Ontogenetic Shifts in the Number of Axons in the Olfactory Tract and Optic Nerve in Two Species of Deep-Sea Grenadier Fish (Gadiformes: Macrouridae: Coryphaenoides)

Abstract

Neuroanatomical studies of the peripheral sense organs and brains of deep-sea fishes are particularly useful for predicting their sensory capabilities and ultimately their behavior. Over the abyssal plane (between 2,000 and 6,000 m), communities of grenadiers (Gadiformes: Macrouridae) play an important ecological role as predator-scavengers. Previous studies suggest that these fishes rely heavily on chemosensation, especially olfaction. Furthermore, at least one species, Coryphaenoides armatus, undergoes an ontogenetic shift in the relative size of the optic tectum and the olfactory bulbs, suggesting. a shift from a reliance on vision to olfaction during ontogeny, apparently in association with a shift to a more scavenging lifestyle. Here, we compared the olfactory and visual sensory inputs to the brain in C. armatus, and in a second, closely-related species, Coryphaenoides profundicolus, by assessing the total number of axons (myelinated and unmyelinated) in the olfactory tract and optic nerve in a range of individuals from both species. In C. armatus, the numbers of axons in both tract and nerve increased with body size, with the total number of axons in the olfactory tract being far greater than the number of axons in the optic nerve. These differences became more pronounced in larger animals. In the two smaller C. profundicolus individuals (≤315 mm SL), there were more axons in the optic nerve than in the olfactory tract, but the opposite situation was found in larger individuals. As in C. armatus, the number of olfactory tract axons also increased with body size in C. profundicolus, but in contrast, the number of optic nerve axons decreased in this species. These results suggest that both C. armatus and C. profundicolus undergo an ontogenetic shift in sensory orientation, with olfaction becoming relatively more important than vision in larger animals. The differences in the ratio of olfactory tract to optic nerve axons in C. armatus indicate that olfaction is of Lisney et al. Olfactory and Visual Inputs in Deep-Sea Fish particular importance to larger individuals of this species. In both species, the percentage of myelinated axons in the olfactory tract was relatively low, but we found evidence for interspecific and ontogenetic variation in the percentages of myelinated axons in the optic nerve.

Convergence of Olfactory Inputs within the Central Nervous System of a Cartilaginous and a Bony Fish: An Anatomical Indicator of Olfactory Sensitivity

“…Similar work is required in other taxa, including fishes, for which ontogenetic shifts in relative OB size have been documented [Lisney et al, 2007[Lisney et al, , 2017. A recent study by Lisney et al [2018] showed that the total number of axons (UM and M pooled) in the OT of two deep-sea fish (Coryphaenoides armatus and Coryphaenoides profundicolus) increased with ontogeny. This study reveals that the number of secondary inputs increases with ontogeny and predicts a relative shift in OB size [Lisney and Collin, 2006;Lisney et al, 2007].…”

Ontogenetic Shifts in Brain Size and Brain Organization of the Atlantic Sharpnose Shark, <b><i>Rhizoprionodon terraenovae</i></b>

“…In mammals, postnatal brain growth is attributed to development and increase of fibers, as also demonstrated in fishes [Huber and Rylander, 1992], as well as glial elements [Iaskin, 2011]. Furthermore, changes in brain growth may also be attributed to the emergence of new synapses [Gheusi et al, 2000] as well as increased myelination of established synapses [Lisney et al, 2018]. As research in these additional factors in elasmobranchs is scarce [Yopak et al, 2014], future studies should quantify rates of neurogenesis and synaptogenesis in sharks to more completely understand the elements contributing to brain growth.…”

“…In the abyssal grenadier (C. armatus), smaller individuals use their rostrum to dig in muddy substrate to find benthic invertebrates and possess a relatively enlarged optic tectum and relatively reduced olfactory bulbs; larger individuals swim above the bottom to detect their prey and exhibit the converse pattern, with a relatively reduced optic tectum and relatively enlarged olfactory bulbs [Wagner, 2003]. These ontogenetic shifts are not restricted to size of brain regions, but are also reflected in optic nerve and olfactory tract axon numbers in some species [Lisney et al, 2018]. Additionally, many larval fish are planktivorous, while adults shift to a benthic feeding style [Wanzenböck and Schierner, 1989]; this shift in habitat and feeding mode is similarly marked by a relative decrease in optic tectum size [Fuiman, 1988;Kotrschal, 1989, 1990;Kotrschal et al, 1990;Montgomery and Sutherland, 1997].…”

“…Fishelson and Baranes [1997] similarly demonstrated that the number of lamellae in the Oman shark, Iago omanensis, increased into adulthood, while gradually developing secondary folds, likely indicating the importance of olfaction in detecting prey. Indeed, increased reliance on a sensory system, resulting in growth of peripheral sensory organs, may also correspond to marked changes in the associated brain regions in fishes [Lisney et al, 2018].…”

Massive Loss of Olfactory Receptors But Not Trace Amine-Associated Receptors in the World’s Deepest-Living Fish (Pseudoliparis swirei)

“…Increased acuity in chemosensory abilities such as olfaction and taste as compensation for loss of vision was reported in cave fishes [23,24], whereas acceleration of OR gene loss was shown to coincide with the acquisition of acute vision in haplorhines [11]. In addition, two species of deep-sea grenadier fishes living between 2000 and 6000 m depth were reported to have undergone an ontogenetic shift in sensory orientation, with olfaction being more important than vision in large individuals [25]. Therefore, it is of great interest to examine how environmental adaptations reshape the hierarchical structure of the olfactory receptor repertoires in deep-living fishes.…”