Modulation in Persistent Organic Pollutant Concentration and Profile by Prey Availability and Reproductive Status in Southern Resident Killer Whale Scat Samples

Abstract

Persistent organic pollutants (POPs), specifically PCBs, PBDEs, and DDTs, in the marine environment are well documented, however accumulation and mobilization patterns at the top of the food-web are poorly understood. This study broadens the understanding of POPs in the endangered Southern Resident killer whale population by addressing modulation by prey availability and reproductive status, along with endocrine disrupting effects. A total of 140 killer whale scat samples collected from 54 unique whales across a 4 year sampling period (2010-2013) were analyzed for concentrations of POPs. Toxicant measures were linked to pod, age, and birth order in genotyped individuals, prey abundance using open-source test fishery data, and pregnancy status based on hormone indices from the same sample. Toxicant concentrations were highest and had the greatest potential for toxicity when prey abundance was the lowest. In addition, these toxicants were likely from endogenous lipid stores. Bioaccumulation of POPs increased with age, with the exception of presumed nulliparous females. The exceptional pattern may be explained by females experiencing unobserved neonatal loss. Transfer of POPs through mobilization of endogenous lipid stores during lactation was highest for first-borns with diminished transfer to subsequent calves. Contrary to expectation, POP concentrations did not demonstrate an associated disruption of thyroid hormone, although this association may have been masked by impacts of prey abundance on thyroid hormone concentrations. The noninvasive method for measuring POP concentrations in killer whales through scat employed in this study may improve toxicant monitoring in the marine environment and promote conservation efforts.

Population growth is limited by nutritional impacts on pregnancy success in endangered Southern Resident killer whales (Orcinus orca)

“…Lundin et al [8,50] showed that POPs, namely PCBs, DDTs, and PBDEs, increase in circulation in SRKWs when Fraser River Chinook abundance is lowest, presumably due to increased fat metabolism in response to nutritional stress. Mobilization of contaminants into circulation also occurs during the energetic demands of lactation, with an estimated 70–90% lactation transfer of maternal toxicant burden in primiparous females [51].…”

“…High POP burden has specifically been associated with disruption of reproduction success and reduced calf survival in marine mammals [52–55]. Most notably, Lundin et al [8] found increased Persistent PCBs, the group of PCBs considered more persistent and more toxic [56], in the female whales classified with UPg’s (73%; 95% CI, 61–85) compared to all other female reproductive groups (range 43–56%). Further evidence in support of the occurrence of UPg in this population is the unexpected inverse in bioaccumulation of POPs with age in “nulliparous” mature females (3 of 4 nulliparous whales had an unsuccessful pregnancy defined by fecal hormone measures).…”

“…All correlations between hormone concentrations and fish abundance used Albion Test Fishery CPUE data lagged by 12 days from the time a sample was collected; the 12 day lag was derived from estimates of Chinook swim time from the study area to the test fishery, which was also in agreement with the lag time that resulted in the best fit model between prey abundance and nutritional hormones [5,8]. The CPUE data were log 10 transformed to achieve normality.…”

“…Only 78 individuals (J pod = 24 individuals; K pod = 19 individuals; L pod = 35 individuals) remain in the current population as of December, 2016 [3]. Reduced availability of their preferred prey, threatened and endangered Chinook salmon, appears to be at the core of the SRKW decline [4–7], although exposure to toxicants [8], and pressure from vessel disturbance may also contribute to these cumulative effects [9]. …”

Climate change–contaminant interactions in marine food webs: Toward a conceptual framework

“…Reduced abundance of their primary prey, Chinook salmon ( Oncorhynchus tshawytscha ), during warming ocean episodes has coincided with subsequent periods of higher mortality in resident killer whale populations (Ford et al., ). As PCBs are fat‐soluble contaminants that amplify in food webs, productivity‐related reduction in lipids may concentrate PCBs in the diminishing blubber stores of marine mammals (Jenssen et al., ; Lundin et al., ; McKinney et al., ; Ross et al., ). While pollution risks by PCBs, noise and disturbance, and reduce prey abundance (i.e., Chinook salmon) are known to affect these killer whales (Alava et al., ; Cullon et al., ; Ford et al., ; Hickie et al., ; Lundin et al., ; Ross et al., ), the combined impact of climate change and PCBs on this top predator and its prey is poorly understood.…”