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NCER Grantee Research Project Results

Sublethal Impacts of Copper on Olfaction and Olfactory-Dependent Behaviors in Coho Salmon

EPA Grant Number: F5D40859
Title: Sublethal Impacts of Copper on Olfaction and Olfactory-Dependent Behaviors in Coho Salmon
Investigators: McIntyre, Jenifer K.
Institution: University of Washington
EPA Project Officer: Jones, Brandon
Project Period: September 28, 2005 through September 23, 2008
Project Amount: $105,081
RFA: STAR Graduate Fellowships (2005)
Research Category: Academic Fellowships

Description:

Objective:

In mixed-use watersheds that support salmon, non-point source water quality degradation typically involves a complex mixture of metals, pesticides, oil, and other anthropogenic contaminants. Of these, dissolved copper is one of the most pervasive pollutants in storm water. Copper is neurotoxic to fish and is known to be acutely lethal to salmon at relatively high concentrations. However, the sublethal effects of this contaminant, at concentrations more commonly found in urban streams, are less well understood. Olfactory receptors of salmon are particularly vulnerable to the neurotoxic effects of copper because they are directly exposed to ambient water. Olfaction subserves many critical aspects of the life histories of Pacific salmonids, and a reduction or loss of olfactory capacity could therefore have important negative consequences for salmon survival, distribution, or reproduction. This in turn could limit the productivity of wild populations, including those that are currently listed as threatened or endangered under the ESA. The objective of this research is to address the need for sublethal toxicological information by focusing on the effects of copper on olfaction and olfactory-mediated behaviors in salmon.

Approach:

I will characterize and integrate sublethal impacts of copper exposure on salmonids at the levels of olfactory neurophysiology, individual behavior, and population dynamics. This work will focus on coho salmon since this species favors small streams that are often the receiving waters for non-point source runoff. I will first assess the bioavailability of copper to olfactory receptor neurons (ORNs), then characterize the olfactory-mediated effects of non-point source copper pollution on both the neurophysiology and the behavior of salmonids at important life history stages, and finally integrate these impacts into a demographic population model.

  1. Bioavailability of copper to ORNs is a critical question. In terms of acute lethality, the toxicity of copper and other metals is a function of water chemistry parameters including hardness, alkalinity, pH, and dissolved organic matter, and is described by the Biotic Ligand Model (BLM). Contrary to expectations based on the BLM, preliminary studies with Pacific salmon exposed to copper at high, medium, and low hardness showed no protective effect in terms of copper’s sensory neurotoxicity. I will undertake a complete factorial laboratory study to determine the extent to which conventional water chemistry parameters affect the toxicity of copper to ORNs. This is crucial to determining whether the BLM, a model structured around metal uptake across the gills, can be applied to toxicity of the salmon olfactory system.
  2. The bulk of the research will assess olfactory-mediated effects of non-point source copper pollution on important life history stages of coho salmon. Survival of juvenile coho will be tested in natural arenas with real predators, expanding on previous research that showed reduced anti-predator response in juvenile coho after realistic copper exposures. This research will combine laboratory measures of olfactory neurophysiology with behavioral observations of predator-prey interactions. I will also conduct field studies to evaluate the impacts of copper on coho migratory behavior. Migration studies will involve exposing returning adults to environmentally realistic levels of copper. Subsequently, the movement, timing, and overall return rates of adult salmon will be monitored as they migrate back to their natal streams to spawn. Copper effects on reproductive synchronization will be tested in laboratory experiments. Sexually maturing males will be exposed to the urine of pre-ovulatory or ovulating females after exposure to copper. By measuring blood hormone levels and related endocrine endpoints (i.e., milt production), I will be able to test the hypothesis that copper interferes with the olfactory detection of the female priming pheromone(s) by the male and, by extension, causes reproductive desynchronization in pre-spawning pairs. Established techniques will be used for olfactory recordings, predation trials, measures of reproductive synchronization, pre-spawning behavior, and homing behavior.
  3. To evaluate the impacts of non-points source pollution at the scale of natural populations, empirical data will be incorporated into an integrated life cycle model specifically tailored to the anadromous life histories of Pacific salmon. This will allow for estimates of a change in intrinsic population growth rate ( l) and other demographic parameters as a function of sublethal copper toxicity across multiple life stages of individual animals. For the purpose of population modeling, I will use copper detections in surface waters of the Puget Sound Basin (greater Seattle metropolitan area) and the well-studied coho populations within the Puget Sound evolutionarily significant unit (e.g.,the index runs of Snohomish county). Modeling will emphasize sublethal copper toxicity, fish condition, and coho productivity in urban and urbanizing watersheds.

Supplemental Keywords:

copper, olfaction, sublethal, neurotoxicity, neurophysiology, electro-olfactogram, EOG, salmon, coho, urban, storm water, streams, Biotic Ligand Model, behavior, predator avoidance, homing, reproduction, population modeling,, RFA, Scientific Discipline, Ecosystem Protection/Environmental Exposure & Risk, Monitoring/Modeling, Biochemistry, Environmental Monitoring, anthropogenic stress, aquatic toxins, environmental impact, copper, stormwater runoff, fish models, Biotic Ligand Model

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The perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.

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