Five Species ofParasitic (Siphonostomatoida: Pandaridae) from the Body Surface ofa White Captured in Morro , California1

George W Benz,2 Henry F. Mollet,3 DavidA. Ebert,3 Corrine R. Davis,4 and Sean R. Van Sommeran 5

Abstract: Five pandarid (Copepoda) species, Dinemoura produeta, D. latiftlia, Eehthrogaleus eoleoptratus, Pandarus bieolor, and Aehtheinus oblongus, were collected from the external body surface of a white shark, Careharodon eareharias, taken from Morro Bay in the northeastern Pacific Ocean off central . This is the first report ofparasitic copepods collected from C. eareharias captured in the northeastern Pacific along the West Coast ofNorth America. It is proposed that the species-rich infections of some white may be the result of the wide wanderings of individual sharks through waters inhabited by other elasmo­ branchs.

THE WHITE SHARK, Anthosoma crassum (Abildgaard, 1794), pri­ (Linnaeus, 1758), is a widely distributed marily infect close phylogenetic relatives coastal and offshore species inhabiting tropi­ of the white shark (i.e., other members of cal and amphitemperate continental and in­ or [e.g., see Hewitt sular shelves (Compagno 1984a). The species 1969]). Other species, e.g., Pandarus smithii is commonly infected by siphonostomatoids Rathbun, 1886, and Eehthrogaleus eoleoptratus (Copepoda), and globally at least 18 species of (Guerin-Meneville, 1837), infect more dis­ these ectoparasites have been reported from tantly related inshore or offshore elasmo­ C. carcharias (e.g., see Yamaguti 1963, Lewis branchs that share habitat with C. earcharias 1966, Cressey 1967a,b, 1970, Hewitt 1967, (see Yamaguti 1963, Compagno 1984a,b). 1969,1979, Kensley and Grindley 1973, Ka­ Multiple infections of sharks by siphon­ bata 1979, Love and Moser 1983, Hogans ostomatoids are common; however, it is and Dadswell 1985, Pillai 1985, Benz 1986, unusual (G.W.B., pers. obs.) for an individual Oldewage and Smale 1993). To date, all co­ shark to be simultaneously infected by more pepod species known to infect white sharks than three species externally or by more than also infect other sharks. Some of these spe­ six species in its entirety (i.e., general body cies, e.g., Nemesis Risso, 1826, and surface, olfactory sacs, and buccal and bran­ chial chambers). Hewitt (1979) reported eight siphonostomatoid species from a white shark (three species from the branchial chamber, 1 Manuscript accepted 8 April 2002. 2 Corresponding author: Tennessee Aquarium and five species from the general body surface) Tennessee Aquarium Research Institute, One Broad caught in Pukeria Bay (Pacific Ocean near Street, Chattanooga, Tennessee 37401 (phone: 706-694- Wellington, New Zealand). Our report 4666; fax: 706-694-3957; E-mail: [email protected]). documents the infection of the general body 3 Moss Landing Marine Laboratories, 8272 Moss surface of a white shark by five siphon­ Landing Road, Moss Landing, California 95039. 4 University of California, One Shields Avenue, ostomatoid species, and it is the first report Davis, California 95616. of parasitic copepods from a white shark 5 Pelagic Shark Research. Foundation, S. C. Yacht captured along the West Coast of North ------Marb0r-,--Santa-Gruz-,--Galif0rlUa-9$060~------l\m.erica. Elasmooranch: nomenclature ana- systematics used herein follow Compagno Pacific Science (2003), vol. 57, no. 1:39-43 (1999a,b). © 2003 by University of Hawai'i Press On 23 November 2000 a female white All rights reserved shark (4.33 m total length, 772 kg) was caught

39 40 PACIFIC SCIENCE· January 2003

