Impaired behavioural response to alarm substance in rainbow trout exposed to copper nanoparticles

Abstract

To date, studies of the toxicity of engineered nanoparticles (NPs) in fish have not fully considered effects on olfactory-mediated behaviours, despite their ecological importance. In this study the effects of copper NPs (Cu NPs) on the anti-predator behavioural responses of juvenile rainbow trout (Oncorhynchus mykiss) to trout alarm substance was investigated. Individual fish were exposed for 12h to a control (no added Cu), 50μgl(-1) of Cu as Cu NPs, or 50μgl(-1) Cu as CuSO4, after which fish behaviours were analyzed in 10min periods before and after the addition of the alarm substance stimulus. The response of control fish to deionised water (negative control, no alarm substance stimulus) was also analyzed. The alarm substance elicited a behavioural response in the control fish characterized by an immediate freeze response and the slower resumption of swimming activity compared to negative controls exposed to the sham deionised water stimuli. In fish exposed to Cu NPs, the behavioural response to alarm substance was eliminated, with no significant difference in behaviours compared to negative controls. In comparison, exposure to 50μgl(-1) Cu as CuSO4 decreased, but did not eliminate the response of fish to alarm substance, which indicated a significantly greater effect of Cu NPs on olfactory mediated behaviours than of the equivalent concentration of Cu as CuSO4. Measurement of total Cu concentrations in the tissues of fish demonstrated no significant accumulation of Cu from any treatment in gill, liver or brain, confirming the effects of Cu NPs, and to a lesser extent CuSO4, on behavioural responses were mostly associated with the interaction of the materials with the external surfaces of the fish. Scanning electron microscopy revealed that Cu as CuSO4 caused a pronounced depletion of ciliated sensory and non-sensory cells in the olfactory rosette surrounding the midline raphe, whereas Cu NPs had no impact on the structure of the rosette. However, exposure to Cu NPs caused a significant increase in the ratio of oxidized to reduced glutathione in brains of fish, indicating some systemic oxidative stress that was not observed in either controls or fish exposed to CuSO4. Overall, the study showed that the olfactory mediated behaviours of fish were potentially more sensitive to Cu NPs than CuSO4 and NPs elicited effects via a mechanism that is distinct from that of the metal salt.

Use of an exposure chamber to maintain aqueous phase nanoparticle dispersions for improved toxicity testing in fish

“…Because NPs in exposure chambers were less affected by sedimentation, expression of the mortality data gathered from this exposure series relative to the initial gravimetric dose is also more accurate, because the concentration of NPs in the vicinity of the organism was less variable over time. Furthermore, for metallic NPs, such as the AgNPs and CuNPs used in the present study, which have a metal ion dissolution component to toxicity [15][16][17], high rates of sedimentation of particulate matter away from the test organism may lead to overestimating the importance of metal ions remaining in suspension to the toxicity of NPs. Whether the lower LC50 for Ag and CuNP exposures recorded in the present study indicate a nanoscalespecific effect is unclear.…”

The role of metals in mammalian olfaction of low molecular weight organosulfur compounds

“…Furthermore, nanoparticles elicited effects by a mechanism distinct from that of the metal salt. 105 …”

Effects of subchronic exposure to zinc nanoparticles on tissue accumulation, serum biochemistry, and histopathological changes in tilapia (Oreochromis niloticus)

“…Various fish species (e.g., rainbow trout, carp, and zebrafish) have been used as model animals to investigate toxicological effects of a number of metal and metal oxide NPs, such as Ag (Imani et al, ), Cu (Shaw et al, ; Sovová et al, ), ZnO (Hao & Chen, 2012, ; Ates et al, ; Kaya et al, ), CuO (Zhao et al, ; Ates et al, ), TiO 2 (Hao et al, ; Boyle et al ), Fe 2 O 3 (Remya et al, ; Saravanan et al ; Zhang et al ). To date, studies attempting to elucidate the adverse effects of ZnNPs have been conducted only recently by a handful of groups (Ates et al, 2103b; Abdel‐Khalek et al, 2015); therefore, there is a need for comprehensive studies detailing the ecotoxicological effects of ZnNPs.…”