9357 - Laserfiche WebLink

Home Browse Search

Effects of copper on olfaction of Colorado pikeminnow '. centration, the magnitude of toxic effect increases with ex- posure time. One explanation for the observed response is that sensitivity of the sensory system or receptors changed with time. If this explanation is correct, then compensatory mechanisms induced by initial exposure must have facilitated physiological adap- tation and the development of tolerance within 96 h. A time- dependent response of the olfactory system has been observed by other investigators [24] and is consistent with the general adaptation syndrome [25,26]. The general adaptation syn- drome describes the response of physiological systems to stressors as a three-phase time-dependent process that includes an initial loss of ability caused by exposure followed by a period of physiological adaptation that ends when compen- sating mechanisms are unable to sustain the level of activity required to offset effects of the stressor. Our data suggest that the initial loss of ability occurred during the first 24 h of exposure and was reflected by the lower response rate of fish to skin homogenate. By 96 h, induction of protective mech- anisms allowed recovery of olfactory ability, which increased the frequency of detection and response to skin homogenate in copper concentrations <66 I-Lg/L. Fish exposed to higher copper concentrations either were not able to compensate or needed more time for protective mechanisms to be induced sufficiently to offset effects of exposure. Other data support our hypothesis that loss of olfactory ability followed by recovery can occur within 96 h. Several investigators have reported that olfactory receptors of fish are damaged or destroyed in <24 h by exposure to copper con- centrations ranging from 0.02 to 7,600 mg/L [27-31]. In ad- dition, investigators have reported that regeneration of olfac- tory cells after exposure to copper occurs within 8 d to 12 weeks [7,24,30,32] and that effects and recovery of ability are exposure dependent [24,31]. Copper concentrations in most studies of structural damage to olfactory cells are much higher than those in our investigation. Consequently, other copper- specific data documenting repair of structural damage in the olfactory organ are not available for the concentration range and 96-h exposure duration that we used. However, Cancalon [33] observed regeneration of olfactory receptors in fish within 96 h of exposure to low concentrations (0.03-0.1 %) of a de- tergent. Thus, it is possible that protective mechanisms in Col- orado pikeminnow were induced and regeneration of olfactory receptors occurred within the 96-h exposure period. Potential protective mechanisms There are several potential protective mechanisms that may decrease effects of long-term exposure to copper on olfactory receptors by sequestering, eliminating, or reducing absorption of toxicants. First, exposure to copper has been shown to in- crease mucus production in fish [24,34]. Mucus provides a protective coat over olfactory sensory cells. Odorants or con- taminants must diffuse through the mucus layer before they can stimulate or inhibit receptor cells [35]. Increased mucus production induced by contaminant exposure increases thick- ness of the mucus coat [34]; consequently, time required for toxic solutes to diffuse to olfactory receptors may increase. Miller and Mackay [36] showed that mucus is a strong copper chelater. Thus, in addition to the physical advantages of a thicker mucus coat, the affinity of mucus for contaminants may prevent diffusion to olfactory receptors, and sloughing of excess mucus may physically remove chelated toxicants from the olfactory chamber. Whitear [37] hypothesized that che- Environ. Taxieal. Chern. 20,2001 911 moreceptors in fish may have a neuroendocrine link to sur- rounding cells in the epidermis. If this function exists for ol- factory receptors of fish, it may influence mucus secretion of the epidermis by controlling goblet and superficial epithelial cells. Such an association would provide a basis for a feedback mechanism in which olfactory receptor cells could optimize local mucus production by increasing it when harmful solutes are present and decreasing it under normal conditions to im- prove sensitivity to information-containing odorants. A second potential protective system is induction of de- toxifying mechanisms. The olfactory epithelium of a number of fishes contains high levels of cytochrome P-450 monoox- ygenase, which can be activated by exposure to heavy metals [9]. Presence of this enzyme system in olfactory tissues sug- gests the ability to eliminate or sequester toxic solutes. A third potential protective system involves a sequestering function of melanophores in the olfactory organ. After 60-d exposure to copper at 20 I-Lg/L, Julliard et al. [38] observed a correspondence between regeneration of olfactory structure in rainbow trout (Oncorhynchus mykiss) and increasing metal concentrations in melanosomes in melanophores. They suggest that the correspondence is evidence of a mechanism that con- tributes to recovery of olfactory ability despite continued cop- per exposure. Implications of this investigation The regenerative capacity and variable senSItivIty of the olfactory system of fish is probably an evolutionary adaptation to injury during normal life [9]. These abilities may give a false impression that there is a margin for error when assessing potential effects of environmental contaminants on fish. How- ever, evidence suggests that fish that are acclimated to chemical exposure suffer reduced olfactory ability compared with un- exposed fish [24]. In addition, intermittent loss and recovery of olfactory ability can potentially have a high biological cost. Olfaction in fishes facilitates a variety of ecological interac- tions including predator avoidance, feeding in patchy envi- ronments, mating, and migration [39]. Although the temporal scale of these behaviors may be short (e.g., predator avoidance may occur in seconds), they facilitate intense interactions that have important outcomes like survival or death. Results of this study and available water-quality data suggest that copper concentrations in the Yampa River may occasionally inhibit olfactory ability of resident Colorado pikeminnow. The Yampa River was selected for comparison in this study because data are available that describe its water quality characteristics, adult Colorado pikeminnow inhabit the river all year, and spawn- ing occurs in the river from late June through early August. However, the Yampa River is considered to be one of the more pristine large rivers in the Colorado River Basin. Conditions in other rivers may warrant greater concern. There are a variety of contaminant sources in the Colorado River Basin including natural hot springs, municipal releases, irrigation returns, and historic mining. The potential for ex- isting sources of contamination to result in adverse ecological effects is compounded by demand for water in the West. As resources are diverted for municipal, industrial, and agricul- tural uses, less water will be available for dilution. If increases in water use outpace the process of pollution abatement within the Colorado River Basin, frequency and magnitude of con- taminant-induced toxic effects will increase even if contami- nant inputs remain constant. Geographical distribution of Col- orado pikeminnow has been greatly reduced and reproducing