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The Olfactory System in Fish: Structure, Function, and Role in Behavior

December 2004
Journal of Ichthyology 44(Supplement 2):S180–S223

Authors:

Lomonosov Moscow State University

The paper reviews recent studies of the olfactory system in fishes. The anatomy and morphology of the olfactory organ in fish with different systematics and modes of life are considered, as well as the cellular composition of the olfactory epithelium, the structure of the olfactory bulb and the olfactory tract. The basic functional parameters of the olfactory system are presented: spectra, sensitivity, the speed of adaptation, the nature and the sources of olfactory signals, their modern classification, basic methodologies for the study of the olfactory function, and characteristics of ventilation of the olfactory cavity. Information about the mechanisms of olfactory orientation in fish and their ability to determine the individual, group, population, and species identity of individuals is systematized. The role of the olfactory reception in reproductive, parental, feeding, defensive, territorial, schooling, and migration behavior is considered. The time course of the development of the olfactory organ in ontogeny is traced, and the terms of the appearance and development of responses to different natural chemical stimuli are determined. The susceptibility of the olfactory organs to negative effects of chemical pollutants is shown. Data are presented on the dynamics of regeneration processes, especially regarding recovery of the olfactory system after acute effects of chemical pollutants.

. Number of lamellae in the olfactory organ of fish of different systematic groups (from Yamamoto, 1982)

…

. The number of lamellae in the olfactory rosette of left and right olfactory organs of Claris batrachus (from Goel, 1980)

…

. The number of receptor cells in the olfactory organ of some species of cyclostomata, fish, and other vertebrates

…

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Content may be subject to copyright.

S180

Journal of Ichthyology, Vol. 44, Suppl. 2, 2004, pp. S180–S223.

Chemoreception, the ability to perceive chemical

stimuli, is the oldest evolved way to obtain information

about the environment. It is thought to have appeared

more than 500 million years ago (Hara, 1992a). Not

only ﬁsh and other vertebrates, but such primitive

organisms as bacteria and protozoans have well-devel-

oped chemoreception. Chemocommunication is the

exchange of information between animals via chemical

signals. It is hypothesized (Sepp, 1959) that analysis of

the information incoming via chemoreceptors brought

about the evolution of the primary nervous centers and,

later, the central nervous system.

Three independent chemosensory systems are usu-

ally distinguished in ﬁshes: olfaction, taste, and the

general chemical sense (Parker, 1912). All these sen-

sory systems have one thing in common: they perceive

chemical stimuli. Fish, like most other animals, per-

ceive the most diverse information stream with olfac-

tion. The perception of olfactory signals allows ﬁsh to

distinguish conspeciﬁc individuals, determine their

species and population identity, and brings about differ-

ent behavioral patterns: reproductive, schooling, defen-

sive, migration, parental, agonistic, territorial, etc.

(Malyukina

et al.

, 1969; Kleerkoper, 1969; Liley, 1982;

Døwing, 1986).

Special studies of the olfactory system in ﬁsh have

continued for more than one hundred years. The ﬁrst

works on the morphology of the olfactory organ in ﬁsh

were conducted in the 19th century, also in Russia, on

sturgeon. The olfactory receptor cells were described,

and the ability of the ﬁsh to respond to olfactory stimuli

and determine their source was shown (Dogel, 1886;

Kleerkoper, 1969). Studies of the olfactory system in

ﬁsh became most active during the last 30–40 years,

when different electrophysiological methods, behav-

ioral recording methods, underwater observation, and

electronic microscopy became widely used.

Comprehensive studies of the olfactory system in

ﬁsh began in Russia in the mid-1940’s with the works

of A.P. Andriyashev (1944, 1945), followed by

D.S. Pavlov (1959, 1962), and M.P. Aronov (1961,

1962). Morphological studies of the olfactory organ in

ﬁsh were conducted from the middle of the 1950s

(Bakhtin and Filyushina, 1974; Pyatkina, 1975, 1976;

Bakhtin, 1977; Bronshtein, 1977). Diverse studies of

the olfactory system in ﬁsh were conducted in Moscow

State University from 1967, when a special laboratory

was founded in the Department of Ichthyology

(G.A. Malyukina, G.V. Devitsyna, E.A. Marusov,

A.O. Kasumyan, N.E. Lebedeva, L.S. Chervova,

T.V. Golovkina, N.I. Pashchenko, S.S. Sidorov). Stud-

ies of chemical signalization in ﬁsh were conducted at

the Severtsov Institute of Ecology and Evolution, Rus-

sian Academy of Sciences (Vinogradova and Manteifel,

1982, 1984). The results of this large and comprehen-

sive work have been summarized in numerous publica-

tions, including many surveys and analytic reviews (Fle-

rov, 1962; Shmalgauzen, 1962a; Malyukina

et al.

, 1969,

1980; Shparkovskii, 1980; Manteifel, 1987; Pavlov and

Kasumyan, 1994).

This paper reviews the basic results of recent studies

of the olfactory system in ﬁsh, considering characteris-

tics and the diversity of its structural organization, func-

The Olfactory System in Fish: Structure, Function,

and Role in Behavior

A. O. Kasumyan

Moscow State University, Vorob’evy gory, Moscow, 119899 Russia

Received March 19, 2004

Abstract

—The paper reviews recent studies of the olfactory system in ﬁshes. The anatomy and morphology of

the olfactory organ in ﬁsh with different systematics and modes of life are considered, as well as the cellular

composition of the olfactory epithelium, the structure of the olfactory bulb and the olfactory tract. The basic

functional parameters of the olfactory system are presented: spectra, sensitivity, the speed of adaptation, the

nature and the sources of olfactory signals, their modern classiﬁcation, basic methodologies for the study of the

olfactory function, and characteristics of ventilation of the olfactory cavity. Information about the mechanisms

of olfactory orientation in ﬁsh and their ability to determine the individual, group, population, and species iden-

tity of individuals is systematized. The role of the olfactory reception in reproductive, parental, feeding, defen-

sive, territorial, schooling, and migration behavior is considered. The time course of the development of the

olfactory organ in ontogeny is traced, and the terms of the appearance and development of responses to different

natural chemical stimuli are determined. The susceptibility of the olfactory organs to negative effects of chem-

ical pollutants is shown. Data are presented on the dynamics of regeneration processes, especially regarding

recovery of the olfactory system after acute effects of chemical pollutants.

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S181

tional parameters and the role in different behavioral

patterns, as well as its formation during ontogeny.

The Structure of the Olfactory Organ

The olfactory organ is a peripheral part of the olfac-

tory system. It is a paired structure. The olfactory organ

in most ﬁsh species is well developed and is located on

the dorsal surface of the head to the rostrum and medial

1 mm

(a)

(b)

Fig. 1.

Head of minnow

Phoxinus phoxinus.

(a) lateral

view; (b) view from above (from Pashchenko and

Kasumyan, 1983).

nostrilbridgenostril

Anterior Nasal Posterior

Olfactory

cavity

Raphe

Accessory

olfactory sac

Fig. 2.

Basic structural elements of the olfactory organ in

ﬁsh (sagittal section) (from Zeiske

et al.

, 1992).

2 mm

Nasopharyngeal duct

Olfactory lamellae

a-a

Nasal duct Nasal valve

a-a

nostril

Fig. 3.

Head of hagﬁsh

Myxine glutinosa

, sagittal sec-

tion.

a-a

—olfactory organ, frontal section (from Zeiske

et al.

, 1992).

in en

(‡)

(b)

Olfactory organ

in en

Fig. 4.

Protopterus annectens

: (a) head (sagittal section),

(b) olfactory organ. “in” anterior olfactory opening, “en”

posterior olfactory opening (from Zeiske

et al.

, 1992).

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KASUMYAN

of the eyes (Fig. 1). Water gets into the olfactory organ,

the nasal or olfactory cavity via the anterior opening or

the anterior nostril, and gets out via the posterior olfac-

tory opening or posterior nostril. These openings are

divided by a skin nasal bridge or nasal bridge. The nasal

bridge of many ﬁshes has a skinny nasal ridge directing

water into the anterior nostril. Olfactory lamellae form-

ing the olfactory rosette are located at the bottom of the

nasal cavity. The surface of the lamella is covered by

the olfactory epithelium. Certain ﬁsh have accessory or

ventilation olfactory cavities (Fig. 2).

This general scheme of the olfactory organ has

many different types and modiﬁcations (Zeiske

et al.

1992). The structure of the olfactory organ may signif-

icantly differ in representatives of different taxonomic

groups of ﬁsh and cyclostomata (hagﬁsh and lamprey)

depending on their mode of life and behavior.

The enormous diversity of the olfactory organ, and

its size, position and structure in ﬁsh may be demon-

strated by many examples. For instance, in cyclosto-

mata,

Petromyzontes

lampreys and Myxini, unlike ﬁsh,

the olfactory organ represents an unpaired structure

(Fig. 3). Based on this morphological trait, lampreys

and myxini have earlier been included (by Haeckel)

into the group Monorhini, and all other vertebrates with

paired olfactory organ were collapsed into the group

Dirhini. But monorhiny in cyclostomata has a second-

ary origin because the olfactory nerve in lampreys and

myxini is paired and the olfactory organ is really split

into two parts by a partition (Tretyakov, 1915).

The olfactory cavities in most ﬁsh are not linked

with the oral cavity. However, this link was found in

myxini and some ﬁsh, e.g., chimaera

Chimaera mon-

strata

, dipnoans (Dipnoi), and certain teleosts such as

the

Astroscopus

stargazers,

Gymnodraco acuticeps

and in ﬁsh of the family Echelidae and Ochichthyidae

(Anguilliformes), so that water can pass into the oral

cavity from the nasal cavity during breathing (Fig. 4)

(Dahlgren, 1908; Mees, 1962; Holl, 1973; Jakubowski,

1975; Derivot, 1984). Myxini and stargazers have a

special valve in the nasopharingeal canal, directing the

water ﬂow from the nasal cavity to the oral cavity

(Fig. 3) (Døwing and Holmbers, 1974). The nasophar-

ingeal canal is blind in lampreys. It does not open into

the oral cavity, but ends at the ﬁrst gill openings

(Tretyakov, 1915, Kleerkoper and van Erkel, 1960;

Bermar, 1969; Theisen, 1976).

In such ancient ﬁsh as dipnoans and cartilaginous

Chondrichthys, the olfactory organs are located at the

ventral surface of the head (Fig. 5), whereas in repre-

sentatives of all other taxonomic groups, olfactory

organs are located at the dorsal surface of the head

(Shmalgauzen, 1962a; Kleerekoper, 1969; Bronshtein,

1977; Yamamoto, 1982).

The structural diversity of the olfactory organ is pro-

nounced in many other morphological characteristics,

such as the position of the inﬂow and outﬂow openings

leading to the olfactory organ, their size, the presence

of the nasal bridge dividing these openings, and the size

of the ridge. For example, in carps Cyprinidae, perches

Percidae, cods Gadidae, salmons Salmonidae, and

2 mm

Fig. 5.

Head of the lemon shark

Negaprion brevirostrus

, view from below. The box surrounds the inlet opening and the large skin

outgrowth nasal ﬂap partially closes it (from Zeiske

et al.

, 1096, 1987).

(a)

(b)

Fig. 6.

Head of juvenile stellate sturgeon

Acipenser stella-

tus

: (a) normal olfactory organ; (b) abnormal olfactory

organ (without the nasal bridge) (from Kasumyan, 2002).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S183

many other ﬁsh species, nostrils are well pronounced

and located close to each other and the nasal bridge

bears a large ridge, forming a kind of funnel which

directs water into the nasal cavity (Fig. 1) (Pashchenko

and Kasumyan, 1983; Døving, 1986; Zeitske

et al.

1992). Sturgeons Acipenseridae (Fig. 6) have a nasal

bridge, but the ridge is very small or absent (Kasumyan,

2002). When these ﬁsh are raised in artiﬁcial condi-

tions, this ridge may be partly or completely destroyed

by pathogenic bacteria. The proportion of artiﬁcially

raised sturgeon juveniles without the nasal ridge may

reach several dozen percent. It is accepted that such

abnormalities are associated with poor water quality

and the presence of pollutants (Shmalgauzen, 1957,

1962b; Podushka, 1999; Goryunova

et al.

, 2000).

The nasal bridge is not formed in sharks (Fig. 5), but

the lateral and medial edges of the olfactory opening of

these ﬁsh have well developed skin outgrowths (lamel-

lae) directed toward each other. They do not coalesce

but overlap each other. The sizes of these outgrowth are

so large that in many species of sharks and rays

(

Scyliorhinus canicula

Raja clavata

Trygon pastinaca

etc.) they cover a special nasal-oral groove, going from

the nasal to oral cavity and providing a link between

them. These outgrowths are motile in certain sharks

(Shmalgauzen, 1962a; Zeiske

et al.

, 1986, 1987).

in en

Moray eel,

Rhinomuraena ambonensis

Japanese lycodont,

Lycodontis javanicus

fifteen-spined stickleback,

Spinachia spinachia

tetradon,

Tetraodon nigropunctatus

Siphonostoma typhle

bedotia,

Bedotia geayi

Fig. 7.

Positioning and relative size of the olfactory organ in ﬁsh (from Zeiske

et al.

, 1992).

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KASUMYAN

The olfactory organ is not conspicuous in all spe-

cies. In certain species, the openings leading to the

olfactory organ are so small that they are quite difﬁcult

to discern on the head of the ﬁsh, as in

Bedotia geayi.

Syphonostoma typhle

they are not only small but also

closely adjoin each other (Fig. 7) (Melinkat and Zeiske,

1979). The ﬁfteen-spined stickleback

Spinachia spina-

chia

has only one olfactory opening, as in the garﬁsh

Belone belone

, but, unlike the stickleback, it is wide

(Fig. 8) (Theisen

et al.

, 1980; Theisen, 1982). An uni-

tary olfactory opening not separated into anterior and

posterior nostrils can be found in other sticklebacks

Gasterosteidae, garﬁshes Belonidae, Hemirhamphidae,

Pomacentridae,

Zoarces viviparus

Liparis montaqui

pike

Esox lucius

, etc. (Pipping, 1926; Liermann, 1933;

Holl and Meinel, 1968; Theisen

et al.

, 1980). Only the

posterior opening, in the form of a narrow rudimentary

slit, is retained in greenlings

Hexagrammos.

An olfac-

tory organ with only one opening is called monoter-

mous, while the more typical ditermous has two olfac-

tory openings (Døving, 1986).

In some ﬁsh, mostly bottom-dwelling and inactive,

burrowing in the bottom substrate or hiding among

stones and weeds, nostrils have the form of short or

long pipes. Such nostrils are characteristic of many

moray eels, such as

Lycodontis javanicus

and

Rhino-

muraena ambonensis

(Fig. 7), and several species of

eels Anguillidae, catﬁshes

Siluridae

, snakehead

Channa

, Polypteridae,

Gaidropsarus

, etc. (Holl

et al.

1970). In some cases, these pipes are separated from

each other and have special valves, inﬂow in the ante-

rior pipe and outﬂow in the posterior pipe. In dipnoans,

posterior nostrils open into the oral cavity, but the ﬁsh

catch the air with the oral cavity rather than the olfac-

tory organ (Shmalgauzen, 1962a).

In Tetraodontidae,

Tetraodon nigropunctatus

, nos-

trils are completely absent and the olfactory organ is

located within tentacle-like outgrowths above the head

surface. The inner cavity of these outgrowths is covered

with olfactory epithelium (Fig. 7) (Wiedersheim, 1887,

cit in Zeiske

et al.

, 1992; Shmalgauzen, 1962a).

Fish differ by the presence or absence of accessory

olfactory sacs. These relatively large structures are

characteristic of relatively inactive bottom species or

species living in still water, dipnoans, Polypteridae,

ﬂatﬁshes Pleuronectidae, eels Anguilliformes, perches

Perciformes and several other ﬁsh (Eaton, 1956; Holl

et al.

, 1970; Kapoor and Ojha, 1973; Jakubowski,

1975). But there are many exceptions from this general

rule. For example, accessory sacs are present in Clu-

peidae, Salmonidae, Mugilidae, Scombridae and sev-

eral other pelagic ﬁsh with high swimming activity

(Burne, 1909; Shmalgauzen, 1962a; Betmar, 1972).

Accessory sacs are primarily used for the ventilation

of the nasal cavity, therefore they are often called olfac-

tory ventilation sacs (Zeiske

et al.

, 1992). Another

function of olfactory sacs is the production of olfactory

mucus by numerous mucous cells in the epithelium of

the accessory sacs. Receptor cells are absent in this epi-

thelium (Shmalgauzen, 1962a; Kapoor and Ojha, 1972,

1973; Bronshtein, 1977). The olfactory organ may be

linked with the oral cavity when the wall at the distal

area of the ventral accessory sac is perforated, as is

observed in the American stargazer

Astroscopus gutta-

tus

or in

Gymnodraco acuticeps

(Atz, 1952a, 1952b;

Jakubowski, 1975).

The number of accessory sacs varies from one to

four. They may deviate from different parts of the basic

olfactory cavity, and are named depending on the scull

bones which they closely adjoin: lacrymal, ethmoidal,

suborbital, supraorbital, etc. For example, in ﬂatﬁshes,

clupeids, and salmons, accessory sacs open to the nasal

cavity from the posterior part, in certain perches, in the

rostral part. Accessory sacs are usually smaller than the

basic nasal sacs, but in smelts

Osmerus

, the sole acces-

sory sac is several times larger than the basic.

There is a pronounced variability in the number of

olfactory lamellae (Table 1). In cyprinids, sturgeons,

salmonids, percids, and several other groups of ﬁshes,

the number of lamellae in the olfactory organ is several

dozen, in some species, such as

Holopagus guentheri

from the family Lutjanidae, their number reaches 230

(Pfeiffer, 1964). However, ﬁsh exist in which olfactory

lamellae are few or are completely absent. For example,

from one to three lamellae are found in the olfactory

organ of the rainbow ﬁsh Melanotaeniidae,

Hemiram-

phus sajori

, in the ﬁfteen-spined stickleback

Spinachia

spinachia

, and the Washington sand lance

Ammodytes

personatus.

The mosquito ﬁsh

Gambusia agifﬁ

, guppy

Poecilia reticulata

, sand lance

Ammodytes lancea

Syphonostoma typhle

have no olfactory lamellae (Lier-

mann, 1933; Holl, 1965). Garﬁsh

Belone belone

also

has no olfactory lamellae. The olfactory organ of these

rapidly swimming ﬁsh represents a depression with a

large club-shaped outgrowth on the bottom. Its rostral

surface, directed to the water current, has shallow

0.5 mm

Fig. 8.

Olfactory organ of garﬁsh

Belone belone.

Arrow

points the rostro-caudal direction (from Theisen

et al.

1980).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S185

lamellae and ridges which only approximately resemble

true olfactory lamellae (Fig. 8) (Theisen

et al.

, 1980).

The olfactory organs of ﬂatﬁshes and most other

representatives of Pleuronectiformes located at the

eyed and blind sides of the body signiﬁcantly differ in

size and number of lamellae in the olfactory rosette. In

Pleuronectes platessa

Solea solea

, and many other

representatives of this genus, the number of lamellae in

the olfactory organ at the eyed side is 1.5–2.0 times

greater than at the blind side (Table 1) (Harvey, 1996).

In ﬁsh with symmetrical body shape, rosettes in the left

and right organs have the same number of lamellae

(Table 2).

The basic function of olfactory lamellae is increase

the area of the olfactory epithelium bearing the receptor

cells which perceive chemical stimuli. It was counted

that the overall area of the olfactory rosette in

Calam-

oichhys sp.

, with a length of 41 cm, is 3200 mm

(Pfe-

iffer, 1968). The same function is realized by secondary

lamellae on the surface of basic olfactory lamellae. The

secondary lamellae are well pronounced in salmonids,

garpikes, sturgeons, burbot

Lota lota

, pike

Esox lucius

(Pfeiffer, 1963; Holl, 1965; Devitsyna, 1972; Zeiske

et al.

, 1987; Devitsyna and Kazhlayev, 1992, 1993;

Hara

et al.

, 1993; Chen and Arratia, 1994). Secondary

lamellae may be oriented parallel or perpendicular to

the base of the primary lamella, and in some cases,

along the diagonal (Chen and Arratia, 1994). In sharks,

there are also tertiary lamellae (Fig. 9) (Zeiske

et al.

1987). The lateral surface of olfactory lamellae in the

striped eel catﬁsh Plotosus lineatus represents a system

of areas isolated from each other by ascending ridges

(Fig. 10) (Theisen et al., 1991).

Olfactory lamellae form the olfactory rosette (Fig.

11). There exist several types of olfactory rosettes dif-

fering by the position of lamellae: radial (Acipens-

eridae, Esocidae), arrow-like (Cyprinidae, Salmo-

nidae), parallel (Pleuronectidae, Lepisosteus, Lophii-

formes), and bilateral (Anguilliformes, Siluriformes,

Dipnoi, Amia, Chondrychthyes). There exist numerous

transitory forms between these basic types (Fig 12).

Closely related species of ﬁsh, for example, belonging to

the same family, usually have olfactory rosettes of the

same or similar type (Kleerekoper, 1969; Yamamoto,

1982; Zeiske et al., 1992; Chen and Arratia, 1994).

In spite of signiﬁcant morphological variability, sex

dimorphism in the structure of the olfactory organ is

Table 1. Number of lamellae in the olfactory organ of ﬁsh of

different systematic groups (from Yamamoto, 1982)

Orders and species Number of lamellae

Anguilliformes:

Anguilla japonica 108

Conger myriaster 120

Microdonophis erado 112

Gymnothorax kikado 102

Pleuronectiformes:

Paralichthys olivaccus 22/19

Pleuronichthys cornutus 15/9

Zebrias zebra 40/30

Areliscus joyneri 64/34

Clupeiformes:

Clupandon punctatus 26

Sardinops melanosticta 24

Engraulis japonica 28

Scorpaeniformes:

Sebastes inermis 16

Minous monodactylis 23

Hypodytes rubripinnis 7

Hexagrammus otakii 21

Platycephalus indicus 20

Vellitor centopomus 12

Tetraodotiformes:

Triacanthus brevirostris 22

Fugu niphobles 6

Navodon modestus 1

Rudarius arcodes 0

Ostracion tuberculatus 0

Atheriniformes:

Atherion elymus 3

Iso hawaiiensis 3

Hemiramphus sajori 1

Cheilopogon agoo 1

Cololabis saira 1

Orysias latipes 0

Gambusia afﬁnis 0

Note: For ﬂatﬁshes, the number of lamellae in the olfactory organs

on the eyed and blind sides of the body is presented.

Table 2. The number of lamellae in the olfactory rosette of left

and right olfactory organs of Claris batrachus (from Goel, 1980)

Body length, cm Number of lamellae

left organ right organ

9.5 26 27

12.0 33 33

12.6 34 34

13.8 43 43

14.3 45 45

15.0 50 50

16.1 51 52

16.5 55 55

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KASUMYAN

rather uncommon in ﬁsh. The exception from this rule

is only such extremely specialized species of ﬁsh as

deep-sea anglers Lophiiformes and a few other bathy-

pelagic and mesopelagic ﬁshes: luminous anchovy

Myctophiformes, Saccopharyngidae, Monognathidae,

Gonostomatidae (Marshall et al., 1967, 1979; Caruso,

1975; Bertelsen, 1980; Nielsen and Bertelsen, 1985; Ber-

telsen and Nielsen, 1987; Baird et al., 1990). The olfactory

organ and other parts of the olfactory system in males of

many of these ﬁsh are much more developed than in

females (Fig. 13). This is associated with the extremely

important role of olfaction in the search by males for ripe

females of these species during the reproductive period.

Olfactory Epithelium

The olfactory epithelium covers the olfactory lamel-

lae. Its width in different ﬁsh ranges from 20 to 130 µm

(Bronshtein, 1977). Cells of different types are

included into the epithelium, mostly receptor, support,

mucous, and basal (Fig. 14).

Receptor cells. Olfactory receptor cells are the pri-

mary sensitive cells, that is, they represent nervous cells

(sensory neurons). Receptor cells have a thick dendrite,

which goes out from the central (nuclear) part of the

neuron and reaches the surface of the epithelium. The

apical part of the dendrite terminates at a rounded tip

(knob) which projects over the surface of the epithe-

lium. In ﬁsh, receptor cells in the olfactory epithelium

are represented by two different types: ciliated and

0.5mm

1 mm

(a)

(b)

Fig. 9. Secondary lamellae: the olfactory rosette of the Arctic

char Salvelinus alpinus (a) and the olfactory lamella of the lemon

shark Negaprion brevirostrus (b) (from Zeiske et al., 1987).

0.1 mm

0.02 mm

(a)

(b)

Fig. 10. Lateral surface of the olfactory lamella in the

striped eel catﬁsh Plotosus lineatus at different magniﬁca-

tion (from Theisen et al., 1991).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S187

microvillous receptor cells (Bernshtein, 1977; Yama-

moto, 1982; Zeiske et al., 1992). Recently, a third type

of cells has been found in the olfactory epithelium of

different ﬁsh species: crypt cells. They are relatively

rare and their knob does not reach the surface of the epi-

thelium but opens in a small cavity located directly

under the external surface of it (Hansen and Zeiske,

1998; Hansen and Finger, 2000; Zeiske et al., 2003).

The knob of receptor ciliated cells bears weakly

motile cilia. Their number ranges from 4 to 20 and the

length reaches 5–10 µm, and diameter, 0.25–0.30 µm.

The number of microvilli in microvillous receptor cells

is signiﬁcantly larger, from 30 to 80. Their length

ranges from 0.5 to 3–5 µm, diameter about 0.1 µm

(Bannister, 1965; Gemne and Døving, 1969; Schulte,

1972; Bronshtein, 1977; Sorensen and Caprio, 1998).

Numerous ciliated–microvillous receptor cells can be

found in the olfactory epithelium of certain ﬁshes (e.g.

in sturgeons), the knobs of these cells bear both cilia

and microvilli (Pyatkina, 1975, 1976). Cilia of receptor

cells move slowly and asynchronously and are usually

stretched along the surface of the epithelium. A long

central process, the axon, goes out from the opposite

side of the receptor cell (Fig. 14).

Special protein receptor molecules are contained in

the cellular membrane of cilia and microvilli. When the

receptor protein contacts the olfactory substance, a

complicated cascade of molecular transformations

occurs in the cell, which is called the signal transduc-

tion process. This process changes the functioning of

the ion channels in the cell, generation of receptor

potential, and its distribution as an electric nervous

impulse from the generation location to the primary and

secondary olfactory centers (Brand and Bruch, 1992).

The central (nuclear) part of the receptor cell is

located in the olfactory epithelium at different levels.

Five such layers are usually distinguished in the epithe-

lium. The lower the layer with the nucleus of the recep-

tor cell, the longer its dendrite, which reaches the outer

surface of the epithelium. It was found that the nuclear

part of ciliated receptor cells is usually located in

deeper layers of the olfactory epithelium than in

microvillous. Therefore, its dendrites are longer. The

shortest dendrites are characteristic of crypt receptor

cells, which are located in the upper layer of the epithe-

lium (Hansen and Finger, 2000; Hamdani et al., 2001a;

Hamdani and Døving, 2002).

