Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss) exposed to copper: Neurophysiological and histological effects on the olfactory system

Abstract

Abstract-Olfactory epithelial structure and olfactory bulb neurophysiological responses were measured in chinook salmon and rainbow trout in response to 25 to 300 g copper (Cu)/L. Using confocal laser scanning microscopy, the number of olfactory receptors was significantly reduced in chinook salmon exposed to Ն50 g Cu/L and in rainbow trout exposed to Ն200 g Cu/L for 1 h. The number of receptors was significantly reduced in both species following exposure to 25 g Cu/L for 4 h. Transmission electron microscopy of olfactory epithelial tissue indicated that the loss of receptors was from cellular necrosis. Olfactory bulb electroencephalogram (EEG) responses to 10 Ϫ3 M L-serine were initially reduced by all Cu concentrations but were virtually eliminated in chinook salmon exposed to Ն50 g Cu/L and in rainbow trout exposed to Ն200 g Cu/L within 1 h of exposure. Following Cu exposure, EEG response recovery rates were slower in fish exposed to higher Cu concentrations. The higher sensitivity of the chinook salmon olfactory system to Cu-induced histological damage and neurophysiological impairment parallels the relative species sensitivity observed in behavioral avoidance experiments. This difference in species sensitivity may reduce the survival and reproductive potential of chinook salmon compared with that of rainbow trout in Cu-contaminated waters.

Effect of Acute Copper Sulfate Exposure on Olfactory Responses to Amino Acids and Pheromones in Goldfish (Carassius auratus)

“…This raises the possibility that copper may disturb the sense of smell via direct interaction with signal transduction pathways in addition to physical destruction of the sensory cells. The fact that the inhibitory effects of low copper concentrations on EOG responses in Atlantic salmon tended to weaken immediately after wash-out and that both mono-and divalent copper species were effective inhibitors of olfaction prior to any physical damage occurring within the epithelium (20), together with elimination of responses in olfactory bulb electro-encephalogram (EEG) in salmonids (21,25) confirm that the effect is not caused by changes in the electrical conductance of the water due to copper. Sensitivity to L-serine and 3-MT in our study was also partially reversible, as some recovery occurred shortly after wash-out.…”

“…Copper in the micromolar range causes immediate reduction of electro-olfactogram (EOG) amplitude evoked by amino and bile acids in salmonids (20)(21)(22)(23). However, this inhibition is transient, and recovery is seen after one hour.…”

“…Similarly, a few hours of copper exposure (0.3-3 µM) causes necrosis of olfactory receptors in chinook salmon (Oncorhynchus tshawytscha). Yet some receptor cells survive and respond to L-serine (21). In brown trout (Salmo trutta), exposure to copper causes rapid apoptosis, when half the olfactory neurons die after one day of treatment and the epithelium takes six days to recover (27).…”

Quantifying Fish Swimming Behavior in Response to Acute Exposure of Aqueous Copper Using Computer Assisted Video and Digital Image Analysis

“…Copper has been shown to cause changes in activity levels such as hypoactivity in bluegill 22 (Lepomis macrochirus rafinesque) and changes in locomotor and feeding activity of brook trout 23 (Salvelinusfontinalis). At least some juvenile fish rely on their sense of smell to detect and avoid predators, and copper-induced chemosensory deprivation may impact behaviors related to detecting alarm chemicals 24,25,26 . The olfactory epithelium is damaged due to copper exposure thereby affecting sensory mechanisms which could result in disorientation, behavioral avoidance, reduced feeding and any other behaviors that are guided by olfaction 27 .…”

Variability in Sensory Ecology: Expanding the Bridge Between Physiology and Evolutionary Biology

“…Fish olfaction, for example, is altered by water chemical pollution (e.g., Bertmar 1982;Hansen et al 1999), with potential impacts on natural water discrimination along chemical gradients, such as salinity or home stream odor (Hubbard et al 2000), or social recognition (Ward et al 2008). There is also concern that increasing noise levels in the oceans (produced by sonars and shipping, for example) confuse the acoustic signals that cetaceans and other aquatic organisms use to navigate, communicate, and locate food (e.g., Richardson et al 1998;Frantzis 1998;Doak et al 2007).…”