Predicting consequences of POP-induced disruption of blubber glucose uptake, mass gain rate and thyroid hormone levels for weaning mass in grey seal pups
[en] Persistent organic pollutants (POPs) are endocrine disruptors that alter adipose tissue development, regulation and function. Top marine predators are particularly vulnerable because they possess large fat stores that accumulate POPs. However, links between endocrine or adipose tissue function disruption and whole animal energetics have rarely been investigated. We predicted the impact of alterations to blubber metabolic characteristics and circulating thyroid hormone (TH) levels associated with polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine pesticides (OCPs) on suckling mass gain and weaning mass in wild grey seal pups. Glucose uptake by inner blubber was a strong predictor of whole animal mass gain rate, which in turn, resulted in heavier weaning mass. Weaning mass was predicted to increase by 3.7 ± 1.59 (sem) %, through increased mass gain rate, in the absence of the previously reported suppressive effect of dioxin-like PCB (DL-PCBs) on blubber glucose uptake. PBDEs were, conversely, associated with faster mass gain. Alleviation of this effect was predicted to reduce weaning mass by 6.02 ± 1.86% (sem). To better predict POPs effects on energy balance, it is crucial to determine if and how PBDEs promote mass gain in grey seal pups. Weaning mass was negatively related to total T3 (TT3) levels. A 20% (range = 9.3–31.7%) reduction in TT3 by DL-PCBs partially overcame the effect of DL-PCB -mediated reduction in blubber glucose uptake. Overall, DL-PCBs were thus predicted to reduce weaning mass by 1.86 ± 1.60%. Organohalogen impacts on whole-animal energy balance in grey seal pups appear to partially offset each other through opposing effects on different mechanisms. POP effects were generally minor, but the largest POP-induced reductions in weaning mass were predicted to occur in pups that were already small. Since weaning mass is positively related to first-year survival, POPs may disproportionately affect smaller individuals, and could continue to have population-level impacts even when levels are relatively low compared to historical values. Our findings show how in vitro experiments combined with measurements in vivo can help elucidate mechanisms that underpin energy balance regulation and help to quantify the magnitude of disruptive effects by contaminants and other stressors in wildlife.
Research center :
CART - Centre Interfacultaire d'Analyse des Résidus en Traces - ULiège
Disciplines :
Chemistry Aquatic sciences & oceanology
Author, co-author :
Bennett, Kimberley; Abertay University > School of Applied Sciences > Division of Health Sciences
Robinson, Kelly; University of St Andrews > Scottish Oceans Institute > Sea Mammal Research Unit
Armsrtong, Holly; Abertay University > School of Applied Sciences > Division of Health Sciences
Moss, Simon; University of St Andrews > Scottish Oceans Institute > Sea Mammal Research Unit
Scholl, Georges ; Université de Liège - ULiège > Département de chimie (sciences) > Center for Analytical Research and Technology (CART)
Tranganida, Alexandra; Abertay University > School of Applied Sciences > Division of Health Sciences
Eppe, Gauthier ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie analytique inorganique
Thomé, Jean-Pierre ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Debier, Cathy; Université Catholique de Louvain - UCL > Louvain Institute of Biomolecular Science and Technology
Hall, Ailsa; University of St Andrews > Scottish Oceans Institute > Sea Mammal Research Unit
Language :
English
Title :
Predicting consequences of POP-induced disruption of blubber glucose uptake, mass gain rate and thyroid hormone levels for weaning mass in grey seal pups
Publication date :
July 2021
Journal title :
Environment International
ISSN :
0160-4120
eISSN :
1873-6750
Publisher :
Elsevier, United Kingdom
Volume :
152
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Pollutants, Hormones and Adipose Tissue in Seals - PHATS
AMAP, 2018. AMAP Assessment 2018: Biological Effects of Contaminants on Arctic Wildlife and Fish. Arctic Monitoring and Assessment Programme (AMAP), Tromsø, Norway. vii+84 pp. available at https://www.amap.no/documents/download/3080/inline.
Arsenescu, V., Arsenescu, R.I., King, V., Swanson, H., Cassis, L.A., Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ. Health Perspect. 116 (2008), 761–768, 10.1289/ehp.10554.
