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Males of several seal species are known to show aggressive copulating behaviour, which can lead to injuries to or suffocation of females. In the North Sea, grey seal predation on harbour seals including sexual harassment is documented and represents violent interspecific interaction.
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Read More »The presented fatal cases of 11 adult, female harbour seals could be traced back to interspecific copulation with a grey seal bull via detection of spermatozoal structures in the female reproductive tracts as well as grey seal DNA verification. Pathological changes seen in the genital tracts included haemorrhagic or suppurative vaginal discharge, genital lacerations and abortion. Death occurred due to septicaemia with β-haemolytic streptococci. The narrow period, within which the strandings happened, coincided with the breeding season of grey seals in the North Sea. As such incidences have not been reported before in the Wadden Sea area, they provide new insights into interspecific interactions between the two native seal species. The majority of annually recovered seals by the German stranding scheme are juveniles34. Previous instances of unusually large numbers of adult mortalities were exclusively seen during the epizootic events caused by influenza and morbillivirus34,35,36. However, this was excluded in the present case as the virological tests were all negative. Furthermore, it is exceptional that only females were affected that were either pregnant or at least demonstrated a recent pregnancy. This fact also doubles the death toll to potentially 22 animals in the context of this event. In contrast to the winter breeding season of grey seals, the pupping season of harbour seals in the Wadden Sea starts in June48. Both, the pregnancy as well as the season allows the assumption that the female harbour seals themselves were not interested in mating at this point. Along the coastline of Dithmarschen, there are several sandbanks close to the shore, where harbour seals haul out routinely and grey seals are known to visit these occasionally. Seals are generally polygamous and depending on the group size, the sex ratio and the social system, different aggressive mating strategies can develop53,56,57,58,59. Injuries during interspecific interactions become more likely if there is great disparity in size and weight52. This is also reported for the here involved species, as a juvenile or young adult grey seal bull can easily over-power and subdue a female harbour seal25,26,60. The behavioural response of the female during mating is important for the stimulation of the male. If the female is incompatible, juvenile, seriously injured, or dead, the response may be inadequate and could result in multiple mountings and/ or longer mating attempts11,19. In the presented cases, vaginal discharge and a swelling of the vulva in some cases were the only external lesions. Microbiological investigations of the 11 female carcasses revealed synergistic β-haemolytic streptococci infections together with E. coli in various organs. It is known that the changed immune response and physiology during pregnancy may facilitate septic infections with fatal progression49. This also might have been a driving co-factor of the presented cases. In pinnipeds, β-haemolytic streptococci are commensal bacteria and range among the most frequently detected pathogens regarding secondary septic infections50,51. A mass die-off in cape fur seals (Arctocephallus pusillus) including abortions in high numbers was attributed to starvation, high parasite burdens and following secondary infections with β-haemolytic streptococci52. Similarly, in German waters, high parasite loads and associated morphological changes in the respiratory or digestive tract often lead to secondary septicaemia in seals34. In contrast to this, the herein reported harbour seals were all in good nutritional status with low parasite burdens. Furthermore, a retrospective data analysis revealed that from 2015–2020, nine out of 24 adult female harbour seals retrieved from the German North Sea died due to septicaemia with β-haemolytic streptococci and Escherichia coli. In four cases, the animals had suffered from serious alterations of mainly the gastrointestinal tract, leading to the septic spread of these opportunistic bacteria. Of the 11 female harbour seals, six showed vaginal and/ or uterine lacerations, where the bacteria could have entered the bloodstream. Additionally, superficial lesions (erosions and ulcerations) can disrupt the epithelial barrier function of the vagina and facilitate the entry of opportunistic pathogens leading to infection. The haemorrhagic discharge and microscopically verified vaginitis underline an intra vital vaginal defect and infection in the six animals. However, macroscopically, lacerations or inflammation of the genital tract could not be documented in all seals. Histological analysis verified hyperaemia and haemorrhages in several organs as typical findings of septicaemia. As there were no signs of either haematoma in soft tissues or bone or cartilage fractures, the contribution of blunt trauma and/ or compression to the haemorrhages cannot be finally clarified. Furthermore, fibrino-suppurative inflammation in the reproductive tracts with intralesional spermatozoal heads were found in three out of six sampled animals. The embedding of spermatozoa within the inflammatory exudate is an indicator of intra vital copulation. Using transmission electron microscopy, the detached tails of the spermatozoa were depictable within a meshwork of extravasated fibrin (see supplementary materials, Fig. 1). The disintegration of spermatozoal structures reflects autolytic and heterolytic processes. Still, it is not possible to use the decomposition status of the spermatozoa to suggest a specific timeframe of copulation. The genital lacerations point towards traumatic copulation and to an assailant larger than a harbour seal. All formalin-fixed and paraffin-embedded (FFPE) tissues of harbour seal reproductive tracts with histological spermatozoa were tested via PCR and contained grey seal DNA. FFPE samples of other organs of the affected animals, as well as unrelated cases retrieved from the local archive were used as control samples to exclude false positive signals due to contamination and did not contain grey seal DNA. Environmental contamination of the harbour seal reproductive tracts with grey seal DNA to an extent causing a positive PCR reaction still seems unlikely. Therefore, it can be assumed that the spermatozoa within the samples are of direct grey seal origin. As stated before, male intromission and ejaculation in interspecific mating attempts is not always successful due to anatomical and behavioural incompatibility11,20,22,53. Accordingly, intralesional sperm is not an obligatory finding in suspected cases of interspecific mating, but it can be critical for identifying the assailant.
