Daphnia magna’s sense of competition: intra-specific interactions (ISI) alter life history strategies and increase metals toxicity

Ecotoxicology, May 2016

This work investigates whether the scale-up to multi-animal exposures that is commonly applied in genomics studies provides equivalent toxicity outcomes to single-animal experiments of standard Daphnia magna toxicity assays. Specifically, we tested the null hypothesis that intraspecific interactions (ISI) among D. magna have neither effect on the life history strategies of this species, nor impact toxicological outcomes in exposure experiments with Cu and Pb. The results show that ISI significantly increased mortality of D. magna in both Cu and Pb exposure experiments, decreasing 14 day LC50 s and 95 % confidence intervals from 14.5 (10.9–148.3) to 8.4 (8.2–8.7) µg Cu/L and from 232 (156–4810) to 68 (63–73) µg Pb/L. Additionally, ISI potentiated Pb impacts on reproduction eliciting a nearly 10-fold decrease in the no-observed effect concentration (from 236 to 25 µg/L). As an indication of environmental relevance, the effects of ISI on both mortality and reproduction in Pb exposures were sustained at both high and low food rations. Furthermore, even with a single pair of Daphnia, ISI significantly increased (p < 0.05) neonate production in control conditions, demonstrating that ISI can affect life history strategy. Given these results we reject the null hypothesis and conclude that results from scale-up assays cannot be directly applied to observations from single-animal assessments in D. magna. We postulate that D. magna senses chemical signatures of conspecifics which elicits changes in life history strategies that ultimately increase susceptibility to metal toxicity.

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Daphnia magna’s sense of competition: intra-specific interactions (ISI) alter life history strategies and increase metals toxicity

Ecotoxicology Daphnia magna's sense of competition: intra-specific interactions (ISI) alter life history strategies and increase metals toxicity Kurt A. Gust 0 1 2 3 4 Alan J. Kennedy 0 1 2 3 4 Nicolas L. Melby 0 1 2 3 4 Mitchell S. Wilbanks 0 1 2 3 4 Jennifer Laird 0 1 2 3 4 Barbara Meeks 0 1 2 3 4 Erik B. Muller 0 1 2 3 4 Roger M. Nisbet 0 1 2 3 4 Edward J. Perkins 0 1 2 3 4 0 SpecPro Technical Services , San Antonio, TX , USA 1 Environmental Laboratory , US Army , Engineer Research and Development Center , Vicksburg, MS , USA 2 & Kurt A. Gust 3 Department of Ecology, Evolution & Marine Biology, University of California , Santa Barbara, Santa Barbara, CA , USA 4 Marine Science Institute, University of California , Santa Barbara, Santa Barbara, CA , USA This work investigates whether the scale-up to multi-animal exposures that is commonly applied in genomics studies provides equivalent toxicity outcomes to single-animal experiments of standard Daphnia magna toxicity assays. Specifically, we tested the null hypothesis that intraspecific interactions (ISI) among D. magna have neither effect on the life history strategies of this species, nor impact toxicological outcomes in exposure experiments with Cu and Pb. The results show that ISI significantly increased mortality of D. magna in both Cu and Pb exposure experiments, decreasing 14 day LC50 s and 95 % confidence intervals from 14.5 (10.9-148.3) to 8.4 (8.2-8.7) lg Cu/L and from 232 (156-4810) to 68 (63-73) lg Pb/L. Additionally, ISI potentiated Pb impacts on reproduction eliciting a nearly 10-fold decrease in the noobserved effect concentration (from 236 to 25 lg/L). As an indication of environmental relevance, the effects of ISI on both mortality and reproduction in Pb exposures were sustained at both high and low food rations. Furthermore, even with a single pair of Daphnia, ISI significantly Daphnia; Intra-specific interactions; Ecotoxicology; Metals toxicity; Standard toxicity assays - increased (p \ 0.05) neonate production in control conditions, demonstrating that ISI can affect life history strategy. Given these results we reject the null hypothesis and conclude that results from scale-up assays cannot be directly applied to observations from single-animal assessments in D. magna. We postulate that D. magna senses chemical signatures of conspecifics which elicits changes in life history strategies that ultimately increase susceptibility to metal toxicity. Introduction Daphnia magna is an important model species in ecotoxicology for which standard assays have been developed for use in regulatory toxicity assessment (ASTM 2012; USEPA 2002) . Over the past 10 years, Daphnia spp. have become increasingly utilized as genomic model organisms (Colbourne et al. 2011) and used in toxicogenomic investigations to determine molecular and mechanistic effects of contaminant exposures (Ananthasubramaniam et al. 2015) . In order to meet minimum mRNA requirements for toxicogenomics methods, a common practice has been to scale up exposures to include 10–100 s of Daphnia per exposure replicate. This type of scale-up procedure has been applied in a number of toxicogenomics studies with D. magna (i.e. Stanley et al. 2013; Campos et al. 2013; Garcia-Reyero et al. 2009, 2012; Poynton et al. 2007; Shaw et al. 2007) where the expression results were directly applied to understand the results observed in standard-scale, single animal exposures. In order to draw these inferences among exposure methods, the authors have made the assumption that exposure scaling has no effect on the outcome of the test. Thus far, we have found no published studies that have explicitly tested this critical assumption for D. magna in ecotoxicological exposures, in context with genomics investigations. When scaling up a toxicity assay such as the standard D. magna reproduction test (ASTM 2012) from a single animal to multi-animal exposure experiment, it becomes logistically challenging to quantify reproductive output. Note that the cited ASTM method allows the experimentalist discretion to test either signal or multiple organisms within a single replicate chamber. Thus, many researchers run scale-up toxicity assays in parallel, where the latter is used to quantify reproduction and the former to examine toxicogenomic effects. However, animals exposed in the scale-up tests could potentially experience intra-specific competition, whereas individuals in the standard assays would not. The adverse effects of contaminant exposure on survival, reproduction and/or population structure can be exacerbated by intraspecific competition among Daphnia (Knillmann et al. 2012; Foit et al. 2012; Liess and Foit 2010; Viaene et al. 2015) . In this context, researchers are often careful to scale up both exposure volume and food per individual to help minimize the potential for intraspecific competition among Daphnia in the multi-animal exposures, thus minimizing confounding effects of intraspecifi (...truncated)


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Kurt A. Gust, Alan J. Kennedy, Nicolas L. Melby, Mitchell S. Wilbanks, Jennifer Laird, Barbara Meeks, Erik B. Muller, Roger M. Nisbet, Edward J. Perkins. Daphnia magna’s sense of competition: intra-specific interactions (ISI) alter life history strategies and increase metals toxicity, Ecotoxicology, 2016, pp. 1126-1135, Volume 25, Issue 6, DOI: 10.1007/s10646-016-1667-1