CORDIS - EU research results

The independent and interactive effects of multiple stressors on reproduction and development in cetaceans

Final Report Summary - CETACEAN-STRESSORS (The independent and interactive effects of multiple stressors on reproduction and development in cetaceans)

This project aimed to assess the potential interactive effects of individual and multiple stressors on reproduction in cetaceans. As well as identify the potential importance of individual stressors as contributors to risk. The short-beaked common dolphin (Delphinus delphis), an abundant species that frequently strands in the North East Atlantic (NEA) and New Zealand (NZ) and inhabits waters of the Hauraki Gulf, NZ year-round, will be the one of the focal species within the study, in addition to the harbour porpoise in the NEA. Tasks involved undertaking detailed necropsies of stranded animals in the UK and NZ for sampling and assessing health status, and analysis of ‘historical’ samples and data; assessment of age, diet, nutritional condition, blubber sex hormone levels, evidence of acute and chronic stress, and pollutant levels in individuals (sum25PCBs lipid); and investigation of gonadal form and function, with a focus on genital system pathologies - including the identification of reproductive and developmental toxicological endpoints.

The main analyses to date revealed evidence of reproductive dysfunction in both NEA harbour porpoises and common dolphins. For both species, NE Atlantic populations exhibited lower pregnancy rates and longer calving intervals than other populations of conspecifics; including common dolphins in NZ waters, with an estimated pregnancy rate of 36% vs. 26% for common dolphins in the NEA. As female cetaceans can offload their lipophilic pollutant burdens through transplacental transfer and primarily lactation as pollutants are mobilised from blubber to lipid rich milk, we assessed for evidence of reproductive failure both directly, e.g. through observations of foetal death, and indirectly by using individual PCB burdens. Results suggested that reproductive failure could have occurred in up to 39% or more of mature female porpoises (19.7%, 25 of 127, of which were from direct observations of foetal death, aborting, dystocia or stillbirth). Within the mature sample, 18.9% (24 of 127) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. These included malignant tumours such as cervix squamous cell carcinoma, benign tumours such as leiomyoma, papilloma-like lesions and vaginal plaques, endometritis, and other infections and inflammations of the reproductive tract. Some of these were previously reported as reproductive and endocrine toxicity endpoints in animals and humans.

Reproductive failure in mammals due to exposure to polychlorinated biphenyls (PCBs) can occur either through endocrine disrupting effects or via immunosuppression and increased disease risk. To investigate further, full necropsies and determination sumPCBs lipid weight in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). Resting mature females (non-lactating or non-pregnant) had significantly higher mean sumPCBs (18.5 mg/kg) than both lactating (7.5 mg/kg) and pregnant females (6 mg/kg), though not significantly different to sexually immature females (14.0 mg/kg). Using multinomial logistic regression models ΣPCBs was found to be a significant predictor of mature female reproductive status, adjusting for the effects of confounding variables such as age, nutritional status, health status, season etc. Resting females were more likely to have a higher PCB burden. Health status (proxied by “trauma” or “infectious disease” causes of death) was also a significant predictor, with lactating females (i.e. who successfully reproduced) more likely to be in good health status compared to other individuals. Based on contaminant profiles (>11 mg/kg lipid), at least 29/60 (48%) of resting females had not offloaded their pollutant burden via gestation and primarily lactation. Where data were available, these non-offloading females were previously gravid, which suggests foetal or newborn mortality. Further, 12.6% of the mature female sample presented with evidence of foetal death or abortion during their second and third trimesters. There was no significant interaction among variables health status and ΣPCBs in the multinomial model, however PCBs-mediated effects on reproduction could arise via immunosuppression and increased disease risk. Female’s health status played an important factor in the occurrence of reproductive failure, as 86% of the foetal death/aborting group died as a result of infectious disease or other causes such as starvation and neoplasia – though on the whole nutritional status was adequate and thus was not a limiting factor in reproductive success.

Ultimately difficulties arose in showing casual associations between cases of reproductive dysfunction and sumPCBs concentration due to female’s capabilities in offloading pollutant burdens. Nevertheless, when all ages were considered 47% of individuals in the current study had ∑PCBs concentrations above the threshold for adverse health effects in marine mammals, which included 52% of sexually immature females and 53% of resting mature females.

A similar analysis was undertaken on common dolphins. However, only females classified as “healthy” were included in the analysis, i.e. females that individuals were not suffering from any infectious and non-infectious disease that might inhibit reproduction and were in good to moderate nutritional condition. Within this sample 26% (6 of 23) of mature females exhibited evidence off reproductive failure. In these cases, female pollutant burdens ranged from 17.9 to 62.4 mg/kg sum25PCBs lipid. A larger sample size of common dolphins was used to assess for evidence of reproductive dysfunction and 15.8% (17 of 107) of individuals presented with reproductive system pathologies. These included precocious mammary gland development in sexually immature females, vagina calculi, ovarian tumours (including a rare case of either a Mesothelioma or Schwannoma tumour), atrophic ovaries and the first reported case of an ovotestis in a cetacean species. Where pollutant data were available, the majority of females were above the threshold for adverse health effects in marine mammals.

Preliminary results suggest that reproductive dysfunction in NEA harbour porpoises and common dolphins may be related to PCB exposure occurring either through endocrine disrupting effects or via immunosuppression and increased disease risk. Declines of major organochlorine concentrations in biota have been slow due to global cycling and long-half lives of pollutants (up to 100 years), and as of 2005 1.1 million ton of PCB containing equipment, corresponding to 350,000 ton of PCB containing liquid, still required disposal by EU Member States. Taking this into consideration, as well as inherited maternal pollutant burdens in first born offspring and generational epigenetics effects, raises concerns about the current and future population-level effects of PCBs on the North-east populations of harbour porpoises and common dolphins.
For conservation strategies to be successful, it is important to understand the causes of any identified trend in abundance and the physiological and pathological responses of organisms to their changed environment. This project confronted an important emerging challenge in marine conservation within and outside Europe, how to assess the effects of individual and multiple stressors on reproduction and development in cetaceans. A greater scientific understanding of processes limiting reproductive success will help in conservation management of European cetacean species. Results will enable a broader understanding of the impact of stressors on reproductive physiology and pathology which is essential for the conservation and management of both populations. Results from this study are being disseminated at a number of inter-governmental meetings, conferences and workshops. Results will feed into the implementation of the ASCOBANS Conservation Plan for the Harbour Porpoise in the North Sea, as well as a draft Conservation Plan for the North-east Atlantic Common Dolphin Population that will be submitted by the Fellow to CMS/ASCOBANS in September 2015.