Receptor cells occur in the olfactory epithelium in

areas covering the side surface of olfactory lamellae.

They are absent on ridges of lamellae, and on vaults of

the olfactory cavity. Areas of the olfactory epithelium

bearing receptor cells are named receptor zones or

receptor (sensory) epithelium. These zones alternate

Fig. 11. Olfactory rosette of the goldﬁsh Carassius auratus.

Gambusia affinis, Poecilia reticulata

Ammodytes personatus

Acanthogobius, Odontamblyopsys, Navodon

Gasterosteus aculeatus

Acipenseridae, Esox

Salmonidae, Clupeidae

Cyprinidae

Anguilliformes, Amia, Lota

Plotosus, Pleuronectes, Lepisosteus

Lophiiformes, Fugu niphobles

Cololabis, Cheilopogon, Hemiramphus

Fig. 12. Types of olfactory rosettes in ﬁsh. Arrow points the

rostral (R) and caudal (C) directions.

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KASUMYAN

with zones of non-receptor epithelium. The distribution

of receptor cells at the lateral surface of lamellae in dif-

ferent ﬁsh species may differ. Continuous, large-zone,

ﬁne-zone, and irregular types of sensory epithelium

distribution are usually distinguished (Fig. 15) (Yama-

moto and Ueda, 1979; Yamamoto, 1982).

The average density of receptor cells in the receptor

epithelium ranges from 20–30 thousand per mm2 to

400–500 thousand per mm2, and their total number

ranges between several dozens to a hundred thousand to

several dozen million or more (Holl, 1965; Holl et al.,

1970; Zeiske et al., 1976, 1979; Thommesen, 1983;

Devitsyna and Attar, 1988). The density of ciliated and

microvillous cells may differ in different areas of olfac-

tory lamellae but the total number of ciliated cells is

two times more than microvillous (Thommesen, 1983).

The largest number of receptor cells has been found in

the common wels Silurus glanis which approach cer-

tain mammals (dog) with well-developed olfaction

(Table 3). It should be noted that linear growth in ﬁsh

and the associated increase of the number of receptor

cells occurs throughout their whole life, therefore, large

individuals have larger olfactory organs and more

receptor cells (Pashchenko, 1986). All types of receptor

cells are present in most groups of ﬁsh, teleosts, carti-

laginous, Chondrostei (sturgeons), and in myxini

(Theissen, 1976; Yamamoto, 1982; Eistein, 1982;

Zeiske et al., 1992). But Elasmobranchs and some dip-

(a) (b)

(c)

Fig. 13. Olfactory organ and brain of Cyclothone microdon

(Gnatostomidae): (a) and (b) male, view from above and lat-

eral, (c) female, from above; (1) olfactory rosette, (2) olfac-

tory bulb, (3) telencephalon (from Marshall, 1979).

crc

aon mrc cc bc

Fig. 14. Basic cell elements in the olfactory epithelium of

ﬁsh: a. axons of receptor cells; (c) club; (bc) basal cells;

(f) ﬂagellae; (crc) ciliated receptor cell; (k) kinocilia;

(m) microvilli; (cc) ciliate cell; (mrc) microvillous receptor

cell; (sc) supporting cells; (on) olfactory nerve;

(mc) mucous cell (from Zeiske et al., 1992).

(‡) (b) (c) (d)

Fig. 15. Types of the distribution of the receptor epithelium

on lateral side of olfactory lamellae: (a) continuous; (b)

large-zonal; (c) irregular; (d) small-zonal (from Yamamoto,

1982).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S189

noans (Neoceratodus fosteri) have only microvillous

receptor cells, whereas Polypteridae, coelacanths,

Crosspterigi, the river lamprey Lampetra ﬂuviatilis,

marine lamprey Pteromyzon marinus and probably other

lampreys have only ciliated cells (Thornhill, 1967; Reese

and Brightman, 1970; Theissen, 1972; Bronstein, 1976;

Zeiske et al., 1987; Van Denbossche et al., 1995).

Ciliated, microvillous and crypt cells specialize in

perception of different groups of chemical stimuli

(Thommesen, 1982, 1983; Hamdani et al., 2000,

2001a, 2001b; Sato and Suzuki, 2001; Hamdani and

Døving, 2002, 2003; Weltzen et al., 2003). Within all

these groups, the cells probably have further functional

specialization. Unlike amphibians, reptiles and other

vertebrates, this specialization in ﬁsh is not associated

with zonality in the distribution of different receptor

types in the olfactory epithelium (Yamamoto, 1982;

Ngai et al., 1993).

Supporting cells. Supporting cells surrounding the

receptor cells are represented in the olfactory epithe-

lium by two different types: the supporting cells, i.e.,

cells with a free surface not bearing any specialized

structures, and ciliated cells, i.e., cells bearing numer-

ous kinocilia on the surface facing the cavity of the

nasal sac. The number of kinocilia in one ciliate cell

may reach several dozen, they have a length of up to

5 µm and a diameter 0.2–0.3 µm. Kinocilia of the cili-

ated cells move synchronously, and their activity is

responsible for the ventilation of the olfactory cavity in

areas located between close lamellae of the olfactory

rosette, and in many ﬁsh species, ventilation of the

whole olfactory organ (Døving, 1986). The function of

these cells is very important because they provide for

the transport of water which carries the signal to the

receptor cells.

Goblet cells. Goblet cells are very numerous in the

olfactory epithelium. They are located in its upper layer

and may differ in size. Small and large mucous cells are

usually distinguished. The function of these cells is

associated with the production of a special olfactory

mucus, which covers the surface of the olfactory epi-

thelium. This mucous layer or glycocalix completely

covers cilia and microvilli of the receptor cells and the

bases of kinocilia of the ciliated cells. The olfactory

mucus includes mucopolysaccharides, proteins, lipids,

and different ions (Doroshenko and Pinchuk, 1974;

Bronshtein, 1977).

It is hypothesized that glycocalix plays an important

role in chemoreception and that molecules of signal

substances are ﬁrst introduced into the mucus, interact

with its components, and only then reach the receptor

areas in the cellular membrane of cilia and microvilli.

The mucus creates optimal conditions for the molecular

processes involved into the interaction between the sig-

Table 3. The number of receptor cells in the olfactory organ of some species of cyclostomata, ﬁsh, and other vertebrates

Species Number of receptor cells Body length or age Source

Cyclostomata

river lamprey Petromyzon marinus 800 Kleerokoper, Van Erkel, 1960

Fishes

verkhovka Leucaspius delineatus 35 5.5 cm Devitsyna and Attar, 1988

sand lance Ammodytes lancea 200–300 – Holl, 1965

minnow Phoxinus phoxinus 900 – ″

river perch Perca ﬂuviatilis 2.000–3.000 – ″

trigla Trigla corax 4.000 – ″

pike Esox lucius 6.000 54 cm Devitsyna and Attar, 1988

blue bream Abramis ballerus 6.000 30 cm ″

burbot Lota lota 11.000 – Gemne, Døving, 1969

bream Abramis brama 27.000 40 cm Devitsyna and Attar, 1988

wels Silurus glanis 155.000 62 cm ″

Amphibians

ﬁre-bellied toad Bombina bombina 500 adult Khmelevskaya, 1972

gray toad Bufo bufo 2.400 ″″

marsh frog Rana ridibunda 2.650 ″″

Mammals

humans Homo sapiens 10.000 – Brunn, 1892

rabbit Oryctolagus cuniculus 100.000 – Allison, Warwick, 1949

dog Canis familiaris 224.000 – Neyhaus, Müller, 1954

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KASUMYAN

nal substance (ligand) and the receptor proteins

(Sorensen and Caprio, 1998).

It is thought that the olfactory mucus has important

protective functions, protecting ﬂagella and microvilli

of receptor cells from mechanical disturbances by

small particles transmitted by water currents. The

important protective function of the mucous is

revealed by the fact that secretion of olfactory mucus

signiﬁcantly increases when the water is contaminated

by various chemical agents (detergents, heavy met-

als). The production of olfactory mucus in ﬁsh of the

same family is most pronounced in marine (cod

Gadus morhua, navaga Eleginus navaga) than in

freshwater (burbot Lota lota) representatives

(Devitsyna, 1972).

Basal cells. Basal cells are located in the deepest

layer of the olfactory epithelium at the basal membrane.

New cells of the olfactory epithelium, receptor, sup-

porting, and mucous, having limited longevity, develop

and differentiate from basal cells. Receptor cells are

renewed every 7–10 days. Old cells of the epithelium

degenerate and their content is either secreted into the

nasal cavity or is phagocytized by lymphatic cells (Gra-

ziadei and Monti-Graziadei, 1978; Cancalon, 1982;

Pashchenko and Kasumyan, 1984).

The ability of the olfactory epithelium, primarily the

receptor cells, for constant renewal is an extremely

important adaptation, allowing the ﬁsh to retain the

capacity to obtain olfactory information when the prob-

ability of receptor cell destruction and disturbances is

very high. The olfactory epithelium, including the

receptor cells, directly opens into the environment and

is weakly protected from its negative effects. Particles

suspended in water may damage the epithelium (abra-

sive effects). Iridioviruses and bacteria, as well as dif-

ferent parasitic organisms, microsporidia, fungi, and

small crustaceans may also cause signiﬁcant distur-

bances of the olfactory epithelium. Receptor cells may

be disturbed after a sharp change of water salinity in

anadromous and catadromous migrants. Deep struc-

tural disturbances and complete degeneration of many

elements of the olfactory epithelium may be caused by

chemical contaminants (detergents, heavy metals, low

pH) (Bertmar, 1972; Devitsyna, 1977; Doroshenko and

Pinchuk, 1978; Pashchenko and Kasumyan, 1984;

Baatrup and Døving, 1990; Klaprat et al., 1992; Morri-

son and Plumb, 1994; Watson et al., 1998).

The Olfactory Nerve

and the Olfactory Tract

Axons of all receptor cells after the basal membrane

of the olfactory epithelium are joined into the single

nerve, the n. olfactorius (pair I of brain nerves). The

olfactory nerve links the olfactory organ with the pri-

mary olfactory centers: paired olfactory bulbs (bulbus

olfactorius) to which the olfactory information comes

as electric impulses (Fig. 16).

Nervous ﬁbers, i.e., axons of receptor cells, branch

in the olfactory bulb and form a surface ﬁbrous layer.

The glomerular layer of the olfactory bulb, formed by

glomerules, is located under it. Glomerules represent a

complex interlacement of myriad branches of the olfac-

tory nerve and dendrites of mitral cells interacting with

synaptic contacts (Døving, 1986; Satou, 1992;

Sorensen and Caprio, 1998). The relationships between

the number of axons of receptor cells and the number of

mitral cells ranges from 40 : 1 in verkhovka Leucaspius

delineatus to 1000/4000 : 1 in cod Gadus morhua, blue

bream Abramis ballerus, and bream Abramis brama. In

the common wels Silurus glanis, the relationship

between these cells exceeds 12000 : 1 (Døving and

Gemne, 1965; Devitsyna, 1977; Devitsyna and Attar,

1988). It is thought that the higher the ratio, the more

developed are the functional capacities of the olfactory

system (Døving, 1986).

The layer of mitral and ruffed cells is located

below the layer of glomerulas. Each intercalary cell

connects several mitral cells and each mitral cell, in

turn, may have contacts with different intercalary

cells, which causes the formation of large neuronal

assemblages.

An aggregation of granular cells forming the ante-

rior olfactory nucleus (nucleus olfactorius anterior) is

situated under the layer of mitral and intercalary cells.

Granular cells have synaptic contacts with mitral and

intercalary cells. Centrifugal effects from the secondary

olfactory center (nucleus olfactorius posterior), located

in the telencephalon and involved in the central regula-

tion of the olfactory bulb, affect granular cells. The pri-

mary and secondary olfactory centers are connected by

a tract formed by axons of mitral and intercalary cells,

along with centrifugal ﬁbers incoming to granular cells

Fig. 16. Scheme of the olfactory bulb in ﬁsh: (1) axons of

olfactory receptor cells; (2) glomerula; (3) mitral cell;

(4) ruffed cell; (5) granule cell; (6) axons forming the olfac-

tory tract; (7) centrifugal axons (from Satou, 1992).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S191

(they belong to the system of the 0 pair of brain nerves,

terminal nerve n. terminalis) (Sorensen and Caprio,

1998). Lateral and medial ﬁbers are distinguished in the

olfactory tract, each of which, in turn, is separated into

smaller segments (Sheldon, 1912; Holmgren, 1920;

Døving and Gemne, 1965). Olfactory bulbs are con-

nected by interbulbar links passing via the forebrain

(Satou, 1992).

In most ﬁsh species, olfactory bulbs are located

adjacent to the forebrain and the olfactory nerve is quite

long. Such bulbs are called sessille. But in cyprinids,

catﬁshes, cods, and sharks, holocephali and Mormy-

ridae, olfactory bulbs are remote from the forebrain and

are adjacent to the olfactory organ (Døving, 1986).

Olfactory nerves in these ﬁsh are short but the olfactory

tracts, going from olfactory bulbs to olfactory centers in

the forebrain, are of signiﬁcant length. Such bulbs are

called stalked (Fig. 17). In Characidae and some other

ﬁsh, olfactory bulbs are located in the middle between

the olfactory organ and the forebrain.

Morphological and functional zonality has been

found in the olfactory bulb of ﬁsh in recent years (Hara

and Zang, 1996, 1998; Laberge and Hara, 2001;

Nikonov and Caprio, 2001). For example, the axons of

ﬂagellated receptor cells come to the ventral surface of

the olfactory bulb, whereas axons of microvillous

receptor cells arrive at the dorsal surface (Morita and

Finger, 1998). When the olfactory epithelium is stimu-

lated by different chemical substances, the electric

activity is recorded in different areas of the olfactory

bulb. For example, in the channel catﬁsh Ictalurus

punctatus, electric activity goes to the medial part of the

olfactory bulb via axons of ciliated cells sensitive to

fatty acids, and via axons of cells sensitive to free

amino acids, electric activity goes to the ventral part of

the olfactory bulb (Hansen et al., 2003). Signals caus-

ing different behavioral patterns come to secondary

centers via different ﬁbers of the olfactory tract (Døv-

ing and Selset, 1980). For example, olfactory signals

bringing about food search behavior in the silver carp

Carassius carassius come via the lateral ﬁber of the

olfactory tract whereas signals causing defensive

behavior, via the medial segment of the medial ﬁber of

the olfactory tract. The lateral segment of the medial

ﬁber may be involved in the mediation of chemical sig-

nals responsible for the stimulation of sexual behavior

(Døving and Selset, 1980; Stacey and Kyle, 1983;

Hamdani et al., 2000, 2001b; Hamdani and Døving,

2002, 2003; Weltzein et al., 2003). Studies of topo-

graphic and functional specialization in the olfactory

system of ﬁsh are continued quite intensely. They are

very important for understanding the evolutionary path-

ways of the secondary olfactory system: the vomerona-

sal (Jacobian) organ, lacking in ﬁsh (Eistein, 1992). In

mammals, this highly specialized system is involved in

the perception of sexual signals (Meredith and Fernan-

dez-Fewell, 1994; Døving and Trotier, 1998).

Ventilation of the Olfactory Organ

The water, bearing olfactory stimuli, must enter the

olfactory organ to reach the receptor cells. The different

information which is hidden in chemical stimuli will

only be obtained by the ﬁsh in this case, allowing them

to perform the necessary behavioral response. The ven-

tilation of the nasal cavity, i.e., the inﬂow of water, is

conducted by several ways (Pipping, 1927).

The simplest and the most widespread way is asso-

ciated with the directed ﬂow of water created either

when the ﬁsh swims or due to the current. This method

is called pressure ventilation. The water ﬂows into the

olfactory organ due to anatomical characteristics of the

olfactory organ, mostly nostrils. The anterior nostril,

via which the water enters the olfactory cavity, usually

is a kind of short pipe, round in section, with quite hard

and widened walls (Fig. 18). Therefore, the walls of the

4(a)

(b)

Fig. 17. Types of olfactory bulbs in ﬁsh. Brain and structural

elements of the olfactory system in the Arctic char Salveli-

nus alpinus (a) and catﬁsh Silurus glanis (b): (1) telenceph-

alon; (2) olfactory bulb; (3) olfactory tract; (4) olfactory

nerve; (5) olfactory organ (from Døving, 1989 and

Jakubowski and Kunysz, 1979, respectively).

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KASUMYAN

pipe do not occlude by the force of the current, and the

aperture of the nostril is retained (Pashchenko and

Kasumyan, 1986). The posterior nostril in most ﬁsh

species is larger in size, usually has an elongated shape

and its walls are thicker. The olfactory rosette located at

the bottom of the olfactory sac may be seen via the wide

aperture of the posterior nostril in such ﬁsh as stur-

geons, many cods, etc. (Kasumyan, 2002). In ﬁsh with

a monotremous olfactory organ, pressure ventilation is

also possible, but it has a certain speciﬁcity. If the single

olfactory opening is large, and the olfactory cavity rep-

resents a depression, water exchange occurs even after

very small movements of the ﬁsh (garﬁsh Belone

belone and pike Esox lucius). When the single olfactory

opening is small in size, as in ﬁfteen-spined stickleback

Spinachia spinachia (Fig. 7), the directed movement of

water and water exchange (absence of recirculation)

depend on the speciﬁc internal architecture of the organ

(Fig. 18) (Theisen, 1982).

The second method for water ﬂow into the olfactory

organ is active ventilation, depending on the work of

accessory sacs or ciliated nonsensory cells of the olfac-

tory epithelium. The ﬁsh in which the ventilation of the

olfactory sac occurs primarily because of the work of

accessory sacs are called cyclosmats (Døving et al.,

1977). The volume of these sacs, which are located

between the bones of the skull, changes in correlation

with the rhythmical breathing movements of the ﬁsh.

Due to characteristics of hydrodynamics of the olfac-

tory organ and sometimes also because of special

valves, the intake of a new portion of water after the

reduction of pressure in accessory sacs occurs via the

olfactory opening, and the release, via the posterior

opening. Cyclosmats may regulate the ventilation of

the olfactory cavity by increasing the gill and jaw mot-

orics. Cyclosmats include numerous representatives of

ﬂatﬁshes, wrasses Labridae, some cyprinids, and such

species as Sebastodes melanops, Lampris quattus,

Bedotia geayi and other (Johnson and Brown, 1962;

Kapoor and Ojha, 1972; Oelschlãger, 1976; Døving et

al., 1977; Melinkat and Zeiske, 1979). For example, a

sharp increase of the volume of the accessory sacs (and

therefore rapid inhalation of large water volume into

the nasal cavity) in ﬂatﬁshes and perhaps in other ﬁsh

occurs during “coughing,” characteristic sharp move-

ments of the gular membrane, opercula and jaws (Nev-

itt, 1992). These movements become more intense

when the ﬁsh is presented with an olfactory stimulus

(food extract), which allows us to consider coughing as

an analogue of smelling, characteristic of terrestrial

mammals.

The ﬁsh which do not have accessory sacs, in which

active ventilation is performed by ciliated nonsensory

cells, are called isosmats (Døving et al., 1977). Such

ﬁsh include the European wels Silurus glanis, Lepisos-

teus osseus, Clarias batrachus, Labeo rohita, Rhino-

muraena ambonensis, Polypterus ornatipinnis, and

many other species having no accessory nasal sacs

(Pfeiffer, 1968; Holl et al., 1970; Schulte and Holl,

1971; Ojha and Kapoor, 1972; Bashor et al., 1974;

Jakubowski and Kunysz, 1979; Goel, 1980). The ante-

rior nostrils in isosmat ﬁsh often have the form of pipes,

which helps to suck the water layers at a distance from

the ﬁsh body (Døving, 1986).

The speed of water intake into the olfactory organ

due to ciliated nonsensory cells is, while insigniﬁcant,

still obvious in experiments. When a suspension of

Indian Ink is introduced in proximity of the olfactory

organ of ﬁsh immobilized by myorelaxant, it is possible

to determine the time needed for particles to pass via

the olfactory organ, which usually ranges from 6–7 to

9–10 s (Parker, 1910; Teichmann, 1959). In Lepisosteus

(a)

(b)

(c)

Fig. 18. Scheme of pressure ventilation of the olfactory

organ in ditremous and monotremous ﬁshes, minnow Phox-

inus phoxinus (a) and ﬁfteen-spined stickleback Pungitius

pungitius (b, c). Arrow points to the basic directions of

water ﬂow (from Pashchenko, 1986 and Theisen, 1982,

respectively).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S193

osseus, water is pumped with a rate of 2.2 mm/s. At this

speed 400–600 ms is enough for water to pass over the

lateral surface of the lamella (Bashor et al., 1974). The

maximum speed of the current in water inhaled into the

olfactory organ in small cyprinodontid ﬁsh is 12–

17 mm/s, at the release, 30–35 mm/s (Kux et al., 1988).

On the whole, water exchange in the olfactory tract in

cyclosmats occurs faster than in isosmats (Døving,

1986). During pressure ventilation, the speed of water

exchange does not increase signiﬁcantly and even in

such fast swimming ﬁsh as tuna and scombers, the

olfactory organ which has accessory sacs and a poste-

rior nostril has a valve. However, constant movement of

the ﬁsh provides for a constant intake of water into the

olfactory organ (Døving, 1986).

Ventilation of the olfactory organ in most ﬁsh

involves both methods: pressure ventilation and the

work of accessory olfactory sacs allows rapid water

exchange in the olfactory organ, and ciliated nonsen-

sory cells allow the transfer of water with smells into

the narrow spaces between the olfactory lamellae

where receptor cells are located. In some ﬁsh (wels Sil-

urus glanis), the distance between the lamellae is only

30–50 µm (Devitsyna and Attar, 1988).

Functional Characteristics

of the Olfactory System

Olfactory spectra. The olfactory stimuli for ﬁsh

include numerous chemical substances (amino acids,

bile acids, their salts and their derivatives, prostogland-

ines, steroids, nucleotides, amines and polyamines,

etc.), different extracts, wash-offs, exometabolites of

plants and animals, etc. (Fig. 19) (Kleerkoper, 1969;

Malyukina et al., 1969; Døving, 1986). The ﬁsh char-

acterized by high sensitivity to a wide spectrum of

olfactory stimuli (mostly natural in origin, and evoked

different behavioral patterns) belong to the group of

macrosmatics. Microsmatics respond to only a limited

range of odors. However, the sensitivity to these smells

may be as high as in macrosmatic ﬁsh. An intermediate

group of mediosmatics is also sometimes distin-

guished. The concepts of micro and macrosmatics are

used not only with ﬁsh but also many other animals

(Frisch, 1941b).

Olfactory spectra are characterized by speciﬁcity

when species different in systematic position and life

mode are compared. For example, the amino acids cys-

teine, leucine, glutamine and aspartic acids are

extremely efﬁcient olfactory stimuli for one–year old

juveniles of the Atlantic salmon Salmo salar and juve-

niles of some other salmonid ﬁsh but have no effect on

sturgeons, Fundulus heteroclitus, Menidia menidia

(Sutterlin, 1975; Mearns, 1985, 1986). However, sig-

niﬁcant similarity of olfactory spectra is observed in

closely related species. For example, the olfactorily

efﬁcient amino acids almost completely coincide in

four representatives of the order Siluriformes, in the

channel catﬁshes Ictalurus punctatus, I. catus, I. serra-

canthus from the family Ictaluridae and the catﬁsh

Arius felis of the family Ariidae (electrophysiological

recording) (Caprio, 1980, 1982). The same results were

obtained by behavioral tests conducted on ﬁve species

of sturgeon: from twenty free amino acids only glycine

(in some species, also L-alanine) released the food

search response in the Russian sturgeon Acipenser gul-

denstaedtii, Siberian sturgeon A. baerii, stellate stur-

geon A. stellatus, green sturgeon A. medirostris, and in

the beluga Huso huso (Table 4) (Kasumyan and Tauﬁk,

1994; Kasumyan, 1994, 1999). Based on phylogenetic

relationships of sturgeon revealed using karyological

analysis, one can conclude that the olfactory spectra of

ﬁsh are extremely stable and are retained without

changes for millions of years. (Fig. 20). In channel cat-

ﬁsh, this number is 75–80 million years (Caprio, 1980).

Olfactory sensitivity. Fish have extremely high

sensitivity to olfactory stimuli and do not differ from

terrestrial animals, such as mammals, in this respect.

The threshold or the threshold concentration of solution

causing signiﬁcant electrophysiological responses in

the olfactory system may reach very low values, up to

10–9–10–13 M (Table 5) (Hara, 1992b). Different ways

to record electric activity have been used in experi-

ments: from the whole olfactory epithelium, from sep-

arate receptor cells, or from the olfactory nerve, olfac-

tory tract or individual nervous ﬁbers (Fig. 21). Calcu-

lations showed that when the threshold concentration is

equal to 10–11 M, electric responses in the olfactory sys-

tem of salmonid ﬁsh will be recorded even when the

stimulus is the water from a basin 25 × 10 × 2 m

(500000 l in volume) in which only one drop (50 µl) of

gall is dissolved (Døving, 1989). Also, calculations of

the active olfactory space (in which the concentration

of natural olfactory substances exceeds the threshold

level) created by the tilapia Oreochromis mossambicus

are interesting (Frade et al., 2002) (Table 6).

Threshold concentrations of chemical substances

which could evoke behavioral responses in ﬁsh are

Clean Stimulus

Recorder

Output

Electrodes

Olfactory

water solution

device

rosette

Fig. 19. Setting for the recording of electroolfactogram in

ﬁsh (scheme).

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KASUMYAN

Table 4. The intensity of food search response (points) of sturgeon to amino acids solutions (10–4 M) (from Kasumyan and

Tauﬁk, 1994)

Amino acid Russian sturgeon

Acipenser gueldenstaedtii Siberian sturgeon

Acipenser baerii Stellate sturgeon

Acipenser stellatus Green sturgeon

Acipenser medirostris Beluga

Huso huso

Alanine 0.8* 0.5* 1.7 – 0

Arginine 0 0 0 – –

Asparagine 0 0 0 – –

Aspartic acid 0 0 0 – –

Valine 0 0 0 – –

Histidine 0 0 0 – –

Glycine 2.5* 2.6 1.2 1.4 0.5

Glutamine 0 0 0 – –

Glutamic acid 0 0 0 – –

Isoleucine 0 0 0 – –

Leucine 0 0 0 – –

Lysine 0 0 0 – –

Methionine 0 0 0 – –

Norvaline 0 0 0 – –

Proline 0 0 0 – –

Serine 0 0 0 – –

Tyrosine 0 0 0 – –

Threonine 0 0 0 – –

Phenylalanine 0 0 0 – –

Cysteine 0 0 0 – –

* Responses of ﬁsh to solutions with the concentration 10–5 M.

