SHARK ATTACKS ON A WHALE SHARK (RHINCODON TYPUS) AT NINGALOO REEF, WESTERN AUSTRALIA

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1 BULLETIN OF MARINE SCIENCE, 78(2): , 2006 NOTE SHARK ATTACKS ON A WHALE SHARK (RHINCODON TYPUS) AT NINGALOO REEF, WESTERN AUSTRALIA Ben Fitzpatrick, Mark Meekan, and Allison Richards The planktivorous whale shark, reputed to attain lengths of up to 18 m, is the world s largest fish (Coleman, 1997). The immense size of whale sharks may offer a refuge from predation (Peters, 1983) by large sharks and killer whales, Orcinus orca (Linnaeus, 1758), similar to other marine megafauna such as cetaceans (Pitman et al., 2001). At present, there is only one published observation that suggests that whale sharks might be susceptible to any top order predator other than man (Fertle et al., 1996). However, very little is known of the biology and ecology of these animals, and the lack of predation records on whale sharks may simply reflect the fact that they usually inhabit tropical oceanic waters, far from coastal regions where predation is likely to be observed. Ningaloo Reef in Western Australia hosts an aggregation of whale sharks in coastal waters from March to June. The predictable arrival of whale sharks has led to the development of a lucrative ecotourism industry that allows divers to observe sharks in shallow waters on the seaward edges of the fringing coral reef. During these whale shark encounters, attacks by a predator, possibly a tiger shark, Galeocerdo cuvier (Péron and Lesueur in Lesueur, 1822), or great white shark, Carcharodon carcharias (Linnaeus, 1758), and ectoparasitic sharks (Isistius spp.) were documented. Encounters with the same whale shark 3 mo and then 1 yr later recorded wound healing. This time series provides insight into the predation risk faced by whale sharks despite their size and their ability to recover from attacks that cause substantial wounds. The photographs shown here were taken by snorkelers from ecotourism boats at Ningaloo Reef during 2003 and A 5.5 m male shark was initially photographed in April 2003 (Figs. 1, 2). The length of the shark was estimated visually by tour operators using the known lengths of snorkelers in the water beside the shark. At this time, the shark displayed wounds from at least three attacks. There was a deep wound to the left flank that had partially healed and within this wound were numerous oval shaped scars where plugs of flesh had been removed. These oval marks were consistent with bites from the ectoparasitic cookie cutter shark (Isistius spp.) (Jones, 1971). A large shark had also removed most of the dorsal fin (Figs. 1, 2). Unlike the healed perimeter of the flank wound, there was torn and severed skin, connective tissue, and muscle at the edge of the dorsal fin wound, suggesting that it was very recent. A relatively minor wound was also evident on the right flank of the shark with teeth marks from two bites also clearly from those of a large shark in a similar position to the wound on the left flank (Fig. 2). What appeared to be a tooth protrudes from one of the bite incisions on the right flank below the midline and in line with the center of the dorsal fin (Fig. 2). The clean and sharp edges of these bites suggest that this wound occurred recently, probably at the same time as the removal of the dorsal fin. Despite these wounds, the shark appeared to react normally to swimmers and there was no indication of behavior that might have attracted the attention of predators. Bulletin of Marine Science 2006 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 397

2 398 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 2, 2006 Figure 1. Photograph taken in April 2003 of wounds to a 5.5 m female whale shark at Ningaloo Reef. Note numerous scars from cookie cutter sharks in healing wound on left flank. Photo credit: anonymous. A photograph taken in July 2003 shows the wounds on the left side of the whale shark and the remains of the dorsal fin 3 mo after the first encounter (Fig. 3). The left flank wound had partially healed, although a circular scar in the center suggests that the animal was still undergoing attacks from cookie cutter sharks. Healing of the wound to the dorsal fin had also progressed and the edges were no longer ragged. A photo taken 1 yr later in June 2004 shows that these wounds had almost completely healed (Fig. 4). Potential culprits for the large wounds on this whale shark are the tiger shark, great white shark, or possibly large individuals of the shark genus Carcharinus. All of these predators occur at Ningaloo Reef (Last and Stevens, 1994; B.F., unpubl. data) and are known to feed on large cetaceans (Compagno, 1984; Long, 1991; Silber and Brown, 1991) and sharks (Fertl et al., 1996; Fergusson et al., 2000). Furthermore, basking shark flesh has been found in the stomachs of white sharks (Springer and Gold, 1989). Killer whales have been reported to attack prey as large as basking sharks in the temperate waters of New Zealand and southern California and have been observed attacking a whale shark in the Gulf of California (Fertl et al., 1996). However, based on the shape of the bite and teeth marks on the whale shark, killer whales can be excluded as the predator in this case. The shape and position of the wounds to the whale shark suggest that either a tiger shark or great white may have been responsible for the bites on the dorsal fin and right flank. On average, the dorsal fin height of a 5.5 m whale shark is approximately 42 cm (Press et al., Charles Darwin University, unpubl. data). To inflict a bite of the size shown in Figures 1 and 2, a tiger shark would have to be at least 3.5 m total length