in a gill net set in water 60 m deep 1861): four adult females, one of which was approximately 4.8 km from shore in Morro collected from about the cloaca (possibly on a Bay, California (35° 10' N, 120° 40' W). ). Dinemoura latifolia has been col­ Upon its landing, the shark was moved and lected from white sharks before this report frozen, and later thawed and examined. On at (Lewis 1966, Hewitt 1967, Benz 1986); how­ least two occasions during this period cope­ ever, to our knowledge this is the first such pods were collected from the external body report from the northeastern Pacific along surface of the shark; however, the exact at­ the West Coast of . This co­ tachment location of all parasites was not pepod has been reported from the Atlantic, recorded. The olfactory sacs, and buccal and Pacific, and Indian Oceans and it is primarily branchial chambers of the shark were not a parasite of pelagic lamnids (Cressey 1967a, thoroughly examined for parasites, and it is Hewitt 1967). In northeastern Pacific waters possible that during the capture or transport along the West Coast of North America D. period some ectoparasites may have been latifolia infects the shark, Lamna di­ dislodged accidentally and lost or removed tropis Hubbs & Follett, 1947, and the shortfin from the shark by curious bystanders. Col­ mako (Wilson 1935, Cressey 1968, Deets lected copepods, fixed in 10% formalin or 1985) in addition to the white shark. 70% ethanol, were sent to G.W.B. for iden­ Eehthrogaleus eoleoptratus (Guerin-Mene­ tification. All ofthe specimens were identified ville, 1837): one immature female collected as pandarids (Siphonostomatoida: Pandar­ from about the cloaca (possibly on a pelvic idae), and the species and number of speci­ fin). Eehthrogaleus eoleoptratus has been re­ mens were as follows (all specimens have ported from white sharks before this report been retained in the personal collection of (Yamaguti 1963, Hewitt 1967, 1979); how­ G.W.B.). ever, to our knowledge this is the first such Dinemoura produeta (Muller, 1785): one report from the northeastern Pacific along adult female collected from about the cloaca the West Coast of North America. This (possibly on a pelvic fin). Dinemoura produeta has been collected in the Atlantic, has been collected from white sharks before Pacific, and Indian Oceans, where it has been this report (Hewitt 1967); however, to our reported from squaliforms, lamniforms, and knowledge this is the first such report carcharhiniforms, with most reports linking from the northeastern Pacific along the West it to pelagic hosts (e.g., see Yamaguti 1963, Coast of North America. The species is well Kabata 1979, Pillai 1985). In addition to the known from the Atlantic and Pacific Oceans, white shark, in northeastern Pacific waters E. but according to Hewitt (1967) and Kabata eoleoptratus has been reported from the leop­ (1979) it has only been reported once (from ard shark, semifaseiata Girard, 1854, an unknown host) from the Indian Ocean. off California by Russo (1975); from the This copepod is primarily a parasite ofpelagic salmon shark off British Columbia by Bere lamniforms of the families Lamnidae and (1930); from the blue shark, Prionaee glauea Cetorhinidae (Hewitt 1967). In northeastern (Linnaeus, 1758), off California by Pappas (as Pacific waters along the West Coast ofNorth reported in Love and Moser 1983) and Deets America D. produeta infects the shortfin mako, (1985); and from the smooth hammerhead, lsurus oxyrinehus Rafinesque, 1810 (Heegaard Sphyrna zygaena (Linnaeus, 1758), off Cali­ 1945, Cressey 1968, Deets 1985), in addition fornia by Deets (1985). to the white shark. Geographic records listed Pandarus bieolor Leach, 1816: one adult by Hewitt (1967) suggest (especially those female (partial specimen consisting of cepha­ documenting distribution within the Atlantic lothorax and thorax) collected from about the ------Oceaff}-rnat-IX-proaucta is more common in cloaca (possibly-on a pelvrc--fur)~-Pimtlarus -bt~­ cooler temperate regions than its congener color has been reported from the white shark D. latifolia. before this report (Hewitt 1979); however, to Dinemoura latifolia (Steenstrup & Lutken, our knowledge this is the first such report Parasitic Copepods from a White Shark . Benz et at. 41

