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Feeding Anatomy, Filter-Feeding Rate, and Diet of Whale Sharks Rhincodon

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Feeding Anatomy, Filter-Feeding Rate, and Diet of Whale Sharks Rhincodon G Model ZOOL-25212; No. of Pages 14 ARTICLE IN PRESS Zoology xxx (2010) xxx–xxx Contents lists available at ScienceDirect Zoology journal homepage: www.elsevier.de/zool Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico Philip J. Motta a,∗, Michael Maslanka b,1, Robert E. Hueter c, Ray L. Davis b,2, Rafael de la Parra d, Samantha L. Mulvany a, Maria Laura Habegger a, James A. Strother e, Kyle R. Mara a, Jayne M. Gardiner a, John P. Tyminski c,3, Leslie D. Zeigler b,4 a Department of Integrative Biology, University of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620, USA b Georgia Aquarium, 225 Baker Street, Atlanta, GA 30313, USA c Center for Shark Research, Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236, USA d Proyecto Domino, Comision Nacional de Areas Naturales Protegidas, P.O. Box 518, Cancun, Quintana Roo, Mexico 77500, Mexico e Department of Ecology and Evolution, University of California, Irvine, CA 92697, USA article info abstract Article history: The feeding anatomy, behavior and diet of the whale shark Rhincodon typus were studied off Cabo Catoche, Received 5 October 2009 Yucatan Peninsula, Mexico. The filtering apparatus is composed of 20 unique filtering pads that com- Received in revised form pletely occlude the pharyngeal cavity. A reticulated mesh lies on the proximal surface of the pads, with 15 December 2009 openings averaging 1.2 mm in diameter. Superficial to this, a series of primary and secondary cartilagi- Accepted 22 December 2009 nous vanes support the pads and direct the water across the primary gill filaments. During surface ram filter feeding, sharks swam at an average velocity of 1.1 m/s with 85% of the open mouth below the Keywords: water’s surface. Sharks on average spent approximately 7.5 h/day feeding at the surface on dense plank- Ram filter feeding Shark diet ton dominated by sergestids, calanoid copepods, chaetognaths and fish larvae. Based on calculated flow Plankton speed and underwater mouth area, it was estimated that a whale shark of 443 cm total length (TL) filters 3 3 3 Feeding rate 326 m /h, and a 622 cm TL shark 614 m /h. With an average plankton biomass of 4.5 g/m at the feeding site, the two sizes of sharks on average would ingest 1467 and 2763 g of plankton per hour, and their daily ration would be approximately 14,931 and 28,121 kJ, respectively. These values are consistent with independently derived feeding rations of captive, growing whale sharks in an aquarium. A feeding mech- anism utilizing cross-flow filtration of plankton is described, allowing the sharks to ingest plankton that is smaller than the mesh while reducing clogging of the filtering apparatus. © 2010 Elsevier GmbH. All rights reserved. 1. Introduction the water must pass, and upon which the prey are supposedly trapped before swallowing (Gudger, 1941b, p. 86). The very detailed The whale shark Rhincodon typus (Smith, 1828) is the world’s descriptions of the cranial anatomy by both authors are at odds with largest fish as well as the largest filter feeding fish, yet its feeding the poorly described filtering apparatus. To date Gudger’s descrip- biology is still poorly understood. Denison (1937) provided one of tion remains the most complete description of a unique filtering the earliest and most thorough descriptions of the head, followed apparatus found in no other fish. Comparing this filtering apparatus by seminal work by Gudger (1941a,b) who described the shark as to that of the basking shark Cetorhinus maximus and the megamouth having a huge mouth, small teeth and “curious gill arches” com- shark Megachasma pelagios, Taylor et al. (1983) and Sanderson and posed of sponge-like masses of filtering gill sieves through which Wassersug (1993) both concluded that the filtering apparatus of the whale shark is incapable of sustaining a high rate of water flow through it. ∗ Better understood, but still controversial, is the diet of this cir- Corresponding author. Tel.: +1 813 974 2878; fax: +1 813 974 3263. cumglobal giant. Early scientists recognized that, despite its size, E-mail address: [email protected] (P.J. Motta). 