3 NOTES 399 Figure 2. April 2003 photograph of the right flank of the same whale shark as in Figure 1. Note the lines of teeth marks above and below the midline of the shark. Photo credit: anonymous. (TL) based on the relationship between bite width and TL for this species (Heithaus, 2001a). Up to 17% of tiger sharks caught on drumlines set in Shark Bay to the south of Ningaloo Reef were of this size (Heithaus, 2001b). By comparison, published relationships between bite width and TL for white sharks (Bass et al., 1973) show that a bite of this size could have been produced by a white shark of 4 m TL. Figure 3. July 2003 photograph of the left side of the whale shark. Note healing to wounds and presence of bite scar of cookie cutter shark in center of wound near tail. Photo credit: S. Gibson.

4 400 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 2, 2006 Figure 4. June 2004 photograph of the left side of the whale shark. Photo credit: A.R. Due to healing, it is impossible to determine the likely culprit for the large wound on the left hand flank of the animal. This wound occurred some time prior to the most recent attacks, and additional attacks by cookie-cutter sharks may have retarded healing. It is notable that this older, larger wound occurs in the same position, but on the opposite side of the body, to the more recent shark attack on the right flank. This area may be a preferred site for attack by predators because the body shape and the projecting midline ridge forward of the caudal peduncle make it relatively easy to bite. Additionally, whale sharks often float at the surface to feed with their tails hanging below them to feed (Wilson, 2002). As white sharks are known to attack prey on the surface from below or behind (McCosker, 1985), the tail area may be more likely to be bitten (Long, 1991; Long and Jones, 1996). Such behavior is thought to account for the predominance of scars from white shark attacks in the region of the caudal peduncle of cetaceans (Long, 1991). The rear flanks may also be the body part that is presented to a predator by a whale shark fleeing attacks. While there are numerous accounts of white and tiger sharks scavenging whale carcasses (Randall, 1973; Pratt et al., 1982; McCosker, 1985; Springer and Gold, 1989; Bright, 2002), there are relatively few records of sharks attacking living megafauna approaching the size of this whale shark. An attack on a 3 m adult male elephant seal, Mirounga angustirostris (Gill, 1866) by a 4.7 m white shark was documented by Le Boeuf et al. (1982) and scars from shark attacks have been observed on adult humpback whales (Naessig and Lanyon, 2004). Shark attacks on adult whales may be common, but may go unnoticed by observers at the surface if they tend to occur on the underside and flanks of animals (Naessig and Lanyon, 2004). At approximately 5.5 m, the whale shark that was the subject of attacks at Ningaloo appears to be one of the largest living prey of sharks. These photographs are the first evidence of attacks by cookie cutter sharks on a whale shark. The bites by cookie cutter sharks were focused within the large healing wound inflicted on the left flank of the animal. Scars from cookie cutter sharks have not been recorded on other whale sharks at Ningaloo Reef and it seems likely that the tough skin of whale sharks may normally provide an effective defense from attacks

