Reproductive Failure in UK Harbour Porpoises Phocoena phocoena: Legacy of Pollutant Exposure?

Abstract

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 of summed 25 polychlorinated biphenyls congeners (∑PCBs lipid weight) in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). In sexually mature females, 25/127 (19.7%) showed direct evidence of reproductive failure (foetal death, aborting, dystocia or stillbirth). A further 21/127 (16.5%) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. Resting mature females (non-lactating or non-pregnant) had significantly higher mean ∑PCBs (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. 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. Furthermore, a lower pregnancy rate of 50% was estimated for "healthy" females that died of traumatic causes of death, compared to other populations. Whether or not PCBs are part of an underlying mechanism, we used individual PCB burdens to show further evidence of reproductive failure in the North-east Atlantic harbour porpoise population, results that should inform conservation management.

Fig 1. Frequency distribution of age profiles for female reproductive status categories in UK stranded harbour porpoises (n = 250).

Fig 2. Total number of corpora scars (corpora albicantia and corpora lutea) in UK stranded harbour porpoise ovaries as a function of age (n = 225).

Dashed box highlights three females that presented with higher than expected number of corpora scars.

Fig 3. ΣPCBs as a function of (a) corpora scar number (n = 266) and (b) age (n = 254).

Graphs exclude two neonates ranging between 86.9–159.7 mg/kg in ΣPCBs. Blue line represents the threshold level (9 mg/kg ΣPCBs mg/kg lipid) for adverse health effects.

Fig 4. Accumulation of PCBs with age in male stranded UK harbour porpoises.

Fitted regression line and 95% CI values are shown, n = 257. Annual ΣPCB accumulation rate is 1.11 mg/kg.

Fig 5. Box plots of (a) female reproductive status and ΣPCBs, and (b) cause of death groups and ΣPCBs.

The dark horizontal line indicates the median, and the dashed blue line the mean. Outliers are highlighted by blue circles.