L. reissneri shows the unpaired olfactory organ unlike the jawed vertebrates, Osteichthyes and Chondrichthyes, having paired structures at both sides of the snout (Kasumyan, 2004). The position of the jawed vertebrate’s olfactory organ was general at the ventral part of the snout in Chondrichthyes and at the dorsal part of the snout in Osteichthyes (Zeiske et al., 1992). Interestingly, however, that of L. reissneri is located at the top of the head. Of the same cyclostomata, lamprey has the same position to that of L. reissneri (Kleerekoper and Erkel, 1960) but hagfishes are above the oral cavity (Theisen, 1973; 1976). Such top positions of the olfactory organ in L. reissneri as well as in other lampreys may reflect their phylogeny as representative of the lower taxa, not higher taxa such as teleost.
The olfactory organ of L. reissneri is characterized by a tube form of single nostril, a single gourd-like chamber, a nasal valve, a nasopharyngeal pouch, a longitudinal arrangement of lamellae, a continuous distribution of the SE, the ciliated SCs, and the AOO, as the same structure in the sea lamprey Petromyzon marinus (Kleerekoper and Erkel, 1960). Among those characters, a tube form of the nostril of L. reissneri are responsible for its habitat, where has a somewhat slow-water currents, being occupied by water plants, gravels and pebbles (Kim and Park, 2002; Fig. 1B). The tube form also may be suitable for its ecology that the fish burrows its body into the sand at daytime during the lifetime from the ammocoetes to the adult stage (Kim and Park, 2002). Kim et al. (2019) noted that with a contraction and a relaxation of the accessory nasal sac, the tubular nostril helps generate a force to suck water into the olfactory canal. In addition, Cox (2008) opined that the tubular structure assists to reduce thicker “boundary layer” occurring on the snout surface of inactive fishes. The “boundary layer”, generated by a friction when fish swims forward, disturbs to sense external chemical odors and generally is thicker in an inactive fish than fast-swimming fish (Cox, 2008). So, tube form on the head of L. reissneri seems to be a morphological adaptation and a positional strategy for the reduction of “boundary layer” and effective olfaction under sandy ground.
Meanwhile, L. reissneri has 19–20 lamellae in number and are different from the sea lamprey P. marinus with 25 (Kleerekoper and Erkel, 1960) and other hagfishes, Myxine glutinosa, Eptatretus stoutii and E. deani, with 7 lamellae (Theisen, 1976). Generally, in teleost fish, the lamellar number of the olfactory organ is species-specific: absence (Conidens laticephalus of the Order Gobiesociformes, Oryzias latipes and O. sinensis of the Beloniformes, and Periophthalmus modestus, P. magnuspinnatus of the Perciformes), only one (Hemiramphus sajori, Cheilopogon agoo, and Cololabis saira of the order Atheriniformes), up to 120 (Conger myriaster of Anguilliformes) and 230 lamellae (Holopagus guentheri of Perciformes) (Yamamoto, 1982; Kasumyan, 2004; Kim et al., 2019). It was known that the increase of lamellae leads to the increase of distributional area of olfactory receptor neurons (Kasumyan, 2004). Teichmann (1954) also documented that microsmatic catfishes with greater lamellar number show more active response to any chemical stimulant than one with lesser lamellae. At least, the greater number in lamellae of L. reissneri may be more likely to have higher olfactory dependence than other cyclostomata hagfishes with less.
In fish’s olfactory epithelium, it is common that the SE is a simple pseudostratified layer with numerous neurons and the NSE is a stratified squamous layer consisting of stratified epithelial cells (Hara, 1986). Interestingly, the SE and NSE of L. reissneri consist of a simple pseudostratified layer, first findings, not reporting in other cyclostomatas and P. marinus. Almost jawed fishes has shown the NSE formed from a stratified squamous layer which has various-shaped cells from columnar or cuboidal types in deeper layer to squamous or flattened types at the surface (Hara, 1986; Ghosh and Chakrabarti, 2009; Kim et al., 2018; 2019). In contrast, as the NSE of L. reissneri is a histological organization unlike those of the above higher taxa, it may be considered a specific histological character of lamprey belonging to the cyclostomata.
In jawed fishes, the length of olfactory sensory cilia varies by species: 2–3㎛ in Daniro rerio (Hansen and Eckart, 1998), the maximum 10㎛ in Acipenser baeri (Hansen and Zielinski, 2005), 10–30㎛ similarly in Lota lota L. (Gemne and Doving 1969) and Calamoichthys calabaricus (Schulte and Holl, 1971). Further, lampreys show a different length in related congeneric species: 0.2–0.5 ㎛ in L. reissneri (this study) vs. 5–6 ㎛ in L. fluviatilis (Thornhill, 1967). Menco (1980) reported that in a comparative study of frog, ox, rat, and dog using a freeze-fracturing the effectiveness of ciliary mechanism to sense external odors is related to the increase of cilia area by number, length, and any attaching component. Twisted ciliary aggregations become packed mat within mucus and then may help make mucus film covering the olfactory surface (Farbman, 1992).
Consequently, the anatomy and histology of the olfactory organ of L. reissneri may well reflect its microhabitat where water flows slowly and bottom structure consists of sand, gravels and pebbles, and its ecological habit that fish burrows its body into sandy ground. Among the characters, both 19–20 lamellae and the ORN’s short ciliary length are at least regarded as a useful taxonomic character for lamprey.