Baker, N.A., Karounos, M., English, V., Fang, J., Wei, Y., Stromberg, A., Sunkara, M., Morris, A.J., Swanson, H.I., Cassis, L.A., Coplanar polychlorinated biphenyls impair glucose homeostasis in lean C57BL/6 mice and mitigate beneficial effects of weight loss on glucose homeostasis in obese mice. Environ. Health Perspect. 121 (2013), 105–110, 10.1289/ehp.1205421.
Baker, N.A., Shoemaker, R., English, V., Larian, N., Sunkara, M., Morris, A.J., Walker, M., Yiannikouris, F., Cassis, L.A., Effects of adipocyte aryl hydrocarbon receptor deficiency on PCB-induced disruption of glucose homeostasis in lean and obese mice. Environ. Health Perspect. 123 (2015), 944–950, 10.1289/ehp.1408594.
Ballard, F.J., Hanson, R.W., Leveille, G.A., Phosphoenolpyruvate carboxykinase and the synthesis of glyceride-glycerol from pyruvate in adipose tissue. J. Biol. Chem. 242 (1967), 2746–2750.
Barton K (2018). MuMIn: Multi-Model Inference. R package version 1.42.1. https://CRAN.R-project.org/package=MuMIn.
Beck CA, Bowen WD, Iversen SJ (2000) Seasonal changes in buoyancy and diving behaviour of adult grey seals. J Exp Biol 203: 2323-2330. Available at https://jeb.biologists.org/content/203/15/2323.
Beltran, R.S., Testa, J.W., Burns, J.M., An agent-based bioenergetics model for predicting impacts of environmental change on a top marine predator, the Weddell seal. Ecol. Model. 351 (2017), 36–50, 10.1016/j.ecolmodel.2017.02.002.
Bennett, K.A., Speakman, J.R., Moss, S.E.W., Pomeroy, P., Fedak, M.A., Effects of mass and body composition on fasting fuel utilisation in grey seal pups (Halichoerus grypus: Fabricius): an experimental study using supplementary feeding. J. Exp. Biol. 210 (2007), 3043–3053, 10.1242/jeb.009381.
Bennett, K.A., Hughes, J., Stamatas, S., Brand, S., Foster, N.L., Moss, S.E.W., Pomeroy, P.P., Adiponectin and insulin in grey seals during suckling and fasting: relationship with nutritional state and body mass during nursing in mothers and pups. Physiol. Biochem. Zool. 88 (2015), 295–310, 10.1086/680862.
Bennett, K.A., Robinson, K.J., Moss, S.E.W., Millward, S., Hall, A.J., Using blubber explants to investigate adipose function in grey seals: glycolytic, lipolytic and gene expression responses to glucose and hydrocortisone. Sci. Rep., 7, 2017, 7731, 10.1038/s41598-017-06037-x.
Brown, T.M., Ross, P.S., Reimer, K.J., Veldhoen, N., Dangerfield, N.J., Fisk, A.T., Helbing, C., PCB related effects thresholds as derived through gene transcript profiles in locally contaminated ringed seals (Pusa hispida). Environ. Sci. Technol. 48 (2014), 12952–12961, 10.1021/es5032294.
Brouwer, A., Reijnders, P.J.H., Koeman, J.H., Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid deficiency in the common seal (Phoca vitulina). Aquat. Toxicol. 15 (1989), 99–105, 10.1016/0166-445X(89)90008-8.
Bustnes, J.O., Moe, B., Hertzke, D., Hanssen, S.A., Norstad, T., Sagerup, k., Gabrielsen, G.W., Borgå, K., Strongly increasing blood concentrations of lipid-soluble organochlorines in high arctic common eiders during incubation fast. Chemosphere 79 (2010), 320–325, 10.1016/j.chemosphere.2010.01.026.
Castelli, M.G., Rusten, M., Goksøyr, A., Routti, H., mRNA expression of genes regulating lipid metabolism in ringed seals (Pusa hispida) from differently polluted areas. Aquat. Toxicol. 146 (2014), 239–246, 10.1016/j.aquatox.2013.11.015.
