South Pacific Study Vol. 22, No. 2, 2002

Olfactory Organs of Two Pelagic Teleost Fish—Opah(Lampris guttatus) and Dolphin fish
(Coryphaena hippurus)
Ralph R. MANA, and Gunzo KAWAMURA

Abstract
Olfactory organs of two pelagic teleost species—opah (Lampris guttatus) and dolphin fish (Coryphaena
hippurus) were investigated with scanning electron microscope. Gross morphological observation showed that inboth fish the paired olfactory organ is situated on the snout. Anterior and posterior openings are present in bothfish. Numerous number of lamellae radiate around a short raphe. Olfactory ventilation sac is present in both fish
but is more developed in opah. Olfactory sensory epithelium is found intermingled as islets or patches within thenonsensory epithelium. Ciliated olfactory receptor neuron and microvillous olfactory receptor neuron are observedin both fish with the former being more abundant. The population of receptor neurons is estimated to be ~3.0 and~7.7 million in opah and dolphin fish respectively. Ciliated nonsensory cell is rare or absent in all lamellae
examined while goblet cells are observed in both sensory and nonsensory epithelia. Epidermal cells forming
microridge of finger-print like patterns are the primary cells forming the nonsensory epithelium.
Keywords: Coryphaena hippurus, Lampris guttatus, olfactory organ, pelagic fish

Introduction
Vision and chemoreception are probably the most important sensory systems used inoceanic fish in search of food in vast pelagic environment. Olfaction in particular has shownto induce prey-searching behaviors and feeding responses in little tuna (Euthynnus affinis)
and yellowfin tuna (Thunnus albacares) (VAN WEEL, 1952). ATEMA et al. (1980) demonstrated that the yellowfin tuna can form chemical (olfactory) search image in procurementof food as a convenient system that enables the fish to switch to a major food source while
ignoring less abundant food source. As a means to delay dilution of potent cues in open
ocean, prey odors and other chemical cues are being entrained in lipid components ofliposomes so as to provide persistent arousal and search cues for tunas (WILLIAMS et al.,1992) and other pelagic critters. Recently, similar chemosensory information carriers arefound in land animals (LAZAR et al., 2001).
Olfactory cues are detected by the olfactory organ and relevant behaviors are released
in any given organism. Literature showed that structures of olfactory organ of Genus
Thunnus were studied especially its relevance to Scombridae taxonomy (IWAI and
NAKAMURA, 1964). GOODING (1963) revealed that the skipjack (Katsuwonus pelamis) has
a well-developed olfactory organ and showed that the olfactory ventilation sac may function
Laboratory of Fish Ethology, Kagoshima University, 4-50-20 Shimoarata, Kagoshima 890-0056, Japan.

54South Pacific Study Vol. 22, No. 2, 2002

as a pumping device to draw in water into the olfactory chamber during swimming. Byscanning electron microscopy YAMAMOTO and UEDA (1979) first studied the olfactoryorgans of bluefin tuna (Thunnus thynnus) and other small pelagic fish. MANA et al. (1998)
also revealed that the olfactory organs of some large pelagic species possess two types ofolfactory receptor neurons—ciliated and microvillous olfactory receptor neurons on thelamellar surface, both of which are comparable to the receptor neurons found in red sea
bream (Pagrus major) (MANA, 2001). Further the olfactory system in bigeye tuna (Thunnus
obesus) and striped marlin (Tetrapturus audax) not only possess an olfactory ventilation sac
but the density of olfactory neurons ranged from 40 000–68 000/mm2 (MANA, 2000).
To reveal the diversity of olfactory systems in pelagic fish, the olfactory organs of
opah (Lampris guttatus) and dolphin fish (Coryphaena hippurus) were investigated withscanning electron microscopy. Results indicated that opah has a well-developed olfactory
ventilation sac with ~3.0 million olfactory receptor neurons in one rosette while dolphin fishhas ~7.7 million olfactory receptor neurons per rosette. Adaptive morphological features ofthe olfactory systems of pelagic fish are discussed in relation to pelagic mode of life.

