DOI: 10.7589/2011-12-348 Journal of Wildlife Diseases, 48(4), 2012, pp. 1057–1062 # Wildlife Disease Association 2012

Mortality Related to Spotted Ratfish ( colliei) in Pacific Harbor Seals (Phoca vitulina) in State

Adrianne M. Akmajian,1,4 Dyanna M. Lambourn,1,5 Monique M. Lance,1 Stephen Raverty,2 and Joseph K. Gaydos31Washington Department of and Wildlife, Marine Mammal Investigations, 7801 Phillips Road SW, Lakewood, Washington 98498, USA; 2 Health Centre, British Columbia Ministry of Agriculture and Food, 1767 Angus Campbell Road, Abbotsford, British Columbia V3G 2M3, Canada; 3 The SeaDoc Society, University of California–Davis Wildlife Health Center, Orcas Island Office, 942 Deer Harbor Road, Eastsound, Washington 98245, USA; 4 Makah Fisheries Management, PO Box 115, Neah Bay, Washington 98357, USA; 5 Corresponding author (email: [email protected]) Downloaded from http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf by guest on 25 September 2021 ABSTRACT: Tissue perforation and penetration head and esophagus (Table 1). All car- by dorsal fin spines of spotted ratfish (Hydro- casses were necropsied to determine the lagus colliei) were responsible for the death of cause of mortality, major tissues were seven harbor seals (Phoca vitulina) in Wash- ington State (USA) between 2006 and 2011. In collected and preserved in 10% neutral six , necropsy revealed spines or spine buffered formalin, and representative parts that had perforated the esophagus or samples were frozen. Tissues from four stomach and migrated into vital tissues, result- harbor seals and two Steller sea lions in ing in hemothorax, pneumothorax, pleuritis, good postmortem condition were sub- and peritonitis. In a seventh case, a ratfish spine was recovered from the mouth of a harbor mitted to the Animal Health Center in seal euthanized due to clinical symptoms of Abbottsford, British Columbia, Canada, encephalitis. Gross examination revealed an for histology and ancillary diagnostics abscess within the left cerebrum, which was (Table 1). To the best of our knowledge, attributed to direct extension of inflammatory infiltrate associated with the ratfish spine. mortality by ratfish spine injury has not Between 2009 and 2011, spotted ratfish spines been previously reported in harbor seals; were also recovered from the head or neck however, spines from stingray species region of three Steller sea lions (Eumetopias have caused esophageal and tissue perfo- jubatus) and one California sea lion (Zalophus ration leading to mortality in several other californianus). Ratfish-related trauma appears to be a novel mortality factor for harbor seals in marine mammal species (Obendorf and Washington State and could be related to Presidente, 1978; Walsh et al., 1988; increased ratfish abundance and a shifting prey Duignan et al., 2000; McFee and Lips- base for harbor seals. comb, 2009). Key words: , Hydrolagus col- Hemothorax, pneumothorax, and pyo- liei, Phoca vitulina,predator-prey,spotted ratfish, Washington State. thorax due to ratfish spines penetrating the esophagus or lung were the most common Spotted ratfish (Hydrolagus colliei), lesions noted in harbor seals (Table 1). In which have a poisonous spine attached to five cases, dark-red fluid (WDFW0506-02, their dorsal fin (Fig. 1), occur from 2008-SJ004, WDFW2011-010) or opaque southeast Alaska, USA, to Baja California, exudate (GI09-12, WDFW2010-029) was Mexico (Barnett et al., 2009). Between identified throughout the thoracic cavity 2006 and 2011, spotted ratfish dorsal fin (Table 1). In the case of an adult harbor spines or spine parts were found embed- seal with near-term fetus (WDFW2011- ded in or perforating vital tissues in seven 021), a ratfish spine was found free-floating harbor seals (Phoca vitulina) that were in the abdominal cavity, having perforated found stranded in Washington State, USA the stomach and caused a septic peritonitis. (Table 1). Additionally, three Steller sea One yearling harbor seal (WDFW2011- lions (Eumetopias jubatus) and one Cali- 029) was found stranded on the Washing- fornia sea lion (Zalophus californianus) ton outer coast exhibiting neurologic symp- recovered during this period were identi- toms, including body tremors and ataxia. fied with ratfish spines embedded in the The animal was euthanized, and gross

