Olfaction in teleosts plays a significant role in searching for food, alerting danger, social communication, and navigation. Despite the ecological significance of this sensory modality, studies on olfaction of tunas and billfishes are limited primarily due to logistical difficulties involved with capturing and preserving these large, highly migratory species. This study aims to provide the first comprehensive characterisation of the morphology of the peripheral olfactory organs of Southern bluefin tuna (SBT), Thunnus maccoyii, using multimodal bioimaging techniques and theoretical hydrodynamics to understand structure-function relationships for a pelagic mode of life.
Gross morphological examination and 3D imaging reveals that SBT have paired olfactory chambers situated anterior to their large eyes. Thick epidermal tissue completely covers the olfactory chambers, with water entering the chamber via a narrow, oval inlet and exiting via a slit-like outlet. A round olfactory rosette sits directly beneath the inlet and has about 45 lamellae radiating from a short central raphe. Scanning electron microscopy (SEM) of the lamellae reveals a series of novel morphological adaptations. The olfactory epithelium on each lamella is divided into either small discrete oval pits or larger, irregularly shaped depressions intermingled with non-sensory epithelia. The surface of these olfactory depressions possesses both ciliated (cORN) and microvillous (mORN) olfactory receptor neurons in different densities, with mean densities of 84,405 mm-2 and 5,839 mm-2, respectively. Ciliated non-sensory cells are present in the periphery of the olfactory epithelium, with mean densities of 879 mm-2.
The arrangement of the inhalant and exhalent olfactory openings and the gross morphology of the olfactory chamber facilitates high levels of ventilation via forward motion of the fish. Based on the hydrodynamics of the incoming flow of seawater, the dispersal of water into the interlamellar space and the topography of the olfactory epithelium, the distribution of olfactory receptors is organised to optimise interactions of water-borne stimuli. These results indicate that both macroscopic and microscopic adaptations of the olfactory organs of SBT have evolved to suit its pelagic lifestyle, and in a unique way compared to many other pelagic teleosts, and that olfaction is an important driver of behaviour in this species.