Coetzee, B.W.T., Chown, S.L., A meta-analysis of human disturbance impacts on Antarctic wildlife. Biol. Rev. 91 (2015), 578–596, 10.1111/brv.12184.
Chiba, I., Sakakibara, A., Goto, Y., Isono, T., Yamamoto, Y., Iwata, H., Tanabe, S., Shimazaki, K., Akahori, F., Kazusaka, A., Fujita, S., Negative correlation between plasma thyroid hormone levels and chlorinated hydrocarbon levels accumualted in seals from the coast of Hokkaido, Japan. Environ. Toxicol. Chem. 20 (2001), 1092–1097, 10.1002/etc.5620200521.
Debier C, Pomeroy P P, Dupont C, Joiris C, Comblin V, Le Boulengé E, Larondelle Y, Thomé J-P (2003) Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar Ecol Prog Ser 247: 237−248 DOI: www.jstor.org/stable/24866462.
Debier, C., Chalon, C., Le Boeuf, B.J., de Tillesse, T., Larondelle, Y., Thomé, J.-P., Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast. Aquat. Toxicol. 80 (2006), 149–157, 10.1016/j.aquatox.2006.08.002.
Desforges, J.P., Hall, A., McConnell, B., Rosing-Asvid, A., Barber, J.L., Brownlow, A., De Guise, S., Eulaers, I., Jepson, P.D., Letcher, R.J., Levin, M., et al. Predicting global killer whale population collapse from PCB pollution. Science 361 (2018), 1373–1376, 10.1126/science.aat1953.
Dimitriadis, G., Mitrou, P., Lambadiari, V., Maratou, E., Raptis, S.A., Insulin effects in muscle and adipose tissue. Diabetes Res Clin Prac 93 (2011), S52–S59, 10.1016/S0168-8227(11)70014-6.
Dirinck, E.L., Dirtu, A.C., Govindan, M., Covaci, A., Van Gaal, L.F., Jorens, P.G., Exposure to persistent organic pollutants: relationship with abnormal glucose metabolism and visceral adiposity. Diabetes Care 37 (2014), 1951–1958, 10.2337/dc13-2329.
Elmore SE, La Merrill MA (2019) Oxidative phosphorylation impairment by DDT and DDE Front Endocrinol. DOI: 10: 22. 0.3389/fendo.2019.00122.
Flores-Delgado, G., Marsch-Moreno, M., Kuri-Harcuch, W., Thyroid hormone stimulates adipocyte differentiation of 3T3 cells. Mol. Cell. Biochem. 76 (1987), 35–43, 10.1007/BF00219396.
Fox J & Weisberg S (2011). An {R} Companion to Applied Regression, Second Edition. Thousand Oaks CA: Sage. URL: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.
Fox J, Friendly M, Monette G. (2018). heplots: Visualizing Tests in Multivariate Linear Models. R package version 1.3-5. URL https://CRAN.R-project.org/package=heplots.
Friendly, M., HE plots for Multivariate General Linear Models. J Comp Graph Stat 16 (2007), 421–444, 10.1198/106186007X208407.
Goerke, H., Weber, K., Bornemann, H., Ramdohr, S., Plotz, J., Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota. Mar Poll Bull. 48 (2004), 295–302, 10.1016/j.marpolbul.2003.08.004.
Green, D.S., Johnson-Ulrich, L., Couraud, H.E., Holekamp, K.E., Anthropogenic disturbance induces opposing population trends in spotted hyenas and African lions. Biodiversity Conservat. 27 (2018), 871–889, 10.1007/s10531-017-1469-7.
Gross J & Ligges U (2015) nortest: Tests for Normality. R package version 1.0-4. https://CRAN.R-project.org/package=nortest.
Gouveia CHA, Miranda-Rodrigues M, Martins GM, Neofiti-Papi B (2018) Thyroid hormone and skeletal development. Chapter 16 In Thyroid Hormone Ed: G Litwack. Vitamins and Hormones 106: 383-472. Elsevier. DOI: 10.1016/bs.vh.2017.06.002.
Hall, A.J., McConnell, B.J., Barker, R.J., The effect of total immunoglobulin levels, mass and condition on the first-year survival of grey seal pups. Funct. Ecol. 16 (2002), 462–474, 10.1046/j.1365-2435.2002.00649.x.
