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Modulation in persistent organic pollutant concentration and profile by prey availability and reproductive status in Southern Resident killer whale scat samples Jessica I. Lundin, Gina Ylitalo, Rebecca K. Booth, Bernadita Anulacion, Jennifer Hempelmann, Kim Parsons, M. Bradley Hanson, and Samuel K. Wasser Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b00825 • Publication Date (Web): 17 May 2016 Downloaded from http://pubs.acs.org on May 23, 2016
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Modulation in persistent organic pollutant concentration and profile by prey availability and reproductive status in Southern Resident killer whale scat samples
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Authors: Jessica I. Lundina,*, Gina M. Ylitalob, Rebecca Bootha, Bernadita Anulacionb, Jennifer A. Hempelmannb, Kim M. Parsonb,c, M. Bradley Hansonb, Samuel K. Wassera
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Author affiliations: aCenter for Conservation Biology, Department of Biology, University of Washington, Seattle, WA; bNorthwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA; cAlaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA
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*Corresponding author:
Jessica I. Lundin, Ph.D. Department of Biology Center for Conservation Biology Johnson Hall 231, Box 351800 Seattle, WA 98195 Telephone: 206-552-3698 Fax: 206-616-2011 Email:
[email protected] 1 ACS Paragon Plus Environment
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Persistent organic pollutants (POPs), specifically PCBs, PBDEs, and DDTs, in the marine
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environment are well documented, however accumulation and mobilization patterns at the top of
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the food-web are poorly understood. This study broadens the understanding of POPs in the
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endangered Southern Resident killer whale population by addressing modulation by prey
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availability and reproductive status, along with endocrine disrupting effects. A total of 140 killer
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whale scat samples collected from 54 unique whales across a 4-year sampling period (2010-
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2013) were analyzed for concentrations of POPs. Toxicant measures were linked to pod, age,
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and birth order in genotyped individuals, prey abundance using open-source test fishery data, and
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pregnancy status based on hormone indices from the same sample. Toxicant concentrations were
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highest and had the greatest potential for toxicity when prey abundance was the lowest. In
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addition, these toxicants were likely from endogenous lipid stores. Bioaccumulation of POPs
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increased with age, with the exception of presumed nulliparous females. The exceptional pattern
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may be explained by females experiencing unobserved neonatal loss. Transfer of POPs through
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mobilization of endogenous lipid stores during lactation was highest for first-borns with
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diminished transfer to subsequent calves. POP concentrations did not demonstrate an associated
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disruption of thyroid hormone, which was expected, although this association may have been
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masked by impacts of prey abundance on thyroid hormone concentrations. The noninvasive
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method for measuring POP concentrations in killer whales through scat employed in this study
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may improve toxicants monitoring in the marine environment and promote conservation efforts.
ABSTRACT
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INTRODUCTION
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Persistent Organic Pollutants (POPs) are lipophilic compounds that are resistant to degradation.
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As apex predators, odontocete (toothed) whales are susceptible to pronounced biomagnification
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of POPs.1, 2 The endangered Southern Resident killer whale (SRKW; Orcinus orca) population,
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consisting of 3 family groups, or pods, referred to as J, K, and L, experienced an unexplained
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20% decline in their population in the late 1990s. Exposure to POPs associated with deleterious
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physiologic effects,3 particularly polychlorinated-biphenyls (PCBs), polybrominated
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diphenylethers (PBDEs), and dichloro-diphenyl-trichloroethanes (DDTs), as well as decreased
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prey availability, were proposed as major risk factors to this population in the Recovery Plan,3
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and remain current threats.4 The SRKW population forage almost exclusively on salmonids
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between late spring and fall, particularly Fraser River Chinook salmon (Oncorhynchus
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tshawytscha).5-7 Diet has been highlighted as the most likely source of exposure to POPs for
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SRKWs.8, 9
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POPs are lipophilic compounds that readily bioaccumulate in adipose tissue. The concentration
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of these toxicants generally increase with age, particularly the POPs more resistant to
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biotransformation.10, 11 It is hypothesized that systemic concentrations of these compounds, and
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associated bioavailability to target organs, increase when fat-metabolism occurs in response to
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decreased prey availability.12 Lactating females also mobilize endogenous free fatty acid and
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lipoprotein stores during milk production; 2-4 kg of milk converts to 1 kg of calf mass gain,13
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consequently transferring high-levels of toxicants to nursing young. Decreased POP loads have
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been reported in lactating female killer whales,14 harp seals (Phoca groenlandica),15 gray seals
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(Halochoerus gryous),16-18 and polar bears (Ursus maritimus)19.
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Blubber biopsy samples previously collected on the SRKWs indicate that PCB exposures in this
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population exceed a toxicity threshold for marine mammals (17,000 ng/g lipid) extrapolated
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from studies of immunologic and reproductive effects in seals, otters, and mink.14, 20-22
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Additionally, POPs can disrupt endocrine systems through interference with cellular messaging
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systems (i.e., hormones) responsible for the regulation of developmental processes, metabolism,
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immune function, and reproduction.23 Risk assessments of other cetacean populations suggest
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that current levels of contamination may impair immune24-28 and reproductive
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systems.29-34
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The ability to test hypotheses relating to temporal trends in bioaccumulated toxins has been
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constrained by low sample acquisition of tissue biopsies, or collections from necropsied animals.
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In this study we capitalized on a novel sample collection approach to monitor trends in toxicant
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concentrations across seasons and years using killer whale fecal samples.35, 36 Concentration and
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chemical profile of circulating toxicants were characterized by prey abundance, age-sex class,
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and reproductive class in this endangered SRKW population. Endocrine disruption from
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toxicant exposure was evaluated using hormone measures37, 38 from the same scat samples.
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METHODS
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Sample collection
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A total of 263 SRKW scat samples were collected May through October from 2010 to 2013.
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Samples were located by detection dogs trained to locate SRKW scat floating on the water’s
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surface.39-41 Samples were scooped off of the surface of the water, as previously described,35 and
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frozen at -20 ºC until processed in the lab. Collections occurred from mid-May through mid-
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October, when the SRKWs appear with regularity in the areas around the San Juan Islands and
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Puget Sound of Washington state, collectively referred to as the Salish Sea. The study period
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aligned with peak run times for Fraser River Chinook salmon, the preferred seasonal prey of the
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SRKWs.7
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Life history data
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Age, sex, family lineage, and reproductive status of whales genotyped in this study were
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determined using annual population census data collected through photo-identification since
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1976 by the Center for Whale Research.42 Age-sex class43-45 was defined as juveniles (either
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sex,
