Subtle alterations in swimming speed distributions of rainbow trout exposed to titanium dioxide nanoparticles are associated with gill rather than brain injury

The effects of engineered nanomaterials on fish behaviours are poorly understood. The present study aimed to determine the locomotor behaviours of trout during waterborne exposure to titanium dioxide nanoparticles (TiO2 NPs) as well as inform on the underlying physiological mechanisms involved. Trout were exposed to either control (without TiO2), 1 mg l−1 TiO2 NPs or 1 mg l−1 bulk TiO2 for 14 days. Titanium dioxide exposure resulted in 31 (bulk) and 22 fold (nano) increases in the Ti concentrations of gill tissue compared to controls, but there were no measurable increases of Ti in the internal organs including the brain. Gill pathologies were observed in both TiO2 treatments. Locomotor behaviours were quantified using video tracking software and the proportion of time spent swimming at high speed (>20 cm s−1) was significantly decreased in fish exposed to TiO2 NPs, compared to controls, but not fish exposed to bulk TiO2. The shift in swimming speed distribution in the TiO2 NP-exposed fish was associated with decreased area of red pulp in the spleen, increases in haematocrit and whole blood haemoglobin, all consistent with a compensation for respiratory hypoxia without the accumulation of plasma lactate. Fish exposed to TiO2 NPs also retained competitive abilities when paired with controls in aggressive social encounters. The duration of competitive contests, the level of aggression and contest outcome were not affected by NP exposure. Neurological injury did not explain the changes in locomotor behaviour, although there was some apparent enlargement of the blood vessels on the brain. Whole brain homogenates showed a statistically significant increase in oxidative stress defences such as the total glutathione pool, but without loss of Na+K+-ATPase or acetylcholinesterase activities.

► Exposure to titanium dioxide nanoparticles altered locomotor behaviours in trout.
► Rainbow trout decreased the proportion of time spent swimming at high speeds.
► The shift in swimming speeds was associated with gill injury and respiratory stress.
► Subtle changes in haematology and spleen support the idea of a developing hypoxia.
► Brain injury from TiO2 was not the cause of the changes in behaviour.