Effects of multigenerational exposure to elevated temperature on reproduction, oxidative stress, and Cu toxicity in Daphnia magna

https://doi.org/10.1016/j.ecoenv.2016.06.034Get rights and content

Highlights

  • Multigenerational effects of temperature on Daphnia magna were evident.

  • Elevated temperature aggravated Cu-induced oxidative stress in D. magna.

  • Offspring were more vulnerable to oxidative stress than parents.

Abstract

This study evaluated the effect of temperature (20 and 25 °C) on reproduction, oxidative stress, and copper (Cu) toxicity in Daphnia magna across three generations (F0, F1, and F2). Exposing D. magna to elevated temperature significantly decreased the number of offspring per female per day, the time to first brood, and body length compared to exposure to the optimal temperature (p<0.05). In addition, elevated temperature induced a significantly higher production of reactive oxygen species and lipid peroxidation (p<0.05). These findings suggest that D. magna likely responded to thermal stress by investing more energy into defense mechanisms, rather than growth and reproduction. In addition, oxidative stress at the elevated temperature gradually increased with each generation, possibly owing to the reduced fitness of the offspring. Exposing D. magna to 25 °C (EC50=34±3 µg L−1) substantially increased the median effective concentration of Cu in all generations compared to exposure to 20 °C (EC50=25±3 µg L−1), indicating a decrease in acute toxicity at elevated temperature. However, elevated temperature significantly increased the oxidative stress induced by a sublethal concentration of Cu (10 µg L−1). The interaction between elevated temperature and Cu exposure appears to be synergistic; however, this needs to be confirmed using multiple generations in a long-term experiment.

Introduction

Temperature is the most important abiotic environmental factor that influences the behavior, physiology, phenology, and distribution of organisms, especially ectotherms (Chen and Stillman, 2012). For example, elevated temperature promoted accelerated molting and maturity in Moina micrura (Chen et al., 2015), and other changes in reproduction, such as total number of offspring and time to first brood (Engert et al., 2013). In addition, elevated water temperature may accentuate oxidative stress by increasing metabolic rate (Abele et al., 2002, Speakman, 2005, Williams et al., 2012). The formation of reactive oxygen species (ROS) and catalase (CAT) was accelerated in D. magna at elevated temperature (Becker et al., 2011). Increased lipid peroxidation and antioxidant enzyme activity, such as CAT and glutathione S-transferase, were also found in fish after exposure to elevated temperature (Madeira et al., 2013, Vinagre et al., 2012). Therefore, understanding the impact of thermal stress in aquatic systems is important as aquatic animals are subject to seasonal and daily temperature fluctuations (Sappal et al., 2014). As such, global warming is now regarded as a major threat for aquatic ecosystems (Williams et al., 2012).

Many studies have investigated the effect of temperature on metal toxicity in ectotherms (Heugens et al., 2006, Martínez-Jerónimo et al., 2006, Yang and Chen, 1996). Generally, elevated temperature may directly affect the toxicity of metal by increasing metabolic rate, including uptake and accumulation rates (Heugens et al., 2003, Muyssen et al., 2010, Wang et al., 2014). Toxic metals are well-known to generate ROS and cause oxidative damage to biomolecules (Lushchak, 2011, Vergauwen et al., 2013b), raising the possibility of synergistic effects between elevated temperature and metal exposure on oxidative stress (Lushchak, 2011, Muyssen et al., 2010). For instance, oxidative damage to lipids and activities of antioxidant enzymes was increased in Perna viridis exposed to mercury at an elevated temperature (Verlecar et al., 2007). However, a negative relationship between metal toxicity and water temperature has also been reported (Mubiana and Blust, 2007, Perschbacher, 2005). For instance, lower acute toxicity and internal concentration of copper (Cu) with increasing water temperature was observed in Enchytraeus crypticus (Cedergreen et al., 2013). Thus, the overall effect of temperature on metal toxicity remains equivocal.

Recently, multigenerational exposure to elevated temperature has gained much attention owing to the predicted impacts of global warming (Loureiro et al., 2015, Walsh et al., 2014). Changes in the maternal environment can lead to a reduction in the performance or quality of offspring (Marshall and Uller, 2007). For instance, Caenorhabditis remanei that were exposed to heat stress produced offspring that were more vulnerable to the stress of elevated temperature (Sikkink et al., 2014). Since ectothermic animals may encounter the additional stress of chemical exposure, the interactive effects with elevated temperature should be investigated across multiple generations (Noyes et al., 2009). Therefore, the aims of this study were: (1) to evaluate multigenerational effects of temperature (20 and 25 °C) on reproduction and oxidative stress in Daphnia magna across three generations (F0, F1, and F2); (2) to evaluate interactive effects of temperature on Cu toxicity toward D. magna. We used a freshwater filter-feeding crustacean, D. magna, as a model organism, as it is a recognized test organism for ecotoxicology studies, and serves as a vital link between producers (algae) and secondary consumers (fish) in aquatic food chains (Lampert, 2006). In addition, we used Cu as a model metal as it is a well-known toxicant for D. magna and a widely found contaminant in water bodies in Korea (Kim et al., 2012b, Yoo et al., 2013).

Section snippets

Measurements of reproduction and body length

D. magna were obtained from the National Institute of Environmental Research, Korea and had been cultured in the laboratory since 2010. Daphnids were grown in Elendt M4 medium (pH=7.8±0.1 and hardness=250±25 mg L−1 CaCO3) under a 16:8-h light: dark photoperiod at 20 °C. The culture medium was renewed twice weekly and organisms were fed daily with approximately 5×106 cells mL−1 of Chlorella spp.

For multigenerational testing, D. magna were exposed to two temperature treatments (20 and 25 °C) for

Multigenerational effects of temperature

Effects of temperature on reproduction of D. magna (<24-h-old) are shown in Fig. 1. Exposure to 25 °C significantly decreased both number of offspring per female per day and time to first brood, compared to the exposure to 20 °C (p<0.05). Although the total number of offspring per female was higher at 25 °C than at 20 °C, a larger number of broods at elevated temperature showed lower number of offspring per female per day (data not shown). Moreover, the effect of temperature on reproductive traits

Conclusion

D. magna exposed to elevated temperature (25 °C) showed reduced growth and reproduction compared to those exposed to the optimal temperature (20 °C), possibly due to allocating limited energy to defense against oxidative stress. In addition, continuous exposure to elevated temperature reduced the capacity for offspring generations (F1 and F2) to respond to oxidative stress. Since aquatic organisms may require over three generations to acclimatize to environmental change, multigenerational effects

Acknowledgments

This work was supported by the Korea Ministry of Environment as “Development of integrated model for climate change impact and vulnerability assessment” and by a Korea University Grant.

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