Ontogenesis and cytomorphology of the nasal olfactory organs in the Oman Shark,Iago omanensis (Triakidae), in the Gulf of Aqaba, Red Sea

Abstract

Background: Sharks (Selachi) are among the largest predators in deep and shallow seas, feeding on live and dead prey. Olfaction is one of the central senses by which they forage, especially at night and in deep water. The organs responsible for this function are the olfactory rosettes, which are situated in their nares. This study follows the ontogenesis and cytological development of the olfactory rosettes of the Oman shark, Iago omanensis, found in the Gulf of Aqaba, Red Sea, at depths of 150-1500 m.Methods: The sharks were collected bimonthly by means of a specially designed vertical standing net and sacrificed by an overdose of MS222. The olfactory rosettes were extracted from the adults and embryos, then fixed and prepared for EM and LM studies.Results: Iago is a placental, matrotrophic species with a maximal dimension of 800 mm TL (total length). It reproduces all year round, giving birth to a maximum of four (occasionally five) young of 170-180 mm TL. In newborn and adult fish the nasal olfactory organs are as described for other sharks, composed of olfactory lamellae with secondary folds. The number of lamellae increases during embryogenesis up to a maximum of 28-32 in adults. The primary nasal placodes first appear in larvae of 10-14 mm on the dorso-lateral part of the head and then become gradually displaced to the ventral position, typical for adults. Ontogenesis of the nasal rosettes is characterized by a gradual development of the lamellae and their secondary folds, with a concomitant ripening of the sensory elements (ciliated, microvillar, and rod-like bearing cells), as well as glandular and supporting cells and cells containing kinocilia that agitate the nasal water flow.Conclusions: The released young possess functional olfactory organs and developed neural transmission across the olfactory bulb and tract, to the olfactory lobes in the brain, enabling them to forage from birth. Presented data show the occurrence in I. omanensis of two types of ciliated and microvillar cells. Ciliated and rod-bearing sensory neurons are described for the first time in sharks. Anat.

Clarification of the Terminology of the Olfactory Lamellae in Chondrichthyes

“…The peripheral olfactory organ of Chondrichthyes, the olfactory rosette, is located in the olfactory chamber and it is characterized by a central support called the raphe, which bears folds, which bear smaller, secondary folds (Holl, ; Meng and Yin, ; Theisen et al, ; Zeiske et al, ; Savel'ev and Chernikov, ; Takami et al, ; Fishelson and Baranes, ; Kajiura et al, ; Schluessel et al, ; Theiss et al, ; Abel et al, ; Schluessel et al, ; Timm and Fish, ; Cox, ; Howard et al, ; Ferrando et al, ).…”

“…While the number of lamellae is associated with ontogeny in teleost fish, the number of lamellae is not affected by age or size in Chondrichthyes (Theiss et al, ). Although the number of folds in the olfactory organ of Chondrichthyes is not so regular to be considered as a taxonomic character, average values differ sufficiently among species, thus they have been recorded and sometimes compared (Asai, ; Holl, ; Meng and Yin, ; Takami et al, ; Fishelson and Baranes, ; Kajiura et al, ; Schluessel et al, ; Theiss et al, ; Meredith and Kajiura, ; Arif, ; Ferrando et al, ). A higher number of folds lead to a greater sensory surface area in a given volume but, as stated above, the sensory surface area appears not strictly linked to the olfactory capability (Meredith and Kajiura, ).…”

“…(e) Two facing folds and the slice of raphe between them is considered an olfactory lamella in some other papers regarding Elasmobranchii with elongated raphe. 1 Asai, ; 2 Holl, ; 3 Meng and Yin ; 4 Meng and Yin, ; 5 Theisen et al, ; 6 Zeiske et al, ; 7 Takami et al, ; 8 Fishelson and Baranes, ; 9 Kajiura et al, ; 10 Schluessel et al, ; 11 Theiss et al, ; 12 Abel et al, ; 13 Meredith and Kajiura, ; 14 Schluessel et al, ; 15 Arif, ; 16 Cox, ; 17 Howard et al, ; 18 Rygg et al, ; 19 Ferrando et al, ; 20 Ferrando et al, . CC = connective capsule; F = fold; R = raphe.…”

“…d) (Asai, ; Meng and Yin, ; Theisen et al, ; Zeiske et al, ; Abel et al, ; Arif, ; Rygg et al, ; Cox, ; Ferrando et al, ) or a two‐folds structure (Fig. e) (Takami et al, ; Fishelson and Baranes, ; Kajiura et al, ; Schluessel et al, ; Theiss et al, ; Meredith and Kajiura, ; Ferrando et al, ).…”

Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve

“…Moreover, as other cartilaginous fishes, it possesses a highly developed sense of smell that is easily accessible to different experimental approaches, and represents an important emerging model for olfactory development studies. The structure and ultrastructure of the adult olfactory bulb and olfactory epithelium have been described in sharks and rays (elasmobranchs), including S. canicula (olfactory epithelium/placode: Theisen et al 1986; Takami et al 1994; Ferrando et al 2006, 2007a, 2009, 2010; Schluessel et al 2008; olfactory bulb: Dryer and Graziadei 1993, 1996) but, although some genetic data in early embryos are available (Sauka-Spengler et al 2001; O’Neill et al 2007) studies on the development of the olfactory system are really scarce (Fishelson and Baranes 1997; Ferrando et al 2007b; Ferreiro-Galve et al 2012a). As far as we know, no axonal tracing studies of the olfactory system have been performed in developing cartilaginous fishes so far.…”