Prediction of long-term variation in offspring metabolism due to BPA in eggs in rainbow trout using the DEB model

Abstract

Bisphenol A (BPA) in eggs prior to fertilization was found to induce long-term metabolic disturbances in juvenile rainbow trout (Oncorhynchus mykiss). Here we describe these imprinting effects in a Dynamic Energy Budget (DEB) framework, which allows interpretation of the data in an energy allocation context. First, DEB parameters for control rainbow trout were optimized using data extracted from 12 studies in the literature. Several modes of action on DEB parameters were then tested in order to correctly predict weight differences observed in rainbow trout in response to 5 different concentrations of BPA in eggs prior to fertilization. Reduced energy conductance v̇ at day 0, followed by an exponential recovery, was found to closely fit the experimental data. Effects on v̇ lasted beyond the disappearance of the chemical from the body, suggesting an imprinting effect of BPA on energy mobilization from the reserve. Our model predicts that early changes in DEB parameters lead to permanent and irreversible impairment of the metabolic growth acceleration in rainbow trout. Highlights ► A control DEB model was obtained for rainbow trout using data extracted from 12 studies. ► Mode of action of BPA exposure prior fertilization was investigated at 5 different concentrations. ► BPA imprints DEB parameters long after being cleared from the animal. ► Impaired DEB parameters at early life stages lead to irreversible changes related to acceleration factor. 1 Introduction Rainbow trout (Oncorhynchus mykiss), a native species from North America, is highly adaptive to a wide range of environments and widely distributed across all continents. This species primarily resides in freshwater, while their anadromous form, called steelhead trout, are euryhaline and migrates from river to ocean (McCormick et al., 2013). Rainbow trout is at the top of the food chain and, therefore, of major ecological importance. They are also the main freshwater cultured fish species in Europe, with a total value of almost 3 billion USD in 2015 (FAO Fisheries and Aquaculture Department, 2017). Trout is therefore of key importance ecologically and economically, motivating numerous research programs in understanding the effect of environmental factors on fish performance, including growth, immune function and coping with stressor. Bisphenol A (BPA) is a widely used industrial compound, especially in the manufacture of plastics and epoxy resins, and ubiquitously found in the aquatic environment. BPA is an endocrine-disrupting compound and affects various aspects of animal performance, including embryonic development (

Effect of the plastic pollutant bisphenol A on the biology of aquatic organisms: A meta‐analysis

“…The consequence of BPA exposure correlates with reductions in behavioural activities (Yokota et al., 2000), cardiovascular function (Schirling, Bohlen, Triebskorn, & Köhler, 2006), development and growth (Aluru, Leatherland, & Vijayan, 2010) and locomotor performance (Little & Seebacher, 2015). BPA exposure during development can also have persistent effects into adulthood via epigenetic modifications (Jašarević et al., 2011), suggesting that short‐term exposures to BPA have lasting consequences on life history (Sadoul, Augustine, Zimmer, Begout, & Vijayan, 2019; Thomas, Birceanu, Sadoul, & Vijayan, 2018).…”

Modelling the effects of variability in feeding rate on growth – a vital step for DEB-TKTD modelling

“…In other studies, f has been fixed to one during calibration and then estimated for independent data ( Sadoul et al, 2018 ). This approach was not followed in this study as it is based on observed growth rather than feeding data, so the mechanistic basis is unclear.…”

“…DEB has been applied to a wide range of taxa, with parameters available in the Add My Pet (AmP) library ( Marques et al, 2018 ). The majority of DEB-TKTD studies thus far have focused on invertebrates ( Ashauer and Jager, 2018 ) and more recently fish ( Zimmer et al, 2018 , Sadoul et al, 2018 ), with very few studies concerning terrestrial vertebrates ( Martin et al, 2019 , Desforges et al, 2017 ).…”

The role of Dynamic Energy Budgets in conservation physiology

“…The DEB model has been applied to reconstruct environmental concentrations of pollutants that the mussels would have experienced ( van Haren et al , 1994 ). In another study, Sadoul et al (2019) looked at how exposure to Bisphenol A during the egg phase of rainbow trout impairs the growth of adult fish. The authors reconstructed the stress upon metabolism based on observed changes in growth.…”