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Studies on The Olfactory Biology and Behavioral Responses to Copper Exposure of The Native Indicator Species Delta Smelt (Hypomesus transpacificus)

Abstract

The Delta Smelt (Hypomesus transpacificus) is a small Osmerid native to the San Francisco Bay Delta (Bay-Delta) in California. Delta Smelt population has declined dramatically since the species was declared as endangered in 1993, and now has been listed as critically endangered by the International Union for Conservation of Nature (IUCN). The Bay Delta is a highly modified ecosystem, and the Delta Smelt has been used as an indicator species to assess the overall health of this ecosystem. Recently, a wealth of evidence exists showing that anthropogenic intervention and change in ecosystems leads to alteration in the sensory perception of the environment by aquatic animals compromising survival in highly modified environments. One of the main modalities used by aquatic organisms to assess and survive in the wild is the olfactory system. The olfactory system is involved in pivotal functions such as recognition of predators, kin recognition, mating, foraging and migration. The olfactory system is highly susceptible to contaminants including copper, which is a common contaminant and a well-studied and measurable olfactory toxicant of fish. A link between the olfactory biology and the effects of common contaminants (i.e., copper) found in the Bay Delta on Delta Smelt is lacking. I studied the basic morphological characteristics of the olfactory organ (olfactory rosette) of Delta Smelt using histological, immunohistochemical and ultrastructural techniques; the olfactory mediated behavioral responses to predation related odorants using a behavioral standardized assay and tracking software; and finally, I evaluated morphological changes of the olfactory epithelium and behavioral responses to alarm cues after copper exposures using concentrations of 2, 8 and 32 µg/L and two exposure times (24 and 96 hours). The Delta Smelt can be classified as a macrosmatic fish, based on the morphological features of the olfactory rosette. This fish has multilamellar, paired olfactory rosettes containing a highly specialized olfactory epithelium. The olfactory epithelium was composed by several populations of cells including sensory neurons with distinct morphology and immunocytochemical features. Delta Smelt have a highly sophisticated and sensitive response to predation related odorants. They detect alarm cues in a concentration dependent fashion using olfaction and display specific behaviors (escape responses and freezing) upon detection that all together are considered as olfactory mediated antipredator behaviors. Finally, I demonstrated using histopathological and immunohistochemical techniques that Delta Smelt olfactory epithelium is highly susceptible to copper exposure at concentrations commonly found in the Bay Delta and considered as sublethal. Moreover, there were differential effects on antipredator behaviors after exposure to copper for 24 and 96 hours. Fish exposed to 8 µg/L of copper for 24 hours showed severe damage to the olfactory epithelium and hyperexcitability when presented to alarm cues. At higher concentrations, the epithelium was severely damaged, the antipredator response was absent and there were signs of histological and behavioral toxicity. The results of these experiments demonstrate that Delta Smelt is a highly olfactory species and establishes that copper contamination can impair olfactory responses at environmentally relevant concentrations in this endangered fish.

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