1 Current address: Department of Nutrition, Smithsonian Conservation Biology it had a unique filtering apparatus and subsisted on plankton Institute, Washington, DC 20013, USA. near the surface (Gill, 1905). Gudger (1941a) noted that in addi- 2 Current address: Marine Science Center, 100 Lighthouse Drive, Ponce Inlet, FL tion to planktonic crustaceans, Rhincodon had been conclusively 32127, USA. demonstrated to feed on squid and cuttlefish. He postulated that 3 Current address: 14271 Appalachian Trail, Davie, FL 33325, USA. 4 Current address: Disney’s Animal Kingdom, Animal Nutrition Center, Lake Buena an invertebrate diet is insufficient to maintain this species, and Vista, FL 32830, USA. summarized observations of whale sharks purportedly ingesting 0944-2006/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.zool.2009.12.001 Please cite this article in press as: Motta, P.J., et al., Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology (2010), doi:10.1016/j.zool.2009.12.001 G Model ZOOL-25212; No. of Pages 14 ARTICLE IN PRESS 2 P.J. Motta et al. / Zoology xxx (2010) xxx–xxx schooling clupeids. Since those early, and often anecdotal, stud- Catoche, on the northeastern corner of the Yucatan Peninsula, Mex- ies, numerous dietary analyses have been conducted at whale ico. The area sampled ranged from 21◦41.545 to 21◦45.811N and shark aggregation sites. These analyses, based on stomach contents, 86◦59.898 to 87◦09.866W, where bottom depth ranged between fecal samples, behavioral observations, and plankton tows, indi- 10 and 20 m. Between April and September each year at least sev- cated that whale sharks primarily feed on a variety of planktonic eral hundred whale sharks aggregate in the area to feed on plankton organisms. These include euphausids, copepods, chaetognaths, associated with a seasonal upwelling. Population estimates range crab larvae, molluscs, siphonophores, salps, sergestids, isopods, as high as 1400 sharks visiting the region every summer, with amphipods, stomatopods, coral spawn, and fish eggs. In addition, sharks ranging in size from 1.5 to 13 m total length (TL) and a they also feed on small squid and fish (Silas and Rajagopalan, sex ratio of approximately 1 female per 2.6 males (Hueter et al., 1963; Taylor, 1994, 1996, 2007; Clark and Nelson, 1997; Taylor 2008). Observations were confined to surface ram filter feeding and Pearce, 1999; Heyman et al., 2001; Wilson and Newbound, as low underwater visibility (due to dense plankton abundance) 2001; Duffy, 2002; Jarman and Wilson, 2004; Hacohen-Domene et mostly prevented sub-surface observations. Observations gener- al., 2006; Hoffmayer et al., 2007; Nelson and Eckert, 2007; Meekan ally occurred between 07:00 and 14:00 h. Feeding sharks were et al., 2009). tracked with a motor vessel at a distance of approximately 2–5 m, We now know that whale sharks use at least three methods of taking care not to alter the shark’s natural behavior. With the vessel filter feeding. The most readily observable, due to its location, is moving at the same rate as, and parallel to, the animal, swimming surface ram filter feeding or surface active feeding. When feeding in speed was recorded for 33 sharks with either a Garmin GPS MAP this manner, the whale shark swims at the surface with the dor- 276C or a Garmin eTrex Venture GPS (Garmin International Inc., sal surface of the head and usually the dorsal fin and upper lobe of Olathe, KA, USA). The swimming speed of each shark was recorded the caudal fin exposed. With its body pitched upwards, the open two to three times and an average taken. Swimming speed recorded mouth is held partially out of the water, and the animal swims at in this manner closely matched water flow velocity independently relatively slow speeds (0.3–1.5 m/s),1 ramming the water and food recorded by means of calibrated lasers, as described below. Shark through its filtering apparatus. The shark is occasionally seen to TL was estimated to the nearest half-meter for each shark two to “cough”, back-flushing water and particles out of its mouth before three times by motoring within 2–3 m of, and parallel to, the shark resuming feeding (Clark and Nelson, 1997; Heyman et al., 2001; and comparing its total length to one-meter markings on the boat Nelson and Eckert, 2007; Taylor, 2007). During stationary/vertical gunwale. The average of these length estimates was recorded. In suction feeding the shark either remains relatively horizontal or addition, for a subset of these sharks, a pair of calibrated green assumes a nearly vertical position, stops or almost ceases swim- laser pointers set 50 cm apart were projected on the head, allowing ming, and actively suctions in plankton or small fish with repeated total length to be estimated later from still or video pictures using opening and closing of its mouth. When in the vertical position, the the ratio of internasal distance or distance of snout to pectoral fin shark’s mouth is positioned just below the surface (Gudger, 1941a; origin, first gill slit, or dorsal fin origin to total length (see Section Heyman et al., 2001; Nelson and Eckert, 2007). During sub-surface 2.5). passive feeding/passive feeding, the shark swims slowly (0.2–0.5 m/s) Above-water video of bubbles or pieces of flotsam was recorded (see footnote 1) below the surface with the mouth wide open, fil- as they entered a shark’s open mouth (see electronic supplement, tering the food from the water (Nelson and Eckert, 2007; Taylor, Shark 9 2007 aerial view surface ram filter feeding).
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