Table 5. Olfactory sensitivity of cyclostomata and ﬁsh to some types of chemical substances (based on electrophysiological

data) (from Hara, 1992b)

Species L-amino acids, M:

L-amino acids steroids F-prostaglandins

Myxine glutinosa 10–5–10–6 10–5–10–6

Negaprion brevirostris 10–7–10–8

Salmo salar 10–5–10–9

Salvelinus fontinalis 10–7–10–8

Salvelinus namaycush 10–7–10–9 10–8–10–9

Salvelinus alpinus 10–7–10–9 10–8–10–9 10–9–10–11

Oncorhynchus mykiss 10–7–10–8 10–9–10–10

Oncorhynchus nerka 10–6–10–7

Oncorhynchus kisutch 10–6–10–7

Ictalurus catus 10–7–10–9

Clarias gariepinus 10–10–10–11

Cyrpinys carpio 10–7–10–9

Carassius auratus 10–8–10–9 10–12–10–13 10–12

Misgurnus anguillicaudatus 10–10–10–13

Mugil cephalus 10–7

Seriola quinqueradiata 10–7

Pagrus major 10–6–10–7

Conger myriaster 10–8–10–9

Anguilla rostrata 10–7–10–9

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S195

higher than in electrophysiological experiments and

usually range from 10–6 to 10–9 M (Table 7). It is possi-

ble to record behavioral responses to lower concentra-

tions than in electrophysiological experiments in only

very rare cases (Murphy et al., 2001). Methods for the

recording of behavioral responses and the types of

aquariums used are also very diverse (Kasumyan,

1990a, 1990b; Marusov, 1990). The most important

requirement is adequacy, i.e., the degree they reﬂect

biological and behavioral characteristics of the species,

the ﬁsh age, motivational state, and the behavioral

response recorded. Many of the devices represent

mazes with different numbers of compartments, one of

which contains the smell stimulus (Fig. 22). When the

researcher uses the methods based on prior training and

conditioned reﬂex to the substance, the threshold con-

centrations may approach or even exceed those

recorded electrophysiologically. For example, using

this methodology, a record ﬁsh sensitivity to smells,

(a)

(b)

(c)

(d)

Fig. 20. Aquariums for the study of behavioral responses of ﬁsh to olfactory stimuli: (a) aquarium with two opposite ﬂows; (b) Y-

like maze with compartment traps; (c) aquarium with four parallel ﬂows; (d) ﬂow-through olfactometer aquarium.

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KASUMYAN

0.5 × 10–18 mg/l of β-phenylethyl alcohol was found in

the eel Anguilla anguilla (Teichmann, 1959).

It should be noted that the above threshold concen-

trations represent ﬁsh sensitivity to artiﬁcial chemical

substances. It was hypothesized (Malyukina et al.,

1974; Devitsyna and Malyukina, 1977) that the thresh-

olds for natural substances may be even lower. How-

ever, there is no experimental support for this hypothe-

sis because the exact nature of natural chemical stimuli

for ﬁsh is still unknown.

There exist no patterns or relationships between the

structure of the stimulus molecule and its olfactory efﬁ-

ciency. It is only known that aliphatic α amino acids

with short carbon chains are more efﬁcient among free

amino acids. Also, L-stereoisomeres of amino acids are

always more efﬁcient than their D-enantiomers (Suzuki

and Tucker, 1971; Hara, 1982, 1994; Caprio, 1982,

1984). Minor structural modiﬁcations of the stimulus

molecule, such as alteration of the position of some

functional group (e.g., the transition of the amino-

group from the α to β-position in the case of amino

acids), inclusion of an additional functional group or

removal of an existing one may cause signiﬁcant alter-

ations of olfactory efﬁciency of the substance (Hara,

1977; Caprio, 1978, 1984). The simplest dipeptides

formed of two highly active amino acids may be inefﬁ-

cient (Hara, 1977, 1982; Caprio, 1978). It was also

found that mixtures of substances may have a very dif-

ferent efﬁciency than their separate components. Such

interactions may include effects of synergism, additism

or antagonism (Kang and Caprio, 1991; Hara, 1994).

CH3

CONH(CH2)2SO3H

HOH

HOCH

CH3

COOH

HOOC SH

NH2

Amino acid

Bile salt

Prostoglandin

Steroid hormone

Fig. 21. Types of chemical substances representing efﬁcient olfactory stimuli for ﬁsh (from Hara, 1992b).

Table 6. Threshold concentrations of urine, bile, and feces

for the olfactory system of the Mossambique tilapia Oreo-

chromis mossambicus, the rate of extraction of these excre-

tions and creation of the active olfactory space

Source

of olfactory

stimuli

Threshold

solution

Rate of excre-

tion, ml/(h kg)

(body weight)

Olfactory

space, l/(h kg)

(body weight)

Urine 1 : 10–6.9 4.26 616

Bile 1 : 10–5.2 0.0008 2.2

Feces 1 : 10–4.9 0.5 18

Table 7. Olfactory sensitivity of ﬁsh to L-isomers of free

amino acids (based on behavioral experiments)

Species Threshold con-

centration, M Source

Anguilla anguilla 10–8–10–9 Sola et al., 1993

Salmo salar 5 × 10–9 Mearns, 1989

Salmo trutta 5 × 10–6 ″

Salvelinus alpinus 4.6 × 10–7 Olsén, 1986

Oncorhynchus kisutch 10–7 Rehnberg,

Schreck, 1986

Ictalurus punctatus 10–7–10–9*Holland, Tee-

ter, 1981

Cyprinus carpio 2 × 10–7 Kruzhalov,

1986

Acipenser

gueldenstaedtii 10–6 Kasumyan,

Tauﬁk, 1994

Acipenser baerii 10–6 ″

Coregonus clupeaformis 10–8–10–10 Jones, Hara,

1985

Thunnus albacares 10–11 Atema et al.,

1980

Carassius carassius 10–7 Kruzhalov,

1990

* Data obtained with the conditioned reﬂex methodology.

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S197

Adaptation. The olfactory system is characterized

by slow adaptation to the acting olfactory stimulus (Ott-

son, 1956; Døving, 1966; Hara and Gorbman, 1967;

Malyukina et al., 1969, 1974; Devitsyna and Maly-

ukina, 1977). Because of this property, olfactory stim-

uli retain their signal value for a prolonged time, which

is important for the orientation of ﬁsh to the source of

the smell or directed movement along the smell corri-

dor as often occurs during ﬁsh migrations. Prior adap-

tation of the olfactory system to a smell may differently

affect the sensitivity to other substances (cross-adapta-

tion) (Caprio and Bird, 1984; Hara, 1994).

The pattern of smell distribution in the water media

enables retention of the signal properties of a substance

and the possibility for the ﬁsh to ﬁnd its source. The

olfactory trace, even in a relatively laminar current, has

a very complex internal structure because of chaotic

alteration of areas with signiﬁcantly different substance

concentrations (Atema, 1988). Therefore, when the ﬁsh

moves along the olfactory corridor, the intensity of the

stimulus affecting the olfactory receptors may vary in a

wide range. Special studies showed that adaptation of

the receptors to the substance in such conditions is

much slower.

Distance and mechanisms of olfactory orienta-

tion. The ability to perceive and respond to trace con-

centrations of olfactory substances and slow adaptation

of the olfactory system allows ﬁsh to obtain informa-

tion with a very remote source. According to some

assessments, olfaction is characterized by the highest

distance in comparison with other sensory systems

(Table 8) (Pavlov and Kasumyan, 1990; Wilson and

Smith, 1984). Longevity of the olfactory trace depends

on such characteristics of the water media as stable cur-

rent direction and pronounced vertical stratiﬁcation.

Observations indicated that ﬁsh could determine the

presence and even identify and ﬁnd the location of an

olfactory lure at a distance of dozens or even hundreds

of meters. The lemon shark Negaprion brevirostrus in

an environment similar to natural (in a large lagoon iso-

lated from the ocean) followed along an olfactory trace

of curvilinear trajectory if the lure was at a distance

exceeding 17 m (Gilbert, 1961; Hobson, 1963). Paciﬁc

salmon (Oncorhynchus) identify spawning rivers by the

smell of the spawning grounds they were born in, even

when these are many dozens or hundreds of kilometers

upstream (Hasler and Scholz, 1983; Stabell, 1992;

Døving and Stabell, 2003).

The ability of ﬁsh to rapidly ﬁnd the source of a

smell depends not only on the level of olfactory sensi-

tivity and the duration of adaptation, but also on the

hydrodynamic characteristics of the media. In a cur-

rent, ﬁsh, in most cases, can ﬁnd the source of the

attracting stimulus, such as food, more easily. In the

absence of current this may require much more time

(Kleerekoper et al., 1975). Observations of the behav-

ior of deep-sea ﬁsh in natural environments indicated

that the higher the current speed, the more rapidly and

more precisely ﬁsh could locate an olfactory lure (Wil-

son and Smith, 1984). However, for ﬁsh inhabiting

slow-moving waters, searching for an olfactory lure in

a current is more difﬁcult (Sherman and Moore, 2001).

Another characteristic of many natural water bodies

which enables the olfactory orientation of ﬁsh is verti-

cal stratiﬁcation, that is, the presence of stable horizon-

tal layers of water with different temperature, salinity,

or current direction or speed (Fig. 23) (Døving et al.,

1994; Døving and Stabell, 2003).

It is accepted that the mechanism of ﬁsh orientation

to the source of smell in currents is based on klinotaxis,

when the ﬁsh moves against the current towards the

source of the stimulus, due to comparisons of the stim-

ulus concentration over a certain time interval. This

mechanism accounts for the directed movements of ﬁsh

Table 8. The possibility of ﬁnding remote food objects with

different sense systems (from Pavlov and Kasumyan, 1990)

Distance, m Sensory systems

More than 100 m olfaction

100–25 olfaction, audition

25–5 olfaction, vision, audition

5–1 vision, olfaction, audition

1–0.25 vision, audition, lateral line, olfaction

Less than 0.25 vision, lateral line, electroreception,

external gustatory sensitivity, general

chemical sense, tactile reception

0external and intraoral gustatory

sensitivity, tactile reception

Note: The sensory systems are listed in an order which corresponds

to their signiﬁcance during the search for remote food.

10 million

> 80 million

H.huso

2n = 118 ± 2 A. stellatus

2n = 118 ± 2 A. baerii

2n = 240 – 260

A. gueldenstaedtii

years ago

Fig. 22. Scheme of phylogenetic relatioships of sturgeon

ﬁshes (from Vasilyev, 1985).

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KASUMYAN

along a smell gradient, from areas with low concentra-

tions to those with high concentrations. Orientation in

stalled water occurs due to tropotaxis, i.e., due to com-

parison of concentrations of the attracting stimulus in

the left and right olfactory organs. The ﬁsh can proba-

bly actively use both mechanisms in natural environ-

ments. This is supported by experiments in bonnethead

sharks Sphyrna tiburo conducted in a round basin. A

special device (2.4 × 0.8 × 1.0 cm) was attached to the

head of the ﬁsh, allowing delivery of the appropriate

quantity of Callinectes sapidus crab extract separately

to the left and right nostrils via thin tubes (Fig. 24). The

Current speed

Depth

Fig. 23. Scheme of possible horizontal currents in a water body, their direction and relative speed.

(a)

(b) (c) (d) (e)

Fig. 24. The behavior of the bonnethead sharks Sphyrna tiburo due to different methods of stimulation with food smells, extract of

the blue crab Callinectes sapidus. (a) Device for delivery of smell to the olfactory organ; (b) and (c) and (d) and (f) ﬁsh movements,

respectively, in stalled water and in the presence of circular current; (b) and (d) after delivery of the stimulus solution into the tank;

(c) and (e) after delivery of the stimulus solution into the olfactory organ (uni- and bilateral stimulation). Arrows point to the ﬁsh

position at the moment of olfactory stimulus delivery (from Johnsen and Teeter, 1985).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S199

ﬁsh constantly moved around the circle along the walls

both in the presence of a circular current and in its

absence. When 10 ml of the extract was released into

the basin in the absence of a current, the ﬁsh lagged in

the olfactory zone and begun short searching move-

ments. The same response was observed when 0.5 ml of

the stimulus was released to both nostrils simulta-

neously. In the presence of a circular current (15 cm/s),

the response to 10 ml of the extract was more compli-

cated. When the ﬁsh found itself in the stimulus zone

(which itself moved in the current as a continuously

eroded spot), it continued to follow forward and there-

fore rapidly left the scent. Turning back, the shark

began to swim along the current until it again reached

the smell spot. Moving more rapidly than the current,

the subject left the scent zone, turned back and begun

swimming against the current until it again entered the

smell spot. Such behavior repeated until the concentra-

tion of the stimulus reduced to below the threshold

value. The responses of the sharks to the administration

of 0.5 ml of the extract to both nostrils simultaneously

was very similar. When the stimulus was released to

only one nostril, the ﬁsh always tended to turn toward

the side in which the stimulus was released rather than

toward clear sea water, or to the side to which the stim-

ulus was administered in a higher concentration (the

differences in concentrations was equal to 50%)

(Johnsen and Teeter, 1985).

Fish can determine the correct direction toward the

source of a smell during prolonged migrations along

the olfactory corridor, based on certain characteristics

of their behavior. Detailed observations of salmon

migrating to their spawning sites indicated that when

approaching the river mouth, the ﬁsh keep at a certain

water layer, periodically moving outside it (Fig. 25)

(Døving et al., 1985; Tanaka et al., 2001). The same

behavior is characteristic of adult American eels

Anguilla rostrata entering the estuary during catadro-

mous migration (Barbin, 1998). It was hypothesized

that the ﬁsh, in this way, could control their spatial posi-

tion as to not lose the zone with the maximum smell

concentration. One possible orientation mechanism in

such cases is tropotaxis. However, unilateral olfactory

deprivation does not cause any disturbances in the

behavior and orientation of migrating salmon. Only

complete dysfunction of the olfactory system can cause

a total loss of orientation (Døving et al., 1985). Move-

ments along curved or zigzag trajectories circular, or

S-like, or ∞-like are characteristic of many ﬁsh search-

ing for the source of the smell (Parker, 1912; Bardach

and Case, 1965; Johnsen and Teeter, 1985; Kasumyan,

1999, 2002).

Horizontal zigzag movements of migrating salmon

are often observed in rivers, especially in places where

large tributaries inﬂow. Such swimming allows the

migrating salmon to remain in those areas of the current

which bear the smell of the home spawning site.

Chemical Signals

Classiﬁcation of chemical signals. Chemical sig-

nals of ﬁsh are very diverse. According to the classiﬁ-

cation used for all animals, chemical signals regulating

interactions between conspeciﬁc individuals are named

pheromones. Interactions between representatives of

different species are regulated by kairomones and

allomones. Kairomones are such interspeciﬁc odors

which bear useful information for the recipient of the

stimulus. When the chemical signal is useful for the

producing individual rather than the recipient, this sig-

nal is called an allomone (Fig. 26) (Karlson and Lüsher,

1959). Chemical signals within these groups are sepa-

rated into sex pheromones, alarm pheromones and

Fig. 25. Vertical movements of the Atlantic salmon Salmo

salar in nearshore zone after approaching the mouth of the

home river. The stripped lines show isotherms with the step

0.2° between 13 and 14°C (from Døving et al., 1985).

Fig. 26. Types of chemical signals regulating intra- and

interspeciﬁc relationships in animals. A and B species

linked by chemocommunication; the darkened circle

depicts the participant of the communication pair, for which

this link is favorable.

Time, min

Depth, m

14°C

13°C

A A

A B

Pheromones

Kairomones

Allomones

Producer Recipient

of the chemical

stimulus of the chemical

stimulus

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JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

kairomones, stress (fear) pheromones, territory mark-

ing pheromones, etc.

Releasing signals and priming signals are distin-

guished among chemical signals as well as among sig-

nals of other modalities (Wilson and Bossert, 1963).

The releaser signals after reception cause rapid behav-

ioral response with relatively short latency. Priming

signals ﬁrst release complex endocrine processes, caus-

ing the secretion of physiologically active substances,

in turn initiating the appropriate alterations of meta-

bolic and regulatory processes. This causes shifts in

metabolism, respiration intensity, alterations of body

pigmentation, stress development, etc.

Sources of smell substances. In terrestrial animals,

smells are usually secreted by special glands. In most

ﬁshes, the glands responsible for the secretion of chem-

ical stimuli are absent. There exist only a small number

of exceptions from this rule among male ﬁsh. For

example, males of Claris gariepinus secrete sex phero-

mones into the seminiferous vesicles, special structures

of the urogenital system of these ﬁsh, and the phero-

mones are then released simultaneously with the secre-

tions of the seminiferous vesicles (Resnik et al., 1987,

1989). The secretion of sex pheromones in males of the

blenny Blennius pavo occurs in preanal blind processes

(anal appendices) (Laumen et al., 1974), in the goby

Gobius jozo, in the mesorchial gland (Colombo et al.,

1980).

Most smell substances represent so-called exome-

tabolites or external metabolites. They are released into

the environment as a result of the living activities of the

ﬁsh with urine or feces, or are excreted via the skin, ﬁrst

being excreted to the skin mucus and then to the envi-

ronment (Stabell et al., 1982; Malyukina et al., 1983;

Hara et al., 1984; Canario, Scott, 1989, 1994; Sorensen,

1992; Moore et al., 1994; Moore et al., 1994; Courte-

nay et al., 1997; Vermeirssen et al., 1997; Yambe et al.,

1999). It is proposed that the excretion of some smell

substances may occur via the gill epithelium (Sorensen

et al., 2000; Li et al., 2002). Exometabolites include

signal substances revealing the species, population,

sex, and individual identity of the individual, the stage

of gonad development, possible stress, and social sta-

tus. Exometabolites may be used for chemical marking

of the territory. Sex pheromones, stress and alarm pher-

omones also belong to exometabolites.

The source of some sex pheromones are gonadal liq-

uids, such as the ovarial and spermatic liquids released

in water during spawning, when the gonadal products

are released (Van Den Hurk and Lambert, 1983; Van

Den Hurk et al., 1987; Sorensen, 1992; Van Den Hurk

and Resnik, 1992).

There exist smells (alarm substance) which are kept

in special epithelial cells. These substances can be

released in the water only when the skin is damaged by

the predator (Frisch, 1941a; Schutz, 1956; Pfeiffer,

1963). In dead ﬁsh, these substances are released in

water spontaneously, most intensely during the ﬁrst

hours after the death (Kasumyan, 1989; Kasumyan and

Tuvikene, 2004).

Representatives of the genus Pardachirus (fam.

Soleidae) have special glands located at the base of the

dorsal and anal ﬁns with external opening by numerous

pores. The secretion developed by these glands has

repellent properties for piscivorous ﬁsh feeding on

small nearshore ﬁsh (Clark, 1981, 1983). On the whole,

the presence of special glands secreting smell sub-

stances is rather unusual for ﬁsh.

The nature of chemical signals. Whereas there

exists a limitation on the size of a distant smell sub-

stance in terrestrial animals required by the volatility

(the molecular weight of volatile substances must not

exceed 300–400 Da), to ﬁsh and other aquatic animals

smell signals have no such limitation. Therefore, chem-

ical signals for ﬁsh may include substances with small

molecular size and large high-molecular substances

with a molecular weight up to 10000 Da or higher

(Kasumyan and Ponomarev, 1987, 1991; Carr et al.,

1996). The only requirement for such substances is sol-

ubility in water, which does not need to be high,

because the ﬁsh can perceive very low trace concentra-

tions of signal substances.

Very different chemical substances satisfy these

requirements. This makes the identiﬁcation of the

chemical structure of natural chemical signals of ﬁsh

and other aquatic organisms very difﬁcult, much more

difﬁcult than in terrestrial animals. For example, the

chemical structure of several hundred pheromones has

been identiﬁed in insects. Many of them have been syn-

thesized artiﬁcially and are applied by humans in indus-

try. A. Butenandt was awarded the Nobel Prize in 1959

for studies associated with the identiﬁcation of the ﬁrst

insect pheromone, the sex pheromone of the silkworm

Bombyx mori, which turned out to be the multi-atom

alcohol bombicol.

Natural smell stimuli in ﬁsh, as in higher animals,

represent multicomponent mixtures of substances,

making the problem of identiﬁcation even more com-

plicated. The chemical nature of no single natural sig-

nal of ﬁsh has been identiﬁed up to the present time.

Attempts to determine the chemical nature of the alarm

pheromone of cyprinid ﬁsh have been made over the

past 60 years by specialists from Germany, Russia,

Switzerland, Canada, Norway, and the USA (Døving

et al., 2004). The most successful studies were of the

sex pheromones of ﬁsh. The basic components of sex

pheromones in teleosts and possibly in cyclostomata

are different steroids and their derivatives as well as

prostaglandins (Adams et al., 1987; Sorensen and Sta-

cey, 1990; Sorensen, 1992).

The Role of Olfaction in Fish Behavior

Olfaction is involved in regulation of almost all

behavioral forms (Kleerekoper, 1969; Malyukina et al.,

1969, 1980; Døving, 1986). This is mainly associated

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S201

with the fact that they live in the aquatic environment,

in which the perception of other stimulus modalities,

such as visual, is often difﬁcult. Diffusion of chemical

substances in water is slow, which makes olfactory

traces relatively long-lasting. With currents, the turbu-

lence of which is not as pronounced as in air, smells

may spread to large distances (Atema, 1980). Another

advantage of olfactory communication is the possibility

to transmit an almost unlimited volume of information

with chemical stimuli, from general to highly speciﬁc.

This can be reached by the ease with which endogenous

chemical substances may form different combinations.

Smells regulate such forms of behavior as feeding,

spawning, parental, defensive, migration, social, and

territorial. In many cases, olfaction is the leading sense,

determining the possibility of a particular behavioral

pattern or repertoire of the species. There are many

experimental studies showing that olfactory deprivation

(blocking the olfactory sensitivity by closing the water

intake into the olfactory organ, cauterizing the olfactory

rosette, treatment of the olfactory epithelium by deter-

gents or salts of heavy metals, cutting or removal of the

olfactory nerve section, extirpation of the olfactory

bulb, etc.) makes spawning very difﬁcult or impossible,

as well as locating food, homing, maintenance of the

group hierarchical structure, etc. (Parker, 1910; Göz,

1941; Frisch, 1941a; Todd et al., 1967; Zeiske, 1968;

Kleerekoper, 1969; Pfeiffer, 1969; Pavlov et al., 1970;

Pollack et al., 1978; Atema, 1980; Honda, 1980a,

1980b; Kasumyan and Pashchenko, 1982; Stacey and

Kyle, 1983; Hasler and Scholz, 1983; Pashchenko and

Kasumyan, 1984; Døving et al., 1984, 1985;

Kasumyan and Pashchenko, 1985; Stabell and Refstie,

1985; Hellstrøm and Døving, 1986; Olsén et al., 1986,

1998; Sorensen, 1992; Liley et al., 1993; Kasumyan

and Kazhlayev, 1993; Zippel, 1993; Zippel et al.,

1993a; Kasumyan and Devitsyna, 1997; Kasumyan,

1999, 2002; Hamdani et al., 2001b; Kasumyan and

Marusov, 2002, 2003). The most diverse is the partici-

pation of the olfactory reception in intraspeciﬁc rela-

tionships in ﬁsh: intraspeciﬁc communications. The

role of olfaction in ﬁsh life is supported by the ability,

found in many species, to memorize olfactory stimuli

and retain the conditioned associations for a very long

time (Vinogradova and Manteifel, 1984; Zippel et al.,

1993a, 1993b; Rekowski et al., 1994).

The smell of the species, population, and individ-

ual. Even early studies revealed that ﬁsh extract sub-

stances create a so-called smell of the species and allow

them to distinguish conspeciﬁc individuals from other

species, even systematically related ones (Wrede,

1932; Göz, 1941; McLennan and Ryan, 1997, 1999).

The smells produced by the ﬁsh are characterized not

only by species but also population and individual spec-

iﬁcity, allowing the ﬁsh to distinguish representatives

of their own population or group from other conspecif-

ics (Døving et al., 1974; Selset and Døving, 1980; De

Fraipont and Thinés, 1986; Groot et al., 1986; Olsén,

1986; Stabell, 1987, 1992; Berti et al., 1989; Courtenay

et al., 1997, 2001; Hiscock and Brown, 2000). Fish

could also discriminate conspeciﬁc individuals (Wrede,

1932; Todd et al., 1967; Carr and Carr, 1985). It has

been shown in territorial ﬁsh and ﬁsh with well devel-

oped hierarchical relationships that individual chemical

signals, the source of which is mucus and urine, could

provide information about the hierarchical status of the

partner, its physiological state (stress), sex, and ripe-

ness of gonads, age and body size. Olfactory depriva-

tion makes the ﬁsh unable to obtain such information

(Todd et al., 1967; Bardach and Todd, 1970; Todd,

1971). Species smells have an attractive effect for many

ﬁsh species, especially schooling (Hemmings, 1966;

Pavlov and Kasumyan, 2000). But such an effect is not

always observed and in some cases, as has been found

in the cod Gadus morhua, the response may range from

attractive to repellent, depending on the concentration

of the smell or the life mode of the ﬁsh during that par-

ticular stage of the life cycle (Malyukina et al., 1980,

1983). Certain cave ﬁsh exhibit an avoidance response

to the smell of conspeciﬁc individuals and other species

(Berti and Zorn, 2001).

Reproductive behavior. The involvement of chem-

ical signalization in ﬁsh reproductive behavior has been

found in all ﬁsh studied. Fish use olfaction to ﬁnd a

partner ready for spawning and determine the readiness

of their gonads. Smell also stimulates the ripening of

gonads and promotes synchronization of spawning.

Sexual smells are mostly used by male ﬁsh; involve-

ment of chemical signalization in the behavior of

females is less pronounced (Colombo et al., 1980;

Liley and Stacey, 1983; Adams et al., 1987; Sorensen,

1992; Olsén and Liley, 1993; McLennan and Ryan,

1997).

The sensitivity of ﬁsh to sex pheromones has been

found in species with different systematics and life

modes. Sex pheromones are very efﬁcient olfactory

stimuli even for microsmatic ﬁsh, which are character-

ized by a narrow olfactory spectrum and do not respond

to many chemical stimuli, such as food odor (pike,

sticklebacks) (Devitsina and Malyukina, 1977; Gol-

ubev and Marusov, 1979, 1984).

Recent studies indicated that a whole complex of

pheromones with both priming and releaser effects is

involved in the chemical regulation of spawning and

sexual behavior. Each sexual pheromone is directed at

speciﬁc chains of a complex behavioral unit and physi-

ological alterations associated with the ﬁnal stages of

ripening and spawning in ﬁsh (Sorensen, 1992;

Sorensen and Stacey, 1999).

The goldﬁsh Carassius auratus is the most studied

object in this respect. This species is a very convenient

laboratory model for the study of ﬁsh pheromones

(Dulka et al., 1987; Sorensen, 1992; Sorensen and Sta-

cey, 1999; Polling et al., 2001). Most sex pheromones

regulating the reproductive behavior in the goldﬁsh

enter the water with urine, portions of which are regu-

larly excreted by females (Fig. 27). Before ovulation,

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KASUMYAN

females of the goldﬁsh secrete 17α, 20β-dihydro-

progesterone. When excreted in water, it works as a

sexual preovulatory pheromone with a priming effect.