Materials and methods
Source of Materials
Specimens used in this study were caught by tuna longline on board Kagoshima University
training vessel, Keiten Maru during ocean cruise at Northern Pacific and South of Okinawa
in 1996–1997. Table 1 showed the localities where fish were sampled, standard body lengthand number of lamellae per olfactory organ.
Ultrastructures
For scanning electron microscopic (SEM) observation, specimen was sacrificed by decapitation. Immediately each nasal sac was flooded with 2.5% glutaraldehyde in 0.1M
cacodylate buffer (pH 7.4) through anterior nasal opening for ~10 min as suggested by
MORAN et al. (1992). Then the rosettes were surgically removed and fixed in the same
fixative for 12 hr. The lamellae were post-fixed in 1% OsO4 for 2 hr. After dehydrated
through a gradient series of ethanol, the lamellae were dried in liquid CO2 critical-point
apparatus Hitachi HCP-2, coated with platinum-palladium in a Hitachi E-1030 ion sputter
and viewed with a Hitachi S-430 scanning electron microscope.
In density analysis of olfactory receptor neurons (ORNs) we estimated the number of
ORNs based on the SEM micrographs that included both nonsensory and sensory regions
to minimize the effect of the unique sensory pattern in both fish. Micrographs were taken
randomly on lamellar surface at a magnification of 2000 depicting an area of 750μm2. The
counts were then converted to density/mm2. Lamellar areas were determined by cutting andweighing of the well-preserved lamellae. A total of 16–24 micrographs from the lamellaeof 3–5 rosettes in each fish species were examined.

Olfactory Organs of Two Pelagic Teleost Fish—Opah (Lampris guttatus) and Dolphin fish (Coryphaena hippurus)

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Results
Gross Morphology of Olfactory Organ
The opah and dolphin fish possess a pair of olfactory organs situated on the dorsolateralside of the head just anterior to the eye (Fig. 1 A, B). The olfactory chambers are not

Fig. 1 Head region showing the position of olfactory nostrils and olfactory organ in(A) dolphin fish and (B) opah. (C) Olfactory chamber of opah exposing theolfactory rosette (or) and an opening leading to a ventilation sac (vs) as shownby the hatched lines. (ai) anterior opening, (po) posterior opening, (e) eye.

connected to the respiratory system in both species. When a pelagic fish swims in open
seas/oceans the water containing odorants enters into the olfactory chamber via an anterior
inlet and exits via a posterior outlet. In both species, the inlet and outlet are separated by anasal bridge of epidermal tissue which is ~1–2 mm wide in both species and the inlet issmaller (~1 mm diameter) than the outlet (~2 mm diameter). In the dolphin fish an

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South Pacific Study Vol. 22, No. 2, 2002

upstanding nasal flap around the inlet probably serves to catch the water into the nasal
cavity from the faster moving layers not immediately in contact with the body when the fish
is swimming. Ventilation sac is present in both species and well-developed in the opah (Fig.
1c) but it was not thoroughly investigated in the dolphin fish. The ventilation sac in the
opah connects to the olfactory chamber by an opening and is situated beneath the lachrymal
bone. There are no muscles attached to the ventilation sac. It was demonstrated that as themouth closed the ventilation sac is compressed and expanded when the mouth is opened.
Olfactory rosette, an outgrowth of the floor of the olfactory chamber comprised numerous
lamellae radiating from a short midline raphe (Fig. 2) and it (olfactory rosette) is seenFig. 2 Semischematic diagrams of olfactory rosettes of (A) opah and (B) dolphin fish.
(r) midline raphe, (l) lamellae. Scale bar = 3 mm.

directly through the anterior opening in both species. The olfactory lamellae contain theolfactory mucosa. The number of lamellae varies between fish in each species and between
the pair of organs in the same specimen. There are 14–16 and 61–64 lamellae in the opahand dolphin fish respectively (Table 1).
Table 1. Sampling area and localities, standard length and number of olfactory lamallae of two pelagicfishSpecies name(Common name)[Japanese name]Area of fishsampling