from the northeastern Pacific along the West In assigning an identity to our specimens and Coast of North America. This copepod has in the remarks that follow we consider A. been collected in the Adantic, Pacific, and oblongus sensu Ho (1975). Achtheinus oblongus Indian Oceans, where it has been reported has been reported (Barnard 1955) from the from squaliforms, lamniforms, and carcharhi­ white shark in Table Bay (Adantic Ocean off niforms (Barnard 1955, Yamaguti 1963, He­ Cape Town, South Africa); however, we be­ witt 1967, Kabata 1979). In addition to the lieve this to be the first such report from white shark, in northeastern Pacific waters the northeastern Pacific Ocean off the West P. bicolor has been reported from the piked Coast of North America. Achtheinus oblongus dogfish, Squalus acanthias Linnaeus, 1758, by has been collected in the Adantic, Pacific, and Wilson (1935) and Deets (1985); from the Indian Oceans, where it has been reported leopard shark by Russo (1975); from the from hexanchiforms, squaliforms, pristio­ broadnose sevengill shark, Notorynchus cepe­ phoriforms, lamniforms, carcharhiniforms, dianus (Peron, 1807), by Russo (1975) and rhinobatiforms, and rajiforms, with most re­ Ebert (1989); from the tope shark, Galeorhinus ports linking it to benthic-dwelling nearshore galeus (Linnaeus, 1758), by Russo (1975); and hosts (see Yamaguti 1963). In addition to the from the bluntnose sixgill shark, Hexanchus white shark, in northeastern Pacific waters griseus (Bonnaterre, 1788) by Ebert (1986). (including the ) A. oblongus Achtheinus oblongus Wilson, 1908 (sensu has been reported from the broadnose seven­ Ho 1975): one young adult and 12 adult gill shark by Wilson (1912); the thresher females, three of which were collected from shark, Alopias vulpinus (Bonnaterre, 1788), by a pelvic fin and nine collected from about Wilson (1921); the piked dogfish by Deets the cloaca (possibly on the pelvic fins). Cres­ (1985); the gray smooth hound, Mustelus cal­ sey (1967a) placed Achtheinus Wilson, 1908, ifornicus Gill, 1864, by Ho (1975) and Deets as a junior of Perissopus Steenstrup (1985); the brown smooth hound, M. henlei & Liitken, 1861, and in doing so he grouped (Gill, 1863), by Russo (1975); the sicklefin 10 Achtheinus spp. as one species that he smooth hound, M. lunulatus Jordan & Gil­ referred to as Perissopus oblongatus (Wilson, bert, 1883, by Wilson (1921); the leopard 1908). Some lapsus prevented Cressey (1967a) shark by Wilson (1908) and Deets (1985); from mentioning an eleventh species of the smooth hammerhead by Wilson (1944); Achtheinus-A. armatus (Dana, 1852) (see the , Rhinobatos produetus Oldewage 1992). Ho (1975) resurrected Ach­ Girard, 1854, by Ho (1975); and the big theinus based on specimens that he referred skate, Raja binoculata Girard, 1854, by Wilson to as A. oblongus, the original species epithet (1911). spelling ofWilson (1908). Ho (1975) justified This report and that of Hewitt (1979) this action based on substantial differences demonstrate that although species-rich infec­ between the dorsal plates and leg armature of tions of sharks by siphonostomatoids are gen­ Achtheinus and Perissopus species. However, to erally unusual, they may not be so regarding date no one has reexamined type specimens the white shark. Four of the five copepod representing the junior synonyms erected species reported herein were also reported by Cressey (1967a) to determine if his action by Hewitt (1979) from the collections he ex­ to lump all Achtheinus spp. as one was well amined. Regarding our report, it is possible founded. We agree with Ho's (1975) assess­ that a thorough examination of the shark's ment of Achtheinus, and we further note buccal and branchial chambers would have (G.W.B., pers. obs.) that adult female repre­ resulted in collections of two additional si­ sentatives of Achtheinus attach to the host by phonostomatoids, Nemesis lamna and Antho­ .