17α, 20β-dihydroprogesterone increases the level of

gonadotropin in male blood and, as a consequence,

increases sperm production (Fig. 28).

Another sexual pheromone is excreted by females of

the goldﬁsh later, during ovulation, and brings about

prespawning behavior of males. This pheromone is a

chemical signal with a releaser effect. It is hypothesized

that a postovulatory releasing pheromone exists, which

appears in the water at the moment of egg release by the

female or immediately before it, and causes sperm

release in males. The function of this pheromone is to

synchronize the spawning of both partners. Fish sex

pheromones represent complex mixtures, the most

active components of which include steroid hormones

or their derivatives and prostaglandins (Fig. 21)

(Sorensen, 1992).

Sex pheromones are characterized by species speci-

ﬁcity and probably participate in the reproductive isola-

tion of related species or even populations of the same

species (McLennan and Ryan, 1997). For example, it

was found in the anadromous and resident forms of the

masu salmon Oncorhynchus masou with similar repro-

ductive ecology that only the smell stimuli produced by

ripe females of the same form are highly efﬁcient for

males (Bloom and Perlmutter, 1978; Honda, 1982;

Liley, 1982).

However, sex pheromones may have signiﬁcant

interspeciﬁc efﬁciency, as has been found in sturgeon.

A solution of the ovarial liquid taken from female Rus-

sian sturgeon Acipenser gueldenstaedtii evoked repro-

ductive behavior not only in conspeciﬁc males but also

in males of the stellate sturgeon A. stellatus

(Kasumyan, 1993, 1999).

As noted above, pheromone regulation of sex

behavior has been found in all ﬁsh species studied. But

it is especially important for those species, in which the

function of non-olfactory systems, mostly vision, is

limited because of lifestyle or ecology. This was dem-

Consecutive 5-min intervals

Number of urine portions excreted

123456789101112

by six females for 5 min

Fig. 27. Time course of urine excretion by ripe females of

the goldﬁsh Carassius auratus (from Appetl and Sorensen,

1999).

17α, 20βP

1200 2000 Sexual

Excretion in water

Spawning

Sexual

sperm

PGFs

ovulation

Maturation

GfH

17α, 20βP

Males

Females

1200

1200 2000 1200

Time of day, h

behavior

of females

synchronization

behavior

of male

Fig. 28. Participation of sex pheromones in regulation of reproductive behavior in the goldﬁsh Carassius auratus (scheme) (from

Sorensen, 1992).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S203

onstrated in a small short-cycle mesopelagic ﬁsh Argy-

ropelecus hemigymnus (family Sternoptychidae, order

Stomiiformes) (Jumper and Baird, 1991). Ripe individ-

uals have a length of about 30 mm and inhabit oceanic

depths from 200 to 600 m. The olfactory organ in males

of these ﬁsh is morphologically developed signiﬁcantly

more than in females. Complicated mathematical com-

putations determined the amount of time the male ﬁsh

would need to ﬁnd a ripe female using vision and olfac-

tion. The computations were based on the behavior and

biology of the species and the data known for sex pher-

omones of ﬁsh. The following was accepted: (1) the

average population density of Argyropelecus hemigym-

nus is about 3 × 10–5 /m3; (2) the swimming speed of

males before and after receiving the signal of female

presence is, respectively, 1.5 and 3.0 cm/s; (3) the

female takes a stationary position during the emission

of the pheromone and produces about 2 ×

1014 molecules; (4) the sensitivity of males to the pher-

omone is 2 × 1010 /m3; (5) the smell spreads homoge-

neously within 10 cm of the horizontal water layer.

Computations indicated that with such parameters,

males, in 90% of the cases, could ﬁnd the presence of

the female 1–2 h after the female begun emission of the

sexual pheromone, and they could ﬁnd the female dur-

ing the subsequent 30 min, if the smell was found at the

distance 20 m from the female. If the male of Argyro-

pelecus hemigymnus relied only on vision (the visual

radius was taken equal to 1 m), it required eight days to

ﬁnd the inactive female or 5–6 days of searching if the

female moved randomly (non-vectorized movements)

(Jumper and Baird, 1991).

Experimental data suggest that smells excreted in

water by ripe females of the mosquitoﬁsh Gambusia

afﬁnis cause the retardation of growth of juveniles and

development of smaller ovaries in females (Luthesky

and Adkins, 2003).

Relationships between parents and offspring.

Chemical signalization is involved in the regulation of

another behavior, relationships between the parents and

the offspring. Many ﬁsh species exhibit different forms

of such relationships. In cichlids defending the brood,

the water from their own brood stimulated behavioral

units associated with parental care. The signal value of

the smell of juveniles is retained during the whole dura-

tion of parental care until the family group is broken.

Defensive behavior. The olfactory regulation of this

behavior involves several chemical signals of danger.

On of the most interested is the alarm pheromone,

which is contained in special epidermal cells of the skin

(club cells) and appears in water when the skin cover of

the ﬁsh is damaged by the predator. The behavioral

response to this signal of danger involves the fright

response and then quick avoidance and hiding. For a

long time, the ﬁsh avoid areas of the habitat where they

encounter this smell (Frisch, 1941a; Schutz, 1956; Pfe-

iffer, 1962, 1977; Smith, 1982, 1992; Wiesenden,

2003). In addition to the releaser effect, the alarm pher-

omone has a priming effect, causing stress responses

(Malyukina et al., 1982; Lebedeva and Golovkina,

1988) and alterations of the body proportions of the ﬁsh

(Stabell and Lwin, 1997).

A defense behavioral mechanism based on the

alarm substance is characteristic of most small freshwa-

ter ﬁshes with different systematics (Pfeiffer, 1977;

Chivers and Smith, 1998). The response to the alarm

pheromone is innate, it does not require prior learning.

The effect of the alarm substance has a pronounced

interspeciﬁc and intra-speciﬁc efﬁciency, but the

strength of the behavioral response of the ﬁsh to the

skin extract of related species is always lower then to

skin extract of conspeciﬁcs (Schutz, 1956; Pashchenko

and Kasumyan, 1983, 1986; Kasumyan and Pono-

marev, 1986b). The adaptive function of the defense

behavior caused by the alarm pheromone is the increase

of the relative protection of prey ﬁsh after one member

of the group is dead.

Detection of predators and transition of ﬁsh to safe

areas is reached due to another signal of danger: the

alarm kairomone. The alarm kairomone is constantly

excreted in water by predatory ﬁsh. The basic source of

the substance is skin and skin mucus (Lebedeva and

Chernyakov, 1978). The behavioral response of non-

predatory ﬁsh to the predator smell resembles the

response to the alarm pheromone but differs by smaller

latency (Marusov, 1976; Malyukina et al., 1990). Per-

ceiving this smell, non-predatory ﬁsh obtain informa-

tion about the presence of the predator and avoid the

dangerous area of the water body. It was found that the

smell of ambush predators has a stronger repellent

effect than pursuit predators. In addition to the releaser

effect, the alarm kairomone also has a priming effect,

altering the pigmentation of the ﬁsh, as was found in the

minnow Phoxinus phoxinus presented with the smell of

the pike Esox luceus. A longitudinal black stripe

appears at the lateral side of the body of this ﬁsh in such

a case (Malyukina et al., 1974, 1990; Marusov, 1976;

Lebedeva and Chernyakov, 1978; Kasumyan and Pash-

chenko, 1985). Having perceived the smell of the pred-

ator, many ﬁsh reduce their swimming activity, termi-

nate feeding, and tend to hide in shelters, and subse-

quently avoid the place where the danger was detected

(Magurran, 1989; Keefe, 1993; Mathis and Smith,

1993; Peterson and Brönmark, 1993; Jacher, 1995;

Boyer et al., 2001; Utne and Bacchi, 1997). The joint

presentation of the alarm pheromone and the predator’s

smell increases the repellent effect (Boyer et al., 2001).

Along with the alarm pheromone, a prolonged effect of

the predator’s smell brings about an increase of the

body depth, which reduces the vulnerability of the prey

ﬁsh (Brönmark and Miner, 1992; Holopainen et al.,

1997; Petterson et al., 2000). Not all ﬁsh capable of

determining the presence of the predator by its smell

have the alarm pheromone in their skin (Utne and Bac-

chi, 1997).

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JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

Recent studies revealed the repellent involvement of

another type of smell stimuli in the chemical signaliza-

tion of danger, the so-called stress or fear pheromone.

Fish excrete the stress pheromone in water after the fear

or fright associated with the appearance of a real pred-

ator or demonstration of its visual model (Malyukina

et al., 1983; Lebedeva et al., 1993; Wiesenden et al.,

1995; Jordão and Volpato, 2000; Bryer et al., 2001).

Different species of fugu (Takifugu pardalis, T. poecil-

onotus, T. vermicularis, T. niphobles) secret tetrodot-

oxin which may have a repellent effect on predators

(Kodama et al., 1985). The same role may be played by

certain substances contained in the skin mucus secreted

by Arius thalassinus (Al-Hassan et al., 1982).

Skin wash-out of mammals, especially bears, has a

strong repellent effect on migrating salmon. This chem-

ical factor received the name “the beast skin factor.”

According to the classiﬁcation of chemical signals, it

belongs to the group of kairomones. The presence of this

smell in water may retard the spawning migration of

Paciﬁc salmon for a prolonged time, and in some cases is

used for temporary retardation of ﬁsh migration. It is

hypothesized that the main active component of this

smell is a small peptide containing L-serine amino acid

(Brett and McKinnon, 1954; Idler et al., 1956).

Natural repellents belonging to the group of

allomones, i.e., interspeciﬁc signals favoring the pro-

ducer include the special secret of the Red Sea Moses

sole Pardachirus marmoratus. A white milky-colored

secretion in these small nearshore ﬁsh is secreted by the

gland located at the base of the dorsal and anal ﬁns. The

total volume of secretions in large sole (20 cm and more

in length) can reach 2 ml. The pores via which they are

excreted to the environment are located in the rostral

parts of these ﬁns. The total number of pores exceeds

200. The secretions appear in water after the ﬁsh is

frightened, and have a repellent effect on sharks catch-

ing prey. They never tried to catch live soles, whereas

other ﬁsh serving as lure on a throat line were swal-

lowed almost immediately. The sole could be caught

only several hours after death or if the mucus was

removed from the body. The repellent effect was pro-

nounced both in artiﬁcial conditions (basins) and in

nature. The repellent response was observed in several

species of shark and a few moray eels (Clark, 1981,

1983).

The active component of this secretion, which was

called pardaxine (from Pardachirus) represents a small

peptide composed of 162 amino acids with a molecular

weight of 17 kDa (Primor et al., 1978). Subsequently, it

was found in another sole species, Pardachirus pavoni-

nus, that the secretion may contain three different par-

daxines having the same number of amino acid resi-

dues. All have active surfactant properties and by their

pharmacological properties resemble melittine, the

basic component of bee poison. Several steroid-like

monoglucosides called pavonines were also found in

the secretion, which not only had repellent but also

toxic and hemolytic effects (Tachibana et al., 1984,

1985; Thompson et al., 1986).

The ﬁnding of a natural shark repellent attracted a

lot of attention because multiple attempts to create an

anti-shark repellent had not been successful, in spite of

great effort and means directed to this task (Baldridge,

1990). The need to create or ﬁnd a shark repellent ﬁrst

appeared in the US immediately after participation in

World War II. The US Government, the Navy and the

Air Force directed much attention to rapid solution of

this problem. The fear of being attacked by sharks dur-

ing accidents and military actions on the sea was very

signiﬁcant among the personnel even though the real

threat was minimal. For example, the number of shark

attacks on humans in 2000, the record year for all

recorded history, was less than one hundred, and not all

these attacks resulted in human death.

The ﬁrst experiments directed toward ﬁnding a

shark repellent were conducted in the Woods Hole

Institute of Oceanography, and then on a wider scale, in

Hawaii and the Bahamas in conditions closely resem-

bling natural. A variety of artiﬁcial substances were

tested, along with numerous natural extracts, wash-

outs, biologically active substances, poisons, and irri-

tants. But all these substances either had no effect or

were too inefﬁcient. The strongest repellent effect was

obtained from an extract of rotten shark meat (after 4–

6 days at 20°C) (Gilbert and Gilbert, 1973). Chemical

analysis identiﬁed a large quantity of acetic acid and

copper ions. This became the base for the “Shark

Chaser” repellent, representing a mixture of copper

acetate (20%) and nigrosine stain (80%). Unfortu-

nately, the efﬁciency of this repellent was too low, and

in some cases, e.g., during food excitation of the shark,

it was completely absent. All attempts to create a more

reliable shark repellent were unsuccessful and these

projects were continuously closed. The history of these

studies is described in several publications (Gilbert and

Springer, 1963; Tester, 1963; Hodson and Mathewson,

1981; Sisneros and Nelson, 2001).

Feeding behavior. The long-distance nature of

olfactory reception makes this sensory system

extremely important in obtaining information about

food availability and presence and the selection of the

most appropriate direction to search in. The olfactory

system is the most important for both close and remote

food searching in many ﬁsh species, especially those

with poor vision (night, bottom, deep-sea and some

other ﬁshes) (Groot, 1971).

The behavioral response of ﬁsh to food smells is

very diverse. In less active ﬁsh, which spend most of

their time in shelters waiting for prey, the tendency to

seek out food is weakly pronounced or absent. The per-

ception of the food smell by these ﬁsh is clear from the

alteration of the ﬁsh posture, ﬁn movements, eye move-

ments, increased breath rate, jaw movements, cough,

etc. (Fig. 29) (Atema, 1980; Jones, 1992). In non-terri-

torial freely swimming ﬁsh, the food search is well pro-

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S205

nounced and differs in species with different life strat-

egy and food behavior pattern (Fig. 30) (Atema, 1980;

Kasumyan and Ponomarev, 1989; Pavlov and

Kasumyan, 1998). The sensitivity to food smells is

associated with the life mode of the ﬁsh: the lowest con-

centration threshold is characteristic of benthivorous

ﬁsh, and the highest threshold is characteristic of

pelagic planktivorous ﬁsh, the feeding behavior of

which is primarily based on visual reception (Table 9).

It was found, regarding food smells, that ﬁsh form

an olfactory image of the food objects, i.e., the food

smell provides information not on the presence of some

abstract food object but on a certain speciﬁc prey organ-

ism with speciﬁc behavioral and behavioral character-

istics (McBridge et al., 1962; Atema et al., 1980;

Kasumyan and Ponomarev, 1986a). The ability to form

the olfactory images optimizes the food search and

makes it more efﬁcient, pointing to an important role of

olfaction in the regulation of feeding behavior in ﬁsh.

The experimental support for this conclusion includes

experiments on the study of feeding behavior of ﬁsh to

smells of known and unknown food objects and smells

of different food types (Fig. 31).

Migrations. Olfactory reception is an important

sensory component of the migratory behavior in many

ﬁsh species. Orientation using smell during prolonged

migrations is most pronounced in salmonids, adult indi-

viduals of which return from the areas of feeding in the

sea to their home rivers and their tributaries for spawn-

ing (Hasler, 1966; Stabell, 1992; Døving and Stabell,

2003). This phenomenon, returning to the home area or

the territory, is called homing, whereas erroneous

choice of the spawning place and wandering in differ-

ent locations is called straying.

It is determined that homing in salmonids is based

on olfactory imprinting, an important biological char-

acteristic of many animals representing a speciﬁc form

of learning (Wisby and Hasler, 1954; Hasler and

Scholz, 1983). Imprinting was discovered by renowned

Austrian zoologist, the 1973 Noble Prize winner Kon-

rad Lorenz. Imprinting occurs in animals during the so-

called sensitive period, a limited period of time when it

is possible.

Imprinting of the home smell in salmonid ﬁsh

occurs during the short period of time when juveniles

terminate their period of life in the fresh water and pre-

pare for downstream migration to the sea (Hasler and

Scholz, 1983). This period is called smoltiﬁcation, and

is marked by a complex of physiological and biochem-

ical processes preparing the ﬁsh for marine life. Smolt-

iﬁcation is controlled by the hormonal system (thyroid

hormones) (Scholz et al., 1985; Yamauchi et al., 1985).

Technically very complex, prolonged studies (includ-

ing observation of homing and straying in anosmic and

intact salmons, imprinting of juveniles to an artiﬁcial

substance morpholone, transition of the migrating juve-

niles from one river system to another, etc.) indicated

that the sensitive period in salmon smolts may last from

several days to a few hours. It was hypothesized that not

only the smell of the home area of the river is imprinted,

but also the whole pathway of the migrating ﬁsh from

the home area to the river mouth (Harden Jones, 1968;

Hansen et al., 1987; Quinn et al., 1989). These smells

serve as points of orientation for the returning adults

not only in the river but also in the open sea (Wisby and

Hasler, 1954; Groves et al., 1968; Døving et al., 1985;

Stabell, 1992; Døving and Stabell, 2003). It was

hypothesized that the smell of the home river is

imprinted by juvenile sturgeon as well (Boiko et al.,

1993; Kasumyan, 1999).

Chemical markers of the home spawning site

include speciﬁc smells of this area. It was proposed that

the smell is created by substances appearing in water by

wash-outs or drains from adjacent land areas, along

with extracts of local aquatic plants and animals

(Hasler and Scholz, 1983). Electrophysiological exper-

iments indicated that samples of fresh water taken from

different water bodies cause responses of different

intensities in the olfactory system of salmonid ﬁsh, not

only in adults (Sato et al., 2000). There is also a phero-

Unfolding Small shifts and

Increased respiration

Barbel

Mouth

Rapid eye

movements

and moving fins posture alterations

frequency

movements

openings, cough

Fig. 29. Characteristics of the behavioral response to food

smells in inactive ﬁsh or ambush predators.

Table 9. Olfactory sensitivity of ﬁsh with different life

modes to water extract of food (Chironomidae larvae)

Species Threshold

concentration, g/l

carp Cyrpinys carpio 10–4–10–5

goldﬁsh Carassius auratus 10–4

Russian sturgeon

Acipenser gueldenstaedtii 10–4

Stellate sturgeon Acipenser stellatus 10–4

Minnow Phoxinus phoxinus 10–4

Gudgeon Gobio gobio 10–4

grass carp Ctenopharyngodon idella 10–3

verkhovka Leucaspius delineatus 10–2

Beluga Huso huso 10–1–10–2

paddleﬁsh Polyodon shathula 10–1–10–2

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JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

mone homing hypothesis proposed by Norwegian zool-

ogist Hans Nording, that the smell of the home popula-

tion living in the river is the orientation marker for

migrating adults (Nording, 1971, 1977). This hypothe-

sis is probably not universal and cannot be applied to

cases when young leave the river long before the begin-

ning of the spawning migration of adults, as, for exam-

ple, in the pink salmon Oncorhynchus gorbuscha.

(a)

(b) (c)

(e)(d)

(f) (g)

Fig. 30. Feeding behavior of ﬁsh with different ecology after stimulation with food smells: (a) carp Cyprinus carpio, goldﬁsh Car-

assius auratus, (c) minnow Phoxinus phoxinus, (d) zebraﬁsh Brachydanio rerio, (e) verkhovka Leucaspius delineatus, (f) chum

salmon Oncorhynchus keta, (g) grayling Thymallus thymnallus, (h) and (i) paddleﬁsh Polyodon spathula. The light silhouette is the

behavior of the ﬁsh in the pre-stimulus period, dark silhouette, during the search response.

Bloodworms extract Duckweed extract

Fig. 31. Food search behavior of the grass carp Ctenopharyngodon idella stimulated by extract of bloodworms (Chironomidae lar-

vae) and duckweed Lemna minor.

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S207

However, the orientation markers for such ﬁsh may be

bile acids or their derivatives, which could be retained

for a long time in feces left in the river by juveniles

which had previously left for the sea for feeding (Døv-

ing, personal communication).

Olfaction plays an important role in the migration

behavior of the marine lamprey Petromyzon marinus. It

was found that for spawning, adult lampreys enter only

the rivers or their tributaries inhabited by conspeciﬁc

ammocete larvae. Feeding larvae constantly excrete

several speciﬁc derivates of bile acids. The chemical

markers for adult lampreys include petromyzonole

(3α7α12α24-tetrahydroxy-5α-cholan-24-sulphate) and

allocholic acid (3α7α12α-trihydroxy-5α-cholan-24-ic

acid). These substances are excreted only by larvae and

cannot be found in excretes of lampreys after metamor-

phosis. Petromyzole sulphate and allocholic acid are

perceived with olfaction (Bjerselius et al., 2000; Li

et al., 1995, 2002). It was found that each ammocete

larva on average excretes these substances with a rate of

16 and 5 ng/h, respectively, which is quite enough for

supra-threshold concentrations of the pheromone

(Polkinghorne et al., 2001). However, the characteristic

sexual behavior in female lampreys is observed only in

response to conspeciﬁc males ready for spawning,

excreting sexual pheromone 7α12α24-tetrahydroxy-

5α-cholan-3-on-24-sulphate (3-ketopteromyzonol sul-

phate) (Li et al., 2002; Yun et al., 2002; Siefkes et al.,

2003).

The species smell produced by adult conspeciﬁcs is

the chemical marker for the catadromous ﬁsh Galaxis

fasciatus returning to the home river. This ﬁsh migrates

to the sea after hatching (Baker and Montgomery,

2001b). The attracting stimulus for the glass eels

Anguilla anguilla migrating from the sea to fresh water

may include such natural substances as geosmine and

different pyrazines or thyazoles, which are excreted by

different microorganisms. The sensitivity of ﬁsh to

them reaches 10–9–10–13 mg/l (Tsoi and Sola, 1993;

Sola, 1995).

Territorial behavior. Many ﬁsh are resident and

keep to their home ranges. They are often characterized

by aggressiveness to conspeciﬁcs approaching the resi-

dent’s territory. Some territorial ﬁsh use smells to mark

their home territory. Such smell marks bear the infor-

mation that this territory is occupied. This reduces the

intensity of aggressive contacts within the population.

Additionally, smell marks help ﬁsh not only to protect

their territory from intruders, but also to return if they,

for some reason, need to leave due to feeding migra-

tion, fright, or being moved by the current. Resident

juvenile salmon can mark their territories in rivers by

substances (bile acids and their derivates) which enter

the water with feces (Døving et al., 1980; Seleset,

1980; Seleset and Døving, 1980; Foster, 1985; Stabell,

1987; Courtenay et al., 1997). Removal of the olfactory

organ signiﬁcantly reduces the ability of the ﬁsh (trout

Salmo trutta) to return to their home range (Halvorsen

and Stabell, 1990). In some marine nearshore ﬁsh, ter-

ritorial marking could also depend on bile acids or their

derivatives excreted with feces (Døving, personal com-

munication) or substances from the skin mucus left by

the ﬁsh on stones and other objects.

Olfaction plays the most important role in choosing

the host actinia in clownﬁsh Amphiprion and related

representatives of the genus Premnas (Pomacentridae).

These ﬁsh are territorial and spend most of the time

defended by their actinia. The eggs develop in proxim-

ity to the actinia, but early juveniles do not stay there

and are distributed by currents immediately after hatch-

ing. Reaching a certain age, juveniles return to the reef

zone and easily ﬁnd host actinias. For example,

Amphiprion melanopus usually lives among the tenta-

cles of Entacmaea quadricolor, more rarely, two other

species of actinias, Heteractic crispa and H. magniﬁca.

The errorless choice of the host actinia occurs due to an

innate preference for a speciﬁc actinia smell, which is

further increased by imprinting when the ﬁsh emerge

(Arvedlund and Nielsen, 1996; Arvedlund et al., 1999).

Attempts to artiﬁcially imprint the ﬁsh to the smell of

an actinia which the ﬁsh never encounter in nature were

not successful. The substances causing the actinia smell

which is distinguished by the ﬁsh have been synthe-

sized (amphicumines and their analogues, Murata

et al., 1986; Konno et al., 1990). These chemical sig-

nals with interspeciﬁc effects belong to the category of

allomones.

The Ontogeny of the Olfactory System

Structure development. The development of the

olfactory system begins early in the mid-embryonic

period when the olfactory placode, from which the

future olfactory organ develops, becomes easily dis-

cernible (Zeiske et al., 2003). The olfactory depression

appears in the central part of the placode, either because

of invagination of the outer cell layer or by ﬁrst the

appearance of a cavity and then widening as the cover-

ing cells ﬂake away. The depth and size of the olfactory

depression rapidly increases, and the ﬁrst specialized

cells, including receptor, cells, ciliated nonsensory

cells, supporting, and mucous cells, form (Fig. 32). Up

to the moment of hatching, the number of cells in the

olfactory organ signiﬁcantly increases. Further increase

of the size of the olfactory depression occurs, the ﬁrst

olfactory lamella (raphe) appear, then their number and

size increase, which also increases the number of olfac-

tory receptor cells. The olfactory rosette is formed, and

then the unitary olfactory opening is split into the ante-

rior and posterior nostrils (Teichmann, 1954; Pfeiffer,

1963, 1964; Evans et al., 1982; Zelinski and Hara,

1988; Hansen and Zeiske, 1993; Werner and Lannoo,

1994; Appelbaum and Reihl, 1997; Arvedlund et al.,

2000). In cyprinid ﬁshes, for example, the ﬁrst olfac-

tory raphe appears in the middle of the larval period of

development (stage D1 in the minnow Phoxinus phoxi-

nus and shemaya Chalcalburnus chalcoides, D2 in the

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JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

grass carp Ctenopharyngodon idella, silver carp

Hypophthalmichthys molitrix and carp Cyprinus car-

pio, E in bitterling Rhodeus sericeus. The merging of

the superﬁcial outgrowths and the development of the

nasal split occurs at the end of the larval or at the begin-

ning of the fry period (stages E and F). The ﬁrst side

lamellae, symmetrical with respect to the central raphe,

appear at this time. In this way, the ﬁrst olfactory rosette

consisting of three lamellae appears. Further develop-

ment of new lamellae also occurs in pairs, one from

each side of the central raphe. During the end of the

second fry period of development, the nasal ridge

develops in the nasal split, the number of lamellae in

the rosette becomes even more, seven, and begins to

resemble the rosette of adult individuals by its struc-

ture. The olfactory organ takes a deﬁnitive form (Pash-

chenko and Kasumyan, 1983, 1986).

With further growth of the ﬁsh, the size of the olfac-

tory organ also increases, as does the number of lamel-

lae in the rosette (Fig. 33) (Halama, 1982).The receptor

structures become stronger with the development of the

olfactory organ and its basic structures, especially rap-

idly after the development of the ﬁrst lamellae (Fig.

34). In ﬂatﬁshes, the olfactory organ at the eyed side of

the body develops more rapidly than on the blind side

(Harvey, 1996).

Function development. The terms of development

of the olfactory functions have been quite thoroughly

studied. According to these data, the ability to respond

to olfactory stimuli develops in the olfactory organ

when the ﬁrst receptor cells appear.

