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(Phoca Vitulina Richardsi) by Southern Sea Otters (Enhydra Lutris Nereis) Heather S

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(Phoca Vitulina Richardsi) by Southern Sea Otters (Enhydra Lutris Nereis) Heather S Aquatic Mammals 2010, 36(4), 331-341, DOI 10.1578/AM.36.4.2010.331 Lesions and Behavior Associated with Forced Copulation of Juvenile Pacific Harbor Seals (Phoca vitulina richardsi) by Southern Sea Otters (Enhydra lutris nereis) Heather S. Harris,1 Stori C. Oates,2 Michelle M. Staedler,3 M. Tim Tinker,4 David A. Jessup,1 James T. Harvey,2 and Melissa A. Miller1 1California Department of Fish and Game, Marine Wildlife Veterinary Care and Research Center, 1451 Shaffer Road, Santa Cruz, CA 95060, USA; E-mail: [email protected] 2Moss Landing Marine Laboratories, California State University, 8272 Moss Landing Road, Moss Landing, CA 95039, USA 3Monterey Bay Aquarium, Sea Otter Research and Conservation, 886 Cannery Row, Monterey, CA 93940, USA 4U.S. Geological Survey, Western Ecological Research Center, 100 Shaffer Road, Santa Cruz, CA 95060, USA Abstract Introduction Nineteen occurrences of interspecific sexual Sexual interactions between species have been behavior between male southern sea otters well-documented among marine mammals (Enhydra lutris nereis) and juvenile Pacific harbor (Wilson, 1975; Best et al., 1981; Harcourt, 1993; seals (Phoca vitulina richardsi) were reported Hatfield et al., 1994; Miller et al., 1996; Mortenson in Monterey Bay, California, between 2000 and & Follis, 1997; Cassini, 1998; Hayward, 2003). 2002. At least three different male sea otters were Such behavior has occasionally been observed observed harassing, dragging, guarding, and copu- among pinnipeds with overlapping breeding lating with harbor seals for up to 7 d postmortem. seasons that share the same rookeries, providing Carcasses of 15 juvenile harbor seals were recov- ample opportunities for interaction between adult ered, and seven were necropsied in detail by a vet- or subadult males and heterospecific females erinary pathologist. Necropsy findings from two (Miller et al., 1996). Documentation of hybrid off- female sea otters that were recovered dead from spring within mixed colonies of otariids (Miller male sea otters exhibiting similar behavior are also et al., 1996) and phocids (Kovacs et al., 1997) presented to facilitate a comparison of lesions. The further supports the occurrence of breeding events most frequent lesions included superficial skin between pinniped species. lacerations; hemorrhage around the nose, eyes, Reports also exist of interspecific sexual inter- flippers, and perineum; and traumatic corneal ero- actions occurring outside of the normal breed- sions or ulcers. The harbor seals sustained severe ing season in which a single aggressive male genital trauma, ranging from vaginal perforation opportunistically copulated with females or pups to vagino-cervical transection, and colorectal per- during periods when conspecific males were not forations as a result of penile penetration. One present (Wilson, 1975; Best et al., 1981; Miller harbor seal developed severe pneumoperitoneum et al., 1996; Mortenson & Follis, 1997; Hayward, subsequent to vaginal perforation, which was also 2003). Large-scale mortality has resulted when observed in both female sea otters and has been females and juveniles were physically overpow- reported as a postcoital lesion in humans. This ered and forcibly copulated by much larger het- study represents the first description of lesions erospecific males (Best et al., 1981; Miller et al., resulting from forced copulation of harbor seals 1996; Mortenson & Follis, 1997; Cassini, 1998). by sea otters and is also the first report of pneu- In some cases, male pinnipeds have approached moperitoneum secondary to forced copulation in their subjects on land or in the water, mounted a nonhuman animal. Possible explanations for this and attempted copulation (Wilson, 1975; Best behavior are discussed in the context of sea otter et al., 1981; Harcourt, 1993; Miller et al., 1996; biology and population demographics. Mortenson & Follis, 1997; Hayward, 2003), killed the subject (Best et al., 1981; Harcourt, 1993; Key Words: sea otter, Enhydra lutris nereis, Miller et al., 1996; Mortenson & Follis, 1997), harbor seal, Phoca vitulina richardsi, forced and then continued to guard and copulate with the copulation, interspecific sexual behavior, mating carcass (Best et al., 1981; Miller et al., 1996). trauma, pneumoperitoneum 332 Harris et al. Interspecific mating behavior involving south- (3) carcasses with lesions consistent with mating ern sea otters (Enhydra lutris nereis) was docu- trauma that were recovered from sites where pre- mented previously in the California Channel vious interspecific sexual interactions had been Islands, where two different males were observed reported. In