Hall, A.J., Hugunin, K., Deaville, R., Law, R.J., Allchin, C.R., Jepson, P.D., The risk of infection from polychlorinated biphenyl exposure in the harbor porpoise (Phocoena phocoena): a case–control approach. Environ. Health Perspect. 114 (2006), 704–711, 10.1289/ehp.8222.
Hall, A.J., Gulland, F.M.D., Ylitalo, G.M., Grieg, D.J., Lowenstine, L., Changes in blubber contaminant concentrations in California sea lions (Zalophus californianus) associated with weight loss and gain during rehabilitation. Env Sci Technol 42 (2008), 4181–4187, 10.1021/es702685p.
Hall, A.J., Thomas, G.O., McConnell, B.J., Exposure to persistent organic pollutants and first-year survival probability in gray seal pups. Environ. Sci. Technol. 43 (2009), 6364–6369, 10.1021/es9004398.
Hallgren, S., Sinjari, T., Hakansson, H., Darnerud, P.O., Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch. Toxicol. 75 (2001), 200–208, 10.1007/s002040000208.
Hallgren, S., Darnerud, P.O., Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats – testing interactions and mechanisms for thyroid hormone effects. Toxicology 177 (2002), 227–243, 10.1016/S0300-483X(02)00222-6.
Hammond, J.A., Hall, A.J., Dyrynda, E.A., Comparison of polychlorinated biphenyl (CB) induced effects on innate immune functions in harbour and grey seals. AquatToxicol 74 (2005), 126–138, 10.1016/j.aquatox.2005.05.006.
Helle, E., Olsson, M., Jensen, S., DDT and PCB levels and reproduction in ringed seals from the Bothnian Bay. Ambio 5 (1976), 188–189.
Helle, E., Olsson, M., Jensen, S., PCB levels correlated with pathological changes in seal uteri. Ambio 5 (1976), 261–263.
Hoppe, A.A., Carey, G.B., Polybrominated diphenyl ethers as endocrine disruptors of adipocyte metabolism. Obesity 15 (2007), 2942–2950, 10.1038/oby.2007.351.
Houde, M., Wang, X., Ferguson, S.H., Gagnon, P., Brown, T.M., Tanabe, S., Kunito, K., Kwan, M., Muir, D.C.G., Spatial and temporal trends of alternative flame retardants and polybrominated diphenyl ethers in ringed seals (Phoca hispida) across the Canadian Arctic. Environ Poll 223 (2017), 266–276, 10.1016/j.envpol.2017.01.023.
Irving, L., Hart, J.S., The metabolism and insulation of seals as bare-skinned mammals in cold water. Can. J. Zool. 35 (1957), 497–511, 10.1139/z57-041.
Jackson, E., Shoemaker, R.C., Larian, N., Cassis, L.A., Adipose tissue as a site of toxin accumulation. Compr Physiol 7 (2017), 1085–1135, 10.1002/cphy.c160038.
Jepson, P.D., Law, R.J., Persistent pollutants, persistent threats: Polychlorinated biphenyls remain a major threat to marine apex predators. Science 352 (2016), 1388–1389, 10.1126/science.aaf9075.
Jepson, P.D., Deaville, R., Barber, J.L., Aguilar, À., Borrell, A., Murphy, S., Barry, J., Brownlow, A., Barnett, J., Berrow, S., Cunningham, A.A., et al. PCB pollution continues to impact populations of orcas and other dolphins in European waters. Sci. Rep., 6, 2016, 18573, 10.1038/srep18573.
Kannan, K., Blankenship, A.L., Jones, P.D., Giesy, J.P., Toxicity reference values for the toxic effects of polychlorinated biphenyls to aquatic mammals. Human Ecol Risk Assess 6 (2000), 181–201, 10.1080/10807030091124491.
Kassotis, C.D., Kollitz, E.M., Hoffman, K., Sosa, J.A., Stapletin, H.M., Thyroid receptor antagonism as a contributory mechanism for adipogenesis induced by environmental mixtures in 3T3-L1 cells. Sci Tot Env 666 (2019), 431–444, 10.1016/j.scitotenv.2019.02.273.
