Using energy budgets to combine ecology and toxicology in a mammalian sentinel species

Process-driven modelling approaches can resolve many of the shortcomings of traditional descriptive and non-mechanistic toxicology. We developed a simple dynamic energy budget (DEB) model for the mink (Mustela vison), a sentinel species in mammalian toxicology, which coupled animal physiology, ecology and toxicology, in order to mechanistically investigate the accumulation and adverse effects of lifelong dietary exposure to persistent environmental toxicants, most notably polychlorinated biphenyls (PCBs). Our novel mammalian DEB model accurately predicted, based on energy allocations to the interconnected metabolic processes of growth, development, maintenance and reproduction, lifelong patterns in mink growth, reproductive performance and dietary accumulation of PCBs as reported in the literature. Our model results were consistent with empirical data from captive and free-ranging studies in mink and other wildlife and suggest that PCB exposure can have significant population-level impacts resulting from targeted effects on fetal toxicity, kit mortality and growth and development. Our approach provides a simple and cross-species framework to explore the mechanistic interactions of physiological processes and ecotoxicology, thus allowing for a deeper understanding and interpretation of stressor-induced adverse effects at all levels of biological organization.

[1]  Bas Kooijman,et al.  Dynamic Energy Budget Theory for Metabolic Organisation , 2005 .

[2]  O. Wolkenhauer,et al.  Dynamic energy budget approaches for modelling organismal ageing , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  R. Nisbet,et al.  Extrapolating ecotoxicological effects from individuals to populations: a generic approach based on Dynamic Energy Budget theory and individual-based modeling , 2013, Ecotoxicology.

[4]  S. Safe Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): biochemistry, toxicology, and mechanism of action. , 1984, Critical reviews in toxicology.

[5]  Volker Grimm,et al.  Dynamic Energy Budget theory meets individual‐based modelling: a generic and accessible implementation , 2012 .

[6]  David G. Marr,et al.  The Philosophy and the Approach , 2010 .

[7]  J. A. Reyes,et al.  Reproductive toxicity of commercial PCB mixtures: LOAELs and NOAELs from animal studies. , 1991, Environmental health perspectives.

[8]  E. Calabrese,et al.  Mink as a predictive model in toxicology. , 1992, Drug metabolism reviews.

[9]  John W. Kern,et al.  Growth and reproductive effects from dietary exposure to Aroclor 1268 in mink (Neovison vison), a surrogate model for marine mammals , 2016, Environmental toxicology and chemistry.

[10]  D. Martineau,et al.  Possible mechanisms of action of environmental contaminants on St. Lawrence beluga whales (Delphinapterus leucas). , 1995, Environmental health perspectives.

[11]  U. Eriksson,et al.  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. , 2012, Environmental pollution.

[12]  T. Jager,et al.  A review of DEB theory in assessing toxic effects of mixtures. , 2010, The Science of the total environment.

[13]  H. Heesterbeek,et al.  How resource competition shapes individual life history for nonplastic growth: ungulates in seasonal food environments. , 2009, Ecology.

[14]  James Devillers,et al.  An Individual-Based Model of Zebrafish Population Dynamics Accounting for Energy Dynamics , 2015, PloS one.

[15]  R. Ringer,et al.  Current status of PCB toxicity to mink, and effect on their reproduction , 1977, Archives of environmental contamination and toxicology.

[16]  Tjalling Jager,et al.  DEBkiss or the quest for the simplest generic model of animal life history. , 2013, Journal of theoretical biology.

[17]  B. Sheldon,et al.  Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. , 1996, Trends in ecology & evolution.

[18]  R. Lochmiller,et al.  Trade‐offs in evolutionary immunology: just what is the cost of immunity? , 2000 .

[19]  Jon Barry,et al.  PCB pollution continues to impact populations of orcas and other dolphins in European waters , 2016, Scientific Reports.

[20]  M. Lewis,et al.  Predicting survival, reproduction and abundance of polar bears under climate change. , 2010 .

[21]  Sebastiaan A.L.M. Kooijman,et al.  The Analysis of Aquatic Toxicity Data , 1996 .

[22]  Jens C. Streibig,et al.  Bioassay analysis using R , 2005 .

[23]  R. Dietz,et al.  Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. , 2010, The Science of the total environment.

[24]  E. Ravagnan,et al.  Parameterising a generic model for the dynamic energy budget of Antarctic krill Euphausia superba , 2015 .

