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Feeding Mechanism of the Atlantic Guitarfish Rhinobatos Lentiginosus: Modulation of Kinematic and Motor Activity Cheryl D

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Feeding Mechanism of the Atlantic Guitarfish Rhinobatos Lentiginosus: Modulation of Kinematic and Motor Activity Cheryl D University of Rhode Island DigitalCommons@URI Biological Sciences Faculty Publications Biological Sciences 1998 Feeding Mechanism of the Atlantic Guitarfish Rhinobatos Lentiginosus: Modulation of Kinematic and Motor Activity Cheryl D. Wilga University of Rhode Island, [email protected] Philip J. Motta Creative Commons License Creative Commons License This work is licensed under a Creative Commons Attribution-Noncommercial 3.0 License Follow this and additional works at: https://digitalcommons.uri.edu/bio_facpubs Citation/Publisher Attribution Wilga, C.D. and P.J. Motta. 1998. The feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: Modulation of kinematic and motor activity. Journal of Experimental Biololgy, 201: 3167-3183. Available at http://jeb.biologists.org/content/201/23/3167.full.pdf+html?sid=edcb6850-82b4-4016-a2a3-c574512a0511 JEB1725 This Article is brought to you for free and open access by the Biological Sciences at DigitalCommons@URI. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of DigitalCommons@URI. For more information, please contact [email protected]. The Journal of Experimental Biology 201, 3167–3184 (1998) 3167 Printed in Great Britain © The Company of Biologists Limited 1998 JEB1725 FEEDING MECHANISM OF THE ATLANTIC GUITARFISH RHINOBATOS LENTIGINOSUS: MODULATION OF KINEMATIC AND MOTOR ACTIVITY CHERYL D. WILGA* AND PHILIP J. MOTTA Department of Biological Science, University of South Florida, Tampa, FL 33620, USA *Present address: Department of Ecology and Evolutionary Biology, University of California at Irvine, Irvine, CA 95697-2525, USA (e-mail: [email protected]) Accepted 16 September; published on WWW 10 November 1998 Summary The kinematics and muscle activity pattern of the head feeding behaviors and has not been described previously in and jaws during feeding in the Atlantic guitarfish elasmobranchs. The mechanism of upper jaw protrusion in Rhinobatos lentiginosus are described and quantified using the guitarfish differs from that described in other high-speed video and electromyography to test hypotheses elasmobranchs. Muscle function and motor pattern during regarding the conservation and modulation of the feeding feeding are similar in the plesiomorphic cranial muscles in mechanism. Prey is captured by the guitarfish using the guitarfish and the spiny dogfish probably because of suction. Suction capture, bite manipulation and suction their shared ancestral morphology. Modulation in transport behaviors in the guitarfish are similar to one recruitment of jaw and hyoid depressor muscles among another in the relative sequence of kinematic and motor feeding behaviors in the guitarfish may be a consequence activity, but can be distinguished from one another by of duplication of muscles and decoupling of the jaws and variation in absolute muscle activation time, in the hyoid apparatus in batoids. presence or absence of muscle activity and in the duration of muscle activity. A novel compression transport behavior Key words: Atlantic guitarfish, Rhinobatos lentiginosus, kinematics, was observed that is strikingly different from the other motor pattern, feeding, jaw protrusion, elasmobranch. Introduction Recently, increasing attention has been given to the study of The musculature of the cranium, jaws and hyoid arch has become feeding behavior in sharks (Elasmobranchii) (Moss, 1972, more complex in batoids compared with that of sharks, with the 1977; Tricas and McCosker, 1984; Frazzetta and Prange, 1987; development of several new muscles (Compagno, 1977; Moss, Frazzetta, 1988, 1994; Ferry-Graham, 1997; Wilga, 1997; 1977; Miyake et al. 1992; McEachran et al. 1996; Shirai, 1996). Motta et al. 1997; Wilga and Motta, 1998). These studies have Studies of feeding behavior have revealed that a basic contributed greatly to our understanding of feeding mechanisms kinematic feeding sequence appears to be conserved in in sharks and aquatic vertebrates in general. In contrast, rays, carcharhiniform, lamniform and squaliform sharks (Tricas and skates and guitarfishes [Elasmobranchii: Galea + Squalea McCosker, 1984; Frazzetta and Prange, 1987; Ferry-Graham, (Batoidea)], which comprise more than half (57–58 %) of the 1997; Motta et al. 1997; Wilga, 1997; Wilga and Motta, 1998). total number of elasmobranch species (Compagno, 1977; de However, some sharks are capable of consistently varying Carvalho, 1996), have received comparatively little attention. details of kinematic activity depending on feeding mode Evidence based on morphological characteristics has led (capture versus transport, ram versus suction) or prey type systematists