Kershaw, J.L., Sherill, M., Davison, N.J., Brownlow, A., Hall, A.J., Evaluating morphometric and metabolic markers of body condition in a small cetacean, the harbor porpoise (Phocoena phocoena). Ecol. Evol. 7 (2017), 3494–3506, 10.1002/ece3.2891.
Kim, J., Sun, Q.C., Yue, Y.R., Yoon, K.S., Whang, K.Y., Clark, J.M., Park, Y., 4,4 '-Dichlorodiphenyltrichloroethane (DDT) and 4,4 '-dichlorodiphenyldichloroethylene (DDE) promote adipogenesis in 3T3-L1 adipocyte cell culture. Pesticide Biochem Physiol 131 (2016), 40–45, 10.1016/j.pestbp.2016.01.005.
Kim, Y., Kim, H., Oh, Y., Kwon, W., Lee, M., Bae, J., Woo, M., Kim, J., Yoo, Y., Polychlorinated biphenyl 138 exposure-mediated lipid droplet enlargement endows adipocytes with resistance to TNF-α-induced cell death. Toxicol. Lett. 292 (2018), 55–62, 10.1016/j.toxlet.2018.04.029.
Kight, C.R., Swaddle, J.P., Associations of anthropogenic activity and disturbance with fitness metrics of eastern bluebirds (Sialia sialis). Biol. Conserv. 138 (2007), 189–197, 10.1016/j.biocon.2007.04.014.
Klaus, S., Adipose tissue as a regulator of energy balance. Curr. Drug Targets 5 (2004), 241–250, 10.2174/1389450043490523.
Lang, S., Iversen, S.J., Bowen, W.D., Repeatability in lactation performance and the consequences for maternal reproductive success in gray seals. Ecology 90 (2009), 2513–2523, 10.1890/08-1386.1.
Lee, D.H., Steffes, M.W., Sjödin, A., Jones, R.S., Needham, L.L., Jacobs, D.R. Jr, Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS ONE, 6, 2011, 10.1371/journal.pone.0015977 e15977.
Lee, M.C., Han, J., Lee, S.H., Kim, D.H., Kang, H.M., Won, E.J., Hwang, D.S., Park, J.C., Om, A.S., Lee, J.S., A brominated flame retardant 2, 2′, 4, 4′ tetrabrominated diphenyl ether (BDE-47) leads to lipogenesis in the copepod Tigriopus japonicus. Aquat. Toxicol. 178 (2016), 19–26, 10.1016/j.aquatox.2016.07.002.
Lefcheck, J.S., piecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Meth Ecol Evol 7 (2016), 573–579, 10.1111/2041-210X.12512.
Lidgard, D.C., Boness, D.J., Bowen, W.D., McMillan, J.I., State dependent male mating tactics in the grey seal: the importance of body size. Behav. Ecol. 16 (2005), 541–549, 10.1093/beheco/ari023.
Louis, C., Dirtu, A.C., Stas, M., Guiot, Y., Malarvannan, G., Das, K., Costa, D.P., Crocker, D.E., Covaci, A., Debier, C., Mobilisation of lipophilic pollutants from blubber in northern elephant seal pups (Mirounga angustirostris) during the postweaning fast. Env Res 132 (2014), 438–448, 10.1016/j.envres.2014.04.016.
Lühmann, K., Lille-Langøy, R., Øyegarden, L., Kovacs, K.M., Lydersen, C., Goksøyr, A., Routti, H., Environmental pollutants modulate transcriptional activity of nuclear receptors of whales In Vitro Environ. Sci. Technol. 54 (2020), 5629–5639, 10.1021/acs.est.9b06952.
Martineau, D., Lemberger, K., Dallaire, A., Labelle, P., Lipscomb, T.P., Michel, P., Mikaelian, I., Cancer in wildlife, a case study: Beluga from the St. Lawrence Estuary, Québec. Canada. Environ Health Perspect 110 (2002), 285–292, 10.1289/ehp.02110285.
Mellish, J.-A.E., Iversen, S.J., Bowen, W.D., Variation in milk production and lactation performance in grey seals and consequences for pup growth characteristics. Physiol. Biochem. Zool. 72 (1999), 677–690, 10.1086/316708.
