Do titanium dioxide nanoparticles induce food depletion for filter feeding organisms? A case study with Daphnia magna

Highlights

• Algae sediment more quickly in presence of nTiO₂.

• Food depletion is not the main factor for the life history response of Daphnia.

• nTiO₂ potentially alters the nutritious quality of algae.

Abstract

Although nanoparticles are increasingly investigated, their impact on the availability of food (i.e., algae) at the bottom of food chains remains unclear. It is, however, assumed that algae, which form heteroagglomerates with nanoparticles, sediment quickly limiting the availability of food for primary consumers such as Daphnia magna. As a consequence, it may be hypothesized that this scenario – in case of fundamental importance for the nanoparticles impact on primary consumers – induces a similar pattern in the life history strategy of daphnids relative to situations of food depletion. To test this hypothesis, the present study compared the life-history strategy of D. magna experiencing different degrees of food limitation as a consequence of variable algal density with daphnids fed with heteroagglomerates composed of algae and titanium dioxide nanoparticles (nTiO₂). In contrast to the hypothesis, daphnids’ body length, weight, and reproduction increased when fed with these heteroagglomerates, while the opposite pattern was observed under food limitation scenarios. Moreover, juvenile body mass, and partly length, was affected negatively irrespective of the scenarios. This suggests that daphnids experienced – besides a limitation in the food availability – additional stress when fed with heteroagglomerates composed of algae and nTiO_2. Potential explanations include modifications in the nutritious quality of algae but also an early exposure of juveniles to nTiO₂.

Introduction

The nanotechnology industry is growing exponentially and contributes trillions of dollars to the global economy (Pearce, 2012). Particularly, titanium dioxide nanoparticles (nTiO₂) are frequently applied in various products including textiles, sunscreens and facade paints (e.g., Windler et al., 2012). Consequently, the unintended release of these nanoparticles (NPs) into aquatic ecosystems, for instance, via wastewater treatment plant effluents is inevitable (Kiser et al., 2009). Following their release, nTiO₂ interact with environmental factors and further anthropogenic chemicals modifying their fate and potential adverse effects in aquatic life (Schaumann et al., 2015). It was, for instance, shown that dissolved organic carbon (DOC) coats the surface of nTiO₂ (Philippe and Schaumann, 2014). This coating, in turn, influences the NPs’ fate and alters their acute and chronic toxicity (Seitz et al., 2015).

However, little is known about the potential impact of nTiO₂ or more generally NPs on the interaction among organisms of different trophic levels. While it was documented that nTiO₂ irradiated with ultra violet (UV) light reduces the predation success of gammarids on mayfly nymphs (Kalčíková et al., 2014) and that NPs can be transferred along aquatic food chains (Zhu et al., 2010), it seems largely unclear how NPs may alter the availability and quality of food at the bottom of the autotrophic and heterotrophic food chain. Campos et al. (2013) suggested that nTiO₂ form heteroagglomerates with algal cells, which rapidly increase in size and thus sediment. As a result of this process the availability of food for filter feeding organisms such as daphnids is depleted impacting the species’ life history strategy, namely reproduction. These authors also reported similar effects in situations of a continuous re-suspension of the heteroagglomerates from the sediment suggesting that the energy and nutrients stored in the algae may not be physiologically accessible for Daphnia. It was, however, unclear if the pattern of energy allocation by the test species is comparable to food depletion scenarios. Moreover, potential impacts in the individual size and weight of the offspring – a measure of fitness of the next generation (Boersma, 1997) – were not assessed.

Therefore, the present study aimed at filling this gap by performing three independent chronic reproduction studies using Daphnia magna as test organism. During a first experiment (i.e., food-limitation test), the daphnids were fed with different amounts of algae over the entire study duration of 21 days. Thereby, a baseline for the life history response of D. magna under different food depletion scenarios was set. During a second experiment (i.e., flow-through test), a defined amount of algae was aged in presence of increasing concentrations of nTiO₂ for 3 days and subsequently transferred to a flow-through system. In a final experiment (i.e., semi-static test) algae and nTiO₂ were aged directly in the test beaker for 24 h (without daphnids) and the test species was transferred from an old to a fresh medium every 3 days. Thereby, an initial and every third day reoccurring peak in the availability of nTiO₂ and algae from the water column shortly after the medium exchange, as assumed in the flow-through test system, was avoided. During the course of these experiments, the number of aborted eggs, the number of offspring, their individual size and weight were quantified daily. The latter two endpoints were not assessed during the semi-static test. At the termination of each experiment, adult daphnids’ body length and body weight were analyzed. This combination of endpoints from the different experiments allows for a more complete interpretation of the energy allocation of Daphnia under the different stress scenarios. It was hypothesized that in all experiments the limited availability of food (i.e., algae settle quickly when forming heteroagglomerates with nTiO₂) induces comparable life history responses in D. magna.