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FIGURE 1. Spotted ratfish (Hydrolagus colliei) spine found penetrating the esophagus and lacerating the dorsal aorta of a harbor seal (Phoca vitulina) stranded in San Juan Islands, Washington State, USA. Scale bar is in centimeters. necropsy revealed an abscess in the left and Presidente, 1978). Mortality of several cerebrum. A ratfish spine in the left jaw bottlenose dolphins (Tursiops truncatus) muscle had migrated from under the stranded in South Carolina and Florida, tongue to the base of the skull. It is USA, was also attributed to tissue perfo- suspected that perforation of the skull by ration by stingray spines (Walsh et al., the spine lead to infection and brain 1988; McFee and Lipscomb, 2009). Sim- abscessation. ilar to the yearling harbor seal with The cause of mortality of the California abscessed cerebrum (WDFW2011-029), and Steller sea lions was presumed to be stingray spines have been found to be unrelated to the finding of ratfish spines associated with abscesses in the head and (Table 1). The ratfish spine found in one neck region of leopard seals (Hydrurga adult Steller sea lion (2010-SJ006) was leptonyx) and oral abscesses of northern located adjacent to the esophagus, cranial elephant seal (Mirounga angustirostris) to the diaphragm, and was encapsulated yearlings (Obendorf and Presidente, with only minor hemorrhage in surround- 1978). A stingray spine that migrated from ing tissue. A ratfish spine impaled in the the esophagus into the hypaxial muscle of lip of a Steller sea lion pup (WDFW2010- a killer whale (Orcinus orca) was found 022) could have resulted in difficulty with enclosed in fibrous tissue (Duignan et al., prehension and mastication, contributing 2000). This same biologic response to to the poor nutritional state of the animal encapsulate penetrating foreign objects at necropsy. Ratfish spines were also likely occurred in the Steller sea lion that found embedded in the soft palate and had a walled-off ratfish spine (2010- cheek muscle of the California sea lion SJ006). and third Steller sea lion but could not be Although spotted ratfish have rarely associated with mortality due to carcass been reported in the diet of marine decomposition. mammals, they have been documented Tissue perforation by stingray spines in the diet of northern elephant seals reported in other marine mammal species within the California Current (Antonelis has resulted in pathologies similar to those and Fiscus, 1980; Condit and Le Boeuf, described here. In an Australian fur seal 1984). Parts from ratfish have also been (Arctocephalus pusilus), the barbed spine identified in the stomachs of northern fur of a stingray perforated the esophagus and seals (Callorhinus ursinus) and Steller sea migrated into the tricuspid valve of the lions from the British Columbia coast heart, causing a pericarditis (Obendorf (Spalding, 1963). Ratfish have also been TABLE 1. Necropsy findings of stranded in Washington State, USA, found with spotted ratfish ( Hydrolagus colliei ) spines.

Histology Species and identification no. Age class Sex a Carcass condition Stranding date Gross necropsy findings performed? Cause of death

Phoca vitulina Adult M Moderate 22 May 2006 Dorsal spine penetrating N Pleural perforation and (WDFW0506-02) decomposition right caudal lung hemothorax Phoca vitulina (2008-SJ004) Adult F Fresh 11 May 2008 Dorsal spine penetrating Y Hemothorax, pleuritis esophagus Eumetopias jubatus Adult F Moderate 7 June 2009 Dorsal spine in left N Undetermined due to (WDFW2009-039) decomposition masseter muscle; bullet in carcass condition perimandibular tissue Phoca vitulina (GI09-12) Adult M Fresh 15 July 2009 Dorsal spine penetrating right N Pyothorax and pneumo- caudal lung thorax Phoca vitulina Adult M Fresh 10 February 2010 Dorsal spine penetrating left N Pyothorax, pleuritis (WDFW2010-029) caudal lung Zalophus californianus Adult M Moderate 24 March 2010 Dorsal spine in right masseter N Undetermined due to (WDFW2010-049) decomposition muscle carcass condition Eumetopias jubatus Adult M Fresh 8 April 2010 Dorsal spine encapsulated Y Blunt trauma, presumed (2010-SJ006) in tissue adjacent to killer whale attack esophagus Phoca vitulina Adult M Fresh 11 February 2011 Dorsal spine in right lung Y Hemothorax, pleuritis (WDFW2011-010) Phoca vitulina Adult F Moderately fresh 26 April 2011 Dorsal spine free floating in YGastricperforationand (WDFW2011-021) abdomen peritonitis 1059 COMMUNICATIONS SHORT Eumetopias jubatus Pup M Moderately fresh 30 April 2011 Dorsal spine embedded Y Malnutrition (WDFW2011-022) in lip Phoca vitulina Yearling F Fresh 30 May 2011 Dorsal spine in left masseter Y Euthanized, bacterial and (WDFW2011-029) muscle, brain abscess protozoal encephalitis

a M 5 male, F 5 female. Downloaded from http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf by guest on 25 September 2021 September 25 on guest by http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf from Downloaded 1060 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf by guest on 25 September 2021

