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 et al. Aquatic Mammals Journal, 36(4), 331-341, November 29 2010. DOI: 10.1578/AM.36.4.2010.331
Abstract: Nineteen occurrences of interspecific sexual behavior between male southern sea otters (Enhydra lutris nereis) and juvenile Pacific harbor seals (Phoca vitulina richardsi) were reported in Monterey Bay, California, between 2000 and 2002. At least three different male sea otters were observed harassing, dragging, guarding, and copulating with harbor seals for up to 7 d postmortem. Carcasses of 15 juvenile harbor seals were recovered, and seven were necropsied in detail by a veterinary pathologist. Necropsy findings from two female sea otters that were recovered dead from male sea otters exhibiting similar behavior are also presented to facilitate a comparison of lesions. The most frequent lesions included superficial skin lacerations; hemorrhage around the nose, eyes, flippers, and perineum; and traumatic corneal erosions or ulcers. The harbor seals sustained severe genital trauma, ranging from vaginal perforation to vagino-cervical transection, and colorectal perforations as a result of penile penetration. One harbor seal developed severe pneumoperitoneum subsequent to vaginal perforation, which was also observed in both female sea otters and has been reported as a postcoital lesion in humans. This study represents the first description of lesions resulting from forced copulation of harbor seals by sea otters and is also the first report of pneumoperitoneum secondary to forced copulation in a nonhuman animal. Possible explanations for this behavior are discussed in the context of sea otter biology and population demographics.
Key Words: sea otter, Enhydra lutris nereis, harbor seal, Phoca vitulina richardsi, forced copulation, interspecific sexual behavior, mating trauma, pneumoperitoneum
Introduction
Sexual interactions between species have been
well-documented among marine mammals
(Wilson, 1975; Best et al., 1981; Harcourt, 1993;
Hatfield et al., 1994; Miller et al., 1996; Mortenson
& Follis, 1997; Cassini, 1998; Hayward, 2003).
Such behavior has occasionally been observed
among pinnipeds with overlapping breeding
seasons that share the same rookeries, providing
ample opportunities for interaction between adult
or subadult males and heterospecific females
(Miller et al., 1996). Documentation of hybrid offspring within mixed colonies of otariids (Miller
et al., 1996) and phocids (Kovacs et al., 1997)
further supports the occurrence of breeding events
between pinniped species.
Reports also exist of interspecific sexual interactions occurring outside of the normal breeding season in which a single aggressive male
opportunistically copulated with females or pups
during periods when conspecific males were not
present (Wilson, 1975; Best et al., 1981; Miller
et al., 1996; Mortenson & Follis, 1997; Hayward,
2003). Large-scale mortality has resulted when
females and juveniles were physically overpowered and forcibly copulated by much larger heterospecific males (Best et al., 1981; Miller et al.,
1996; Mortenson & Follis, 1997; Cassini, 1998).
In some cases, male pinnipeds have approached
their subjects on land or in the water, mounted
and attempted copulation (Wilson, 1975; Best
et al., 1981; Harcourt, 1993; Miller et al., 1996;
Mortenson & Follis, 1997; Hayward, 2003), killed
the subject (Best et al., 1981; Harcourt, 1993;
Miller et al., 1996; Mortenson & Follis, 1997),
and then continued to guard and copulate with the
carcass (Best et al., 1981; Miller et al., 1996).
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Discussion
The behavioral observations and lesions described in this study are extreme examples of the spectrum of mating-associated trauma observed in southern sea otters. Copulation normally occurs in the water where the male sea otter will approach the female from behind, grip her around the chest with his forepaws, and grasp her nose or the side of her face with his teeth (Kenyon, 1969; Staedler & Riedman, 1993). Females often initially resist copulatory attempts, but eventually will submit, and the pair may roll and spin in the water, with the male positioned dorsal to the female during copulation (Kenyon, 1969). Immature males sometimes mimic this pre-copulatory behavior while playing with each other, including facial biting, spinning nose to nose, and mounting each other from behind (M. Staedler, unpub. data, 2000-2010).
