), elevation (66 msec), and total bite time (100 msec). Buccal valves assist the unidirectional ¯ow of water into the mouth and out of the gill chambers. Food capture under these experimental conditions appears to be a stereotyped modal action pattern but with signi®cant interindividual variability in timing of kinematic events. Ginglymostoma cirratum ex- hibits a suite of specializations for inertial suction feeding that include (1) the for- mation of a small, anteriorly directed mouth that is approximately round and lat- erally enclosed by modi®ed labial cartilages; (2) small teeth; (3) buccal valves to prevent the back¯ow of water; and (4) extremely rapid buccal expansion. Sharks that capture food by inertial suction have faster and more stereotyped capture be- havior than sharks that primarily ram feed. Inertial suction feeding, which has evolved multiple times in sharks, represents an example of functional convergence with inertial suction feeding bony ®shes. HE feeding apparatus of vertebrates is a prey with an open mouth resulting in some an- T complex mechanical system with obvious terior or lateral displacement of water, such as importance to ®tness. Understanding the dy- in the white shark Carcharodon carcharias (Dia- namics of the prey capture mechanism in an mond, 1985; Tricas and McCosker, 1984; Sims, evolutionary framework gives insight into the 2000). Biting, which may accompany ram, oc- constraints and ¯exibility that govern changes curs when a shark swims toward the prey, stops, in this key system (Lauder, 1990). Studies of car- and then bites or removes pieces off the prey, tilaginous ®shes, bony ®shes, amphibians, and such as in the cookiecutter shark Isistius brasi- reptiles have produced evolutionary hypotheses liensis (LeBoeuf et al., 1987; Motta and Wilga, regarding the transition from aquatic to terres- 2001). trial prey capture (Lauder, 1985; Lauder and The mechanics and function of suction feed- Reilly, 1994; Wilga et al., 2000). Sharks, skates, ing are controversial (Muller et al., 1982; Nor- and rays (elasmobranchs) possess a radically dif- ton and Brainerd, 1993; Van Damme and Aerts, ferent suspensorium and jaw structure from 1997). The clearest terminology is that of Van that of the bony ®shes. In spite of the structural Damme and Aerts (1997), who suggest that suc- differences, elasmobranchs and bony ®shes tion feeding includes a continuum of behaviors have evolved a similar suite of prey capture ranging from sucking in just enough water to mechanisms including suction, grasping, biting, keep the prey item from escaping as the pred- gouging, and ®lter feeding (Moss, 1977; Motta ator swims over it (compensatory suction) to and Wilga, 2001). the entrainment of the prey item in a column Aquatic prey capture in sharks and bony ®sh- of water that is transported toward the motion- es may be accomplished through ram, biting, or less predator (inertial suction). Bony ®shes spe- suction. Ram feeding, which occurs when the cialized for inertial suction feeding typically predator overswims the prey, may encompass have a small, laterally enclosed mouth, protru- feeding events that establish a continuous cur- sible upper jaw, reduced dentition, and strongly rent in the mouth and over the gills. This occurs developed abductor muscles. Buccal expansion in the ®lter feeding basking shark Cetorhinus is large and rapid, and there is a wave of expan- maximus or when the predator approaches the sion and subsequent compression that travels q 2002 by the American Society of Ichthyologists and Herpetologists MOTTA ET AL.ÐNURSE SHARK FEEDING 25 posteriorly such that the engulfed body of water and prey is carried into and through the buccal cavity (Lauder, 1980a; Muller et al., 1982; Liem, 1993). However, suction feeding in sharks and rays has only been investigated in a few species (Wu, 1994; Ferry-Graham, 1998; Pretlow-Ed- monds, 1999). Buccal expansion is rapid and includes the use of labial cartilages and upper jaw protrusion to form a somewhat round and laterally enclosed mouth that is small to inter- mediate in size, and an anterior to posterior wave of expansion and compression draws the Fig. 1. Phylogeny of neoselachians according to food into the mouth (Ferry-Graham, 1998; Wil- Shirai (1996) with placement of Carcharhinus perezi ac- ga and Motta, 1998a). cording to G. J. P. Naylor (pers. comm.) incorporating Inertial suction feeding is hypothesized to be prey capture types (R 5 ram feeding; S 5 suction the ancestral form of prey capture for the bony feeding; S/F 5 suction ®lter feeding) based on the 5 ®shes (Lauder, 1985). In contrast, fossil evi- following kinematic