FIGURE 2. Spotted ratfish (Hydrolagus colliei). Photograph by Nick Brown. The caudal-facing dorsal spine held opposed to the body in this image is capable of being erected cranially and dorsally to sit perpendicular to the length of the body. noted in the stomach of a single California seals (Lance and Jeffries, 2007; Scordino, sea lion from California (summary by 2010). Spalding, 1963) and a single harbor seal The majority of animals collected in this from the Nisqually River in South Puget study were found with no food items in Sound, Washington State (Scheffer and the stomach; however, five of seven harbor Sperry, 1931). seals were found in good to excellent Spotted ratfish are the most abundant nutritional condition as determined by groundfish in and trans- sternal blubber depth (2.6–4 cm in adults boundary waters of Washington and Brit- and 1.7 cm in one yearling), making it ish Columbia (Palsson et al., 1997, 2003). unlikely that consumption of ratfish was due In trawl surveys of central Puget Sound, to desperation feeding. Histopathology of spotted ratfish were dominant between the yearling harbor seal (WDFW2011-029) 80 to 160 m, but were also collected in revealed a severe meningoencephalitis; the shallower (40 m) waters (Reum, 2006). On contribution of this inflammation to alter- the Washington coast, spotted ratfish were ations in behavior and possible effects on among the 20 most abundant groundfish prey selection are unknown. A single fish caught between 55 and 550 m (Keller bone was found in the stomach of the harbor et al., 2008). Despite being one of the seal with near-term fetus (WDFW2011- most common species found in bottom 021). One adult harbor seal (WDFW2010- trawls from this region, with the exception 029), with only 0.8-cm sternal blubber of one report documenting a ratfish in the depth, had up to 18 otoliths, multiple stomach of an adult female harbor seal cephalopod beaks, and other fish parts. All (Scheffer and Sperry, 1931), spotted sea lion stomachs were found empty. ratfish have not been identified in the We were unable to determine the food habits of Washington State harbor significance of ratfish-related trauma as a SHORT COMMUNICATIONS 1061 mortality factor for harbor seals in Wash- by the Washington Department of Fish and ington State. Necropsies of stranded Wildlife, and permits from the National harbor seals and other pinnipeds began Marine Fisheries Service (Scientific Re- in Washington State in the late 1970s search Permits 782-1446 and 782-1702). contingent on available funds and research interest. Since 2001, funding from the LITERATURE CITED John H. Prescott Marine Mammal Rescue ANTONELIS, G. A., AND C. H. FISCUS. 1980. The Assistance Grant Program has allowed for pinnipeds of the California Current. California increased, systematic necropsy effort Cooperative Oceanic Fisheries Investigations throughout the state. Ratfish-related mor- Report 21: 68–78. BARNETT, L. A. K., R. L. EARLEY,D.A.EBERT, AND Downloaded from http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf by guest on 25 September 2021 tality, however, was not noted prior to G. M. CAILLIET. 2009. Maturity, fecundity, and 2006. Harbor seals and Steller and Cali- reproductive cycle of the spotted ratfish, Hydro- fornia sea lions are generalist predators lagus colliei. Marine Biology 156: 301–316. and commonly switch prey species based CONDIT, R., AND B. J. LE BOEUF. 1984. Feeding habits on seasonal and local abundance (Weise and feeding grounds of the northern elephant seal. Journal of Mammalogy 65: 281–290. and Harvey, 2008; Sigler et al., 2009; DUIGNAN, P. J., J. E. B. HUNTER,I.N.VISSER,G.W. Scordino, 2010). In 2011 alone, four JONES, AND A. NUTMAN. 2000. Stingray spines: A animals were collected with ratfish spines, potential cause of killer whale mortality in New both from inland and coastal waters Zealand. Aquatic Mammals 26: 142–147. (Fig. 2); however, it is not known whether KELLER, A. A., B. H. HORNESS,E.L.FRUH,V.H. ratfish as a harbor seal prey item is SIMON,V.J.TUTTLE,K.L.BOSLEY,J.C. BUCHANAN,D.J.KAMIKAWA, AND J. R. WALLACE. increasing or is affected by availability of 2008. The 2005 U.S. West Coast bottom trawl other prey species. It is possible that the survey of groundfish resources off Washington, relatively high bioavailability of ratfish in Oregon, and California: Estimates of distribu- Washington waters, as noted by Palsson et tion, abundance, and length composition. US al. (1997), has led to more harbor seals Department of Commerce, NOAA Technical Memo NMFS-NWFSC-93, Seattle, Washington, testing them as viable prey. To the best of 136 pp. our knowledge, this is the first report of LANCE, M. M., AND S. J. JEFFRIES. 2007. Temporal spotted ratfish–related mortality in marine and spatial variability of harbor seal diet in the mammals. San Juan archipelago. Final report to SeaDoc This project was funded by the John H. Society Research Agreement No. K004431-25. Washington Department of Fish and Wildlife, Prescott Marine Mammal Rescue Assis- Olympia, Washington, 25 pp. tance Grant Program, Washington De- MCFEE, W. E., AND T. P. LIPSCOMB. 2009. Major partment of Fish and Wildlife, and the pathological findings and probable causes of National Marine Mammal Laboratory. mortality in bottlenose dolphins stranded in Special thanks go to stranding network South Carolina from 1993 to 2006. Journal of Wildlife Diseases 45: 575–593. volunteers who helped collect samples, OBENDORF, D. L., AND P. J. A. PRESIDENTE. 1978. especially Amy Traxler and the San Juan Foreign body perforation of the esophagus County Marine Mammal Stranding Net- initiating traumatic pericarditis in an Australian work, and staff and volunteers from Wash- fur seal. Journal of Wildlife Diseases 14: 451– ington Department of Fish and Wildlife 454. Marine Mammal Investigations and Casca- PALSSON, W., J. C. HOEMAN,G.D.BARGMANN, AND D. E. DAY. 1997. 1995 State of Puget Sound dia Research Collective, particularly Jessie bottomfish stocks (revised). Washington Depart- Huggins, Josh Oliver, Bethany Diehl, and ment of Fish and Wildlife, Olympia, Washing- Ericka Hundrup. Photographs are published ton, Report No. MRD97-03, 98 pp. with permission by Joe Gaydos and Nick ———, S. HOFFMANN,P.CLARKE, AND J. BEAM. 2003. Brown. Samples were collected under the Results from the 2001 transboundary trawl survey of the southern Strait of Georgia, San Marine Mammal Stranding Agreement held Juan Archipelago and adjacent waters. Washing- by the San Juan County Marine Mammal ton Department of Fish and Wildlife, Mill Stranding Network, the 109h Authority held Creek, Washington, 117 pp. 1062 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 4, OCTOBER 2012