Facial biting by the male commonly results in the development of skin and soft tissue lacerations of the female’s nose and face that can occasionally be fatal (Foott, 1970; Staedler & Riedman, 1993). Trauma associated with mating was a primary or contributing cause of death for 11% of fresh dead southern sea otters examined between 2000 and 2003 (Kreuder et al., 2003). In one prior report on breeding-associated mortality, a tagged territorial male sea otter held a struggling female underwater until her body became limp and then copulated repeatedly with her carcass (Staedler & Riedman, 1993). Ten months later, this same male was observed with the carcass of another female sea otter. In both cases, the male was swimming, diving, guarding, and copulating with the carcass. In other marine mammal species, females and juveniles of both sexes are sometimes injured or killed during mating attempts by male conspecifics (Campagna et al., 1988; Le Boeuf & Mesnick, 1991; Rose et al., 1991; Staedler & Riedman, 1993; Atkinson et al., 1994; Kiyota & Okamura, 2005). A male-biased adult sex ratio might increase the probability of these aggressive and sometimes fatal interactions (Le Boeuf & Mesnick, 1991). Mobbing, in which a group of males attempts to mount a single adult female or an immature seal of either sex, has been documented for Hawaiian monk seals (Monachus schauinslandi) (Johanos & Kam, 1986; Atkinson et al., 1994; Johanos et al., 1994). Associated with severe, sometimes fatal skin and soft tissue lacerations to the dorsal integument (Johanos et al., 1994), mobbing has most often been observed in monk seal populations that have a greater ratio of subadult and adult males compared to breeding-age females (Hiruki et al., 1993).
In the polygynous mating systems of sea otters and many pinnipeds, males typically establish a dominance hierarchy based on age, size, and relative fitness such that subdominant males will have limited access to receptive females of the same species (Le Boeuf, 1972, 1974). Where species overlap geographically, interspecific sexual interactions could be the result of a subdominant male seeking a female surrogate. Male southern sea otters become sexually mature at approximately 5 y of age, although often they are unable to successfully defend territories for several more years (Riedman & Estes, 1990). Sexually mature male sea otters may establish and defend aquatic territories in kelp-dominated regions with high female density from which they exclude all other males except dependent pups and recently weaned immature sea otters. Subadult and adult males that are unable to establish territories are usually segregated from reproductive females and territorial males, aggregating with other nonterritorial males in “male areas” that occur at several locations throughout the range, often in sand-bottom habitats like Monterey Bay (Jameson, 1989; Riedman & Estes, 1990). Many nonterritorial male sea otters frequently move long distances between male areas and travel in winter toward the range peripheries where food resources might be more abundant (Jameson, 1989; Tinker et al., 2008). During the 5 to 10 y leading up to this study, increases in age-specific mortality have disproportionately affected females, with the result that the sex ratio has become skewed toward males (Tinker et al., 2006). An increasingly male-biased sex ratio might have elevated the likelihood of intragender conflicts, including aggressive, forced matings that could result in significant morbidity and mortality. This gender shift in the sea otter population may have triggered the increased aggregation of transient, nonterritorial males in the Monterey Bay region throughout the study period, particularly around Moss Landing. The majority of observed forced copulatory events occurred in Elkhorn Slough in Moss Landing, a region characterized by both a major harbor seal rookery and a large population of nonterritorial male sea otters. Both tagged males that engaged in sexual behavior with harbor seals in the present study appeared to be nonterritorial transients based on direct observation of behavior over prolonged periods. These subdominant sea otters would have been denied access to female conspecifics by territorial males and may have simply redirected normal sexual responses toward sympatric phocids. In the current study, strong links were established between observed interspecific copulatory behavior displayed by male sea otters toward harbor seals and specific lesions found during necropsy of the affected harbor seals. The distribution of superficial wounds in harbor seals preferentially over the nose, eyes, and sides of the face and neck is consistent with typical sea otter mating behavior and correlates with notes from direct observation of these interactions. Based on prior reports (Wilson, 1975; Best et al., 1981; Miller et al., 1996; Mortenson & Follis, 1997; Hayward, 2003), pinniped-initiated mating trauma typically has a more dorsal wound distribution because males grasp females from behind with their front flippers; bite them on the dorsal surface of the head, neck, and body to position them; and use the weight of their bodies on land to restrain females to facilitate copulation (Cline et al., 1971; Le Boeuf, 1972; Allen, 1985; Rose et al., 1991).