---- eriiOeaaing ilieirantennaedeeplYin me-SKill­ soma erassum, oecausemese species arelmown~--­ whereas those representing Perissopus attach to infect these body regions on white sharks by cementing the enlarged myxal region of collected elsewhere (e.g., see Hewitt 1979), their maxillipeds to the host's placoid scales. and they are known to exist along the West 42 PACIFIC SCIENCE· January 2003

Coast of North America on other lamnids Literature Cited (Love and Moser 1983). What facilitates the species-rich infections Barnard, K. H. 1955. South African parasitic of individual white sharks by siphonostoma­ Copepoda. Ann. S. Afr. Mus. 41:223-312. toids remains unknown. This phenomenon Benz, G. W. 1986. Distributions of siphon­ cannot be explained by the large size that ostomatoid copepods parasitic upon large white sharks can attain, because the whale pelagic sharks in the western North At­ shark, Rhincodon typus Smith, 1828, and the 1antic. Syllogeus 58:211-219. , Cetorhinus maximus (Gunne­ Bere, R. 1930. Parasitic copepods from the rus, 1765), each grow to be considerably Vancouver Island region. Fish. Res. Board larger (Compagno 1984a,b) and yet they are Can. Misc. Spec. Rep. (BioI.) 259. not known to be similarly infected. Further­ Boustany, A. M., S. F. Davis, P. Pyle, S. D. more, from a phylogenetic perspective, Anderson, B. J. Le Boeuf, and B. A. Block. the basking shark and white shark are close 2002. Expanded niche for white sharks. relatives (Compagno 1999a) and their ranges Nature (Lond.) 415:35-36. overlap considerably (Compagno 1984a); Compagno, L. J. V. 1984a. Sharks of the hence it might be expected that these species world: Hexanchiformes to Lamniformes. would be infected by the same species of FAO Fish. Synop. 125, Vol. 4, Part 1. copepods. We feel that it is significant that, --. 1984b. Sharks of the world: Carcha­ together, all of the copepod species reported rhiniformes. FAO Fish. Synop. 125, Vol. from C. carcharias are known to infect a wide 4, Part 2. phylogenetic and ecological range of elasmo­ ---. 1999a. Systematics and body form. branchs. Based on this and on a recent report Pages 1-42 in W. C. Hamlett, ed. Sharks, (Boustany et al. 2002) of the extremely large skates, and rays: The biology of elasmo­ home ranges of at least some white sharks branch fishes. The Johns Hopkins Uni­ that span a variety of inshore and offshore versity Press, Baltimore. provinces, we propose that the species-rich ---. 1999b. Checklist of living elasmo­ infections of some white sharks may be the branchs. Pages 471-498 in W. C. Hamlett, result of the wide wanderings of individual ed. Sharks, skates, and rays: The biology of sharks through waters inhabited by other elasmobranch fishes. The Johns Hopkins elasmobranchs. Unfortunately, to date too University Press, Baltimore. little is known about the biogeography and Cressey, R. 1967a. Revision of the family genetics of the siphonostomatoids that infect Pandaridae (Copepoda: Caligoida). Proc. the white shark to understand if occurrence U.S. Nat!. Mus. 121 (3570): 1-133. patterns and molecular techniques might al­ ---. 1967b. Caligoid copepods parasitic low these parasites to be used as biological on sharks of the Indian Ocean. Proc. U.S. tags to help in studies of shark movements. Nat!. Mus. 121 (3572): 1-21. ---. 