addition, carcasses of two adult female interacting sexually with weaned harbor seal pups sea otters recovered directly from male sea otters (Phoca vitulina richardsi) (Hatfield et al., 1994). by MBA and U.S. Geological Survey (USGS) These sea otters hauled-out on the beach with biologists were included in this study to facilitate harbor seals, harassed and herded pups into the mating lesion identification and classification. water or approached them in the water, grasped them from behind with their teeth and forepaws, Necropsy and Lesion Classification bit them on the nose and face, mounted them, and Harbor seal carcasses were necropsied by biolo- attempted copulation. The harbor seals escaped gists at MLML or by a veterinary pathologist at by diving or by slowly swimming away when the CDFG. Sex was determined, and morphometric sea otters paused to groom. None of these interac- data were recorded, including standard length, tions were known to have resulted in harbor seal axillary girth, and body mass. The age class of mortality. harbor seals was determined using the carcass The primary objectives of this study were to recovery date relative to pupping season, standard document the behavior and lesions resulting from length, body mass, pelage condition, tooth wear, forced copulatory attempts by male sea otters on the presence of milk or prey items in the stomach, juvenile harbor seals. For purposes of comparison, and historical data for previously tagged animals two cases of female sea otters that were killed as (Bigg, 1969; Boulva & McLaren, 1979; Corpe a result of forced copulation by male sea otters et al., 1998). Both sea otters were necropsied by are also presented. Observational data collected the same veterinary pathologist at CDFG as part during these interactions is also included to help of ongoing population health studies. Sea otter interpret this behavior in the context of observed age class was determined using total length, denti- lesions and southern sea otter biology and popula- tion, and tooth wear according to categories pre- tion demographics. viously established by Morejohn et al. (1975). For all carcasses necropsied at CDFG, the same Materials and Methods systematic approach to measuring and quantify- ing gross lesions was employed to facilitate accu- Field Observations rate comparison between cases. All fresh (≤ 72 h Numerous observations of sexual interactions postmortem) cases examined at CDFG included between male sea otters and juvenile harbor full-body radiographs, digital photographs, and seals in Monterey Bay, California, were reported microscopic examination of all major tissues. to local marine mammal stranding authorities Formalin-fixed tissues were paraffin-embedded, between May 2000 and June 2002. Trained biolo- sectioned at 5 µm, and stained with hematoxylin gists from Moss Landing Marine Laboratories and eosin for examination by light microscopy. (MLML), the Monterey Bay Aquarium (MBA), Vaginal and rectal cytology were performed in and the California Department of Fish and Game some cases to screen samples for the presence of (CDFG) independently confirmed these interac- spermatozoa. tions and documented some events using video and still photography. Based on prior studies, avail- Results able behavioral data for each observed interaction were coded into one or more categories, including Field Observations harassing, herding, mate guarding, dragging the Observations of interactions between male subject through the water, and forced copulation sea otters and live and dead juvenile harbor seals (Hatfield et al., 1994). are summarized in Table 1. The most common behaviors of male sea otters that were observed Carcass Collection were mate guarding and dragging pups through Carcasses of juvenile harbor seals were collected the water (Figure 1). Mate guarding has been by the local marine mammal stranding network in described in a variety of species as a male closely Monterey Bay. Coastal stranding locations and cor- attending a female and defending her from rival responding latitudes and longitudes were recorded males during the fertile period (Low, 2005; Willis at the time of carcass recovery. Three criteria were & Dill, 2007). Male sea otters also were observed utilized to select harbor seals for possible case to feed, dive, groom, rest, and copulate with inclusion: (1) carcasses recovered directly from live and dead harbor seals. Interactions between male sea otters, (2) carcasses observed or reported sea otters and juvenile harbor seals lasted up to in the immediate vicinity of a male sea otter, or 7 d after the harbor seals had died. To initiate Forced Copulation of Harbor Seals by Sea Otters 333 Table 1. Demographic and observational data for documented cases of interspecific sexual interactions between male sea otters and juvenile harbor seals (n = 19) Case Male sea numbera Ageb Sexc Dated
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