Localities of fishsampling

Standard Number of lamellae
length inin right
in leftcm
rosetterosetteLampris guttatus(Opah)[Aka mambou]

Northern PacificSouth of Okinawa

18°34' N 132°57' E
22-25°N 127-131°E

101.1
104.9

14

16

Coryphaena hippurus Northern Pacific(Dolphin fish)
South of Okinawa[Shiira]""27°43' N 130°59' E
22-25°N 127-131°E
"
"

104.8
101.5
106.6

61

64

Olfactory Organs of Two Pelagic Teleost Fish—Opah (Lampris guttatus) and Dolphin fish (Coryphaena hippurus)

57

Fine Structures of Olfactory Epithelium
In the opah and dolphin fish the lamellar faces were lined with sensory and nonsensory
epithelia. The sensory epithelium was found separated into patches or intermingled as islets
within the nonsensory epithelia in all lamellae examined (Fig. 3). Both species sensory

Fig. 3 Topographic distribution of sensory epithelium in (A) opah and (B) dolphin
fish. In both species sensory region (se) covers the lamellar face except for thelamellar margins which consist mainly of nonsensory epithelium (ns). Sensory
epithelia which are thrown into islets or patches are surrounded by nonsensory
epithelium in (C) opah and (D) dolphin fish. Scale bar = 0.6 mm for A and B,
30μm for C and D.

epithelia were composed of olfactory receptor neurons (ORNs), sustentacular and goblet
cells. Ciliated olfactory receptor neuron (cORN) and microvillous olfactory receptor neuron

58South Pacific Study Vol. 22, No. 2, 2002

(mORN) which send their axons directly to the sessile type of olfactory bulb were observedin both species. cORN and mORN were confirmed to possess axon-like processes in amarine species (MANA, 2001). The dendrites of cORN are consisted of a protruding knob
(1.0–1.3μm in diameter) which bears 3–8 cilia radiating around it. These apical dendritic
knobs tend to extend further to the surface of the adjacent epithelium in opah than the ones
observed in dolphin fish (Figs. 4–5). This suggests of species specificity since all ORNs

Fig. 4 Sensory epithelium of (A) opah and (B) dolphin fish which bear the ciliatedolfactory receptor receptor neuron (cr) and microvillous olfactory receptor
neuron (mr). (s), sustentacular cell, (e) epidermal cell. White arrows indicate
tapering cilia of cr in (A) which contrast to bloated apical processes of the same
type of neuron in (B). Scale bar = 3.0μm.

Olfactory Organs of Two Pelagic Teleost Fish—Opah (Lampris guttatus) and Dolphin fish (Coryphaena hippurus)

59

Fig. 5 Ciliated nonsensory cell (kn) in (A) opa and goblet cell (g) in (B) dolphin fish.
Note the apical knobs of ciliated receptor neuron are more extended to theneighboring epithelial surface in (A) than in (B). Scale bar = 3.0μm.

observed displayed the similar dendritic knob form. Those cilia were much longer in opah
(5.6μm) with bulbous apical processes than the tapering cilia in dolphin fish (5.0μm) (Fig.
4). The second type of ORN comprised 20–80 microvilli projected from an olfactory knob
which is usually buried in the sensory epithelium in both species. Opah possesses morenumber of microvilli per olfactory knob than dolphin fish. Microvilli of mORN are 1.4μm long and 0.1μm in diameter. There is no evidence so far to suggest motility in the cilia
and microvilli of the ORNs. Another cell type found in the sensory epithelium is thesustentacular cell. They have microvilli-like protrusions on their most apical surface (Figs.
4–5). Ciliated nonsensory cell is rare in both species (Fig. 5). Goblet cells were observedin both sensory and nonsensory epithelia (Fig. 5) of both species. Nonsensory epithelium
consists mainly of epidermal cell with a finger-print like pattern of microridges (Figs. 4–
5).
Density and Population of Olfactory Receptor Neurons
The mean density of ORNs in opah and dolphin fish are 55 000/mm2 and 32 000/mm2
respectively. cORNs are the most abundant in both species while mORNs are occasionallyobserved especially in dolphin fish. Calculation of lamellar area showed that the exact
sensory area in opah is 1.82±0.49 mm2 (mean±SD, n = 4) while the nonsensory area is
2.36±0.50 mm2 (n = 4). In dolphin fish the sensory and nonsensory areas are 1.92±0.37mm2 (mean±SD, n = 6) and 2.49±0.46 mm2 (n = 6) respectively. Therefore the number/lamellae in both species are much higher than density/mm2 (Fig. 6). ORNs found in patches
or islets in dolphin fish tend to be more scattered on lamellar surface than in opah as
indicated from high standard deviation in mean density/lamellar area (Fig. 6 ). Opah with15 lamellae would yield ~3.0 million ORNs in one olfactory rosette. Similarly dolphin fishwith 63 lamellae would yield ~7.7 million ORNs in one olfactory rosette.

