Abstract
Polychlorinated biphenyls (PCBs) are highly toxic and persistent aquatic pollutants that are known to bioaccumulate in a variety of marine mammals. They have been associated with reduced recruitment rates and population declines in multiple species. Evidence to date documents effects of PCB exposures on female reproduction, but few studies have investigated whether PCB exposure impacts male fertility. Using blubber tissue samples of 99 adult and 168 juvenile UK-stranded harbour porpoises (Phocoena phocoena) collected between 1991 and 2017, here we show that PCBs exposures are associated with reduced testes weights in adults with good body condition. In animals with poor body condition, however, the impact of PCBs on testes weights was reduced, conceivably due to testes weights being limited by nutritional stress. This is the first study to investigate the relationship between PCB contaminant burden and testes weights in cetaceans and represents a substantial advance in our understanding of the relationship between PCB exposures and male reproductive biology in cetaceans. As testes weight is a strong indicator of male fertility in seasonally breeding mammals, we suggest the inclusion of such effects in population level impact assessments involving PCB exposures. Given the re-emergent PCB threat our findings are globally significant, with potentially serious implications for long-lived mammals. We show that more effective PCB controls could have a substantial impact on the reproductive health of coastal cetacean species and that management actions may need to be escalated to ensure adequate protection of the most vulnerable cetacean populations.
Highlights
Polychlorinated biphenyls (PCBs) are a group of toxic chemicals compounds that were banned in the EU in the mid-1980s and have been linked to numerous health effects in humans and wildlife (Folland et al, 2016; Liu et al, 2010)
We found that the relationship between PCB blubber concentrations and testes weights is dependent on nutritional condition, whereby PCBs have a greater influence on testes weights in animals that are in good body condition
That PCB concentrations found in the blubber of mature harbour porpoises in good nutritional condition, are negatively associated with testes weights
Summary
Polychlorinated biphenyls (PCBs) are a group of toxic chemicals compounds that were banned in the EU in the mid-1980s and have been linked to numerous health effects in humans and wildlife (Folland et al, 2016; Liu et al, 2010). If PCB burdens can impact both male and female fertility this could have serious consequences on the longterm population viability of marine apex predator populations that are highly-exposed to PCBs. Here, we have used the largest cetacean toxicology strandings dataset globally available to investigate, for the first time, the relationship between PCB blubber concentrations and testes weights in harbour porpoises. We have used the largest cetacean toxicology strandings dataset globally available to investigate, for the first time, the relationship between PCB blubber concentrations and testes weights in harbour porpoises It has been shown previously, in this population, that the reproductive output of healthy females is almost half that of other, less contaminated, populations and it has been hypothesised that reproductive dysfunction in these individuals may be related to PCB exposure (Murphy et al, 2015; Ólafsdóttir et al, 2003). This will help determine whether current risk assessments, which do not account for the possible compounding impacts of reduced male fertility, are appropriate or whether they potentially underestimate the risk posed to populations
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