to propose that batoids arose from squalean sharks, (Ferry-Graham, 1997; Motta et al. 1997; Wilga, 1997; Wilga one of the two main lineages of shark, in the early Jurassic and Motta, 1998). In addition, the relative sequence of activity (Fig. 1) (Carroll, 1988; DE Carvalho, 1996; McEachran et al. in the cranial muscles during feeding in two carcharhiniform 1996; Shirai, 1996). This hypothesis requires the secondary loss sharks, the lemon shark Negaprion brevirostris and the of the craniopalatine articulation and a switch from the bonnethead shark Sphyrna tiburo, appears to be quite orbitostylic jaw suspension of squaleans to the euhyostylic jaw consistent despite the high individual variation (Motta et al. suspension of batoids (Gregory, 1904; Maisey, 1980). 1997; Wilga, 1997). In contrast, some jaw retractor muscles Accordingly, the mandibular, the hyoid and even the branchial may be active during the expansive phase or the recovery phase arches of batoids are highly modified from those of sharks depending on feeding behavior in the spiny dogfish Squalus (Shirai, 1996). The position of the mandibular arch has changed acanthias (capture, manipulation and transport) (Ferry- from anteriorly directed in sharks to ventrally directed in batoids. Graham, 1997; Motta et al. 1997; Wilga, 1997; Wilga and 3168 C. D. WILGA AND P. J. M OTTA Heterodontiformes Materials and methods Galea Orectolobiformes Research specimens Lamniformes Specimens of the Atlantic guitarfish Rhinobatos lentiginosus Carcharhiniformes collected from the Gulf of Mexico off Longboat Key, Sarasota, Chlamydoselachiformes Florida, USA, were obtained from and held at Mote Marine Hexanchiformes Laboratory. The guitarfish were maintained in a 1400 l Squalea Echinorhiniformes semicircular tank provided with continuous fresh flowing sea Dalatiiformes water at approximately 25 °C and fed shrimp (Panaeus sp.) Centrophoriformes three times a week. Quartz–halogen floodlights (3000 W) were Squaliformes used during feeding to acclimatize the animal to the Squatiniformes experimental conditions. All experiments were conducted Pristiophoriformes within 14–30 days after capture. Anatomical dissections were Pristiformes made on four fresh dead R. lentiginosus specimens Batoidea Rhynchobatoidei (52.4–63.5 cm total length, TL) to describe the feeding Rhinobatoidei apparatus. Muscle terminology follows that of Luther (1909), Torpedinoidea Edgeworth (1935), Marion (1905) and Miyake et al. (1992). Rajoidea High-speed video recording and analyses Myliobatoidea For 3 days prior to the experiments, food was withheld from Fig. 1. Elasmobranch phylogeny according to Shirai (1996). Galea, the guitarfish. During the experiments, video recordings were Squalea and Batoidea clades are indicated by blue, green and red made through a 0.5 m×1.7 m acrylic window set into the side lines, respectively. of the tank. The guitarfish were filmed during the feeding experiments using two NAC 200 high-speed video cameras at 200 field s−1. A split screen recorded two camera views: one Motta, 1998). However, it is not known whether the feeding camera was directed at the window to film the lateral view, mechanism in batoids is conserved or whether they also while the second camera was directed at a mirror placed at 45 ° demonstrate variation in kinematics and motor activity. to the floor of the tank in order to film the ventral view The Atlantic guitarfish Rhinobatos lentiginosus (Batoidea: simultaneously. The experimental tank was illuminated by Rhinobatoidei) was chosen as a study animal to provide a basis 3000 W quartz–halogen floodlights. for interpreting batoid feeding mechanisms in the light of our The guitarfish depresses its pectoral fins against the current understanding of shark feeding mechanisms. Many substratum while feeding, and if the body is positioned parallel morphological characters of guitarfish are intermediate to the filming plane, as is usually required for these types of between those of sharks and rays (Compagno, 1977; Shirai, experiments, then the jaws will not be visible because the 1996; McEachran et al. 1996) and may provide insight into the pectoral fin obscures the jaws. Therefore, only feeding events in evolution of the feeding apparatus of sharks and rays. Batoids, which the jaws were visible, i.e. at an angle that is anterolateral including R. lentiginosus, possess a number of morphological to the lateral camera, were used in the analyses. The two cameras specializations that may allow modulation of the ancestral were set to the same magnification. Cranial movements were shark feeding mechanism (Gregory, 1904; Maisey, 1980; measured from the video images recorded during feeding in five McEachran et al. 1996; Shirai, 1996). Phylogenetically, guitarfish (range 50.5–63.5 cm TL): 42 prey captures (mean, five rhinobatoids occupy an important position as the sister-group per individual), 28
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