Mullur, R., Liu, Y.-Y., Brent, G.A., Thyroid hormone regulation of metabolism. Physiol. Rev. 94 (2014), 355–382, 10.1152/physrev.00030.2013.
Murphy, S., Pierce, G., Law, R., Bersuder, P., Jepson, P., Learmonth, J.A., Addink, M., Dabin, W., Santos, M.B., Deaville, R., Zegers, B.N., Mets, A., Rogan, E., Ridoux, V., Reid, R.J., Smeenk, C., Jauniaux, T., López, A., Alonso Farré, J.M., González, A.F., Guerra, A., García-Hartmann, M., Lockyer, C., Boon, J.P., Assessing the effect of persistent organic pollutants on reproductive activity in common dolphins and harbour porpoises. J. Northwest Atlantic Fish Sci., 42, 2010, 153, 10.2960/J.v42.m658.
Noël, M., Dangerfield, N., Jeffries, S., Lambourn, D., Lance, M., Helbing, C., Lebeuf, M., Ross, P.S., Polychlorinated biphenyl related alterations of the expression of essential genes in harbour seals (Phoca vitulina) from coastal sites in Canada and the United States. Arch. Environ. Contam. Toxicol. 73 (2017), 310–312, 10.1007/s00244-016-0362-9.
Oppenheimer, J.H., Schwartz, H.L., Lane, J.T., Thompson, M.P., Functional relationship of thyroid hormone induced lipogenesis, lipolysis, and thermogenesis in the rat. J. Clin. Invest. 87 (1991), 125–137, 10.1172/JCI114961.
Penin, I., Levin, M., Acevedo-Whitehouse, K., Jasperse, L., Gebhard, E., Gulland, F.M.D., De Guise, S., Effects of polychlorinated biphenyls (CB) on California sea lion (Zalophus californianus) lymphocyte functions upon in vitro exposure. Environ. Res. 167 (2018), 708–717, 10.1016/j.envres.2018.08.028.
Pestana, D., Teixeira, D., Meireles, M., Marques, C., Norberto, S., Sá, C., Fernandes, V., Correia-Sá, L., Faria, A., Guardão, L., Guimarães, J., Cooper, W., Sandovici, I., Domingues, V., Delerue-Matos, C., Monteiro, R., Constância, M., Calhau, C., Adipose tissue dysfunction as a central mechanism leading to dysmetabolic obesity triggered by chronic exposure to p, p’-DDE. Sci. Rep., 7, 2017, 1, 10.1038/s41598-017-02885-9.
Peterson, S.H., Hassrick, J., Lafontaine, A., Thomé, J.-P., Crocker, D.E., Debier, C., Costa, D.P., Effects of age, adipose percent, and reproduction on PCB concentrations and profiles in an extreme fasting North Pacific marine mammal. PLoS ONE, 9, 2014, 10.1371/journal.pone.0096191 e96191.
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1-137, URL: https://CRAN.R-project.org/package=nlme.
Pirotta, E., Booth, C.G., Costa, D.P., Fleishman, E., Kraus, S.D., LusseauD, Moretti D., New, L.F., Schick, R.S., Schwarz, L.K., Simmons, S.E., Thomas, L., Tyack, P.L., Weise, M.J., Wells, R.S., Harwood, J., Understanding the population consequences of disturbance. Ecol. Evol. 8 (2018), 9934–9946, 10.1002/ece3.4458.
Polischuk, S.C., Norstrom, R.J., Ramsay, R.J., Body burdens and tissue concentrations of organochlorines in polar bears (Ursus maritimus) vary during seasonal fasts. Env Poll 118 (2002), 29–39, 10.1016/S0269-7491(01)00278-0.
Pomeroy, P.P., Green, N., Hall, A.J., Walton, M.J., Jones, K.C., Harwood, J., Congener-specific exposure of grey seal (Halichoerus grypus) pups to chlorinated biphenyls during lactation. Can. J. Fish. Aquat. Sci. 53 (1996), 1526–1534, 10.1139/f96-087.