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Read More »There are reports of necrophilia in marine mammals and other clades11,19,53,54. In the reported cases with intralesional spermatozoa, an inflammatory response with extravasation of proteinaceous fluid and fibrin, engulfing the spermatozoal heads, underlined an intra vital process. Still, it cannot be excluded that tissue defects without haemorrhage or signs of inflammation are the result of post-mortem mountings. Feeding on victims that died after violent inter- or intraspecific encounters is not reported in other seal species11,20. This might be different in grey seals, as coercive behaviour and predation are sometimes displayed simultaneously43. Most reports of mating-related trauma in pinnipeds refer to external, dorsal head and neck wounds of females after being bitten, pinned down or dragged by males13,55,56,57. Whereas likewise observations for aggressive mating behaviour and external lesions exist for many other vertebrate classes, evidence of internal injuries remains scarce55,58. A well-documented case was reported in several male southern sea otters (Enhydra lutris nereis) force-copulating with juvenile Pacific harbour seals (Phoca vitulina richardsi)53. Necropsies in eight cases revealed vaginal and colorectal perforations of 1–3 cm in size and even a vaginal-cervical translocation in one case. The perforations seen in the vagina were typically located on the dorsal and lateral side. As a result of the lesions, the animals died after developing peritonitis and sepsis. Five out of six lacerations seen in the reproductive tracts of the 11 female harbour seals were also located dorsally in the vagina and/ or uterus. Together with the septic infections caused by β-haemolytic streptococci, there are clear analogies to the reported cases in sea otters. The lacerations of the uterus in two of the presented cases, as well as the dislocation of the foetus into the abdomen could not be explained by penile penetration alone, although the vaginal anatomy of harbour seals indicates that the depth of penetration depends only on the length of the penis22. In the case of a male elephant seal (Mirounga leonina) mounting female cape fur seals (Arctocephalus pusillus), it was observed that the weight of the male forced out the females intestines through the anogenital region20. Even a juvenile male grey seal can outweigh a female harbour seal28,29, but it remains unclear whether the mounting of pregnant females alone can lead to lacerations in the reproductive tract. Rupture of the gravid uterus is reported to be a rare event, and is often associated with severe abdominal trauma or fragility of the uterine wall due to infections or previous operations59. In the reported cases, it cannot be excluded that ascending infections or sepsis led to structural weakness of the uterus with secondary rupture. Since there were no observations of the encounters in the described cases, the extent of violence during the mating attempts and their possible contribution to the genital trauma, as seen in other cases11,19, cannot be assessed.
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Read More »Grey seals are known to engage in inter- and intraspecific interactions, including predation43, cannibalism39,40,41,42 and forced sexual intercourse21 with harbour seals in the wild. The present study is the first one reporting fatal interspecific mating attempts of at least one male grey seal with pregnant harbour seals in the German Wadden Sea. It remains unclear if the described cases are an exception caused by one individual on a local scale. Therefore, future post-mortem investigations should always include a precise examination of genital tracts of harbour seals especially during the grey seal mating season.
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