It has been found that even before transition to

external feeding, prolarvae of several marine ﬁshes

(cod Gadus morhua, Scophtalmus maximus) shows

nonspecialized behavioral responses to such chemical

stimuli as food extracts and free amino acids. The

responses of prolarvae to these stimuli is expressed in

slower swimming, reduction of discrete swimming

movements, reduction of the distance moved per motor

act, and reduction of the distance between the position

of the ﬁsh in three-dimensional space during observa-

tion (Fig. 35). It is hypothesized that such alterations of

locomotor activity cause prolarvae that should soon

switch to external feeding to lag in the zone of the smell

created by potential food objects. The adaptive sense of

this behavior includes an increase in the probability of

(a) (b)

(e) (f)

Fig. 32. Development of the olfactory organ in the Siberian

sturgeon Acipenser baerii: (a) and (b) head part of the

embryo and the olfactory depression (age, 110 h); (c) and

(d) olfactory depression (age 132 and 156 h); (e) and (f) cil-

iated receptor cells and ciliated nonsensory cells (age 120 h).

10 Body length, cm

20 40 50 60 70

Number of olfactory lamellae

30 80

Fig. 33. Increase of the number of olfactory lamellae in the

ontogeny of the grass carp Ctenopharyngodon idella (from

Pashchenko, 1986).

2500

60 Body length, mm

20 100 140 180

500

3500

5500

Number of receptor cells, thousands

4500

1500

Fig. 34. Increase of the number of receptor cells in the

ontogeny of the grass carp Ctenopharyngodon idella (from

Pashchenko, 1986).

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THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S209

food detection during the critically important period of

transition to external feeding (Døving et al., 1994;

Kasumyan et al., 1998).

The development of specialized behavioral

responses to olfactory stimuli begins later, during the

larval period of development. The age of the appear-

ance and development of the olfactory sensitivity to dif-

ferent smells differs. For example, it has been shown in

many cyprinid ﬁsh species that the young begin to

respond to the alarm pheromone at the beginning of the

larval period, in the period of mixed feeding (Fig. 36).

Sensitivity to the alarm pheromone (as well as to the

alarm kairomone) develops slowly and ﬁnishes only in

ﬁngerlings or yearlings. The defensive response to nat-

ural chemical signals of danger forms more slowly than

the ability to detect threshold concentrations of these

smells. Even more time is required for the ﬁsh to

acquire the ability to distinguish the alarm pheromones

of different species (Fig. 37) (Pashchenko and

Kasumyan, 1983, 1986; Døving et al., 2004).

Juveniles begin to respond to food at the same age,

during the prolarval stage. It is clear by the example of

chemical stimuli that development of the olfactory sen-

sitivity occurs in close relationship with the ecology of

juveniles and their general sensory equipment. For

example, responses to food stimuli develop earlier and

more quickly in ﬁsh to which olfaction has a major sig-

niﬁcance in feeding behavior (Fig. 38). For example,

the response to the food odor in sturgeons, whose feed-

ing behavior is signiﬁcantly based on olfaction, appears

just after the transition of larvae to external feeding, and

the sensitivity reaches the deﬁnitive level in the middle

Control

End

Start

010

10–5 M

20 30 40 50 60

End

Start

10–9 M End

Start

10–8 M

End

Start

10–4 M

20 30 40 50 60

End

Start

10–3 M

20 30 40 50 60

End

Start

Distance, mm

Fig. 35. Trajectory of cod Gadus morhua prolarvae stimulated by different concentrations of L-arginine amino acid solutions. Con-

trol: movement of prolarvae in artiﬁcial sea water; End and Start: beginning and termination of observation period, the duration of

recording 1 min. Points depict short-term stops of prolarvae (from Døving et al., 1994).

10–1

30 50 70 90

Body length, mm

Larval Fry period

10–3

10–5

10–7

10–9

Concentration of skin extract, g/l

period

Fig. 36. Change of sensitivity to the alarm pheromone in the

ontogeny of the grass carp Ctenopharyngodon idella (1),

bitterling Rhodeus sericeus (2), kutum Rutilus frisii kutum

(3), zherekh Aspius aspius (4), shemaya Chalcalburnus

chalcoides (5), silver carp Hypophthalmichthys molitrix (6)

(from Kasumyan, 1982).

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JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

of the second month of the juveniles’ life (Kasumyan

and Kazhlayev, 1993; Kasumyan and Tauﬁk, 1994;

Kasumyan, 1999). The sensitivity to food odor devel-

ops less rapidly in cyprinid bentivorous ﬁsh (carp Cyp-

rinus carpio) and even slower in pelagic planktivorous

ﬁsh, for which visual reception is of greater value not

only in juveniles but also in adults (zebraﬁsh Brachy-

danio rerio) (Kasumyan and Ponomarev, 1990).

Effect of Pollutants and Other Destructive Factors

to the Olfactory System

Olfactory receptors are open to the environment and

are susceptible to the effects of different unfavorable

environmental factors, both biological and abiotic. Dif-

ferent organisms may live in the olfactory organ (bacte-

ria, microsporidia, crustaceans) and disturb or elimi-

nate a signiﬁcant part of the olfactory epithelium

(Devitsyna, 1977; Doroshenko and Pinchuk, 1978;

Pashchenko and Kasumyan, 1984; Baatrup and Døv-

ing, 1990; Klaprat at al., 1992; Morrison and Plumb,

1994; Watson et al., 1998). Various chemical pollut-

ants, such as heavy metals and detergents, are very dan-

gerous (Baatrup et al., 1990; Klaprat et al., 1992; Døv-

ing, 1991; Winberg et al., 1992; Kasumyan, 2001).

Even short-term (for few minutes or seconds) effects of

such substances cause rapid degeneration of the olfac-

10–1 10–3 10–5

Larvae, 8–10 mm

intensity, points

Fright reaction

10–1 10–3 10–5

Fry, 16–18 mm

10–1 10–3 10–5

Fry, 25–30 mm

***

10–1 10–3 10–5

Adults, 35–40 mm

***

Bitterling skin

Spined loach skin

Concentration of skin extract, g/l

Fig. 37. The intensity of the fright reaction in the bitterling Rhodeus sericeus amarus of different age groups to the extract of con-

speciﬁc skin and skin of spined loach Cobitis sp. (from Kasumyan and Ponomarev, 1986b). *, **, *** Signiﬁcant differences from

the control, respectively, p < 0.05; p < 0.01; p < 0.001.

2Body length, cm

4 6 8 10 12

Threshold concentration of food extract, g/l, –lg

Fig. 38. Increase of the olfactory sensitivity to chemical

food signals in the ontogeny of carp (1) and sturgeon (2).

intensity, points

Fright reaction

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S211

tory epithelium, as well as the destruction of cilia and

microvilli of receptor cells and kinocilia of ciliated

nonsensory cells, and, as a consequence, the complete

loss of the ability to perceive chemical stimuli by the

ﬁsh (baker and Montgomery, 2001; Beyers and Farmer,

2001).

The loss of sensitivity caused by pollutants is revers-

ible and olfaction may be restored after several hours.

Regeneration occurs due to the formation of new recep-

tor cells and other cell types from the basal cells. The

restoration of the olfactory function may be so rapid as

to outstrip the regeneration of the cellular structures of

the olfactory epithelium (Fig. 39). It was found that

only 1/3 of the overall number of receptor elements

found in intact ﬁsh is enough for normal sensitivity to

smells (Kasumyan and Pashchenko, 1982; Pashchenko

and Kasumyan, 1984). The ability to regenerate and the

ability to restore a normal level of sensitivity due to the

receptor cells pool are extremely important adaptive

mechanisms increasing the functional reliability of the

olfactory system, allowing the ﬁsh to obtain diverse

information from the environment (Kasumyan, 1991).

ACKNOWLEDGMENTS

The author is very grateful to E.A. Marusov for

valuable criticism on the manuscript. This work was

partly supported by the program “Leading scientiﬁc

schools” (project NSh-1334.2003.4) and the program

“Universities of Russia” (topic UR.07.03.011).

REFERENCES

1. M. A. Adams, J. H. Teeter, Y. Katz, and P. B. Johnsen,

Sex Pheromone of the Sea Lamprey (Petromyzon mari-

nus): Steroid Studies, J. Chem. Ecol. 13, 387–395

(1987).

2. J. M. Al Hassan, M. Thomson, and R. S. Criddle, “Com-

position of Proteinaceous Gel Secretion from the Skin

of the Arabian Gulf catﬁsh (Arius thalassinus),” Mar.

Biol. 70, 27–33 (1982).

3. A. C. Allison and R. T. T. Warwick, “Quantitative

Observations on the Olfactory System of the Rabbit,”

Brain. 72, 186–197 (1949).

4. A. P. Andriyashev, “Role of Sensory Organs in the Food

Search of the Silver Rockling,” Zh. Obshch. Biol. 5,

123–127 (1944).

5. A. P. Andriyashev, “Role of the Sensory Organs in Food

Search of Fish,” Proc. Workshop on Methods for the

Study of the Food Resources of Fish Stocks (Acad.

Nauk SSSR, Moscow, 1955), pp. 135–142.

6. S. Appelbaum and R. Riehl, “Scanning Electron Micro-

scopic Observations of the Chemo-and Mechanorecep-

tors of Carp Larvae (Cyprinus carpio) and their Rela-

tionship to Early Behaviour,” Aquat. Living Resour. 10,

1–12 (1997).

7. C. W. Appelt and P. W. Sorensen, “Freshwater Fish

Release Urinary Pheromones in a Pulsatile Manner,” in

Advances in Chemical Signals in Vertebrates, Ed. by

R. E. Johnston, D. Muller-Schwartze, and P. W. Sorensen,

(Kluwer, New York, 1999), pp. 247–256.

8. M. P. Aronov, Role of Sensory Organs in Food Search

of the Drum Corvina umbra, Vopr. Ikhtiol. 1, 194–199

(1962).

9. M. P. Aronov, “Role of Sensory Organs in Obtaining

Food in Fish,” Usp. Sovrem. Biol. 54, 128–145 (1962).

10. M. Arvedlund, K. Larsen, and H. Winsor, “The Embry-

onic Development of the Olfactory System in Amphip-

rion melanops (Perciformes: Pomacentridae) Related to

the Host Imprinting Hypothesis,” J. Mar. Biol. Ass. U.

K. 80, 1103–1110 (2000).

11. M. Arvedlund, M. I. McCormick, D. G. Fautin, and

M. Bildsee, “Host Recognition and Possible Imprinting in

the Anemoneﬁsh Amphiprion melanopus (Pisces: Poma-

centridae),” Mar. Ecol. Prog. Ser. 188, 207–218 (1999).

12. M. Arvedlund and L. E. Nielsen, “Do the Anemoneﬁsh

Amphipnon ocellaris (Pisces: Pomacentridae) Imprint

Themselves to Their Host Sea Anemone Heteractis

magniﬁcii (Anthozon: Actinidae)?” Ethology 102, 197–

211 (1996).

13. J. Atema, “Chemical Senses, Chemical Signals and

Feeding Behaviour in Fishes,” in Fish Behaviour and its

Use in the Capture and Culture of Fishes, (Manila,

1980), pp. 57–101.

14. J. Atema, “Distribution of Chemical Stimuli,” in Sen-

sory Biology of Aquatic Animals Ed. by J. Atema,

A. N. Popper, R. R. Fay, and W. N. Tavolga, (Springer,

New York, 1988), pp. 29–56.

15. J. Atema, K. Holland, and W. Ikehara, “Olfactory

Responses of Yellowﬁn Tuna (Thunnus albacares) to

Prey Odors: Chemical Search Image,” J. Chem. Ecol. 6,

457–465 (1980).

16. J. W. Atz, “Internal Nares in the Teleost Astroscopus,”

Anat. Rec. 113, 105–115 (1952a).

17. J. W. Atz, “Natural Breathing in Fishes and the Evolu-

tion of Internal Nares,” Q. Rev. Biol. 27, 366–377

(1952b).

18. E. Baatrup and K. B. Døving, “Histochemical Demon-

stration of Mecury in the Olfactory System of Salmon

123456

100

Number of receptor cells, %

Concentration of pheromone –lg/l

Time, days

Fig. 39. Increase of the sensitivity to the alarm pheromone

(1) and the number of olfactory receptor cells (2) in the

grass carp Ctenopharyngodon idella after treatment of the

olfactory epithelium with the detergent Triton X-100 (from

Pashchenko and Kasumyan, 1984).

S212

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

(Salmo salar L.) Following Treatments with Dietary

Methylmercuric Chloride and Dissolved Mercuric

Chloride,” Ecotoxicol. Environ. Safety 20, 277–289

(1990).

19. E. Baatrup, K.B. Døving, and S. Winberg, “Differential

Effects of Mercurial Compounds on the Electroolfacto-

gram (EOG) of Salmon (Salmo salar L.),” Ecotoxicol.

Environ. Safety 20, 269–276 (1990).

20. R. C. Baird, G. Y. Jumper, and E. E. Gallaher, “Sexual

Dimorphism and Demography in two Species of Oce-

anic Midwater Fishes (Stomiiformes: Stemoptychidae)

from the Eastern Gulf of Mexico,” Bull. Mar. Sci. 47,

561–566 (1990)

21. C. F. Baker and J. C. Montgomery, Sensory Deﬁcits

Induced by Cadmium in Banded Kokopu, Galaxias fas-

ciatus, Juveniles, Environm. Biol. Fishaa. 62, 455–464

(2001a).

22. C. F. Baker and J. C. Montgomery, “Species-Speciﬁc

Attraction of Migratory Banded Kokopu Juveniles to

Adult Pheromones,” J. Fish Biol. 58, 1221–1229

(2001b).

23. E. K. Bakhtin, “Characteristics of Microstructure of the

Olfactory Organin the Dogﬁsh Squalus acanthias,” Tsi-

tologiya 19, 725–731 (1977).

24. E. K. Bakhtin and E. E. Filyushina, “Ultrastructural

Characteristics of Sectret Formation in Minor Secret

Cellsof the Olfactory Epithelium of Zander and Perch,”

Tsitologiya 16, 90–93 (1974).

25. H. D. Baldridge, “Shark Repellent: Not Yet, Maybe

Never,” Military Medicine 155, 358–361 (1990).

26. L. H. Bannister, The Fine Structure of the Olfactory

Surface of Teleostean Fishes, Quart J. Micr. Sci. 106,

333–342 (1965).

27. G. P. Barbin, “The Role of Olfaction in Homing and

Estuarine Migratory Behavior of Yellow-Phase Ameri-

can Eels,” Can. J. Fish. Aquat. Sci. 55, 564–575 (1998).

28. J. E. Bardach and J. Case, Sensory Capabilities of the

Modiﬁed Fins of Squirrel Hake (Urophycis chuss) and

Searobins (Prionotus carolinus and P. evolans), Copeia,

No. 2, 194–206 (1965).

29. J. E. Bardach and J. H. Todd, “Chemical Communica-

tion in Fish,” in Communication by Chemical Signals,

Ed. by J. W. Johnston jun., D. G. Moulton R.A., and

A. Turk (Appelton-Century-Crofts., New York, 1970),

pp. 205-240.

30. D. P. Bashor, R. W. Beuerman, and D. M. Easton, “Cil-

iary Action and Normal Movement of Odorant Wave

Fronts in Garﬁsh Nasal Capsule of Lepisosteus asseus,”

Experientia 30, 777–779 (1974).

31. E. Bertelsen, “Notes on Linophrynidae V: A Revision of

the Deepsea Anglerﬁshes of the Linophryne arbrifera

Group (Pisccs, Ceralioidei),” Steenstrupia 6, 29–70

(1980).

32. E. Bertelsen and J. G. Nielsen, “The Deep Sea Eel Fam-

ily Monognathidae (Pisces, AnguillifonDes),” Steen-

strupia 13, 141–198 (1987).

33. R. Berti, R. Vezzosi, and A. Ercolmi, “Locomotory

Response of Phreatichthys andruzzii Vinciguerra

(Pisces, Cyprinidae) to Chemical Signals of Conspecif-

ics and Closely Related Species,” Experientia 45, 205–

207 (1989).

34. R. Berti and L. Zom, “Locomotory Responses of the

Cave Cyprinid Phreatichthys andruzzii to Chemical sig-

nals from Conspeciﬁcs and Species: New Findings,”

Environai. Biol. Fisher. 62, 107–114 (2001).

35. G. Bertmar, “The Vertebrate Nose, Remarks on Its

Structural and Functional Adaptation and Evolution,”

Evolution. 23, 131–152 (1969).

36. G. Bertmar, “Ecostructural Studies on Olfactory Organ

in Young and Adult Sea Trout (Osteichthyes, Salmo-

nidae),” Z. Morphol. Okol. Tiere. 72, 307–330 (1972).

37. D. W. Beyers and M. S. Fanner, “Effects of Copper on

Olfaction of Colorado Pikeminnow,” Environm. Toxi-

col. Chem. 20, 907–912 (2001).

38. R. Bjerselius, W. Li, J. H. Teeter, J. G. Seely, et al.,

“Direct Behavioral Evidence that Unique Bile Acids

Released by Larval Sea Lamprey Function as a Migra-

tory Pheromone,” Can. J. Fish. Aquat. Sci. 57, 1–14

(2000).

39. H. D. Bloom and A. Perlmutter, “Possible Pheromone

Mediated Reproductive Isolation in two Species of

Cyprinid Fishes of the Genus Brachydanio,” J. Fish

Biol. 13, 47–50 (1978).

40. N. E. Boiko, R. A. Grigoryan, and A. S. Chikhachev,

Olafctory Imprinting in Juveniles of the Russian Stur-

geon Acipenser guldenstadti, Zh. Evol. Biokhim. Fiz-

iol. 29, 509–513 (1993).

41. J. G. Brand and R. C. Bruch, “Molecular Mechanisms

of Chemosensory Transduction: Gestation and Olfac-

tion,” in Fish Chemoreception, Ed. by T. J. Hara (Chap-

man and Hall, London, 1992), pp. 126–149.

42. J. R. Brett and D. McKinnon, “Some Aspects of Olfac-

tory Perception in Migrating Adult Coho and Spring

Salmon,” J. Fish. Res. Bd. Can. 11, 310–318 (1954)

43. C. Brönmark and L. B. Miner, “Predator-Induced Phe-

notypical Change in Body Morphology in Crucian

Carp,” Science 258, 1348–1350 (1992).

44. A. A. Bronstein Olfactory Receptors of Vertebrates

(Nauka, Leningrad, 1977) [in Russian].

45. A. A. Bronstein, “Some Peculiarities of Fine Structure

of the Olfactory Organ in Elasmobranches,” J. Evol.

Biochem. Physiol. 12, 63–67 (1976).

46. A. Brunn, von, “Beitrage zur mikroskopischen Anat-

omie der menschlichen Nasenhöhle,” Arch. Mikr. Anat

39, 632–651 (1892).

47. P. J. Bryer, R. S. Mirza, and D. P. Chivers, “Chemosen-

sory Assessment of Predation Risk by Slimy Sculpins

(Cottus cognatus): Responses to Alarm, Disturbance

and Predator Cues,” J. Chem. Ecol, 27, 533–546 (2001).

48. R. H. Bume, “The Anatomy of the Olfactory Organ of

Teleostean Fishes,” Proc. Zool. Soc. London. 2, 610–

663 (1909).

49. A. V. M. Canario and A. P. Scott, “Conjugates of Ova-

rian Steroids, Including 17α,20β-dihydroxy-4-pregnen-

3-one (Maturation-Inducing Steroid), Accumulate in

the Urine of a Marine Teleost (Plaice, Pleuronectes pla-

tessa),” J. Endocrinol. 123, 1–4 (1989).

50. P. Cancalon, “Degeneration and Regeneration of the

Olfactory Cells Induced by ZnSO4 and Other Chemi-

cals,” Tissue and Cell. 14, 717–733 (1982).

51. J. Caprio, “Olfaction and Taste in the Channel Catﬁsh:

an Electrophysiological Study of the Responses to

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S213

Amino Acids and Derivates,” J. Comp. Physiol. 123,

357–371 (1978).

52. J. Caprio, “Similarity of Olfactory Receptor Responses

(EOG) of Freshwater and Marine Catﬁsh to Amino

Acids,” Can. J. Zool. 58, 1778–1784 (1980).

53. J. Caprio, “High Sensitivity and Speciﬁcity of Olfactory

and Gustatory Receptors of Catﬁsh to Amino Acids,” in

Chemoreception in Fishes, Ed. by T. J. Hara (Elsevier,

Amsterdam, 1982), pp. 109–134.

54. J. Caprio, “Olfaction and Taste in Fish,” in Comparative

Physiology of Sensory systems, Ed. by L. Bolis, R. D. Key-

nes, and S. H. P. Maddrell (Cambridge Univ. Press,

Cambridge, 1984), pp. 257–283.

55. J. Caprio and R. Bird, Jr., “Electrophysiological Evi-

dence Far Acidic, Basic and Natural Amino Acid Olfac-

tory Receptor Sites in the Catﬁsh,” J. Gen. Physiol. 84,

403–422 (1984).

56. M. G. Carr and J. E. Carr, “Individual Recognition in

the Jnvenue Brown Bullhead (Ictalums nebulosus),”

Copeia, No. 4, 1060–1062 (1985)

57. W. E. S. Carr, J. C. III. Netherton, R. A. Gleeson, and

C. D. Derby, “Stimulants of Feeding Behavior in Fish:

Analyses of Tissues of Diverse Marine Organisms,”

Biol. Bull. 190, 149–160 (1996).

58. J. H. Caruso, “Sexual Dimorphism of the Olfactory

Organs of Lophiids,” Copeia, 380–381 (1975).

59. X.-Y.Chen and G. Arratia, “Olfactory Organ of Aci-

penseriformes and Comparison with other Actinoptery-

gians: Patterns of Diversity,” J. Morphol. 222, 241–267

(1994).

60. D. P. Chivers and R. J. F. Smith, “Chemical Alarm Sig-

nalling in Aquatic Predator-Prey Systems: A Review

and Prospectus,” Ecoscience 5, 338–352 (1998).

61. E. Clark, “Shark Repellent Effect of the Red Sea Moses

Sole, Pardachirus mannoratus,” Nat. Geogr. Soc. Res.

Rep. 13, 177–186 (1981).

62. E. Clark, “Shark Repellent Effect of the Red Sea Moses

Sole,” in Shark Repellents from the Sea: New Perspec-

tives, Ed. by B. J. Zahuranec (Westview Press, Boulder,

1983), pp. 135–150.

63. L. Colombo, A. Muconato, B. P. Colombo, and C. Friso,

“Endocrinology of Teleost Reproduction: A Testicular

Steroid Pheromone in the Black Goby Gobius jozo L.,”

Bol. Zool. 47, 355–364 (1980).

64. S. C. Courtenay, T. P. Quinn, H. M. C. Dupuis, et al.,

“Factors Affecting the Recognition of Population-Spe-

ciﬁc Odours by Juvenile Coho Salmon,” J. Fish Biol.

50, 1042–1060 (1997).

65. S. C. Courtenay, T. P. Quinn, H. M. C.Dupuis, et al.,

“Discrimination of Familty-Speciﬁc Odours by Juve-

nile Coho Salmon: Roles of Learning and Odour Con-

centration,” J. Fish Biol. 58, 107–125 (2001).

66. U. Dahlgren, “The Oral Opening of the Nasal Cavity in

Astroscopus,” Science 27, 993–994 (1908).

67. M. De Fraipont and G. Thines, “Responses of the Cave-

ﬁsh Astyanax mexicanus (Anoptichthys antrobius) to

the Odor of Known and Unknown Conspeciﬁcs,” Expe-

rientia 42, 1053–1054 (1986).

68. J. H. Derivot, “Functional Anatomy of the Peripheral

Olfactory System of the African Lungﬁsh Protopterus

annectens Owen: Macroscopic, Microscopic, and Mor-

phometric Aspects,” Am. J. Anat. 169, 177–192 (1984).

69. G. V. Devitsyna, “Morphology of the Olfactory Organ

in Cods (fam. Gadidae),” Vopr. Ikhtiol. 12, 1094–1103

(1972).

70. G. V. Devitsyna, “Comparative Study of Olfactory Ana-

lyzer Morphology in Fish,” Vopr. Ikhtiol. 17, 129–133

(1977).

71. G. V. Devitsyna and A. A. Kazhlayev, “Development of

Chemosensory Organs in the Siberian Sturgeon Aci-

penser baeri and Stellate Sturgeon A. stellatus,” Vopr.

Ikhtiol. 32, 167–176 (1992).

72. G. V. Devitsyna and A. A. Kazhlayev, “Chemoreception

Organs in Early Juveniles of Paddleﬁsh Polyodon

spathula,” Vopr. Ikhtiol. 33, 142–146 (1993).

73. G. V. Devitsyna and G.A. Malyukina, Functional Orga-

nization of the Olfactory Organ in Fish Micro and Mac-

rosmatics, Vopr. Ikhtiol. 17, 493–502 (1977).

74. G. V. Devitsyna and A. B. Al Attar el Saied, “Cytoarchi-

tectonics and Morphometry of the Olfactory Analyzer

of Fish Micro- and Macrosmatics,” Vopr. Ikhtiol. 28,

837–845 (1988).

75. A. S. Dogel, The Structure of the Olfactory Organ in

Ganoids, Teleost Fish, and Amphibians, Tr. Obshch.

Estestvoispyt pri Kazan Univ. 16, 3–82 (1886).

76. M. A. Doroshenko and L. E. Pinchuk, “New Data on

Secretory Elements of the Olfactory Epithelium of

Some Marine Fish,” Dokl. Akad. Nauk SSSR, 219,

756–758 (1974).

77. M. A. Doroshenko and L. E. Pinchuk, “Characteristics

of Morphology of the Olfactory Epithelium of Marine

Fish Disturbed by Microsporidias,” Biol. Morya, No. 3,

88 (1978).

78. K. B. Døving, “The Inﬂuence of Olfactory Stimuli upon

the Activity of Secondary Neurons in the Burbot (Lota

lota L.),” Acta Physiol. Scand. 66, 290–299 (1966).

79. K. B. Døving, “Functional Properties of the Fish Olfac-

tory System,” in Progress in Sensory Physiology, Vol. 6,

Ed. by D. Ottoson (Springer, Berlin, 1986), pp. 39–104.

80. K. B. Døving, “Molecular Cues in Salmonid Migra-

tion,” in Molecules in Physics, Chemistry and Biology,

Ed. By Jean Maruani. Vol. IV (Academic Press, 1989),

pp. 299–329.

81. K. B. Døving, “Assessment of Animal Behaviour as a

Method to Indicate Environmental Toxocoty,” Compar.

Biochem. and Physiol. 100, 247–252 (1991)

82. K. B. Døving, M. Dubois-Dauphin, A. Holley, and

F. Jourdan, “Functional Anatomy of the Olfactory

Organ of Fish and the Ciliary Mechanism of Water

Transport,” Acta Zool., Stockholm 58, 245–255 (1977).

83. K. B. Døving, G. Gemne, “Electrophysiological and

Histological Properties of the Olfactory Tract of the

Burbot (Lota lota L.),” J. Neurophysiol. 28, 139–153

(1965).