Pomeroy, P.P., Fedak, M.A., Rothery, P., Anderson, S., Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland. J. Anim. Ecol. 68 (1999), 235–253, 10.1046/j.1365-2656.1999.00281.x.
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Rainey NE, Saric A, Leberre A, Dewailly E, Slomianny C, Vial G, Zeliger HI, Petit PX (2017) Synergistic cellular effects including mitochondrial destabilization, autophagy and apoptosis following low-level exposure to a mixture of lipophilic persistent organic pollutants Sci Rep 7: 4728. DOI: 10.1038/s41598-017-04654-0.
Reilly, J.J., Adaptations to prolonged fasting in free-living weaned gray seal pups. Am. J. Physiol. 260 (1991), R267–R272, 10.1152/ajpregu.1991.260.2.R267.
Rigét, F., Vorkamp, K., Bossi, R., Sonne, C., Letcher, R.J., Dietz, R., Twenty years of monitoring of persistent organic pollutants in Greenland biota. A review. Environ Poll 217 (2016), 114–123, 10.1016/j.envpol.2015.11.006.
Rigét, F., Bignert, A., Braune, B., Dam, M., Dietz, R., Evans, M., Green, N., Gunnlaugsdóttir, H., Hoydal, K.S., Kucklick, J., Letcher, R.J., Muir, D., Schuur, S., Sonne, C., Stern, G., Tomy, G., Vorkamp, K., Wilson, S., Temporal trends of persistent organic pollutants in Arctic marine and freshwater biota. Sci Tot Environ 649 (2019), 99–110, 10.1016/j.scitotenv.2018.08.268.
Robinson, K.J., Hall, A.J., Debier, C., Eppe, G., Thomé, J.-P., Bennett, K.A., Persistent organic pollutant burden, experimental POP exposure and tissue properties affect metabolic profiles of blubber from gray seal pups. Environ. Sci. Technol. 52 (2018), 13523–13534, 10.1021/acs.est.8b04240.
Robinson, K.J., Hall, A.J., Scholl, G., Debier, C., Thomé, J.P., Eppe, G., Adam, C., Bennett, K.A., Investigating decadal changes in persistent organic pollutants in Scottish grey seal pups. Aquat. Conserv: Mar Freshwater Ecosys 29:S1 (2019), 86–100, 10.1002/aqc.3137.
Roos, A.M., Bäcklin, B.M.V., Helander, B.O., Rigét, F.F., Eriksson, U.C., Improved reproductive success in otters (Lutra lutra), grey seals (Halichoerus grypus) and sea eagles (Haliaeetus albicilla) from Sweden in relation to concentrations of organochlorine contaminants. Environ Poll 170 (2012), 268–275, 10.1016/j.envpol.2012.07.017.
Rosen, D.A., Renouf, D., Seasonal changes in blubber distribution in Atlantic harbor seals: indications of thermodynamic considerations. Mar. Mammal Sci. 13 (1997), 229–240, 10.1111/j.1748-7692.1997.tb00630.x.
Routti, H., Lille-Langøy, R., Berg, M.K., Fink, T., Harju, M., Kristiansen, K., Rostkowski, P., Rusten, M., Sylte, I., Øygarden, L., Goksøyr, A., Environmental chemicals modulate polar bear (Ursus maritimus) peroxisome proliferator-activated receptor gamma (PPARG) and adipogenesis in vitro. Environ. Sci. Technol. 50 (2016), 10708–10720, 10.1021/acs.est.6b03020.
Rolland, R.M., Schick, R.S., Pettis, H.M., Knowlton, A.R., Hamilton, P.K., Clark, J.S., Kraus, S.D., Health of North Atlantic right whales, Eubalaena glacialis, over three decades: From individual health to demographic and population health trends. Mar. Ecol. Prog. Ser. 542 (2016), 265–282, 10.3354/meps11547.
Sørmo, E.G., Jussi, I., Jussi, M., Braathen, M., Skaare, J.U., Jenssen, B.M., Thyroid hormone status in gray seal (Halichoerus grypus) pups from the Baltic sea and the Atlantic Ocean in relation to organochlorine pollutants. Environ. Toxicol. Chem. 24 (2005), 610–616, 10.1897/04-017R.1.
