Olfactory Morphology of Juvenile Scalloped Hammerhead and Sandbar Sharks and the Effects of Acute Copper Exposure on the Hammerhead Olfactory System

Abstract

Olfaction plays a large role in the excitation and orientation behaviors elasmobranchs display when hunting. These behaviors are dependent on an intact olfactory system, composed of olfactory receptor neurons (ORNs) which detect odorants and send these signals toward the brain. The impact of heavy metal toxicants on the olfactory system in teleosts is well-characterized, with damaged ORNs and decreased or eliminated olfactory-mediated behaviors. The current research is the first examination of the impact of an environmental toxicant on the olfactory system of an elasmobranch, the juvenile scalloped hammerhead shark Sphyrna lewini. The olfactory epithelium of S. lewini was first examined to identify the types of ORNs present and determine a baseline density and total number of ORNs. Microvillar ORNs (mORNs) and crypt neurons (CNs) were identified, with an average of 230 million ORNs for an average 60 cm shark. In comparison, Carcharhinus plumbeus, the sandbar shark, possessed only mORNs, which may indicate that CNs have independently evolved within the Sphyrnidae family. Sphyrna lewini were then exposed to one of three copper (Cu) concentrations for 60 minutes: unfiltered seawater + 0 μg L-1 (0M) Cu, seawater + 29 μg L-1 (0.5 μM) Cu, or seawater + 286 μg L-1 (5 μM) Cu. Electro-olfactogram measurements showed a decrease in olfactory sensitivity after exposure to the elevated Cu concentrations, followed by a complete recovery to baseline sensitivity after a recovery period. The label for olfactory marker protein (OMP) showed no difference in ORN density between the treatment and non-treatment rosettes, regardless of Cu exposure level. Though Cu did impact the olfactory sensitivity of juvenile S. lewini, the lack of damage to OMP and the recovery of sensitivity indicates that the impact was small and reversible. Unrealistically high Cu concentrations did not cause lasting damage to the olfactory sensitivity of an elasmobranch. As coastal pollution increases, olfactory damage from toxicants could lead to the functional removal of elasmobranchs as top predators, resulting in less predation control and subsequent ecosystem shifts. The impact of heavy metal toxicants on elasmobranch olfaction, including the possible permanent effects of Cu on physiology and morphology, warrants further investigation.