60South Pacific Study Vol. 22, No. 2, 2002

Fig. 6 Density of olfactory receptor neurons (ORNs) in two pelagic fish. Bar represents means ± SD of microvillous (mORN) and ciliated (cORN) receptor
neurons on a lamellar surface.

Discussion
This report describes the macromorphology and microstructures of the olfactory organ oftwo pelagic species—opah and dolphin fish. Both fish possess an olfactory ventilation sac
into which the seawater containing odorants is drawn into the olfactory chamber via ananterior inlet when fish opens its jaws and subsequently, the incurrent olfactory water leaves
the olfactory chamber via the posterior outlet when the fish closes its mouth. The same
ventilation system is observed in skipjack (GOODING, 1964), bigeye tuna and striped marlin(MANA, 2000), indicating that even at lower cruising speed the olfactory organ is continuously sampling olfactory water in the fast-swimming pelagic teleosts. At higher swimming
speed it is most likely that water current through olfactory chamber is produced by theforward motion of the fish. Further almost all pelagic species studied so far tend to possessa round rosette or similar form with numerous lamellae radiating around a short midline
raphe (GOODING, 1964; IWAI and NAKAMURA, 1964; YAMAMOTO and UEDA, 1979; MANAet al., 1998; MANA, 2000) and the most rostral part of the rosette reach the anterior opening.
These intrinsic features of olfactory organs display not only an ideal arrangement for fishthat inhabit vast deserts of open oceans but also a central design in pelagic forms. Anothercommon feature in pelagic fish insofar, is the distribution pattern of the sensory epitheliumon lamellar surface—sensory epithelium is found intermingled as islets or patches within
the nonsensory epithelium which may be regarded as a manifestation in fast-swimming
pelagic species. Other types of lamellar topography in YAMAMOTO and UEDA’s (1979)classification would not be an ideal form for fast-swimming fish especially the scombroids(Families Scombridae, Istiophoridae and Xiphiidae) because the olfactory seawater entering
the anterior inlet is of high pressure and any shearing force acting upon the delicate
olfactory mucosa is perhaps reduced by the unique structural pattern of the sensory

Olfactory Organs of Two Pelagic Teleost Fish—Opah (Lampris guttatus) and Dolphin fish (Coryphaena hippurus)

