Biology-Based Modeling To Analyze Uranium Toxicity Data on <i>Daphnia magna</i> in a Multigeneration Study

Massarin, Sandrine; Beaudouin, Rémy; Zeman, Florence Anna; Floriani, Magali; Gilbin, Rodolphe; Alonzo, Frédéric; Péry, Alexandre R.R.

doi:10.1021/es104082e

Cited by 42 publications

(32 citation statements)

References 29 publications

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“…Untangling an effect on maintenance cost or assimilation is, for example, particularly difficult when additional data on oxygen consumption are not available. Consequently, modeling work can fit equally well different MoA for a same contaminant, as observed for the effect of uranium on aquatic species (Augustine et al, 2012;Massarin et al, 2011;Goussen et al, 2015). In our study, the impact of BPA on v is the most suitable mode of action as it yields predictions particularly close to real values.…”

Section: Accepted Manuscript 43 Mode Of Action Of Imsupporting

confidence: 59%

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

Sadoul

Augustine²,

Zimmer³

et al. 2019

Journal of Sea Research

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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 (

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Section: Accepted Manuscript 43 Mode Of Action Of Imsupporting

confidence: 59%

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

Sadoul

Augustine²,

Zimmer³

et al. 2019

Journal of Sea Research

View full text Add to dashboard Cite

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“…They also reported a complementary study showing a loss of gut wall architecture, presence of large necrotic zones and an overall decrease in gut bacteria, in accordance with an effect on assimilation. In a similar way, Massarin et al (2011) analysed uranium toxicity data on D. magna showing a likely effect on assimilation based both on modelling of the growth and reproduction responses and histological analysis of uranium induced damage to the gut wall. The same kind of histological effects was observed on the earthworm Eisenia fetida exposed to soil contaminated with uranium (Giovanetti et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Consequences of a multi-generation exposure to uranium on Caenorhabditis elegans life parameters and sensitivity

et al. 2013

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The assessment of toxic effects at biologically and ecologically relevant scales is an important challenge in ecosystem protection. Indeed, stressors may impact populations at much longer term than the usual timescale of toxicity tests. It is therefore important to study the evolutionary response of a population under chronic stress. We performed a 16-generation study to assess the evolution of two populations of the ubiquitous nematode Caenorhabditis elegans in control conditions or exposed to 1.1 mM of uranium. Several generations were selected to assess growth, reproduction, survival, and dose-responses relationships, through exposure to a range of concentrations (from 0 to 1.2 mM U) with all endpoints measured daily. Our experiment showed an adaptation of individuals to experimental conditions (increase of maximal length and decrease of fecundity) for both populations. We also observed an increase of adverse effects (reduction of growth and fertility) as a function of uranium concentration. We pointed out the emergence of population differentiation for reproduction traits. In contrast, no differentiation was observed on growth traits. Our results confirm the importance of assessing environmental risk related to pollutant through multi-generational studies.

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“…Analysis of uranium toxicity data on Daphnia magna using deb theory concluded that assimilation decreased in response to water-borne exposure to U (Massarin et al, 2010(Massarin et al, , 2011. Their study showed that effects of uranium on growth and reproduction were captured equally well when assuming a decrease in assimilation or an increase in somatic maintenance in the first two generations, but that effects on the third generation were better characterized by a decrease in assimilation.…”

Section: Reproductive Toxicologymentioning

confidence: 99%

Effects of uranium on the metabolism of zebrafish, Danio rerio

et al. 2012

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The increasing demand for nuclear energy results in heightened levels of uranium (U) in aquatic systems which present a potential health hazard to resident organisms. The aim of this study was to mechanistically assess how chronic exposure to environmentally relevant concentrations of U perturbs the complex interplay between feeding, growth, maintenance, maturation and reproduction throughout the life-cycle of an individual. To this end we analysed literature-based and original zebrafish toxicity data within a same mass and energy balancing conceptual framework. U was found to increase somatic maintenance leading to inhibition of spawning as well as increase hazard rate and costs for growth during the early life stages. The fish's initial conditions and elimination through reproduction greatly affected toxico-kinetics and effects. We demonstrate that growth and reproduction should be measured on specific individuals since mean values were hardly interpretable. The mean food level differed between experiments, conditions and individuals. This last 'detail' contributed substantially to the observed variability by its combined effect on metabolism, toxic effects and toxico-kinetics. The significance of this work is that we address exactly how these issues are related and derive conclusions which are independent of experimental protocol and coherent with a very large body of literature on zebrafish eco-physiology.

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Biology-Based Modeling To Analyze Uranium Toxicity Data on Daphnia magna in a Multigeneration Study

Cited by 42 publications

References 29 publications

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

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

Consequences of a multi-generation exposure to uranium on Caenorhabditis elegans life parameters and sensitivity

Effects of uranium on the metabolism of zebrafish, Danio rerio

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