studies: Heterodontus francisci Edmonds et al. (2001); Ginglymostoma cirratum 5 this dence and observations of morphologically sim- study and Robinson and Motta (2002); Orectolobus ma- ilar, but extant sharks indicate that the ancestral culatus 5 Wu (1994); Rhincodon typus 5 Clark and Nel- prey capture behavior in elasmobranchs prob- son (1997); Carcharodon carcharias 5 Tricas and ably involved grasping the prey whole or tearing McCosker (1984); Cephalosyllium ventriosum 5 Ferry- pieces from it, with minimal upper jaw protru- Graham (1997); Triakis semifasciata 5 Ferry-Graham sion or suction. Many of these Paleozoic sharks (1998); Carcharhinus perezi 5 Motta and Wilga (2001); had a grasping dentition, long slitlike jaw and Negaprion brevirostris 5 Motta et al. (1997); Sphyrna ti- amphistylic jaw suspension that permitted little buro 5 Wilga and Motta (2000); Notorynchus cepedianus upper jaw kinesis (Schaeffer, 1967; Moy-Thomas 5 personal observation (PJM); Squalus acanthias 5 Wilga and Motta (1998a); Rhinobatos lentiginosus 5 and Miles, 1971; Maisey, 1980). A variety of ex- Wilga and Motta (1998b). tant elasmobranchs use inertial suction to some degree as their primary feeding method [spiny dog®sh Squalus acanthias (Wilga and Motta, no, 1984; Castro, 2000). This benthic shark rou- 1998a); leopard shark Triakis semifasciata (Russo, tinely uses inertial suction, generating pressures 1975; Talent, 1976; Ferry-Graham, 1998); wob- as low as2760 mm Hg, to capture its prey (Ta- begong Orectolobus maculatus, nurse shark G. cir- naka, 1973; Robinson and Motta, 2002). ratum, and whale shark Rhincodon typus (Wu, During prey capture many ®shes demonstrate 1994; Clark and Nelson, 1997; Robinson and inherent intra- and interindividual variability in Motta, 2002); horn shark Heterodontus francisci their kinematic and motor activity patterns, in (Strong, 1989; Pretlow-Edmonds, 1999; Ed- addition to the ability to modulate or alter these monds et al., 2001); guitar®sh Rhinobatos lenti- patterns in response to differing food types and ginosus (Wilga and Motta, 1998b); and perhaps presentations (Liem, 1980a; Wainwright and the angel shark Squatina californica (Fouts and Turingan, 1993; Nemeth, 1997). Variability may Nelson, 1999)]. Inertial suction feeding elas- occur independently of the ability to modulate mobranchs are found in at least eight families, and may occur among feedings within a food often nested within clades that contain ram and category (Liem, 1978; Chu, 1989, Ferry-Gra- compensatory suction feeders, indicating that ham, 1997). There is ample evidence of exten- inertial suction feeding has evolved indepen- sive variation of prey capture kinematics and dently in several elasmobranch lineages (Fig. 1) motor patterns within species of sharks and rays (Motta and Wilga, 2001). However, functional (Motta et al., 1997; Wilga and Motta, 1998a; Fer- convergence of inertial suction feeding in ry-Graham, 1998), but it is unclear whether an sharks has received little attention (Moss, 1977; apparently morphologically specialized obligate Motta and Wilga, 1999). suction feeding shark such as G. cirratum would Orectolobiformes, which include the nurse demonstrate variability and what effect if any sharks and wobbegongs, are considered special- this would have on prey capture ability. ized inertial suction feeders based on their anat- In this study, we investigated the kinematics omy and feeding kinematics (Moss, 1977; Wu, of suction food capture in G. cirratum and com- 1994; Motta and Wilga, 1999). Ginglymostoma cir- pared it to food capture in other elasmo- ratum is common to shallow waters throughout branchs. Our goals were to (1) determine to the West Indies and south Florida, where it what extent G. cirratum relies on inertial suction feeds on small ®shes and crustaceans (Compag- feeding when presented with one food type; (2) 26 COPEIA, 2002, NO. 1 describe the kinematic pattern of suction food vided with approximately 3000 watts of quartz- capture; (3) compare the kinematics of feeding halogen lights. Because electromyographic ex- to those of other cartilaginous and bony ®shes; periments were being conducted simultaneous- and (4) investigate interindividual variability in ly on these sharks, they had bipolar ®ne wire food capture kinematics and discuss this in light electrodes (0.06 mm diameter alloy wire) im- of prey capture. planted in their cranial muscles. Motta et al. (1997) determined that implantation of electro- myographic leads in the lemon shark Negaprion MATERIALS AND METHODS brevirostris did not affect feeding kinematics.
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