5 NOTES 401 by these ectoparasites. Cookie cutter sharks have also been known to attack basking sharks, the temperate equivalent of the whale shark, but the location of bite marks on these animals was not specified (Tomas and Gomez, 1989). Despite their severity, this series of attacks was ultimately unsuccessful as the whale shark survived. Libraries of whale shark photographs collected at Ningaloo Reef from 1992 to 2004 show that 21% of sharks display scars that resemble bite marks (Press et al., Charles Darwin University, unpubl. data). This suggests that attacks on sharks may be relatively common, although it is unknown what proportion results in death. To date, fatal attacks on whale sharks by killer whales have been recorded in the Gulf of California and whale shark pups have been found in the guts of marlin and a mako shark (Coleman, 1997). Attacks by top order predators thus may account for some of the life history traits of whale sharks such as the tough skin and deep layer of connective tissue on the dorsal surface of sharks. These attributes, and the great size of juvenile and adult whale sharks, may afford some degree of protection from predation. Acknowledgements The authors thank S. Gibson, the Ningaloo Reef whale shark ecotourism industry, the Department of Conservation and Land Management (Exmouth), and an anonymous person for donating the photos in Figures 1 and 2. We also thank J. Stevens and G. Taylor and two anonymous reviewers for comments on draft versions of this manuscript. Literature Cited Bass, A.J., J. D. D Aubrey, and N. Kistnasamy Sharks of the east coast of southern Africa. 1. The genus Carcharhinus (Carcharhinidae), No. 33. Invest. Rep. Oceanogr. Res. Inst., Durban. 168 p. Bright, M Sharks. The Natural History Museum, London. 112 p. Coleman, J. G A review of the biology and ecology of the whale shark. J. Fish. Biol. 51: Compagno, L. V. J Sharks of the world: an annotated and illustrated catalogue of shark species known to date. FAO Fish. Synop FAO species catalogue, vol 4, part 1. Hexanchiformes to Lamniformes. FAO, Rome. 249 p. Fergusson, I. K., L. J. V. Compagno, and M. A. Marks Predation by white sharks (Carcharodon carcharias) upon chelonians, with new records from the Mediterranean Sea and a first record of the ocean sunfish (Mola mola) as stomach contents. Env. Biol. Fish. 58: Fertl, D., A. Acevedo-Gutierrez, and F. L. Darby A report of killer whales (Orcinus orca) feeding on a Carcarhinid shark in Costa Rica. Mar. Mam. Sci. 12: Heithaus, M. R. 2001a. Shark attacks on bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia: attack rate, bite scar frequencies, and attack seasonality. Mar. Mam. Sci. 17: b. The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet and seasonal changes in catch rates. Env. Bio. Fish. 61: Jones, E. C Isistius brasiliensis, a squaloid shark, the probable cause of crater wounds on fishes and cetaceans. Fish. Bull. U.S. 69: Last, P. R. and J. D. Stevens Sharks and rays of Australia. CSIRO, Clayton South. 508 p. Le Boeuf, B. J., M. Riedman, and R. S. Keyas White shark predation on pinnipeds in Californian coastal waters. Fish. Bull. 80:

6 402 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 2, 2006 Long, D. J Apparent predation by a white shark Carcharodon carcharias on a pygmy sperm whale Kogla breviceps. Fish. Bull. 89: and R. E. Jones White shark predation and scavenging on cetaceans in the eastern north Pacific Ocean. Pages in A.P. Klimley and D.G. Ainley. eds. Great white sharks: the biology of Carcharidon carcharias. Academic Press, New York. McCosker, J. E White shark behavior: observations of and speculations about predator and prey strategies. Mem. South. Calif. Acad. Sci. 9: Naessig, P. J. and J. M. Lanyon Levels and probable origin of predatory scarring on humpback whales (Megaptera novaeangliae) in east Australian waters. Wildl. Res. 31: Peters, R. H The ecological implications of body size. Cambridge University Press, Melbourne. 327 p. Pitman, R. L., L. T. Balance, S. I. Mesnick, and S. J. Chivers Killer whale predation on sperm whales: observations and implications. Mar. Mam. Sci. 17: Pratt, H. L., J. G. Cagey, and R. B. Conklin Observations on large white sharks, Carcharodon carcharias, off Long Island New York. Fish. Bull. 80: Randall, J. E Size of the great white shark (Carcharodon). Science 181: Silber G. K. and M. Brown Death of a Bryde s Whale. Pac Disc. 44: Springer V. G. and J. P. Gold Sharks in question. Smithsonian Institution Press, Washington DC. 187 p. Tomas, A. R. G. and U. L. Gomez On the presence of basking shark, Cetorhinus maximus [Gunnerus, 1765] [Elasmobranchii, Cetorhinidae], in the southeastern and southern Brazil. Bull. Inst. Pesca Sao Paulo 16: Wilson S. G A whale shark feeding in association with a school of giant herring at Ningaloo Reef, Western Australia. J. R. Soc. West. Aust. 85: Date Submitted: 27 July, Date Accepted: 15 November, Addresses: University of Western Australia, School of Plant Biology, 35 Stirling Highway, Crawley, WA, 6009 Australia. <oceanwise@bigpond.com>. (M.M.) Australian Institute of Marine Science, PO Box 40197, Casuarina MC, Northern Territory 0811 Australia. (A.R.) WWF Australia, PO Box 293, Exmouth Western Australia, 6707 Australia.

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