Speranza, E.D., Colombo, M., Tatone, L.M., Cappelletti, N., Migoya, M.C., Colombo, J.C., Fatty acid alterations in the detritivorous Prochilodus lineatus promoted by opportunistic feeding on sewage discharges in the Rio de la Plata estuary. J. Fish Biol. 89 (2016), 2024–2037, 10.1111/jfb.13104.
Swanepoel, R.M., Racey, P.A., Shore, R.F., Speakman, J.R., Energetic effects of sublethal exposure to lindane on pipistrelle bats (Pipistrellus pipistrellus). Environ. Pollut. 104 (1999), 169–177, 10.1016/S0269-7491(98)00196-1.
Tabuchi, M., Veldhoen, N., Dangerfield, N., Jeffries, S., Helbing, C.C., Ross, P.S., PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina). Environ. Health Perspect. 114 (2006), 1024–1031, 10.1289/ehp.8661.
Tartu, S., Lille-Langoy, R., Storseth, T.R., Bourgeon, S., Brunsvik, A., Aars, J., Goksoyr, A., Jenssen, B.M., Polder, A., Wiemann, G., Torget, V., Routti, H., Multiple-stressor effects in an apex predator: combined influence of pollutants and sea ice decline on lipid metabolism in polar bears. Sci. Rep., 7, 2017, 16487, 10.1038/s41598-017-16820-5.
van der Plas, S.A., Lutkeschipholt, I., Spenkelink, B., Brouwer, A., Effects of subchronic exposure to complex mixtures of dioxin- like and non-dioxin-like polyhalogenated aromatic compounds on thyroid hormone and vitamin A levels in female Sprague-Dawley rats. Toxicol. Sci. 59 (2001), 92–100, 10.1093/toxsci/59.1.92.
Villanger, G.D., Lydersen, C., Kovacs, K.M., Lie, E., Skaare, J.U., Jenssen, B.M., Disruptive effects of persistent organohalogen contaminants on thyroid function in white whales (Delphinapterus leucas) from Svalbard. Sci Tot Env 409 (2011), 2511–2524, 10.1016/j.scitotenv.2011.03.014.
Villanger, G.D., Gabrielson, K.M., Kovacs, K.M., Lydersen, C., Lie, E., Karimi, M., Sormo, E.G., Jenssen, B.M., Effects of complex organohalogen contaminant mixtures on thyroid homeostasis in hooded seal (Cystophora cristata) mother-pup pairs. Chemosphere 92 (2013), 828–842, 10.1016/j.chemosphere.2013.04.036.
Wagenmakers, E.-J., Farrell, S., AIC model selection using Akaike weights. Psychonom Bull Rev 11 (2004), 192–196, 10.3758/BF03206482.
Wen, Q., Xie, X., Zhao, C., Ren, Q., Zhang, X., Wei, D., Emanuelli, B., Yu, Y., The brominated flame retardant PBDE 99 promotes adipogenesis via regulating mitotic clonal expansion and PPARγ expression. Sci Tot Env 670 (2019), 67–77, 10.1016/j.scitotenv.2019.03.20.
Yadetie, F., Karlsen, O.A., Eide, M., Hogstrand, C., Goksoyr, A., Liver transcriptome analysis of Atlantic cod (Gadus morhua) exposed to PCB 153 indicates effects on cell cycle regulation and lipid metabolism. BMC Genomics, 15, 2014, 481, 10.1186/1471-2164-15-481.
Yadetie, F., Oveland, E., Doskeland, A., Berven, F., Goskoyr, A., Karlsen, O.A., Quantitative proteomics analysis reveals perturbation of lipid metabolic pathways in the liver of Atlantic cod (Gadus morhua) treated with PCB 153. Aquat. Toxicol. 185 (2017), 19–28, 10.1016/j.aquatox.2017.01.014.
Young, R.M., Fat, energy and mammalian survival. Am. Zool. 16 (1976), 699–710, 10.1093/icb/16.4.699.
Zuur, A.F., Ieno, E.N., Elphick, E.S., A protocol for data exploration to avoid common statistical problems. Meth Ecol Evol 1 (2010), 3–14, 10.1111/j.2041-210X.2009.00001.x.
