Persistent Organic Pollutant Burden, Experimental POP Exposure, and Tissue Properties Affect Metabolic Profiles of Blubber from Gray Seal Pups

Abstract

Persistent organic pollutants (POPs) are toxic, ubiquitous, resist breakdown, bioaccumulate in living tissue and biomagnify in food webs. POPs can also alter energy balance in humans and wildlife. Marine mammals experience high POP concentrations, but consequences for their tissue metabolic characteristics are unknown. We used blubber explants from wild, grey seal (Halichoerus grypus) pups to examine impacts of intrinsic tissue POP burden and acute experimental POP exposure on adipose metabolic characteristics. Glucose use, lactate production and lipolytic rate differed between matched inner and outer blubber explants from the same individuals and between feeding and natural fasting. Glucose use decreased with blubber dioxin-like PCBs (DL-PCB) and increased with acute experimental POP exposure. Lactate production increased with DL-PCBs during feeding, but decreased with DL-PCBs during fasting. Lipolytic rate increased with blubber dichlorodiphenyltrichloroethane (DDT) and its metabolites (DDX) in fasting animals, but declined with DDX when animals were feeding. Our data show that POP burdens are high enough in seal pups to alter adipose function early in life, when fat deposition and mobilisation are vital. Such POP-induced alterations to adipose glucose use may significantly alter energy balance regulation in marine top predators with the potential for long term impacts on fitness and survival.

Investigating decadal changes in persistent organic pollutants in Scottish grey seal pups

“…Although the POP concentrations found in the North Sea grey seal pups of this study are all well below the estimated toxic threshold values (Kannan, Blankenship, Jones, & Giesy, 2000), summed concentrations of DL-CB and DDX have been linked to altered glucose uptake, lactate production, and lipolytic rates in the blubber tissue of the same pups that provided the 2016 data for this study (Robinson et al, 2018). Even apparently low concentrations of these chemicals we have shown that comparisons can be made between POP measurements from discrete studies many years apart, particularly for…”

“…There is no long-term monitoring programme for POPs in the UK North Sea grey seals; however, two separate studies were performed 15 years apart to investigate the impact of POPs on survivability Hall et al, 2009) and energy balance (2015-17;Robinson et al, 2018) in grey seal pups. As these two studies have considerable overlap in methodology and measurements, the data were used to investigate whether changes have occurred in blubber POP concentrations in grey seal pups in this region.…”

“…Biopsy sampling and storage were performed as described previously (Hall et al, 2009;Robinson et al, 2018). Briefly, prior to sampling, pups were given a mass-specific dose of intravenous Zoletil™ and subcutaneous injections of Lignol™ at biopsy sites.…”

“…Blubber samples were collected from weaned pups in November and December 2002 (n = 60;31 female and 29 male;Hall et al, 2009), and again in 2015 (n = 30; 18 female and 12 male), 2016 (n = 23; 7 female and 16 male; Robinson et al, 2018), and2017 (n = 29;14 female and 15 male). All sample collection was performed by personal licence holders or designated competent personnel under UK Home Office licence 80/1552 in 2002 and licence 70/7806 in 2015-17.…”

“…POPs such as CBs, BDEs, and organochlorine pesticides (OCPs), including dichlorodiphenyltrichoroethane (DDT), have been linked to endocrine disruption (Noël et al, 2017;Routti et al, 2010;Tanabe, 2002;Villanger et al, 2011Villanger et al, , 2013 and negative impacts on reproductive (Helle, Olsson, & Jensen, 1976b;Hoydal et al, 2017;Murphy et al, 2010;Reijnders, 1986) and immune (Fisk et al, 2005, Hall et al, 2006, Hammond, Hall, & Dyrynda, 2005, reviewed in Desforges et al, 2016Penin et al, 2018) function in marine mammals. POPs have also recently been connected with lipid disruption in a range of phyla (Lee et al, 2016;Speranza et al, 2016;Yadetie et al, 2017), including marine mammals (Castelli, Rusten, Goksøyr, & Routti, 2014;Robinson et al, 2018;Tartu et al, 2017), because they alter pathways that enable individuals to accumulate or mobilize fat reserves appropriately. Viable immune and endocrine function, successful reproductive efforts, and the ability to use energy stores are all crucial to the fitness and survival of individuals in the wild.…”