Cadmium exposure affects Coho salmon ability to smell ... and why it matters

Chase Williams, PhD candidate in the UW School of Public Health Department of Environmental and Occupational Health Sciences (DEOHS) has defended his dissertation. The title is: Mechanisms and Biomarkers of Cadmium Induced Neurobehavioral Impairment in the Olfactory System of Coho Salmon (Oncorhynchus kisutch).  Dr. Evan Gallagher, Director of the University of Washington Superfund Research Program (UW-SRP) and a member of the Center for Ecogenetics and Environmental Health, was his Supervisory Committee Chair.

Chase Williams
Chase Williams
First, I can't resist observing that the defense was held in Roosevelt 2228, a conference room with glass doors commonly called the Fishbowl.

Pacific salmon populations are threatened by many factors, and one contributing factor is thought to be disruption of the olfactory system, the sense of smell, by waterborne pollutants. The salmon olfactory system is in direct contact with the water column making it a sensitive target for chemical disruption by waterborne pollutants. This is important as salmon rely on their sense of smell for many critical functions, such as navigation, finding food and avoiding predators.


The metal cadmium (Cd) is a common pollutant in industrialized and agricultural waterways. Sources of Cd include discharge from industrial operations and fertilizers used in agricultural areas. Research has shown that Cd can impair the function of the olfactory system in zebrafish and trout. It is also known that wild juvenile salmon migrate through pollutant impacted waterways, many of which can contain Cd. 


Chase investigated three questions: (1) Do acute Cd exposures change salmon behaviors that depend on the sense of smell? (2) Does the olfactory system recover after being exposed to Cd? (3) Can we develop a set of molecular biomarkers that reflect Cd induced olfactory dysfunction and injury?


First, juvenile Coho were exposed to two concentrations of Cd for between 8 and 48 hours, followed by a 16-day recovery period. Chase observed the Cohos’ behavioral responses to an alarm odorant in a two-choice maze, after which he examined their olfactory rosettes for changes in histology (tissue anatomy) and gene expression. 

Here is what he found: Exposure to a low-level (3.7 parts per billion or ppb) and a high-level (347 ppb) of Cd disrupted the Cohos’ "olfactory driven alarm behavior". In addition, the 347 ppb exposure level completely blocked their sense of smell within 48hrs. After the 16-day recovery, the fish exposed to both levels of Cd showed only partial recovery of olfactory function. Tissue analysis of the olfactory sensory epithelium (thin tissue lining of hollow structures) showed that the high-level Cd exposure killed many olfactory sensory and non-sensory epithelial cells, explaining the loss of smell. Gene expression of cellular stress/injury biomarkers that were measured in the olfactory rosettes (hmox1, mt1a, nrn1) hinted at the mechanisms.


Based on those findings, Chase then investigated how exposure to Cd impacted Coho salmon behavioral responses to multiple types of odorants, and the effect of Cd on different types of olfactory sensory neurons. Two experiments were done: (1) Juvenile Coho salmon were exposed to one of two concentrations of Cd (2 and 30 ppb) for 48hrs, followed by 16 days of recovery; (2) Another group of juvenile Coho salmon were exposed to lower-levels of Cd (0.3 and 2 ppb) for 16 days, followed by 16 days of recovery. Chase analyzed olfactory driven behaviors in a two-choice maze, using odorants that elicited 3 possible responses: an attraction, an avoidance, or an alarm response. Following the behavioral trials, he again analyzed changes in histology and gene expression within the olfactory rosettes.


What he found was that exposure to Cd altered the Cohos' behavioral responses to the different scents, and in some cases completely reversed their responses, even at the very-low 0.3 ppb Cd exposure level. Surprisingly, these behavioral alterations persisted even after the 16-day recovery period. He found that the low-level Cd exposures did not induce observable injuries in the olfactory sensory epithelial tissue. He also found that Cd builds up quickly and persists in the olfactory sensory epithelium. The accumulation and persistence of Cd in the olfactory system closely mirrored the observed behavioral changes. Analyzing the expression levels of protein and gene markers of the two main types of olfactory sensory neurons, ciliated and microvillar, he found that exposure to the 30 ppb level of Cd predominantly impacted the ciliated olfactory sensory neurons compared to the microvillar olfactory sensory neurons.

A young Coho salmon (photo credit: kellymrk 
http://ian.umces.edu/discforum/index.php?topic=448.0)

Conclusions:

• Exposure to environmentally relevant concentrations of Cd can disrupt salmon olfactory function. There is a partial, but incomplete, recovery of the ability to smell when the exposure ends.

• When the Coho sense of smell is impaired, Coho response to typical odorants changes. Different olfactory neuronal cell types do not all respond the same way to Cd exposures. 

• This data suggest that the mechanisms underlying the behavioral alterations vary depending on the level of Cd exposure. The observed behavioral dysfunction following high-level Cd exposures are likely driven by significant injury to the olfactory epithelium. However, the lack of observable injury to the olfactory epithelium following the low-level Cd exposures suggests that the observed behavioral dysfunction following low-level Cd exposures are most likely driven by disruption of olfactory neuronal signaling.

• The results of this study indicate that juvenile salmon migrating through waterways that contain Cd (and potentially other metals) may have rapid and persistent loss of the ability to smell. An impaired ability for fish to smell has been linked to loss of fitness and increased mortality.

The Superfund Research Program helped to finance this research. Chase was a Student Poster Winner at the 2012 SRP Annual meeting. In 2013 he made a presentation to the SRP Trainee Webinar Series titled: Effects of Cadmium on Olfactory Mediated Behaviors and Molecular Biomarkers in Coho Salmon (Oncorhynchus kisutch). Chase also presented a poster at the 2015 Society of Environmental Toxicology and Chemistry (SETAC) 35th annual meetingDeveloping sensitive markets of cadmium-inhibition of odorant perception in Coho salmon


His work builds on Evan's Gallagher's research on Biochemical Mechanisms of Olfactory Injury in Salmon that can affect salmon survival behaviors such as homing, feeding, and predatory-prey avoidance.   

--Marilyn Hair and Chase Williams



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