[25]  B. Essén-Gustavsson,et al.  Repeated post-exercise administration with a mixture of leucine and glucose alters the plasma amino acid profile in Standardbred trotters , 2012, Acta Veterinaria Scandinavica.

[26]  J. Taylor‐Papadimitriou,et al.  The Breast Cancer-Associated Glycoforms of MUC1, MUC1-Tn and sialyl-Tn, Are Expressed in COSMC Wild-Type Cells and Bind the C-Type Lectin MGL , 2015, PloS one.

[27]  B. Brunström,et al.  Wild mink (Neovison vison) as sentinels in environmental monitoring , 2012, Acta Veterinaria Scandinavica.

[28]  Sebastiaan A L M Kooijman,et al.  Making Sense of Ecotoxicological Test Results: Towards Application of Process-based Models , 2006, Ecotoxicology.

[29]  N. Kristensen,et al.  Energy intake and milk production in mink (MUSTELA vison)‐effect of litter size , 2001, Archiv fur Tierernahrung.

[30]  Hal Caswell,et al.  A model for energetics and bioaccumulation in marine mammals with applications to the right whale. , 2007, Ecological applications : a publication of the Ecological Society of America.

[31]  N. Cedergreen,et al.  Variable Temperature Stress in the Nematode Caenorhabditis elegans (Maupas) and Its Implications for Sensitivity to an Additional Chemical Stressor , 2016, PloS one.

[32]  S. Bursian,et al.  Multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink. 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. , 1998, Journal of toxicology and environmental health. Part A.

[33]  C. Salice,et al.  Plasticity in offspring contaminant tolerance traits: developmental cadmium exposure trumps parental effects , 2013, Ecotoxicology.

[34]  R. Dietz,et al.  Physiologically-based pharmacokinetic modelling of immune, reproductive and carcinogenic effects from contaminant exposure in polar bears (Ursus maritimus) across the Arctic. , 2015, Environmental research.

[35]  Craig Packer,et al.  Reproductive cessation in female mammals , 1998, Nature.

[36]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[37]  S. Kooijman,et al.  From food‐dependent statistics to metabolic parameters, a practical guide to the use of dynamic energy budget theory , 2008, Biological reviews of the Cambridge Philosophical Society.

[38]  S. Safe,et al.  Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. , 1994, Critical reviews in toxicology.

[39]  John W. Kern,et al.  Dietary exposure of mink (Mustela vison) to fish from the upper Hudson River, New York, USA: Effects on organ mass and pathology , 2013, Environmental toxicology and chemistry.

[40]  Tjalling Jager,et al.  A biology-based approach for mixture toxicity of multiple endpoints over the life cycle , 2009, Ecotoxicology.

[41]  S. Jensen,et al.  DDT and PCB [polychlorinated biphenyls] levels and reproduction in ringed seal [Pusa hispida Schreb.] from the Bothnian Bay [Baltic Sea]. , 1976 .

[42]  John W. Kern,et al.  Dietary exposure of mink (Mustela vison) to fish from the upper Hudson River, New York, USA: Effects on reproduction and offspring growth and mortality , 2013, Environmental toxicology and chemistry.

[43]  M. Obbard,et al.  A body composition model to estimate mammalian energy stores and metabolic rates from body mass and body length, with application to polar bears , 2009, Journal of Experimental Biology.

[44]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[45]  T. Jager,et al.  Capturing the life history of the marine copepod Calanus sinicus into a generic bioenergetics framework , 2015 .

[46]  M. Grossman,et al.  Multiphasic Growth Curves in Mink (Mustela vison) Selected for Feed Efficiency , 2003 .

[47]  Sebastiaan A.L.M. Kooijman,et al.  The “covariation method” for estimating the parameters of the standard Dynamic Energy Budget model I: Philosophy and approach , 2011 .

[48]  A. Tauson,et al.  Daily milk intake and body water turnover in suckling mink (Mustela vison) kits. , 1998, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[49]  Michael Grüninger,et al.  Introduction , 2002, CACM.

[50]  S. Kooijman,et al.  A quantitative estimation of the energetic cost of brown ring disease in the Manila clam using Dynamic Energy Budget theory. , 2009 .

[51]  Rod N. Millward,et al.  Contaminant-Adaptation and Community Tolerance in Ecological Risk Assessment: Introduction , 2002 .

[52]  S. Bursian,et al.  Mink as a sentinel species in environmental health. , 2007, Environmental research.