REUM, J. C. P. 2006. Spatial and temporal variation SPALDING, D. J. 1963. Comparative feeding habits of in the Puget Sound food web. Master’s thesis, the fur seal (Callorhinus ursinus), sea lion University of Washington, School of Aquatic (Eumetopias jubata) and harbour seal (Phoca and Fishery Sciences, Seattle, Washington, 80 vitulina) on the British Columbia coast. Master’s pp. thesis, University of British Columbia, Vancou- SCHEFFER, T. H., AND C. C. SPERRY. 1931. Food habits ver, British Colombia, Canada, 113 pp. of the Pacific harbor seal, Phoca richardii. WALSH, M. T., D. BEUSSE,G.D.BOSSART,W.G. Journal of Mammalogy 12: 214–226. YOUNG,D.K.ODELL, AND G. W. PATTON. 1988. SCORDINO, J. 2010. West Coast program Ray encounters as a mortality factor in Atlantic investigations on California sea lion and Pacific bottlenose dolphins (Tursiops truncates). Marine harbor seal impacts on salmonids and other Mammal Science 4: 154–162. fishery resources. Pacific States Marine Fisher- WEISE, M. J., AND J. T. HARVEY. 2008. Temporal

ies Commission, Portland, Oregon, 102 pp. variability in ocean climate and California sea Downloaded from http://meridian.allenpress.com/jwd/article-pdf/48/4/1057/2242073/2011-12-348.pdf by guest on 25 September 2021 SIGLER, M. F., D. J. TOLLIT,J.J.VOLLENWEIDER,J.F. lion diet and biomass consumption: Implications THEDINGA,D.J.CSEPP,J.N.WOMBLE,M.A. for fisheries management. Marine Ecology WONG,M.J.REHBERG, AND A. W. TRITES. 2009. Progress Series 373: 157–172. Steller sea lion foraging response to seasonal changes in prey availability. Marine Ecology Submitted for publication 6 December 2011. Progress Series 388: 243–261. Accepted 11 April 2012.