84. K. B. Døving, E. H. Hamdani, E. Hoglund, et al., “A

Review on the Chemical and Physiological Basis of

Alarm Reactions in Cyprinids,” in Fish Chemosenses,

Ed. by K. Reutter and B. G. Kapoor (Sci. Publishers,

Enﬁeld, 2004).

S214

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

85. K. B. Døving and K. Holmberg, “A Note on the Func-

tion of the Olfactory Organ of the Hagﬁsh Myxine glu-

tinosa,” Acta Physiol. Scand. 91, 430–432 (1974).

86. K. B. Døving, B. Jonsson, and L. P. Hansen, “The Effect

of Anosmia on the Migration of Atlantic Salmon Smolts

(Saimo salar L.) in Freshwater,” Aquaculture 38, 383–386

(1984).

87. K. B. Døving, M. Mårstøl, J.R. Andersen, and

J. A. Knutsen. “Experimental Evidence of Chemokine-

sis in Newly Hatched Cod Larvae (Gadus morhua L.),”

Mar. Biol. 120, 351–358 (1994).

88. K. B. Døving K.B., H. Nordeng, and B. Oakley, “Single

Unit Discrimination of Fish Odours Released Char

(Saimo alpinus L.) Populations,” Comp. Biochem.

Physiol. 47A, 10511063 (1974).

89. K. B. Døving and R. Selset. “Behavior Patterns in Cod

Released by Electrical Stimulation of Olfactory Tract

Bundles,” Science 207, 559–560 (1980).

90. K. B. Døving, V. L. Selset, and G. Tommesen, “Olfac-

tory Sensitivity to Bile Acids in Salmomd Fishes,” Acta

Physiol. Scand. 108, 123–131 (1980).

91. K. B. Døving and O. B. Stabell. “Trails in Open Waters:

Sensory Cues in Salmon Migration,” in Sensory Pro-

cessing in Aquatic Environments, Ed. by S. P. Collin and

N. J. Marshall (Springer, New York, 2003), pp. 39–52.

92. K. B. Døving and D. Trotier, “Structure and Function of

the Vomeronasal Organ,” J. Exp. Biol. 201, 2913–2925

(1998).

93. K. B. Døving K.B., H. Westerberg, and P.B.Johnsen,

“Role of Olfaction in the Behavioural and Neural

Responses of Atlantic Salmon, Saimo salar, to Hydro-

graphic Stratiﬁcation,” Can. J. Fish. Aquat. Sci. 42,

1658–1667 (1985).

94. J. G. Dulka, N. E. Stacey, P. W. Sorensen, and G. J. Van

Der Kraak, “A Steroid Sex Pheromone Synchronizes

Male-Female Spawning Readiness in Goldﬁsh,” Nature

325, 251–253 (1987).

95. R. Eaton, “Notes on the Olfactory Organs in Cen-

trarchidae,” Copeia, No. 3, 196–199 (1956).

96. H. L. Eistein, “Phytogeny of the Vomeronasal System

and Receptor Cell Types in the Olfactory and Vomero-

nasal Epithelia of Vertebrates,” Microscopy Res. Tech.

23, 1–21 (1992).

97. R. E. Evans R.E., B. Zielinski, and T. J. Hara, “Devel-

opment and Regeneration of the Olfactory Organ in

Rainbow Trout,” in Chemoreception in Fishes, Ed. by

T.J.Hara (Elsevier, Amsterdam, 1982), pp. 15–37.

98. B. A. Flerov, “Olfaction in Fish,” Vopr. Ikhtiol. 2, 517–

529 (1962).

99. N. R. Foster N.R, Lake Trout Reproductive Behaviour:

Inﬂuence of Chemosensory Cues from Young of the

Year By-Products, Trans. Amer. Fish. Soc. 114, 794–

803 (1985).

100. P. Frade, P. C. Hubbard, E. N. Barata, V. M. Canário,

“Olfactory Sensitivity of the Mozambique Tilapia to Con-

speciﬁc Odours,” J. Fish Biol. 61, 1239–1254 (2002).

101. K. Frisch, “Über einen Schreckstoff der Fishhaut und

seine biologische Bedeutung,” Z. vergl. Physiol. 29, 46–

145 (1941a).

102. K. Frisch von, “Die bedeutung der Geruchsinnes in Leben

des Fisches,” Nalurwissenschaften 29, 321–333 (1941b).

103. G. Gemne G., K. B. Døving, “Ultrastructural Properties

of Primary Olfactory Neurons in ﬁsh (Lota lota L.),”

Amer. J. Anat. 126, 457–475 (1969).

104. P. W. Gilbert P.W., “The Visual Apparatus of Sharks and

its Probable role in Predation,” Tenth Paciﬁc Sci. Con-

gress, Abstr. Symp. Papers. Honolulu, Hawaii, pp. 176–

177 (1961).

105. P. W. Gilbert and C. Gilbert, “Sharks and Sharks Deter-

rents,” J. Underwater 5, 69–79 (1973).

106. P. W. Gilbert and S. Springer, “Testing Shark Repel-

lents,” in Sharks and Survival, Ed. by P. W. Gilbert

(Health and Company, Boston, 1963), pp. 477–494.

107. H. R. Goel, Functional Anatomy of the Olfactory

Organs in the Fresh Water Indian Catﬁsh Clarias batra-

chus (Linn.), Zool. Poloniae. 28, 5–14 (1980).

108. A. V. Golubev and E. A. Marusov, “Studies of Chemical

Reception by the White Sea Three-Spined Stickleback

(Gasterosteus aculeatus L) during the Reproductive

Period,” Nauch. Dokl. Vyssh. Shkoly. Biol. Nauki,

No. 9, 33–35 (1979).

109. A. V. Golubev and E. A. Marusov, “Some Characteristics of

Chemical Communication in the Three-Spined Stickleback

Gasterosteus aculeatus L (Gasterosteidae),” Vopr. Ikhtiol.

24, 829–835 (1984).

110. V. B. Goryunova, V. G. Shagaeva, and N. F. Shevchenko,

“An Analysis of Developmental Abnormalities in Mor-

phology of the Sturgeon Larvae and Juveniles in the

Volga-Caspian Basin under Conditions of Artiﬁcial

Reproduction,” Vopr. Ikhtiol. 40, 804–809 (2000).

111. H. Göz, “Uber den Art- und Individualgeruch bei Fis-

chen,” Z. vergl. Physiol. 29, 1–45 (1941).

112. P. P. C. Graziadei and G. A. Monti-Graziadei, “Contin-

uous Nerve Cell Renewal in the Olfactory System,” in

Handbook of Sensory Physiology. IX. Development of

Sensory System, Ed. by M. Jacobson (Springer, Heidel-

berg, 1978), pp. 55–83.

113. C. Groot, T. P. Quinn, and T. J. Hara, “Responses of

Migrating Adult Sockeye Salmon (Oncorhynchus

nerka) to Population-Speciﬁc Odours,” Can. J. Zool. 64,

926–932 (1986).

114. S. J. Groot, de, “Only the Inter-Relationships between

Morphology of the Alimentary Tract, Food and Feeding

Behaviour in Flatﬁshes (Pisces: PIeuronectiformes),”

Neth. J. Roy. Soc. B. 5, 121–196 (1971).

115. A. B. Groves A.B., G. B. Collins, and P. S. Trefethen,

“Roles of Olfaction and Vision on Choice of Spawning

Site of Homing Adult Chinook Salmon (O. tshaw-

ytscha),” J. Fish. Res. Bd. Can. 25, 867–876 (1968).

116. L. Halama, “Morphometry of the Olfactory Organs of

the Rainbow Trout (Salrno gairdneri Rich.),” Acta Biol.

Cracoviensia. Ser. Zool. 24, 105–111 (1982).

117. M. Halvorsen and O. B. Stabell, “Homing Behavior of

Displaced Stream-Dwelling Brown Trout,” Anim.

Behav. 39, 1089–1097 (1990).

118. E. H. Hamdani, G. Alexander, and K. B. Døving, “Pro-

jection of Sensory Neurons with Microvilli to the Lat-

eral Olfactory Tract Indicates their Participation in

Feeding Behaviour in Crucian Carp,” Chem. Senses 26,

1139–1144 (200la).

119. E. H. Hamdani and K. B. Døving, “The Alarm Reaction

in Crucian Carp is Mediated by Olfactory Neurones

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S215

with Long Dendrites,” Chem. Senses. 27, 395–398

(2002).

120. E. H. Hamdani and K. B. Døving, “Sensitivity and

Selectivity of Neurons in the Medial Region of the

Olfactory Bulb to Ssin Extract from Conspeciﬁcs in

Crucian Carp, Carassius carassius,” Chem. Senses 28,

181–189 (2003).

121. E. H. Hamdani, A. Kasumyan, and K. B. Døving, “Is

Feeding Behaviour in Crucian Carp Mediated by the

Lateral Olfactory Tract?,” Chem. Senses 26, 1133–1138

(2001b).

122. E. H. Hamdani, O. B. Stabell, G. Alexander, and

K. B. Døving, “Alarm Reaction in the Crucian Carp is

Mediated by the Medial Bundle of the Medial Olfactory

Tract,” Chem. Senses 25, 103–109 (2000).

123. L. P. Hansen, K. B. Døving, and B. Jonsson, “Migration

of Farmed Adult Atlantic Salmon With and Without

Olfactory Sense Released on the Norwegian Coast,” J.

Fish Biol. 30, 713–721 (1987).

124. A. Hansen and T. E. Finger, “Phyletic Distribution of

Crypt-Type Olfactory Receptor Neurons in Fishes,”

Brain Behav. Evol. 55, 100–110 (2000).

125. A. Hansen, S. H. Rolen, K. Anderson et al., “Correla-

tion Between Olfactory Receptor Cell Type and Func-

tion in the Channel Cattish,” J. Neurosci. (2003) (in

press).

126. A. Hansen and E. Zeiske, “Development of the Olfac-

tory Organ in the Zebraﬁsh, Brachydanio rerio,” J.

Comp. Neurol. 333, 289–300 (1993).

127. A. Hansen and E. Zeiske, “The Peripheral Olfactory

Organ in the Zebraﬁsh, Brachydanio rerio: An Ultra-

structural Study,” Chem. Senses 23, 39–48 (1998).

128. T. J. Hara, “Further Studies on the Sructure-Activity

Relationships of the Amino Acids in Fish Olfaction,”

Comp. Biochem. Physiol, A. 56, 559–565 (1977).

129. T. J. Hara, “Structure-Activity Relationships of Amino

Acids as Olfactory Stimuli,” in Chemoreception in

Fishes, Ed. by T. J. Hara (Elsevier, Amsterdam, 1982),

pp. 135–157.

130. T. J. Hara, “Overview and Introduction,” in Fish

Chemoreception, Ed. by T. J. Hara (Chapman and Hall,

London, 1992a), pp. 1–12.

131. T. J. Hara, “Mechanisms of Olfaction,” in Fish

Chemoreception, Ed. by T. J. Hara (Chapman and Hall,

London, 1992b), pp. 150–170.

132. T. J. Hara, The Diversity of Chemical Stimulation of

Fish Olfaction and Gustation, Rev. Fish Biol. Fish. 4, 1–

35 (1994).

133. T. J. Hara and A. Gorbman, “Electrophysiological Stud-

ies of the Olfactory System in the Goldﬁsh, Carassius

auratus L. I. Modiﬁcation of the Electrical Activity of

the Olfactory Bulb by Other Central Nervous Struc-

tures,” Comp. Biochem. Physiol. 21, 185–200 (1967).

134. T. J. Hara, S. MacDonald, R. E. Evans et al., “Morpho-

line, Bile Acids and Skin Mucus as Possible Chemical

Cues in Salmonid Homing: Electrophysiological Eval-

uation,” in Mechanisms of Migration in Fishes, Ed. by

J. D. McCleave, G. P. Amold, J. D. Dodson, and

W. H. Neill (Plenum Press, New York, 1984), pp. 363–

378.

135. T. J. Hara, T. Sveinsson, R. E. Evans, and D. A. Klaprat,

“Morphological and Functional Characteristics of the

Olfactory and Gustatory Organs of Three Salvelinus

Species,” Can. J. Zool. 71, 414–423 (1993).

136. T. J. Hara and C. Zhang, “Spatial Projections to the

Olfactory Bulb of Functionally Distinct and Randomly

Distributed Primary Neurons in Salmonid Fishes,” Neu-

rosci. Res. 26, 65–74 (1996).

137. T. J. Hara and C. Zhang, “Topographic Bulbar Projec-

tions and Dual Neural Pathways of the Primary Olfac-

tory Neurons in Salmonid Fishes,” Neuroscience 82,

301–313 (1998).

138. F. R. Harden Jones, Fish Migration (Edward Arnold,

London, 1968).

139. R. Harvey. “The Olfactory Epithelium in Plaice (Peu-

ronectes platessa) and Sole (Solea solea), Two Flat-

ﬁshes with Contrasting Feeding Behaviour,” J. Mar.

Biol. Assoc. U.K. 76, 127–139 (1996).

140. A. D. Hasler, Underwater Guideposts (University of

Wisconsin Press, Madison, 1966).

141. A. D. Hasler and A. T. Scholz, Olfactory Imprinting and

Homing in Salmon. Investigations into the Mechanism

of the Imprinting Process (Springer, Berlin, 1983).

142. T. Hellstrøm and K. B. Døving, “Chemoreception of

Taurocholate in Anosmic and Sham-Operated Cod,

Gadus morhua,” Behav. Brain Res. 21, 155–162 (1986).

143. C. C. Hemmings, “Olfaction and Vision in Fish School-

ing,” J. Exp. Biol. 45, 449–464 (1966).

144. M. J. Hiscock and J. A. Brown, Kin Discrimination in

Juvenile Brook Trout (Salvelinus fontinalis) and the

Effect of Odour Concentration on Kin Preferences,

Can. J. Zool. 78, 278–282 (2000).

145. E. S. Hobson, “Feeding Behavior in Three Species of

Sharks,” Paciﬁc Science 17, 171–194 (1963).

146. E. S. Hodson and R. F. Mathewson, “Electrophysiolog-

ical Studies in Elasmobranches,” in Sensory Biology of

Sharks, Skates and Rays, Ed. by E. S. Hodson and

R. F. Mathewson (Castle Hause Publ., Castle Hause,

1981), pp. 227–267.

147. A. Holl, “Vergleichende morphologische und histolo-

gische Untersuchungen am Geruchsorgan der Knochen-

ﬁsche,” Z. Morphol. Okol. Tiere. 54, 707–782 (1965).

148. A. Holl, “Funktionsmorphologie der Nase von Chi-

maera monstrosa (Holocephali),” Z. Morphol. Tiere.

74, 271–296 (1973).

149. A. Holl and W. Meinel, Das Gemchsorgan des Tiefseef-

isches Aphanopus carbo (Percomorphi, Trichiuridae),

Helgolander Wiss. Meeresunters. 18, 404–423 (1968).

150. A. Holl, E. Schulte, and M. Meinel, “Funktionelle Mor-

phologic des Geruchsorgans und Histologie der Kop-

fanhange der Nasenmurane Rhinomuraena ambonensis

(Teleostei, Anguillifonnes),” Helgolander wiss. Meere-

sunters. 21, 103–123 (1970).

151. K. N. Holland and T. H. Teeter, “Behavioral and Car-

diac Reﬂex Assays of the Chemosensory Acuity of

Channel Catﬁsh to Amino Acids,” Physiol. Behav. 27,

699–707 (1981).

152. N. Holmgren, “Zur Anatomic und Histologie des Vorder

und Zwischenhims der Knochenﬁsche,” Acta Zool.

Stockh. 1, 137–315 (1920).

153. I. J. Holopainen, J. Aho, M. Vomanen, and

H. Huuskonen. “Phenotypic Plasticity and Predator

Effects on Morphology and Physiology of Crucian Carp

S216

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

in Nature and in the Laboratory,” J. Fish Biol. 50, 781–

798 (1997).

154. H. Honda H., “Female Sex Pheromone of Rainbow

Trout, Saimo gairdneri, Involved in Courtship Behav-

iour,” Bull. Jap. Soc. Sci. Fish. 46, 1109–1112 (1980a).

155. H. Honda, “Female Sex Pheromone of the Loach, Mis-

gumus anguillicaudatus, Involved in Courtship Behav-

iour,” Bull. Jpn. Soc. Sci. Fish. 46, 1223–1225 (1980b).

156. H. Honda, On the Female Sex Pheromones and Court-

ship Behaviour in the Salmonids, Oncorhynchus masou

and O. rhodurus, Bull. Jpn. Soc. Sci. Fish. 48, 47–49

(1982).

157. D. R. Idler, U. Fagerlund, and H. Mayoh, “Olfactory

Perception in Migrating Salmon. I. L-Serine, a Salmon

Repellent in Mammalian Skin,” J. Gen. Physiol. 39,

889–892 (1956).

158. A. Jacher, “Chemically-Induced Habitat Shifts in Bleak

(Albumus albumus L.),” Arch. Hydrobiol. 133, 71–79

(1995).

159. M. Jakubowski, “Anatomical Structure of Olfactory

Organs Provided with Internal Nares in the Antarctic

Fish Gymnodraco acuticeps Boul. (Bathydraconidae),”

Bull. Acad. Pol. Sci., Ser. Sci., Biol. 23, 115–120

(1975).

160. M. Jakubowski and E. Kunysz, “Anatomy and Mor-

phometry of the Olfactory Organ of the European Cat-

ﬁsh Silurus glanis L. (Siluridae, Pisces),” Z. Mikrosk.

Anat. Forsch. 93, 728–735 (1979).

161. P. B. Johnsen and J. H. Teeter, “Behavioral Responses

of Bonnethead Sharks (Sphyrna tiburo) to Controlled

Olfactory Stimulation,” Mar. Behav. Physiol. 11, 283–

291 (1985).

162. H. E. Johnson and C. J. D. Brown, “Olfactory Apparatus

in the Black Rockﬁsh Sebastodes,” Copeia, No. 4, 838–

840 (1962).

163. K. A. Jones, “Food Search Behaviour in Fish and the

Use of Chemical Lures in Commercial and Sports Fish-

ing,” in Fish Chemoreception, Ed. by T. J. Hara (Chap-

man and Hall, London, 1992), pp. 288–320.

164. K. A. Jones and T. J. Hara, “Behavioural Responses of

Fishes to Chemical Cues: Results from a New Bioas-

say,” J. Fish Biol. 27, 495–504 (1985).

165. L. C. Jordão and G. L. Volpato, “Chemical Transfer of

Warning Information in Non-Injured Fish,” Behaviour

137, 681–690 (2000).

166. G. Y. Jumper G.Y., Jr. and R. C. Baird, “Location by

Olfaction: A Model and Application to the Mating Prob-

lem in the Deep-Sea Hatchetﬁsh Argyropelecus hemi-

gymnus,” Am. Nat. 138, 1431–1458 (1991).

167. J. Kang and J. Caprio, “Electro-Olfactogram and Multi-

unit Olfactory Receptor Responses to Complex Mix-

tures of Ammo Acids in the Channel Catﬁsh, Ictalurus

punctatus,” J.Gen. Physiol. 98, 699–721 (1991).

168. A. S. Kapoor and P. P. Ojha, “Studies on Ventilation of

the Olfactory Chambers of Fishes with a Critical

Reevaluation of the Role of the Accessory Nasal Sacs,”

Arch. Biol. 83, 167–178 (1972).

169. A. S. Kapoor and P. P. Ojha, Functional Anatomy of the

Nose and Accessory Nasal Sacs in the Teleost Channa

punctatus Bloch, Acta Anat. 84, 96–105 (1973).

170. P. Karlson and M. Lüsher, “Pheromones”: a New Term

for a Class of Biological Active Substances, Nature.

183, 55–56 (1959).

171. A. O. Kasumyan, “Behavioral Reaction of Male Stur-

geons to the Releaser Postovulatory Sex Pheromone of

Females,” Doklady Biol. Sci. 333, 439–441 (1993).

172. A. O. Kasumyan, “Olfactory Sensitivity of the Sturgeon

to Free Ammo Acids,” Biophysics 39, 519–522 (1994).

173. A. O. Kasumyan, “Olfaction and Taste Senses in Stur-

geon Behaviour,” J. Appl. Ichthyol. 15, 228–232

(1999).

174. A. O. Kasumyan, “Effect of Chemical Pollutants on

Foraging Behavior and Sensitivity of Fish to Food Stim-

uli,” J. Ichthyol. 41, 76–87 (2001).

175. A. O. Kasumyan, “Sturgeon Food Searching Behaviour

Evoked by Chemical Stimuli: A Reliable Sensory

Mechanism,” J. Appl. Ichthyol. 18, 685–690 (2002).

176. A. O. Kasumyan, “Response to the Alarm Pheromone

and the Sensitivity to it in Juvenile Cyprinid Fish,” in

Pheromones and Behavior (Nauka, Moscow, 1982),

pp. 53–64 [in Russian].

177. A. O. Kasumyan, “Dead Fish as a Source of Chemical

Substances,” in Chemical Signals in the Biology of Fish

(Nauka, Moscow, 1989), pp. 168–177.

178. A. O. Kasumyan, “Methods for the Study of the Defen-

sive Responses in Fish. Chemical Signals of Danger,” in

Sensory Physiology of Marine Fish. Methodological

Aspects (Apatity, 1990a), pp. 51–52.

179. A. O. Kasumyan, “Methods for the Study of the Behav-

ioral Response of Fish to Chemical Signals of Food,” in

Sensory Physiology of Marine Fish. Methodological

Aspects (Apatity, 1990a), pp. 52–57.

180. A. O. Kasumyan, “Sensory Mechanisms Providing for

the Reliability of Chemocommunication in Fish,” in

Problems of Chemical Communication in Animals

(Nauka, Moscow, 1991), pp. 263–270.

181. A. O. Kasumyan and G. V. Devitsyna, “Effect of Olfac-

tory Deprivation on Chemosensory Sensitivity and

State of Taste Receptors of Acipenserids,” J. Ichthyol.

37, 823–835 (1997).

182. A. O. Kasumyan and A. A. Kazhlaev, “Formation of

Searching Behavioral Reaction and Olfactory Sensitiv-

ity to Food Chemical Signals during Ontogeny of Stur-

geons (Acipenseridae),” J. Ichthyol. 33, 51–65 (1993).

183. A. O. Kasumyan and E. A. Marusov, “Behavioral Taste

Response of the Minnow Phoxinus phoxinus (Cyprin-

idae) to Chemical Signals under Normal Conditions and

After Acute and Chronic Anosmia,” J. Ichthyol. 42,

659–670 (2002).

184. A. O. Kasumyan and E. A. Marusov, “Behavioral

Responses of Intact and Chronically Anosmiated Min-

nows, Phoxinus phoxinus (Cyprinidae), to Free Amino

Acids,” J. Ichthyol. 43, 528–538 (2003).

185. A. O. Kasumyan and N. I. Pashchenko, “The Role of

Olfaction in the Defense Reaction of the Grass Carp

Ctenopharyngodon idella (Cyprinidae) to Alarm Phero-

mone,” J. Ichthyol. 22, 122–126 (1982).

186. A. O. Kasumyan and N. I. Pashchenko, “Olfactory Per-

ception of the Alarm Kairomone,” Vesti MGU. Ser. 16.

Biol., No. 3, 51–54 (1985).

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S217

187. A. O. Kasumyan and V. Y. Ponomarev, “Study of the

Behaviour of Zebraﬁsh Brachidanio rerio in Response

to Natural Chemical Food Stimuli,” J. Ichthyol. 26, 96–

105 (1986a).

188. A. O. Kasumyan and V. Y. Ponomarev, “About the Spe-

cies Speciﬁcity of Alarm Pheromone in Fish from the

Order of Cypriniformes,” in Chemical Communication

in Animals (Nauka, Moscow, 1986b), pp. 202–207.

189. A. O. Kasumyan and V. Y. Ponomarev, “Biochemical

Features of Alarm Pheromone in Fish of the Order Cyp-

riniformes,” J. Evol. Biochem. Physiol. 23, 20–24

(1987)

190. A. O. Kasumyan and V. Yu. Ponomarev, “Signiﬁcance

of Chemoreception in Feeding Behavior of Cyprinid

Fish,” in Chemical Sensitivity and Chemocommunica-

tion in Fish (Nauka, Moscow, 1989), pp. 123–131.

191. A. O. Kasumyan and V. Y. Ponomarev, “The Ontogeny

of Feeding Behavior in Relation to Natural Chemical

Signals in Cyprinid Fishes,” J. Ichthyol. 30, 89–100

(1990).

192. A. O. Kasumayn and V. Y. Ponomarev, “Chemical Sig-

nals for Natural Feeding of Fish,” J. Ichthyol. 31, 77–86

(1991).

193. A. O. Kasumyan, M. Ryg, and K. B. Døwing, “Effect of

Amino Acids on the Swimming Activity of Newly

Hatched Turbot Larvae (Scophthalmus maximus),”

Marine Biol. 131, 189–194 (1998).

194. A. O. Kasumyan and L. R. Tauﬁk, Behaviour Reaction

of Juvenile Sturgeons (Acipenseridae) to Amino Acids,

J. Ichthyol. 34, 90–103 (1994).

195. A. O. Kasumyan and A. Tuvikene, “Composition and

Rate of Release of Chemical Substances into Water by

Dead Fish,” Proceedings of the 7th International Sym-

posium on Fish Physiology, Toxicology and Water

Quality, Tallinn, Estonia, May 12–15, 2003, Ed. by

G. L. Rupp and M. D. White (U.S. Environmental Pro-

tection Agency, Ecosystems Research Division, Athens,

Georgia, USA., 2004).

196. M. L. Keefe, “Chernically Mediated Avoidance Behav-

ior in Wild Brook Trout Salvelinus fontinalis: the

Response to Familiar and Unfamiliar Predaceous Fishes

and the Inﬂuence on Fish Diet,” Can. J. Zool. 70, 288–

292 (1993).

197. N. B. Khmelevskaya, “Ecological and Morphological

Analysis of the Olfactory System of Tailless Amphibi-

ans,” Abstract of Candidate’s Dissertation in Biology

(MGU, Moscow, 1972).

198. D. A. Klaprat, R. E. Evans, and T. J. Hara, “Environ-

mental Contaminants and Chemoreception in Fishes,”

in Fish Chemoreception, Ed. by T. J. Hara (Chapman

and Hall, London, 1992), pp. 321–341.

199. H. Kleerekoper, Olfaction in Fishes (Indiana University

Press, Bloomington, 1969).

200. H. Kleerekoper, D. Gruber, and J. Matis, “Accuracy of

Localization of a Chemical Stimulus in Flowing and

Stagnant Water by the Nurse Shark, Gyglymostoma cir-

ratum,” J. Comp. Physiol, 98, 257–275 (1975).

201. H. Kleerekoper and G. A. van Erkel, “The Olfactory

Apparatus of Petromyzon marinus L.,” Can. J. Zool. 38,

209–223 (1960).

202. M. Kodama, T. Ogata, and S. Sato, “External Secretion

of Tetrodotoxin from Puffer Fishes Stimulated by Elec-

tric Shock,” Marine Biol. 87, 199–202 (1985).

