Article pubs.acs.org/est
Population-Level Modeling to Account for Multigenerational Effects of Uranium in Daphnia magna Pierre-Albin Biron,† Sandrine Massarin,‡ Frédéric Alonzo,‡,* Laurent Garcia-Sanchez,‡ Sandrine Charles,† and Elise Billoir†,§ Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, F-69622, Villeurbanne, France ‡ Institut de Radioprotection et de Sûreté Nucléaire (IRSN), DEI, SECRE, LME, Cadarache, France § Plateforme de Recherche ROVALTAIN en Toxicologie Environnementale et Ecotoxicologie, 1 avenue de la gare - BP 15173 - Alixan, F-26958, Valence Cedex 9, France †
ABSTRACT: As part of the ecological risk assessment associated with radionuclides in freshwater ecosystems, toxicity of waterborne uranium was recently investigated in the microcrustacean Daphnia magna over a three-generation exposure (F0, F1, and F2). Toxic effects on daphnid life history and physiology, increasing over generations, were demonstrated at the organism level under controlled laboratory conditions. These effects were modeled using an approach based on the dynamic energy budget (DEB). For each of the three successive generations, DEBtox (dynamic energy budget applied to toxicity data) models were fitted to experimental data. Lethal and sublethal DEBtox outcomes and their uncertainty were projected to the population level using population matrix techniques. To do so, we compared two modeling approaches in which experimental results from F0, F1, and F2 generations were either considered separately (F0-, F1-, and F2-based simulations) or together in the actual succession of F0, F1, and F2 generations (multi-F-based simulation). The first approach showed that considering results from F0 only (equivalent to a standard toxicity test) would lead to a severe underestimation of uranium toxicity at the population level. Results from the second approach showed that combining effects in successive generations cannot generally be simplified to the worst case among F0-, F1-, and F2-based population dynamics.
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generations.9 In contrast, results with copper suggested that daphnids may develop a resistance with an increasing survival rate when parents were previously exposed.10 These contrasting results highlight the necessity for multigenerational tests, as toxic effects observed over one generation may under- or overestimate the real effects of pollutants on a longer term. In the case of depleted uranium (U), a previous study demonstrated an increase in sensitivity across three generations of D. magna.11 A dynamic energy budget approach applied to toxicology (DEBtox) was used to address possible mechanisms of action of depleted U.12 DEBtox models mechanistically describe how metabolic costs induced by toxicant exposure come at the expense of energy-dependent processes, including somatic growth and reproduction.13,14 The previous study shows that a decrease in carbon assimilation efficiency is likely and sufficient to explain observed effects in D. magna exposed to depleted U. This mechanism has been confirmed by complementary assimilation measurements using radiolabeled
INTRODUCTION Today it is recognized that ecological risk assessment can markedly improve its biological relevance by considering responses to contaminant exposure at the population level rather than at the organism level.1 From this prospective, population models are particularly helpful tools that allow multiple toxic effects observed under laboratory experiments on organism survival and fecundity to be combined into one population-level endpoint, such as the asymptotic population growth rate. Priority has been recently given to the use of matrix population models2 for their prospective potential in modeling population health, including the effects of toxic compounds on the different age or development stages of organisms within populations.3−6 Studying toxic effects under multigenerational exposure regimes represents another key issue to improve the ecological relevance of risk assessment because natural populations can be exposed to toxicants over several generations. Until now, such multigenerational studies are scarce and their outcomes vary widely among tested pollutants. In Daphnia magna, exposure to waterborne nickel showed increasing effects on growth across two generations7 and on offspring size across seven generations.8 Similarly, increasing sensitivity of daphnid reproduction and survival to americium-241 was observed across three © 2011 American Chemical Society
Received: Revised: Accepted: Published: 1136
August 1, 2011 November 21, 2011 November 24, 2011 November 24, 2011 dx.doi.org/10.1021/es202658b | Environ. Sci. Technol. 2012, 46, 1136−1143
Environmental Science & Technology
Article
in D. magna. Whereas stress functions accounting for sublethal toxic effects are assumed to depend on internal concentration resulting from bioaccumulation in organisms in the standard DEBtox,14 Massarin et al. (2011)12 showed that effects of depleted U on assimilation were immediate and could be linked to external concentration directly. A rapid kinetics was consistent with the observation of severe damages to the intestine epithelial cells. Hence in agreement with Massarin et al. (2011)12 the stress function for assimilation sA was directly linked to exposure concentration c by
food and microscope observations of histological damages on the intestinal epithelium.11,12 Having described toxic effects of depleted U on D. magna life history and physiology, consequences at the population level remain to be examined. The aim of this study is to explore how increasing effects at the individual level among the three successive generations (hereafter referred to as F0, F1, and F2) may alter population responses to U. To do so, DEBtox and survival models are first fitted to survival, growth and reproduction data reported in Massarin et al. (2010).11 Outcomes are then projected from the organism to the population levels using two modeling approaches. In the first approach, uranium effect on asymptotic population growth rate is evaluated in each generation considered separately, assuming that the population behaves asymptotically either like F0, F1, or F2. In the second approach, combined probability of population extinction is investigated, assuming that the population behaves successively like F0, like F1 and finally like F2.
sA (c) = max(0, kA(c − NECA )) (1) that is, sA is null below a sublethal toxicity threshold NECA and proportional to the excess above NECA with an effect intensity coefficient kA. Growth and reproduction processes were respectively modeled by the following eqs 2 and 316 given for ad libitum conditions:
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dl 2 (t , c) = rB (1 − sA (c) − l(t , c)) dl 2 − sA (c) L with l(0, c) = l0 = 0 Lm
MATERIAL AND METHODS Experimental Data. Body length, fecundity, and survival data were taken from previously performed experiments with daphnids exposed to waterborne depleted U.11 Briefly, D. magna was continuously exposed at four treatments corresponding to depleted U concentrations of 0, 10, 25, and 75 μg L−1 for three generations F0, F1, and F2. F0 was initiated with freshly released neonates (