61

epithelium on the lamellar surface to ensure strictly laminar flow 0.2<Re<2.0 (ATEMA,
1988) over and in between the olfactory lamellae; a smooth water flow over the olfactory
mucosa is prerequisite for the olfactory system to detect and encode biologically relevantcues while avoiding adaptation effect on receptors (HARA, and LAW, 1972). The nonsensory
epithelium is comprised mainly of epidermal cells which form a characteristic microridgeof finger-print like pattern and these cells are thought to play a role in supporting tissues
exposed to abrasive forces (UEHARA et al., 1991). Adaptational forces to pelagic way of life
have rendered the kinocilia of nonsensory ciliated cells redundant in pelagic forms. This cell
has a motility function (SLEIGH, 1989) and it is thought to draw in water into the olfactory
cavity and propel olfactory water/mucus over the lamellar surface in fish that possess
nonsensory ciliated cells in high density such as red sea bream (MANA and KAWAMURA,
2002). In planktonic life-form of pelagic fish larvae, kinocilia might be present to aid inlarval olfaction and these kinocilia are becoming redundant as the fish grows. This could
explain the rarity or absence of these cells in all pelagic fish studied so far.
In fish two olfactory receptor neurons are commonly present—cORN and mORN.
Both of these receptor neurons are found in opah and dolphin. However, cORN is more
dominant in both species (Fig. 6). Similarly, cORN is also dominant in bigeye tuna andstriped marlin (MANA, 2000) and in other scombroid fish—yellowfin tuna and albacore tuna(Thunnus alalunga) (MANA, unpublished). The reason as to why one receptor neuron typeis dominant over another is poorly understood in pelagic fish olfaction. However since mostscombroids and other pelagic species are highly migratory, abundant cORN might berelated to migratory behavior in fish, as postulated by PYATKINA (1976). In non pelagic
forms, recent biomolecular studies in goldfish have revealed that mORN express aminoacids receptors (CAO et al., 1998; SPECA et al., 1999). This evidence perhaps strengthened
THOMMESEN’s (1982) suggestion in salmonids that, cORN is more specific to bile salts
while amino acids are detected by mORN. On the contrary, ZIELINSKI and HARA (1988)
showed that only cORN was present in developing rainbow trout and responded to aminoacid stimulation. Further, the sea lamprey (Petromyzon marinus) possesses only cORN and
it’s amino acid receptors are not only restricted to arginine (LI and SORENSEN, 1992) but thefish can also detect bile acids at a threshold concentration of 10–13 M (LI and SORENSEN,
1993). In light of the current evidences on olfactory receptors specificity in fish it can besaid that the responsiveness of olfactory receptor neurons is species-specific. Although little
is known about the olfactory sensitivity in many pelagic fish, yellowfin tuna can detect freeamino acids at threshold 1 × 10–11 M (ATEMA et al., 1980). This threshold concentration issimilar to free amino acids present in open seas (GARRASI et al., 1979). Although the
population of olfactory receptor neurons in the opah (~3.0 million) and dolphin fish (~7.7
million) are much lesser than the adult red sea bream (~13.3 million) (MANA, 2001), it
would be grossly unrealistic to make any kind of comparison between a macrosomatic fish
and the pelagic fish at this stage. Moreover, THOMMESEN (1983) found that adult salmonids(arctic char Salmo alpinus) possess less density of receptor neurons (24 000/mm2 ) and afewer number (~12) of olfactory lamellae which yielded 0.5–1.0 million receptor neurons
per olfactory organ nonetheless, all current evidences point to olfaction as the major sensory

62South Pacific Study Vol. 22, No. 2, 2002

system that guides those long distance migratory salmonid fish to their natal waters tospawn. Thus, all we can say is the pelagic fish have evolved to inhabit the vast oceanic
environment. Evolution of olfactory system in pelagic forms not only has overcome
hydrodynamic constrains in time but this distance chemosensory system is perfectly
designed and tuned to the survival and success of those organisms.
In conclusion, macromorphology and micromorphology of olfactory organs of the
opah and dolphin fish were studied. The results indicated that both species have functional
olfactory systems best evolved for pelagic way of life. Further studies on other pelagic
species olfaction will make us understand the central design of the olfactory system andit’s function in pelagic fish behavior.

Acknowledgments
This research was supported in part by a Grant-in-Aid from the Ministry of Education ofJapan (No. 09760180). We thank the captain and crew members of Keiten Maru for theirsupport during the ocean cruises. The first author (R. R. M) wish to thank Mr. Satoru
Nonaka of Medical Faculty, Kagoshima University for technical assistance in electron
microscopy. R. R. M is also indebted to Ms. Ikuyo Tomisako for general support throughout
the preparation of this paper. We thank Dr. Sadoa Kiyohara for his critical review of themanuscript.

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