203. K. Konno, G. Qin, and K. Nakanishi, “Synthesis of

Amphikuemin and Analogs: A Synonome that Mediates

Partner-Recognition between Anemoneﬁsh and Sea

Anemone, Heterocycles,” 30, 247–251 (1990).

204. N. B. Kruzhalov, “Behavioral Responses of Carp Fin-

gerlings Cyprinus carpio L. to Amino Acids,” Vopr.

Ikhtiol. 26, 1016–1022 (1986).

205. N. B. Kruzhalov, “Attraction and Avoidance Reaction to

Amino Acids in the Silver Carp Carassius carassiug,”

Vopr. Ikhtiol. 30, 169–172 (1990).

206. J. Kux J., E. Zeiske, and Y. Osawa, “Laser Dopler

Velocimetry Measurement in the Model Flow of a Fish

Olfactory Organ,” Chem. Senses and Flavor. 13, 257–

265 (1988).

207. F. Laberge and T. J. Hara, “Neurobiology of Fish Olfac-

tion: A Review,” Brain Res. Rev. 36, 46–59 (2001).

208. J. Laumen, U. Pem, and V. Blum, “Investigations on the

Function and Hormonal Regulation of the Anal Appen-

dices in Blennius pavo (Risso),” J. Exp. Zool. 190, 47–

56 (1974).

209. N. E. Lebedeva, M. Z. P. Vosilene, and T. V. Golovkina,

“Characteristics of Stress in Trout: Extraction of the

Chemical Signal of Danger,” Vopr. Ikhtiol. 33, 281–287

(1993).

210. N. E. Lebedeva and T. V. Golovkina, “Effect of Chemi-

cal Signals of Danger to Hydrocarbon Metabolism in

Carp Fingerlings,” Zh. Evol. Biokhim. Fiziol. 24, 103–

106 (1988).

211. N. E. Lebedeva and Yu. L. Chernyakov, “Chemical Sig-

nal of Danger in the Predator–Prey System in Fish,”

Zh.Evol. Biokhim. Fiziol. 14, 392–397 (1978).

212. W. Li, A. P. Scott, M. J. Siefkes, et al., “Bile Acid

Secreted by Male Sea Lamprey that Acts as a Sex Pher-

omone,” Science 296, 138–141 (2002).

213. W. Li, P. W. Sorensen, and D. D. Gallaher, “The Olfac-

tory System of Migratory Adult Sea Lamprey

(Petromyzon marinus) is Speciﬁcally and Acutely Sen-

sitive to Unique Bile Acids Released by Conspeciﬁc

Larvae,” J. Gen. Physiol. 105, 569–587 (1995).

214. K. Liermann, “Uber den Bau des Geruchsorgans der

Teleostier,” Z. Anat. Entwicklungsgesch 100, 1–39

(1933).

215. N. R. Liley, “Chemical Communication of Fishes,”

Can. J. Fish Aquat. Sci. 39, 22–35 (1982).

216. N. R. Liley, K. H. Olsen, C. J. Foote, and G. J. Van Der

Kraak, “Endocrine Changes Associated with Spawning

Behavior in Male Kokanee Salmon (Oncorhynchus

nerka) and the Effects of Anosmia,” Horm. Behav. 27,

470–487 (1993).

217. N. R. Liley and N. E. Stacey, “Hormones, Pheromones

and Reproductive Behaviour in Fish,” in Fish Physiol-

ogy. Vol. IX. Reproduction, Ed. by W. S. Hoar,

D. J. Randall, and E. M. Donaldson, pp. 1–63 (Aca-

demic, New York, 1983), pp. 1–63.

218. M. M. F. Luthesky and J. W. Adkins, Putative Chemical

Inhibition of Development by Conspeciﬁcs in Mosqui-

toﬁsh, Gambusia afﬁnis, Environ. Biol. Fish. 66, 181–

186 (2003).

S218

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

219. A. Magurran, “Acquired Recognition of Predator Odor

in the European Minnow (Phoxinus phoxinus),” Ethol-

ogy 82, 216–223 (1989).

220. G. A. Malyukina, G. V. Devitsyna, and E. A. Marusov,

“Communication Based on Chemoreception in Fish,”

Zh. Obshch. Biol. 35, 70–79 (1974).

221. G. A. Malyukina, N. G. Dmitrieva, E. A. Marusov, and

G. V. Yurkevich, “Olfaction and Its Role in Fish Behav-

ior,” in Itogi Nauki. 1968. Zoology (VINITI Akad. Nauk

SSSR, 1969), pp. 32–78.

222. G. A. Malyukina, A. O. Kasumyan, and E. A. Marusov,

“Signiﬁcance of Olfaction in Fish Behavior,” in Sensory

Systems (Nauka, Leningrad, 1980), pp. 30–44.

223. G. A. Malyukina, A. O. Kasumyan, and E. A. Marusov,

“Ecological Aspects of Chemical Signalization in Fish,”

Vopr. Ikhtiol. 30, 891–896 (1990).

224. G. V. Malyukina, V. I. Martemyanov, and G. I. Flerova,

“The Alarm Pheromone as a stress Factor for Fish,”

Vopr. Ikhtiol. 22, 338–341 (1982).

225. G. V. Malyukina, E. A. Marusov, and A. K. Karpov,

“Some Characteristics of Chemical Signalization in the

White sea Cod Gadus morhua marisalbi Derjugin

(Gadidae),” Vopr. Ikhtiol. 23, 839–844 (1983).

226. N. B. Marshall, “The Olfactory Organs of Bathypelagic

Fishes,” Symp. Zool. Soc. Lond. 19, 57–70 (1967).

227. N. B. Marshall, Development in Deep-Sea Biology

(Blandford, Poole, 1979).

228. Yu. B. Manteifel, Evolutionary Problems of Systems

Organization of External Chemoreception in Verte-

brates, Systems of Sensory Organs: Morphological and

Functional Aspects of Evolution (Nauka, Leningrad,

1987), pp. 121–132 [in Russian].

229. E. A. Marusov, Ecological Stereotypes of Defensive

Behavior of Fish Caused by Chemical Signals of Dan-

ger, Nauch. Dokl. Vyssh. Shkoly. Biol. Nauki, No. 8,

67–69 (1976).

230. E. A. Marusov, “Basic Methodological Aspects of the

Study of Fish Behavior After Effects of Chemical Sig-

nals,” in Sensory Physiology of Marine Fish. Method-

ological Aspects (Apatity, 1990), pp. 40–42.

231. A. Mathis and R. J. F. Smith, “Fathead Minnows Pime-

phales promelas Leam to Recognize Northern Pike

Esox lucius as Predator on the Basis of Chemical Stim-

uli from Minnows in the Pike’s Diet,” Anim. Behav. 46,

645–656 (1993).

232. J. R. McBride, D. R. Idler, R. E. Jones, and N. Tomlin-

son, “Olfactory Perception in Juvenile Salmon. I.

Observation on Response of Juvenile Sockeye to

Extracts of Food,” J. Fish. Res. Bd Can. 19, 327–334

(1962).

233. D. A. McLennan and M. J. Ryan, “Responses to Con-

speciﬁc and Heterospeciﬁc Olfactory Cues in the

Swordtail Xiphophoms cortezi,” Anim. Behav. 54,

1077–1088 (1997).

234. D. A. McLennan and M. J. Ryan, “Interspeciﬁc Recog-

nition and Discrimination Based upon Olfactory Cues

in Northern Swordtails,” Evolution 53, 880–888 (1999).

235. K. J. Meams, “Response of Atlantic Salmon (Salrno

salar L.) Yearlings to Individual 1-Amino Acids,”

Aquaculture 48, 253–259 (1985).

236. K. J. Meams, “Sensitivity of Brown Trout (Saimo trutta

L.) and Atlantic Salmon (Saimo salar L.) Fry to Amino

Acids at the Start of Exogenous Feeding,” Aquaculture

55, 191–200 (1986).

237. K. J. Meams, “Behavioural Responses of Salmonid Fry

to Low Amino Acid Concentrations,” J. Fish Biol. 34,

223–232 (1989).

238. F. Mees, “Occurrence of Internal Nares in the Genus

Ichthyoscopus (Pisces, Uranoscopidae),” Copeia, 462

(1962).

239. R. Melinkat and E. Zeiske, “Functional Morphology of

Ventilation of the Olfactory Organ in Bedoria geayi Pel-

legrin 1909 (Teleostei, Atherinidae),” Zool. Anz. 203,

354–368 (1979).

240. M. Meredith, G. Femandez-Fewell, “Vomeronasal Sys-

tem, LHRH and Sex Behaviour,” Psychoneuroendoc-

rynology 19, 657–672 (1994).

241. A. Moore, M. J. Ives, and L. T. Kell, The Role of Urine

in Sibling Recognition in Atlantic Salmon Salmo salar

(L.) Parr, Proc. R Soc. Lond, 255, 173–180 (1994).

242. Y. Morita and T. E. Finger, “Differential Projections of

Ciliated and Microvillous Olfactory Receptor Cells in

the Catﬁsh, Ictalurus punctatus,” J. Comp. Neurol. 398,

539–550 (1998).

243. E. E. Morrison and J. A. Plumb, “Olfactory Organ of

Channel Catﬁsh as a Site of Experimental Edwgrdsiella

ictaluri Infection,” J. Aquat. Anim. Health. 6, 101–109

(1994).

244. M. Murata M., K. Miyagawa-Kohshima, K. Nakanishi,

and Y. Naya, “Characterisation of Compounds that

Induce Symbiosis Between Sea Anemone and Anemon-

eﬁsh,” Science 234, 585–587 (1986).

245. C. A. Murphy, N. E. Stacey, and L. D. Corkum, “Puta-

tive Steroidal Pheromones in the Round Goby Neogo-

bius melanostomus: Olfactory and Behavioral

Response,” J. Chem. Ecol. 27, 443–470 (2001).

246. G. A. Nevitt, Do Fish Sniff? A New Method of Olfac-

tory Sampling in Pleuronectid Flounders, J. Exp. Biol.

157, 1–18 (1992).

247. W. Neyhaus and A. Muller, “Das Verhaltnis der Riech-

zellenzahl zur Riechschwelle beim Hund,” Naturwis-

senschaften 41 (10), 1–237 (1954).

248. J. Ngai, A. Chess, M. M. Dowling, N. Necles, Macagno

E.R., and R. Axel, “Coding of Olfactory Information:

Topography of Odorant Receptor Expression in the Cat-

ﬁsh Olfactory Epithelium,” Cell 72, 667–680 (1993).

249. J. G. Nielsen and E. Bertelsen, “The Gulper-Eel Family

Saccopharyngidae (Pisces, Anguilliformes,” Steenstru-

pia 11, 157–206 (1985).

250. A. A. Nikonov and J. Caprio, “Electrophysiological

Evidence for a Chemotopy of Biologically Relevant

Odors in the Olfactory Bulb of the Channel Catﬁsh,” J.

Neurophysiol. 86, 1869–1876 (2001).

251. H. Nordeng. “Is the Local Orientation of Anadromous

Fish Determined by Pheromones?” Nature 233, 411–

413 (1971).

252. H. Nordeng, “A Pheromone Hypothesis for Homeward

Migration in Anadromous Salmonids,” Oikos 28, 155–

159 (1977).

253. H. A. Oelschlager, “Morphologisch-fünktionelle Unter-

suchungen am Geruchsorgan von Lampris guttatus

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S219

(Brunnich, 1788) (Teleostei: Allotriognathi),” Zoomor-

phologie 85, 89–110 (1976).

254. P. P. Ojha and A. S. Kapoor, “Functional Anatomy of

Nose in the Teleost Wallago attu B1 & Schn.,” Arch.

Biol. Liege 83, 105–116 (1972).

255. K. H. Olsén, “Chemo-Attraction between Juveniles of

Two Sympatric Stocks of Arctic Charr, Salvelinus alpi-

nus (L.) and their Gene Frequency of Serum Esterases,”

J. Fish Biol. 28, 221–231 (1986).

256. K. H. Olsén, J. T. Jarvi, I. Mayer, E. Petersson, and

F. Kroon, “Spawning Behaviour and Sex Hormone Lev-

els in Adult and Precocious Brown Trout (Salmo trutta

L.) Males and the Effect of Anosmia,” Chemoecology 8,

9–17 (1998).

257. K. H. Olsén, L. Karlson, and A. Helander, “Food Search

Behavior in Arctic Charr, Salvelinus alpinus (L.),

Induced by Food Extracts and Amino Acids,” J. Chem.

Ecol. 12, 1987–1998 (1986).

258. K. H. Olsén and N. R. Liley, “The Signiﬁcance of

Olfaction and Social Cues in Milt Availability, Sexual

Hormone Status, and Spawning Behavior of Male Rain-

bow Trout (Oncorhynchus mykiss),” Gen. Comp, Endo-

crinol. 89, 107–118 (1993).

259. D. Ottoson, “Analysis of the Electrical Activity of the

Olfactory Epithelium,” Acta Physiol. Scand. 35, 1–83

(1956).

260. G. H. Parker, “Olfactory Reactions in Fihes,” J. Exp.

Zool. 8, 535–542 (1910).

261. G. H. Parker. “The Reaction of Smell, Taste and the

Common Chemical Sense in Vertebrates,” Proc. Acad.

Natur. Sco. Philad. 15, 221–234 (1912).

262. N. I. Pashchenko, “Morphological and Functional

Characteristics of the Development of the Olfactory

Organ in Cyprinid Fish,” Abstract of Candidate’s Dis-

sertation in Biology (Moscow Gos. Univ., Moscow,

1986).

263. N. I. Pashchenko and A. O. Kasumyan, “Degenerative

and Restorative Processes in the Olfactor Lining of

White Amur, Ctenopharyngodon idella (Cyprinidae)

after Treatment with Detergent Triton X-100,” J. Ich-

thyol. 24, 112–121 (1984).

264. N. I. Pashchenko and A. O. Kasumyan, “Morpho-Func-

tional Features of the Olfactory Organ in Cyprinid

Fishes. 1. Morphology and Function of Olfactory Organ

During Ontogeny of the White Amur, Ctenopharyn-

godon idella,” J. Ichthyol. 26, 12–25 (1986).

265. N. I. Pashchenko and A. O. Kasumyan, “Some Morpho-

logical and Functional Characteristics of the Ontogeny

of the Olfactory Organ of Minnow Phoxinus phoxinus

(Cypriniformes, Cyprinidae),” Zool. Zh. 62, 367–377

(1983).

266. D. S. Pavlov, Experiments on the Feeding of Burbot

Lota lota at Different Illumination, Biol. Nauki, No. 4,

42–46 (1959).

267. D. S. Pavlov and A. O. Kasumyan, “Studies of the

Behavior and Sensory Systems in Russia. 2.,” Vopr.

Ikhtiol., 34, 703–718 (1994).

268. D. S. Pavlov and Yu. N. Sbikin, Role od Olfaction in

Feeding of Sturgeon Fish, Zool. Zh. 49, 872–880

(1970).

269. D. S. Pavlov and A. O. Kasumyan, “Sensory Principles

of the Feeding Behaviour of Fishes,” J. Ichthyol. 30,

77–93 (1990).

270. D. S. Pavlov and A. O. Kasumyan, “The Structure of the

Feeding Behaviour of Fishes,” J. Ichthyol. 38, 116–128

(1998).

271. D. S. Pavlov and A. O. Kasumyan, “Patterns and Mech-

anisms of Schooling Behavior in Fish: A Review,” J.

Ichthyol. 40, S163-S231 (2000).

272. L. B. Pettersson and C. Bronmark, Trading off Safety

Against Food: State Dependent Habitat Choice and For-

aging in Crucian Carp, ecologia 95, 353–357 (1993).

273. L. B. Pettersson, P. A. Nilsson, and C. Bronmark, “Pred-

ator Recognition and Defence Strategies in Crucian

Carp, Carassius carassius,” Oikos 88, 200–212 (2000).

274. W. Pfeiffer, “The Fright Reaction of Fish,” Biol. Revs.

Cambridge Phil. Soc. 37, 495–511 (1962).

275. W. Pfeiffer, “The Morphology of the Olfactory Organ of

the Paciﬁc Salmon (Oncorhynchus),” Can. J. Zool. 41,

1233–1236 (1963).

276. W. Pfeiffer, “The Morphology of the Olfactory Organ of

Hoplopagrus guentheri Gill,” Can J. Zool. 42, 235–237

(1964).

277. W. Pfeiffer, “Des Geruchsorgan der Polypteridae

(Pisces, Brachiopterygii),” Z. Morphol. Tiere. 63, 75–

110 (1968).

278. W. Pfeiffer, “Der Geruchsinn der Polypteridae (Pisces,

Branchiopterygu),” Z, Vergl. Physiol. 63, 151–164

(1969).

279. W. Pfeiffer, “The Distribution of Fright Reaction and

Alarm Substance Cells in Fishes,” Copeia, No. 4, 653–

665 (1977).

280. M. Pipping, “Der Geruchssinn der Fische mit beson-

derer Berucksichtigung seiner Bedeutung für das Auf-

suchen des Futters,” Soc. Sci. Fennica Comm. Biol. 2,

1–27 (1926).

281. M. Pipping, “Erganzende Beobachtungen über den

Geruchsinn der Fische mit besonderer Berucksichti-

gung seiner Bedeutung für das Aufsuchen des Futters,”

Soc. Sci. Fennica Comm. Biol. 2, 1–27 (1927).

282. S. B. Podushka, “Abnormalities of the Olfactory Organ

of Sturgeons and their Usa as a Marker of Young

Released from Fishery Farms,” in Research Bulletin of

the Laboratory INENKO, No. 1, 38–57 (1999).

283. K. R. Poling K.R., E. J. Eraser, and P. W. Sorensen,

“The Three Steroidal Components of the Goldﬁsh Pre-

ovulatory Pheromone Signal Evoke Different Behav-

iors in Males,” Comp. Biochem. and Physiol. 129, 645–

651 (2001).

284. C. Polkinghome, J. M. Olson, D. G. Gallaher, and

P. W. Sorensen, “Larval Sea Lamprey Release two

Unique Bile Acids to the Water at a Rate Sufﬁcient to

Produce Detectable Riverine Pheromone Plumes,” Fish

Physiol. Biochem. 24, 15–30 (2001).

285. E. Pollack, Z. Becker, and R. Haynes, “Sensory Control

of Mating in the Blue Guramy, Trichogaster tri-

choptems (Ptsces, Belontiidae),” Behav. Biology. 22,

92–103 (1978).

286. N. Primor, J. Parness, and E. Ziotkin, “Pardaxin: the

Toxic Factor from the Skin Secretion of the Flatﬁsh

Pardachirus marmoratus (Soleidae),” in Toxins: Ani-

S220

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

mal, Plant and Microbial, Ed. by P. Rosenberg (Perga-

mon, New York, 1978), pp. 539–547.

287. G. A. Pyatkina, “Electronic Microscope Study of the

Olfactory Organ of the Sterlet Acipenser rutenus),”

Arch. Anat. Gistol Embriol. 68, 85–93 (1975).

288. G. A. Pyatkina, Receptor Cells of Diffrent Types and the

Quantitative Relations between them in the olfactory

Organ of Larvae and Adult Sturgeons, Tsitologiya 18,

1444–1449 (1976).

289. T. P. Quinn, E. L. Brannon, and A. H. Dittman, “Spatial

Aspects of Imprinting and Homing in Coho Salmon,

Oncorhynchus kisutch,” Fish. Bull. 87, 769–774 (1989).

290. T. S. Reese and M. W. Brightman, “Olfactory Surface

and Central Olfactory Connections in Some Verte-

brates,” in Taste and Smell in Vertebrates, Ed. by

G. E. W. Wolstenholrne and J. Knight (Ciba Found.

Symp., London, 1970), pp. 115–143.

291. B. G. Rehnberg and C. B. Schreck, “The Olfactory

L-Serine Receptor in Coho Salmon: Biochemical Spec-

iﬁcity and Behavioural Response,” J. Comp. Physiol.

A 159, 61–67 (1986).

292. C. Rekowski von., J. Scmilewsld, and H. P. Zippel,

“Behavioral Experiments in Goldﬁsh Conﬁrm Amino

Acids as Olfactory Meaningful Natural Stimuli,” Adv.

Biosci. 93, 491–496 (1994).

293. J. W. Resink, R. Van Den Hurk, G. R. F. O. Van Zoelen,

and E. A. Huisman, “The Seminal Vesicle as Source of

Sex Attracting Substances in the African Catﬁsh, Clar-

ias gariepinus,” Aquaculture 63, 115–127 (1987).

294. J. W. Resink, P. K. Voorthuis, R. Van Den Hurk, et al.,

“Steroid Glukuronides of the Seminal Vesicle as a

Olfactory Stimuli in African Catﬁsh, Clarias gariepin-

nus,” Aquaculture 83, 153–166 (1989).

295. K. Sato, T. Shoji, and H. Ueda, “Olfactory Discriminat-

ing Ability of Lacustrine Sockeye and Masu Salmon in

Various Freshwaters,” Zool. Sci. 17, 313–317 (2000).

296. K. Sato and N. Suzuki, Whole-Cell Response Charac-

teristics of Ciliated and Microvillous Olfactory Recep-

tor Neurons to Amino Acids, Pheromone Candidates

and Urine in Rainbow Trout, Chem. Senses Flavor. 26,

1145–1156 (2001).

297. M. Satou, “Synaptic Organization of the Olfactory Bulb

and Its Projection,” in Fish Chemoreception, Ed. by

T. J. Hara (Chapman and Hall, London, 1992),

pp. 40−59.

298. A. T. Scholz, R. J. White, M. Muvi, and T. Smith,

“Uptake of Radiolabelled Triiodothyronine in the Brain

of Steelhead Trout (Saimo gairdneri) during Parr-Smolt

Transfonnation: Implications for the Mechanism of

Thyroid Activation of Olfactory Imprinting,” Aquacul-

ture 45, 199–214 (1985).

299. E. Schulte, “Untersuchungen an der Regio olfactoria

des Aals, Anguilla anguilla L. I. Feinstruktur des

Riechepithells,” Z. Zeilforsch. 125, 210–228 (1972).

300. E. Schulte and A. Holl, “Feinstruktur des Riechepithels

von Calamoichthys calabaricus J. A. Smith (Pisces,

Brachopterygii),” Z. Zeilforsch. 120, 261–279 (1971).

301. F. Schutz, “Vergleichende Untersuchungen über die

Schreckreaction bei Fischen und deren Verbreitung,” Z.

Vergl. Physiol. 38, 84–135 (1956).

302. A. P. Scott, N. R. Liley, and E. L. M. Vermeirssen, Urine

of Reproductively Mature Female Rainbow Trout,

Oncorhynchus mykiss (Walbaum), Contains a Priming

Pheromone Which Enhances Plasma Levels of Sex Ste-

roids and Gonadotrophin U in Males, J. Fish Biol. 44,

131–147 (1994).

303. R. Selset, “Chemical Methods for Fractionation of

Odorants Produced by Char Smolts and Tentative Sug-

gestions for Pheromone Origins,” Acta Physiol. Scand.

108, 7–13 (1980).

304. R. Selset R. and K. B. Døving, Behaviour of Mature

Anadromous Char (Saimo alpinus L.) Towards Odor-

ants Produced by Smolts of their Own Population, Acta

Physiol. Scand. 108, 113–122 (1980).

305. E. K. Sepp, The History of the Development of the Ner-

vous System in Vertebrates (Medgiz, Moscow, 1959) [in

Russian].

306. R. E. Sheldon, “The Olfactory Tracts and Centers in

Teleosts,” J. Comp. Neurol. 22, 177–339 (1912).

307. M. L. Sherman and P. A. Moore, “Chemical Orientation

of Brown Bullheads, Ameiurus nebulosus, under Differ-

ent Flow Conditions,” J. Chem. Ecol. 27, 2301–2318

(2001).

308. O. I. Shmalgauzen, “Formation of Defect Olfactor

organs in Sturgeons during Artiﬁcial Rearing,” Dokl.

Akad. Nauk SSSR 114, 216–219 (1957).

309. O. I. Shmalgauzen, “Morphological Study of the Olfac-

tory Organs in Fish,” Tr. Inst. Morfol. Zhiv., No. 40,

157–187 (1962a).

310. O. I. Shmalgauzen, “Disturbances in the Development

of the Olfactory Organ in Sturgeon Fish at Certain Rear-

ing Conditions,” Tr. Inst. Morfol. Zhiv., No. 40, 188–

218 (1962b).

311. I. A. Shparkovskii, “Chemical Signalization and Behav-

ior of Fish,” in Signalization and Behavior of Marine

Fish (Nauka, Leningrad, 1980), pp. 91–128.

312. M. J. Siefkes, A. P. Scott, B. Zielinski, et al., “Male Sea

Lampreys, Petromyzon marinus L., Excrete a Sex Pher-

omone from Gill Epithelia,” Biol. Reproduct. 69, 125–

132 (2003).

313. J. A. Sisneros and D. R. Nelson, “Surfactants as Chem-

ical Shark Repellents: Past, Present and Future,” Envi-

ronm. Biol. Fish. 60, 117–129 (2001).

314. R. J. F. Smith, “The Adaptive Signiﬁcance of the Alarm

Substance Fright Reaction System,” in Chemoreception

in Fishes, Ed. by T. J. Hara (Elsevier, Amsterdam,

1982), pp. 327–342.

315. R. J. F. Smith, “Alarm Signals in Fishes,” Rev. Fish

Biol. Fish. 2, 33–63 (1992).

316. C. Sola, “Chemoattraction of Upstream Migrating

Glass Eels Anguilla anguilla to Earthy and Green Odor-

ants,” Environ. Biol. Fish. 43, 179–185 (1995).

317. C. Sola, A. Spampanato, and L. Tosi, “Behavioural

Responses of Glass Eels (Anguilla anguilla) towards

Amino Acids,” J. Fish Biol. 42, 683–691 (1993).

318. P. W. Sorensen, “Hormones, Pheromones and Chemore-

ception,” in Fish Chemoreception, Ed. by T. J. Hara

(Chaptman and Hall, London, 1992), pp. 199–228.

319. P. W. Sorensen and J. Caprio, “Chemoreception,” in The

Physiology of Fishes, 2nd ed., Ed. by D. H. Evans (CRC

Press, Boca Raton, 1998), pp. 375–405.

320. P. W. Sorensen, A. P. Scott, and R.-L. Kihslinger, “How

Common Metabotites Function as Relatively Speciﬁc

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S221

Pheromonal Signals in the Goldﬁsh,” Proceedings of

the Sixth Annual Int. Symp. on the Reproductive Physi-

ology of Fish, Ed. by B. Norberg, O. S. Kjesbu,

G. L. Taranger, E. Andersson, and S. O. Stefansson

(University of Bergen Press, Bergen, 2000), pp. 125–

128.

321. P. W. Sorensen and N. E. Stacey, “Identiﬁed Hormonal

Pheromones in the Goldﬁsh: A Model for Sex Phero-

mone Function in Teleost Fish,” in Chemical Signals in

Vertebrates, Ed. by V. D. W. MacDonald, D. Muller-

Schwarze, and S. E. Natynczuk (Oxford University

Press, Oxford, 1990), pp. 302–314.

