Serum POP concentrations are highly predictive of inner blubber concentrations at two extremes of body condition in northern elephant seals

Highlights

• Serum was a strong predictor of inner blubber for DDTs, PCBs, CHLs, and PBDEs.

• Relationships between serum and outer blubber were stronger for males than females.

• Higher blubber/serum partitioning coefficients in early breeding than late molting.

• Predictive equations provided for seals at two extremes of body condition.

Abstract

Long-lived, upper trophic level marine mammals are vulnerable to bioaccumulation of persistent organic pollutants (POPs). Internal tissues may accumulate and mobilize POP compounds at different rates related to the body condition of the animal and the chemical characteristics of individual POP compounds; however, collection of samples from multiple tissues is a major challenge to ecotoxicology studies of free-ranging marine mammals and the ability to predict POP concentrations in one tissue from another tissue remains rare. Northern elephant seals (Mirounga angustirostris) forage on mesopelagic fish and squid for months at a time in the northeastern Pacific Ocean, interspersed with two periods of fasting on land, which results in dramatic seasonal fluctuations in body condition. Using northern elephant seals, we examined commonly studied tissues in mammalian toxicology to describe relationships and determine predictive equations among tissues for a suite of POP compounds, including ΣDDTs, ΣPCBs, Σchlordanes, and ΣPBDEs. We collected paired blubber (inner and outer) and blood serum samples from adult female and male seals in 2012 and 2013 at Año Nuevo State Reserve (California, USA). For females (N = 24), we sampled the same seals before (late in molting fast) and after (early in breeding fast) their approximately seven month foraging trip. For males, we sampled different seals before (N = 14) and after (N = 15) their approximately four month foraging trip. We observed strong relationships among tissues for many, but not all compounds. Serum POP concentrations were strong predictors of inner blubber POP concentrations for both females and males, while serum was a more consistent predictor of outer blubber for males than females. The ability to estimate POP blubber concentrations from serum, or vice versa, has the potential to enhance toxicological assessment and physiological modeling. Furthermore, predictive equations may illuminate commonalities or distinctions in bioaccumulation across marine mammal species.

Introduction

Persistent organic pollutants (POPs) are lipophilic environmental contaminants that are pervasive in marine food webs and bioaccumulate in organisms, which presents particular concern for long-lived, upper trophic level marine mammals. Although close proximity to POP sources can result in higher POP concentrations (Frouin et al., 2011), even foraging strategies that place animals far from contaminant sources do not insulate them from POP exposure (Peterson et al., 2015). Elevated concentrations of POPs are associated with endocrine, immune, and reproductive effects in marine and terrestrial wildlife (Tanabe, 2002, Debier et al., 2005, Desforges et al., 2016). Among marine mammals, pinnipeds and odontocetes are vulnerable to biomagnification of POPs due to their high trophic position, and therefore are often the target species for POP biomonitoring efforts (Weijs et al., 2010, Yordy et al., 2010b, Lopez et al., 2012).

The internal tissues of marine mammals accumulate and mobilize POPs at varying rates, which presents challenges for interpretation. Blood and blubber are commonly studied tissue compartments because they can be sampled non-lethally and are relatively accessible to researchers. Blood is advantageous for study because it is in direct contact with internal tissues of toxicological concern, including the liver and other organs, and it is responsive to recent foraging (De Swart et al., 1996) or fasting (Louis et al., 2014). Therefore, blood can serve as a relevant indicator of recent contaminant exposure or a reflection of changes in physiological state that may liberate contaminants from storage tissues into circulation. Blood collection from live pinnipeds is generally less invasive than blubber collection, and many studies may store blood samples long term, often the serum or plasma compartments, that could be utilized to compare contaminant exposure over time; however, the relationship between blood and blubber layers may be inconsistent (Lyderson et al., 2002). In contrast, blubber is a lipid-rich tissue used for energy storage in both pinnipeds and odontocetes (Koopman et al., 1996, Strandberg et al., 2008). Within the vertical profile of the blubber layer, metabolic activity and fatty-acid mobilization vary, with inner blubber more metabolically active than outer (Strandberg et al., 2008, Fowler et al., 2014). While recent events such as foraging or fasting may impact contaminant concentrations in blood and inner blubber (Louis et al., 2014), outer blubber or full thickness blubber cores may provide a more relevant indicator of longer-term bioaccumulation (Randhawa et al., 2015). Blubber is often collected in pinnipeds and cetaceans, and in some cases it is the only tissue available to study (e.g., Baron et al., 2015, Hunt et al., 2015).

Northern elephant seals (Mirounga angustirostris) are upper trophic level predators that bioaccumulate POPs as they forage in the northeastern Pacific Ocean (Peterson et al., 2015). The life history of northern elephant seals includes two foraging migrations per year interspersed with fasting periods for breeding and molting on land, which makes them relatively accessible for study among marine mammals (Robinson et al., 2012). Additionally, foraging and fasting life-history phases create dramatically different seasonal body conditions. For example, during the molting fast females spend roughly 4–6 weeks fasting and lose approximately 25% of their mass, of which 41% comes from fat stores (Worthy et al., 1992). Females then go to sea and forage for approximately 7 months, during which time they undergo a 95% mean mass gain (Robinson et al., 2012). At the end of their foraging trip, females return to land and undergo a breeding fast, lasting approximately 4–6 weeks, which occurs as they give birth to a pup and lactate, and results in loss of approximately 40% of their body mass and 57% of their fat stores (Costa et al., 1986, Crocker et al., 2001). After breeding, females once again return to sea for a shorter 2–3 month foraging trip, which ends when they return to land for molting (Robinson et al., 2012). Males undergo a similar proportional loss of body mass (34–41%) and fat stores (54–59%) while on shore for fasting (Deutsch et al., 1990, Crocker et al., 2012). The male breeding fast is longer than females, lasting approximately 2–3 months, while the male molting fast is approximately 4–6 weeks in duration (Le Boeuf et al., 2000). The two male foraging trips at sea each year are similar to each other in duration, lasting approximately 4 months each (Le Boeuf et al., 2000). Because body condition is an important determinant of POP concentrations in blood and blubber (Peterson et al., 2014), effective toxicological risk assessment relies upon understanding POP concentrations at extremes in body condition.

The naturally occurring extremes of body condition of northern elephant seals present an opportunity to examine how body condition impacts the relationships of contaminant concentrations among tissues. We examined commonly studied tissues with higher (serum, inner blubber) and lower (outer blubber) metabolic activity to describe relationships and determine predictive equations among tissues for POPs in northern elephant seals. Our primary focus was to investigate relationships for polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT) and metabolites of DDT, chlordanes (CHLs), and polybrominated diphenyl ethers (PBDEs), although we also included hexachlorobenzene (HCB), hexachlorocyclohexane (α-HCH and β-HCH), and the naturally produced 6-MeO-BDE 47. Specifically, our objectives were to 1) assess serum POP concentrations as a predictor of inner and outer blubber POP concentrations, and inner blubber POP concentrations as a predictor of outer blubber POP concentrations at two body condition extremes, 2) compare serum to blubber relationships between males and females, and 3) use partitioning coefficients to compare blubber/serum POPs and inner blubber/outer blubber POPs relationships between females and males at two naturally occurring extremes of elephant seal body condition.