Limited postmortem examinations of victims of forced copulatory behavior between pinniped species revealed bleeding skin and soft tissue lacerations and hemorrhage on the dorsal aspect of the head and nape (Miller et al., 1996; Mortenson & Follis, 1997), skull fractures with subcutaneous hemorrhage and ocular proptosis (Miller et al., 1996), chest compression or collapse (Best et al., 1981; Miller et al., 1996), and bruising of the distal vagina (Miller et al., 1996), including one female whose intestines were forced out through the anus as a result of crush injury (Best et al., 1981). Ocular trauma, noted in six harbor seals, is an uncommon mating-associated lesion in female sea otters, presumably because sea otter eyes are much smaller and protrude less from the orbit than those of harbor seals. For affected harbor seals, vision loss due to ocular trauma might have restricted their ability to forage and to evade further attacks by male sea otters. Nine animals examined in depth exhibited vaginal and/or colorectal perforation, which provides strong presumptive evidence for forced copulation. Although spermatozoa were not observed in the rectum/colon or vaginal tract on cytology or histopathology, the ejaculate could have been forced into the abdominal cavity or diluted by seawater or body fluids; the males might not have ejaculated; or they might not have been producing spermatozoa. All of these factors could be an effect of immaturity, advanced age, or incomplete species-specific copulatory behavior. In both harbor seals and sea otters, vaginal perforations and avulsions were invariably located at the junction of the vagina with the cervix as would be predicted with traumatic perforation due to forced penetration, particularly for immature harbor seals with small reproductive tracts. In contrast, perforations of the more fragile, thinnerwalled gastrointestinal tract were often multiple and were spaced at variable sites along the distal colon and rectum. The average length for an adult male sea otter os penis is 15 cm (Kenyon, 1969), which correlates well with the depths of the perforations. As demonstrated by HS 14, penetration of the penis through the intestinal wall can result in severe bleeding and leakage of feces into the pelvic cavity and abdomen, leading to septic peritonitis.
One surprising lesion that was observed only in female harbor seals and sea otters was the development of acute, severe pneumoperitoneum in animals with vaginal and/or gastrointestinal perforations. Forced copulation resulted in the passage of air from the vaginal lumen or rectum into the abdomen. These perforations appear to have functioned as one-way valves in some cases, allowing air that was forced in during and after copulation to become trapped in the peritoneum under high pressure. This resulted in a severely distended, tympanic abdominal wall and marked cranial displacement of the diaphragm, leading to tension pneumoperitoneum and increased intraabdominal pressure. The end result was restricted diaphragmatic movement, compression of the thoracic cavity, and severe pulmonary atelectasis. In addition, secondary compression of the vena cava, as seen in SO 2, can also limit venous return, resulting in hypotension, hypoxia, and, in severe cases, acute respiratory distress and circulatory collapse (Kim et al., 2000). In all three cases, the diaphragm was displaced so far cranially and the thoracic cavity so tightly compressed by highpressure air in the abdomen, it was deemed to be acutely life threatening. As observed for SO 1 while alive, free peritoneal air can also significantly increase buoyancy and negatively impact an animal’s ability to dive and forage.
All three animals with pneumoperitoneum exhibited perforation or avulsion of the vaginal tract. One sea otter with pneumoperitoneum had perforations of both the vagina and distal colon, but none of the harbor seals with only colorectal perforations exhibited pneumoperitoneum, indicating that development of tension pneumoperitoneum was more closely associated with vaginal perforation in these animals. However, gastrointestinal perforation cannot be excluded as a potential cause of pneumoperitoneum. In humans, pneumoperitoneum has been reported secondary to colorectal perforation during colonoscopy (Marwan et al., 2007) and introduction of compressed air into the rectum (Kim et al., 2000) but has not been reported in association with anal intercourse. Interestingly, postcoital pneumoperitoneum also has been reported in humans after vigorous sexual intercourse, both secondary to vaginal perforation (Lal et al., 2001; Manchanda & Refaie, 2005) and with an intact vaginal wall (Angel et al., 1988; Johnson et al., 2002). Patients have presented with abdominal distention, abdominal tenderness, vomiting, shoulder pain, dyspnea, and pain on inspiration. In all cases, radiographs revealed free intraperitoneal gas beneath the diaphragm. During sexual intercourse, the penis functioned like a piston, creating a closed system that forced air through a vaginal tear into the peritoneum (Lal et al., 2001; Manchanda & Refaie, 2005); or through the cervix, into the uterus, and out through the fallopian tubes (Angel et al., 1988; Johnson et al., 2002). In humans, this latter event might occur as a result of penile-vaginal disproportion (Manchanda & Refaie, 2005), or for patients in the recent postpartum period (4 to 9 wks postpartum), the cervix could be sufficiently dilated to facilitate passage of air into the uterus during coitus (Angel et al., 1988; Johnson et al., 2002). This could have been a contributing factor for both SO 1 (10 wks postpartum) and SO 2 (dilated cervical os and full-term fetus in the pelvic canal at the time of forced copulation).
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