322. P. W. Sorensen and N. E. Stacey, “Evolution and Spe-

cialization of Fish Hormonal Pheromones,” in Advances in

Chemical Signals in Vertebrates, Ed. by R. E. Johnston,

D. Muller-Schwartze, and P. W. Sorensen (Plenum,

New York, 1999), pp. 15–47.

323. O. B. Stabell, “Intraspeciﬁc Pheromone Discrimination

and Substrate Marking by Atlantic Salmon Parr,” J.

Chem. Ecol. 13, 1625–1643 (1987).

324. O. B. Stabell, “Olfactory Control of Homing Behaviour

in Salmonids,” in Fish Chemoreception, T. J. Hara

(Chapman and Hall, London, 1992), pp. 249–270.

325. O. B. Stabell, M. S. Lwin, Predator-Induced Phenotypic

Changes in Crucian Carp are Caused by Chemical Sig-

nals from Conspeciﬁcs, Environ, Biol. Fish. 49, 145–

149 (1997).

326. O. B. Stabell and T. Refstie, “Inﬂuence of the Olfactory

Sense upon Smolt Transformation in Salmonid Fishes,”

J. Chem. Ecol. 11, 1427–1438 (1985).

327. O. B. Stabell, R. Selset, and K. Sletten, “A Comparative

Chemical Study on Population-Speciﬁc Odorants from

Atlantic Salmon,” J. Chem. Ecol. 8, 201–217 (1982).

328. N. E. Stacey, A. L. Kyle, “Effects of Olfactory Tract

Lesions on Sexual and Feeding Behavior in the Gold-

ﬁsh,” Physiol. Behav. 30, 621–628 (1983).

329. A. M. Sutterlin, “Chemical Attraction of Some Marine

Fish in their Natural Habitat,” J. Fish Res. Board Can.

32, 729–738 (1975).

330. J. S. Suzuki, D. Tucker, “Amino Acids as Olfactory

Stimuli in Freshwater Catﬁsh Ictalurus catus (Linn.),”

Comp. Biochem. Physiol. 40, 399–404 (1971).

331. K. Tachibana, M. Sakaitanai, K. Nakanishi, “Pavoni-

nins: Shark-Repelling Ichthyotoxins from the Defense

Secretion of the Paciﬁc Sole,” Science 226, 703–705

(1984).

332. K. Tachibana, M. Sakaitani, and K. Nakanishi, Pavoni-

nins, Shark-Repelling and Ichthyotoxic Steroid n-

acetylglucosaminides from the Defense Secretion of the

Sole Pardachirus pavoninus (Soleidae), Tetrahedron

41, 1027–1037 (1985).

333. H. Tanaka, Y. Takagi, and Y. Naito, “Swimming Speeds

and Buoyancy Compensation of Migrating Adult Chum

Salmon Oncorhynchus keta Revealed by

Speed/Depth/Acceleration Data Logger,” J. Exp. Biol.

204, 3895–3904 (2001).

334. H. Teichmann, “Vergleichende Untersuchungen an der

Nase der Fische,” Z. Morph. Okol. Tiere. 43, 171–212

(1954).

335. H. Teichmann, “Uber die Leistung des Geruchssinnes

beim Aal (Angilla anguilla),” Z. Vergl. Physiol. 42,

206–254 (1959).

336. A. L. Tester, “The Role of Olfaction in Shark Preda-

tion,” Paciﬁc Sci. 17, 145–170 (1963).

337. B. Theisen, “Ultrastructure of the Olfactory Epithelium

in the Australian Lungﬁsh Neoceratodus forsten,” Acta

Zool. Stockh. 53, 205–218 (1972).

338. B. Theisen, “The Olfactory System in the Paciﬁc Hag-

ﬁsh Eptatretus stoutii, Eptatretus deani and Myxini cir-

cifrons,” Acta Zool. Stockh. 57, 167–173 (1976).

339. B. Theisen, “Functional Morphology of the Olfactory

Organ in Spinachi spinachia (L.) (Teleostei, Gaster-

osteidae),” Acta Zool. Stockh. 63, 247–254 (1982).

340. B. Theisen, H. Breucker, E. Zeiske, and R. Melinkat,

“Structure and Development of the Olfactory Organ in

the Garﬁsh Belone belone (L.) (Teleostei, Atherini-

formes),” Acta Zool. Stockh. 61, 161–170 (1980).

341. B. Theisen, E. Zeiske, and H. Breucker, Functional

Morphology of the Olfactory Organs in the Spiny Dog-

ﬁsh (Squalus acanthias L.) and the Small-Spotted Cat-

shark (Sciliorhinus canicula (L.)), Acta Zool. Stockh.

67, 73–86 (1986).

342. B. Theisen, E. Zeiske, W.L. Silver, et al., “Morphologi-

cal and Physiological Studies on the Olfactory Organ of

the Striped Eel Catﬁsh Plotosus lineatus,” Marine Biol.

110, 127–135 (1991).

343. G. Thommesen, “Speciﬁcity and Distribution of Recep-

tor Cells in the Olfactory Mucosa of Char (Salmo alpi-

nus L.),” Acta Physiol. Scand. 115, 47–56 (1982).

344. G. Thommesen, “Morphology, Distribution and Speci-

ﬁcity of Olfactory Receptor Cells in Salmonid Fishes,”

Acta Physiol. Scand. 117, 241–249 (1983).

345. S. A. Thompson, K. Tachibana, K. Nakanishi, and

I. Kubota, “Melittin-Like Peptides from the Shark-

Repelling Defense Secretion of the Sole Pardachirus

pavoninus,” Science 233, 341–343 (1986).

346. R. A. Thornhill, “The Ultrastructure of the Olfactory

Epithelium of the Lamprey Lampetra ﬂuviatilis,” J. Cell

Sci. 2, 591–602 (1967).

347. J. H. Todd, “The Chemical Languages of Fishes,” Sci.

Amer. 224, 98–108 (1971).

348. J. H. Todd, J. Atema, and J. E. Bardach, “Chemical

Communication in Social Behavior of a Fish, the Yel-

low Bullhead (Ictalurus natalis),” Science 158, 672–

673 (1967).

349. L. Tosi and C. Sola, “Role of Geosmin, a Typical Inland

Water Odour, in Guiding Glass Eel Anguilla anguilla

(L.) Migration,” Ethology 95, 177–185 (1993).

350. D. K. Tretyakov, “Sensory Organs of the River Lam-

prey,” Zap. Imper. Novorossiisk. Univ., Odessa, 8, 1–

644 (1915).

351. A. C. W. Utne and B. Bacchi, “The Inﬂuence of Visual

and Chemical Stimuli from Cod Gadus morhua on the

Distribution of Two-Spotted Goby Gobiusculus ﬂave-

scens (Fabricius),” Sarsia 82, 129–135 (1997).

352. R. Van Den Hurk and J. G. D. Lambert, Ovarian Steroid

Glucuronides Function as Sex Pheromones for Male

Zebraﬁsh, Brachidanio rerio, Can. J. Zool. 61, 2381–

2387 (1983).

353. R. Van Den Hurk and J. W. Resink, “Male Reproductive

System as Sex Pheromone Producer in Teleost Fish,” J.

Exp. Zool. 261, 204–213 (1992).

S222

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

KASUMYAN

354. R. Van Den Hurk, W. G. E. J. Schoonen, G. A. Van

Zoelen, and J. G. D. Lambert, The Biosynthesis of Ste-

roid Glucuronids in the Zebraﬁsh Brachydanio rerio

and their Pheromonal Function as Ovulation Inducers,

Gen. Comp. Endocrynol. 68, 179–188 (1987).

355. J. Van Denbossche, J. G. Seelye, B. S. Zielinski, The

Morphology of the Olfactory Epithelium in Larval,

Juvenile and Upstream Migrant Stages of the Sea Lam-

prey, Petromyzon marinus, Brain, Behav Evol. 45, 19–

24 (1995).

356. V. P. Vasilyev, Evolutionary Caryology of Fishes

(Nauka, Leningrad, 1985) [in Russian].

357. V. M. Vinogradova and Yu. B. Manteifel, “Retention of

Chemical Stimuli and Olfaction in the Sexual Behavior

of the Guppy Poecilia reticulata Peters (Cyprinodonti-

formes, Poecilildae),” Vopr. Ikhtiol. 22, 113–119

(1982).

358. V. M. Vinogradova and Yu. B. Manteifel, Retention of

Chemical Stimuli by Juvenile Guppy Poecilia reticu-

lata Peters (Poeciliidae), Vopr. Ikhtiol. 24, 836–842

(1984).

359. E. L. M. Vermeirssen, A. P. Scott, and N. R. Liley,

“Female Rainbow Trout Urine Contains a Pheromone

which Causes a Rapid Rise in Plasma 17,20β-dihy-

droxy-4-pregnen-3-one Levels and Milt Amounts in

Males,” J. Fish Biol. 50, 107–119 (1997).

360. L. R. Watson, J. M. Groff, R. P. Hedrick, “Replication

and Pathogenesis of White Sturgeon Iridovirus (WS1V)

in Experimentally Infected White Sturgeon Acipenser

transmontanus Juveniles and Sturgeon Cell Lines,” Dis-

eases Aquat. Organisms. 32, 173–184 (1998).

361. F.A. Weltzien, E. Hoglund, E. H. Hamdani, K. B. Døv-

ing, “Does the Lateral Bundle of the Medial Olfactory

Tract Mediates Reproductive Behavior in Male Crucian

Carp?” Chemical Senses and Flavor. 28, 293–300

(2003).

362. R. G. Wemer and M. J. Lannoo, Development of the

Olfactory System of the White Sucker, Catostomus

commersoni, in Relation to Imprinting and Homing: A

Comparison to the Salmonid Model, Environ. Biol.

Fish. 40, 125–140 (1994).

363. E. G. Wilson and W. H. Bossert, “Chemical Communi-

cation among Animals,” in Recent Progress in Hormone

Research. Vol. 19, Ed. by G. Pincus (1963), pp. 673–

716.

364. R. R. Wilson and K. L. Smith, “Effect of Near-Bottom

Currents on Detection of Bait by the Abyssal Grenadier

Fishes Coryphaenoides spp., Recorded In Situ with a

Video Camera on a Free Vehicle,” Marine Biol. 84, 83–

89 (1984).

365. S. Winberg, R. Bjerselius, E. Baatrup., and K. B. Døv-

ing, “The Effect of Cu (11) on the Electro-Olfactogram

(EOG) of the Atlantic Salmon (Salrno salar L.) in Arti-

ﬁcial Freshwater of Varying Inorganic Carbon Concen-

trations,” Ecotoxicol. Environ. Safety 24, 167–178

(1992).

366. W. J. Wisby and A. D. Hasler, Effect of Olfactory

Occlusion on Migrating Silver Salmon (Oncorhynchus

kisutch), J. Fish. Res. Board Can. 11, 472–478 (1954).

367. B. D. Wisenden, “Chemically Mediated Strategies to

Counter Predation,” in Sensory Processing in Aquatic

Environments, Ed. by S. P. Cotlin and N. J. Marshall

(Springer, New York, 2003), pp. 236–251.

368. B. D. Wisenden, D. P. Chivers, and J. F. Smith, “Early

Warning of Risk in the Predation Sequence: Distribu-

tion Pheromone in Jowa Darters (Etheostoma exile),” J.

Chem. Ecol. 21, 1469–1480 (1995).

369. W. L. Wrede, “Versuche über den Artduft der Eiritzen,”

Z. Vergl. Physiol. 17, 510–519 (1932).

370. M. Yamamoto, “Comparative Morphology of Fish

Olfactory Organ in Teleosts,” in Chemoreception in

Fishes, Ed. by T. J. Hara (Elsevier, Amsterdam, 1982),

pp. 39–59.

371. M. Yamamoto and K. Ueda, “Comparative Morphology

of Fish Olfactory Epithelium. X. Perciformes, Beryci-

formes, Scorpaeniformes and Pleuronectiformes,” J.

Fac. Sci. Univ. Tokyo. Sect. 4. 14, 273–297 (1979).

372. K. M. Yamauchi, M. Ban, N. Kasahara, et al., “Physio-

logical and Behavioural Changes Occurring during Olt-

iﬁcation in the Masu Salmon, Oncorhynchus masu,”

Aquaculture 45, 227–235 (1985).

373. H. Yambe, M. Shindo, and F. Yamazaki, “A Releaser

Pheromone that Attracts Males in the Urine of Mature

Female Masu Salmon,” J. Fish Biol. 55, 158–171

(1999).

374. S.-S. Yun, A. P. Scott, M. J. Siefkes, and W. Li, Devel-

opment and Application of an EUSA for Sex Phero-

mone Released by the Male Sea Lamprey (Petromyzon

marinus L.), Gen. and Comp. Endocrinol. 129, 163–170

(2002).

375. E. Zeiske, “Praedispositionen bei Mollienesia sphenops

(Pisces: Poeciliidae) für einen Übergang zum Leben in

subterranen Gewässern,” Z. Vergl. Physiol. 58, 190–222

(1968).

376. E. Zeiske, H. Breucker, and R. Melinkat, “Gross Mor-

phology and Fine Structure of the Olfactory Organ of

Rainbow Fish (Atheriniformes, Melanotaeniidae),”

Acta Zool. Stockh. 60, 173–186 (1979).

377. E. Zeiske, J. Caprio, S.-H. Gruber, “Morphological and

Electrophysiological Studies on the Olfactory Organ of

the Lemon Shark, Negaprion brevirostris (Poey),” in

Indo-Paciﬁc Fish Biology: Proceedings of the Second

International Conference on Indo-Paciﬁc Fishes, Ed.

by T. Uyeno, R. Arai, T. Taniuchi, and K. L. Matsuura

(Ichthyol. Soc. Jap., Tokyo, 1986), pp. 381–391.

378. E. Zeiske, A. Kasumyan, P. Bartsch, and A. Hansen,

“Early Development of the Olfactory Organ in Stur-

geons of the Genus Acipenser: A Comparative and Elec-

tron Microscopic Study,” J. Morphol. and Embryol.

206, 357–372 (2003).

379. E. Zeiske, R. Melinkat, H. Breucker, and J. Kux, “Ultra-

structural Studies on the Epithelia of the Olfactory

Organ of Cyprinodonts (Teleostei, Cyprinodontoidea),”

Cell Tissue Res. 172, 245–268 (1976).

380. E. Zeiske, B. Theisen, and H. Breucker, “Structure,

Development and Evolutionary Aspects of the Periph-

eral Olfactory System,” in Fish Chemoreception, Ed. by

T. J. Hara (Chapman and Hall, London, 1992), pp. 13–

39.

381. E. Zeiske, B. Theisen, and S. H. Gruber, “Functional

Morphology of the Olfactory Organ of Two Carchar-

JOURNAL OF ICHTHYOLOGY Vol. 44 Suppl. 2 2004

THE OLFACTORY SYSTEM IN FISH: STRUCTURE, FUNCTION, AND ROLE IN BEHAVIOR S223

hinid Shark Species,” Can. J. Zool. 65, 2406–2412

(1987).

382. B. Zielinski and T. J. Hara, “Morphological and Physi-

ological Development of Olfactory Receptor Cells in

Rainbow Trout (Salmo gairdneri) Embryos,” J. Comp.

Neurol. 271, 300–311 (1988).

383. H.-P. Zippel, Regeneration in the Peripheral and the

Central Olfactory System: A Review of Morphological,

Physiological and Behavioral Aspects, J. Hirnfosch. 34,

207–229 (1993).

384. H.-P. Zippel, M. Hofmann, D. L. Meyer, and S. Zeman,

“Functional and Morphological Regeneration of Olfac-

tory Tracts and Subtracts in Goldﬁsh,” J. Comp Physiol.

172A, 91–99 (1993a).

385. H.-P. Zippel, R. Voigt, M. Knaust, and Y. Luan, “Spon-

taneous Behaviour, Training and Discrimination Train-

ing in Goldﬁsh Using Chemosensory Stimuli,” J. Comp.

Physiol. 172, 81–90 (1993b).

Translated by S. V. Budaev

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Приведены результаты полевых экспериментов по оценке эффективности химических аттрактантов для лова сазана Cyprinus carpio удебными донными орудиями лова (карповый монтаж с бойлами и макушанка) в естественном водоёме (р. Ахтуба) 19.06–05.09.2018 г. Использованы насадки: подсолнечный шрот и бойлы “Клубника”, “Слива”, “Тутти-фрутти”, “Сладкая кукуруза” и “Мидия”. Через 2–3 сут после начала внесения прикормки (подсолнечный шрот, зёрна кукурузы и пшеницы, глина в соотношении 1 : 1 : 1 : 5) количество сазана на полигоне и его улов повысились и через неделю достигли уровня, остававшегося стабильным до завершения исследования. Всего выловлено 1048 сазанов массой тела 2–14 кг, средний суточный улов составил 7.23 ± 2.13 экз. Уловы при использовании подсолнечного шрота не менялись на протяжении всего исследования (13–15% суммарного вылова), динамика уловов донками с бойлами с разными ароматизаторами различалась. С применением бойлов “Мидия” в начале исследования поймано большинство рыб, затем уловы стали снижаться и прекратились. Но начали повышаться уловы донками с бойлами “Сладкая кукуруза”, достигнув 70–75% вылова в период массового появления на водоёме рыболовов-любителей, использующих зерновые прикормки. Уловы при использовании бойлов с фруктово-ягодными ароматизаторами оставались невысокими. Рыбы, выловленные с применением разных насадок, по размерам не различались. Результаты подтверждают сведения из литературы о важной роли хеморецепции в поведении сазана. Привлечение рыб к месту лова предположительно обеспечивали запаховые вещества приманки, тогда как уловы зависели от запаховых, вкусовых и текстурных качеств насадок. Меняющаяся эффективность пищевых аттрактантов (летний сезон) указывает на пластичность хемосенсорно регулируемых предпочтений рыб.

Behavioural responses to visual and chemical cues in Mozambique tilapia (Oreochromis mossambicus): a putative pheromonal activity for 17β-estradiol 3-glucuronate

Article

Full-text available

Apr 2025
BEHAV ECOL SOCIOBIOL

In reproduction of Mozambique tilapia (Oreochromis mossambicus), chemical communication mainly relies on urinary steroidal glucuronides (sex pheromones) that dominant males release to prime the final ovulation in pre-ovulatory females and increase reproductive readiness. However, the role of steroids in chemical communication in females has received less attention. Here, we aimed to determine whether 17β-estradiol 3-glucuronate released by pre-ovulatory females functions as a reproductive signal towards males. We investigated the preference of focal males to visual, chemical (female conditioned water), and a combination of both stimuli from pre-ovulatory or post-spawning females, as well as 10− 9 M 17β-estradiol 3-glucuronate. Compared to the control zone, where no stimuli were present, males were more responsive (time spent near the stimuli, digging behaviour, and urination frequency) in the visual and visual + chemical zones than in the chemical-only zone. Males preferred pre-ovulatory to post-spawning female-conditioned water. Interestingly, the time spent by focal males near the source of 17β-estradiol 3-glucuronate was similar to pre-ovulatory conditioned water. However, there was no significant difference in digging and urine pulses in response to 17β-estradiol 3-glucuronate compared to the control group. We suggest that male tilapia recognise the ovulation status of females using visual and chemical cues, and 17β-estradiol 3-glucuronate is part of the odorant content released by pre-ovulatory females to communicate their reproductive status.

Fast, bioluminescent blinks attract group members of the nocturnal flashlight fish Anomalops katoptron (Bleeker, 1856)

Article

Full-text available

Jan 2025
Front Zool

Background During their nighttime shoaling, the flashlight fish Anomalops katoptron produce fascinating, bioluminescent blink patterns, which have been related to the localization of food, determination of nearest neighbor distance, and initiation of the shoal’s movement direction. Information transfer e.g., via alarm signals is an important aspect in group living species especially when being under threat. In dark environments, bioluminescence has the potential to accurately transfer such information. Under threat A. katoptron show increased swimming speeds and a higher group cohesion accompanied by fast blink frequencies. Results In this study we used a two-choice paradigm to test the preferences for typical blink characteristics e.g., frequency and duration. Our data show that individuals decided within short periods (< 4 s) for faster blink frequencies of artificial light organs and the preference for the higher blink frequencies became more pronounced as the difference between the presented frequencies increased. The preference correlated with the frequency rather than the duration. Conclusion Our study suggests that fast, bioluminescent blinks of light organs lead to aggregations of A. katoptron.

The anatomical and histological study of the olfactory organ in the Korean anadromous fish, sea rundace Tribolodon hakonensis (Cypriniformes, Leuciscinae)

Article

Dec 2024

Effect of L-alanine exposure during early life stage on olfactory development, growth and survival in age-0 lake sturgeon Acipenser fulvescens

Article

Dec 2024

Environmental factors play an important role in phenotypic development of fishes, which has implications for hatchery-reared fishes that are released into the wild where natural cues are present. There is interest in examining how early exposure to dietary odourants can affect development of olfaction. The aim of our study was to use behavioural, molecular and electro-physiological techniques to evaluate how introduction of the amino acid L-alanine to the rearing environment might influence the development of olfactory perception of dietary cues, growth and survival in lake sturgeon (Acipenser fulvescens), a species of conservation concern. We hypothesized that exposure to amino acids would influence the onset of feeding during dietary transitions from endogenous to exogenous feeding and predicted that the introduction of L-alanine during early development would promote growth and survival of age-0 lake sturgeon. Additionally, we hypothesized that olfaction in lake sturgeon is a developmentally plastic trait, predicting that the addition of L-alanine prior to exogenous feeding would influence mRNA transcript abundance of genes associated with detection of dietary cues. Our approach was to add L-alanine daily from 17 to 20 days post-fertilization (DPF) before the onset of exogenous feeding. We sampled individuals at 17, 21, 26, 31, 50, 65 and 80 DPF. Additionally, olfactory sensitivity to L-alanine was tested at ~1 year via electro-olfactogram (EOG). We observed no significant differences in mortality or EOG response between L-alanine and control treatments; however, significant differences were observed in morphometrics, behaviour and mRNA transcript abundance of all genes throughout development. Our results indicated the olfactory system exhibited developmental plasticity in response to L-alanine treatment until 50–65 DPF, suggesting that environmental odourants may influence early development of key olfactory processes. Our data could inform practises at conservation hatcheries that are used as part of enhancement programmes for lake sturgeon.

Anatomy and histology of the olfactory organ of the javelin goby Synechogobius hasta (Gobiiformes, Gobiidae)

Article

Full-text available

Dec 2024

Hyun Tae Kim

The olfactory organ of Synechogobius hasta was investigated with a focus on its environmental adaptation, using stereo microscopy and light microscopy. This research revealed the following anatomical and histological characteristics: (i) tubular anterior nostril, (ii) one longitudinal lamella, (iii) two accessory nasal sacs, (iv) lymphatic cells in the lower part of the sensory epithelium, (v) four to five villi of olfactory receptor neurons, (vi) abundant blood capillaries beneath the sensory epithelium, and (vii) rod-shaped erythrocytes. These findings hint that the olfactory organ of S . hasta has anatomical and histological adaptations to intertidal pools that undergo periodic hypoxia and increased temperature under stagnant water conditions due to the tidal cycle.

Olfactory sensitivity of the sturgeon to free amino acids

Article

Full-text available

Jan 1994

A. O. Kasumyan

In five sturgeon species of the family Acipenseridae (Russian (Acipenser gueldenstaedti), Siberian (A. baeri), green (A. medirostris), Caspian (A. stellatus) and the beluga (Huso huso)) it was established that in species close in systematic position the olfactory spectra of free amino acids affecting behaviour match both in breadth and composition. Of the 20 free amino acids used (principally L-stereoisomers, 10-4 M) and betaine, behavioural responses were elicited by solutions only of glycine and L-alanine. The efficacy of glycine was higher than that of L-alanine for all species apart from the Caspian sturgeon; L-alanine is ineffective for the beluga. The response pattern of sturgeons to effective amino acids has the clearly marked character of food search behaviour indicating the identity of the signalling significance of these stimuli. The absence of appreciable species specificity of the attitude of sturgeons to the odorous properties of free amino acids sharply contrasts with the substantial species differences of the taste responses.

The role of chemical signals and olfaction in the sexual behavior of the guppy, Poecilia reticulata ( Cyprinodotiformes, Poeciliidae).

Article

Jan 1982

In intact and blinded males of the guppy a marked preference was noted for water in which females had been kept. Elements of sexual behavior were provoked by this water. Successful realization of the sexual behavior of male guppies also depends on visual reception. -from Sport Fishery Abstracts

THE VERTEBRATE NOSE, REMARKS ON ITS STRUCTURAL AND FUNCTIONAL ADAPTATION AND EVOLUTION

Article

Mar 1969
EVOLUTION

Gunnar Bertmar

INTERSPECIFIC RECOGNITION AND DISCRIMINATION BASED UPON OLFACTORY CUES IN NORTHERN SWORDTAILS

Article

Jun 1999
EVOLUTION

Female Xiphophorus montezumae were attracted to olfactory cues from conspecific and heterospecific (X. cortezi and X. nigrensis) males when given a choice between the stimulus and water. When given a choice between conspecific and heterospecific cues, females only demonstrated a strong preference for the conspecific stimulus when it was matched against X. nigrensis. Female X. nigrensis were attracted to olfactory cues from their close relative, X. cortezi, but did not respond to cues from the more distantly related X. montezumae. They preferred the scent of their own males to the olfactory cues of both heterospecific species. Our results indicate that X. cortezi and X. nigrensis share an apomorphic change in some aspect of their olfactory cue-receiver system that is not shared with X. montezumae. We also uncovered an asymmetry in response based on olfactory stimuli in these fishes: X. montezumae is moderately attracted to the cue from X. nigrensis, whereas X. nigrensis does not respond to the cue from X. montezumae at all.

Trails in open waters: sensory cues in salmon migration

Article

Jan 2003

Alarm signals in fishes

Article

Jan 1992
REV FISH BIOL FISHER

R.J.F. Smith

Receptor cells of various types and their proportional interrelation in the olfactory organ of larvae and adults of acipenserid fishes

Article

Jan 1976

G A Pyatkina

Chemoreception

Article

Jan 1998

Comparative morphology of the peripheral olfactory organ in teleosts

Article

Jan 1982

M. Yamamoto

Structure and function of the vomeronasal organ

Article

Nov 1998

Many animals use their vomeronasal organs to gain direct and specific contact with chemical cues released by congeners and in biological fluids. These cues provide information about the physiological status of the emitter and facilitate or regulate social interactions such as sexual relationships. The present review gives a short description of the discovery of the vomeronasal organ and the pivotal findings of Jacobson. The distribution of the organ and its anatomy in some vertebrates are described. The mechanisms for stimulus entry and egress are discussed, and the findings that led to the appreciation of the vomeronasal organ in mammals as a main chemosensory organ for pheromones mediating reproductive status and inducing sexual behaviour are reported. The anatomical, biochemical and functional properties of the receptor neurones are described.

The Olfactory System in Fish: Structure, Function, and Role in Behavior

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