1968. Caligoid copepods parasitic on lsurus oxyrinchus with an example ofhabitat ACKNOWLEDGMENTS shift. Proc. U.S. Nat!. Mus. 125 (3653): 1- We thank D. Jessup (California Depart- 26. ment of Fish and Game) for use of facilities ---. 1970. Copepods parasitic on sharks at the Marine Wildlife Veterinary Care and from the west coast of Florida. Smithson. Research Center; D. Casper (University of Contrib. Zoo1. 38:1-30. California at Santa Cruz) and M. Miller Deets, G. B. 1985. Copepod and chon­ (California Department of Fish and Game) drichthyan coevolution: A cladistic analy------for nelpWitlftlle aissection; S~K-Bunara-;--C----siS:-N1~S~tliesis,-CaIiforruaState UniversIty--- Schloss, and J. Shaw (all Gulf Coast Research at Long Beach, Long Beach, California. Laboratory) for assistance with the literature; Ebert, D. A. 1986. Biological aspects of the and the Tennessee Aquarium Research Insti- sixgill shark, Hexanchus griseus. Copeia tute for general support. 1986:131-135. Parasitic Copepods from a White Shark . Benz et al. 43

---. 1989. Life history of the sevengill sopus ob/ongus (Wilson, 1908) (Copepoda, shark, Notorynchus cepedianus Peron, in two Pandaridae) from southern African sharks northern California bays. Calif. Fish Game with a first description of the male. Crus­ 75:102-112. taceana (Leiden) 63:44-50. Heegaard, P. 1945. Some parasitic copepods Oldewage, W. H., and M. J Smale. 1993. from fishes in the Uppsala University col­ Occurrence of piscine parasitic copepods lection. Ark. Zool. 35A (18): 1-27. (Crustacea) on sharks taken mainly off Hewitt, G. C. 1967. Some New Zealand par­ Cape Recife, South Africa. S. Afr. J Mar. asitic Copepoda of the family Pandaridae. Sci. 13:309-312. N.Z. J Mar. Freshwater Res. 1:180-264. Pillai, N. K. 1985. The fauna of India: Cope­ ---, 1969. Some New Zealand parasitic pod parasites of marine fishes. Zoological Copepoda of the family Eudactylinidae. Survey of India, Calcutta. Zool. Publ. Vic. Univ. Wellington 49:1­ Russo, R. A. 1975. Notes on the external 31. parasites of California inshore sharks. ---. 1979. Eight species of parasitic co­ Calif. Fish Game 61:228-232. pepods on a white shark. N.Z. J Mar. Wilson, C. B. 1908. North American parasitic Freshwater Res. 13: 171. copepods: A list of those found upon the Ho, J-S. 1975. Parasitic Crustacea. Pages fishes of the Pacific Coast with descrip­ 69-72 in E. D. Lane and C. W. Hill, eds. tions ofnew genera and species. Proc. U.S. The marine resources of Anaheim Bay. Natl. Mus. 35:431-481. Calif. Dep. Fish Game Fish Bull. 165. ---. 1911. North American parasitic co­ Hogans, W. E., and M. J Dadswell. 1985. pepods. Descriptions of new genera and Parasitic copepods of the white shark species. Proc. U.S. Natl. Mus. 39:625-634. (Carcharodon carcharius L.) from the Bay of ---. 1912. Descriptions of new species of Fundy. Can. J Zool. 63:740-741. parasitic copepods in the collections of the Kabata, Z. 1979. Parasitic Copepoda of Brit­ United States National Museum. Proc. ish fishes. The Ray Society, London. U.S. Natl. Mus. 42:233-243. Kensley, B., and J R. Grindley. 1973. South ---. 1921. New species and a new genus African parasitic Copepoda. Ann. S. Afr. of parasitic copepods. Proc. U.S. Natl. Mus. 62:69-130. Mus. 59:1-17. Lewis, A. G. 1966. Copepod crustaceans ---. 1935. Parasitic copepods from the parasitic on elasmobranch fishes of the Pacific Coast. Am. MidI. Nat. 16:776­ Hawaiian Islands. Proc. U.S. Natl. Mus. 797. 118 (3524): 57-154. ---. 1944. Parasitic copepods in the Love, M. S., and M. Moser. 1983. A checklist United States National Museum. Proc. of parasites of California, , and U.S. Natl. Mus. 94:529-582. Washington marine and estuarine fishes. Yamaguti, S. 1963. Parasitic Copepoda and NOAA Tech. Rep. NMFS SSRF-777. Branchiura of fishes. Interscience Publish­ Oldewage, W. H. 1992. Description of Peris- ers, New York.