THE ROLE OF THE LATERAL

LINE IN FISH BEHAVIOR

The lateral line is involved in the feeding, defensive,
schooling, reproductive, and migration behavior in
fishes, allows them to orient in darkness and perform
rheoreaction. When the illumination level is high, other
sense organs are involved along with the lateral line, in
the realization that these behavioral forms may be more
important. In nocturnal fish with or cave or deep-sea
fish, the hierarchy of the sensory systems is different
and the information coming from lateral line receptors
becomes most important.

Feeding Behavior
The ability of the fish to respond to small objectsallows them to
determine the presence of the prey,detect its location with high
precision and make adirected strike. The role played by the
lateral line isclear from the location of the lateral line canals,
theirsizes, and the number of neuromasts. For example, the
largest and most conspicuous canals of the lateral linein many
fishes are located on the head, allowing it to obtain
information about the location and movementsof food objects
in proximity to the mouth and thereby catch the prey . In
fish feeding on fallen insects, large neuromasts are located at
the dorsal surface of the headThe feeding behavior of many
predators having awell-developed lateral line is to a large
extent based onthe information provided by the lateral line
receptors.Using the example of the American muskellunge
E. masquinongy, it was shown that visual receptionplays the
major role in the detection of prey and theslow approach to it,
whereas the final strike and catchingof the prey is mostly
based on the lateral lineAfter the lateral line receptors were
turned off (the anterior and posterior nerves of the lateral
line were cut), the directed strike was observed
from a significantly shorter distance, 10.1 cm. Blind
pikes (visual nerve cut) took the prey only if it accidentally
approached closer than 3.2 cm. Fish devoid of
both visual and seismosensory systems did not even try
to catch prey. The loss of any of these two sensory systems
required more precise orientation to the preybefore the final strike: in
fish with the visual nerve or
lateral line nerves cut, the angle between the direction
to the prey and body position was mush larger than in
intact individuals . The ability of blind fish to hunt successfully is
characteristic
of the pike E. lucius (Hofer, 1908; Disler,
1967). Such fish as the burbot Lota lota, catfish Silurus
glanis, eel Anguilla anguilla, Corvina nigra, Gaidropsarus
mediterraneus, and many other nocturnal or twilight
fishes feed much more efficiently in darkness than
in good illumination. The better the development of the lateral line,
the
better developed are neuromasts and canals and the
more successful are the fish in their behavioral
responses. Comparisons of night feeding in the ruffe
G. cernuus and perch P. flavescens indicated that the
former species is more successful in feeding on live
daphnia. It not only can detect the prey from a greater
distance than perch, but also during the movement by
inertia, when the fish does not move fins; in contrast,
perch could catch daphnias only when immobile
(Fig. 35). The more efficient lateral line in the ruffe
depends on structural characteristics of the lateral line:
larger canal neuromasts, and elastic membranes closing
the canals (Jakubowski, 1967; Janssen, 1997). With
respect to the development of lateral line canals, the
ruffe significantly differs from many other representatives
of perches and is more similar to inhabitants of the
bathypelagial zone. It was hypothesized that membranes
sort out the low frequency hydrodynamic noise
evoked when the fish moves forward by inertia: they
remain concave, but the intra-canal liquid does notmove. It is this
time when the fish can successfully
detect the oscillations created by daphnias. According
to another hypothesis, the membrane may be used as a
resonator amplifying the signal from the preyDue to the
lateral line, many fish, most importantly,
pelagic planktivores such as clupeids, certain cyprinids,
and juveniles of many species, can retain the ability to
feed in complete darkness or if their visual reception is
excluded, and catch individual plankton animal (Janssen
et al., 1995). Blocking of lateral line receptors with
streptomycin causes the blind fish to loose this ability
(Blaxter and Hoss, 1981). Experiments on the sculpin
Cottus bairdi feeding at night indicated that the main
role in it is played by canal neuromasts. Blinded fish
(body length 7.5 cm) responded by alteration of their
orientation and directed strikes at live daphnia 2 mm in
size or bead of 3 mm, generating oscillations with the
same frequency as the swimming daphnia 3 Hz (Kirk,
1985). The response distance reaches 5 mm when the
largest neuromasts are stimulated at the lowest side surface
of the head (mandibular canal) and at the gill covers
(opercular canal). When the less sensitive sector of
the lateral line was stimulated, the fish changed its position
in such a way that the source of the stimulus was in
a more sensitive zone and struck only after thisRepositioning,
i.e., such alteration of the body position
that the source of oscillations was in the most sensitive
zone, is very important for precise orientation and
capture of the prey. In most cases (83%), unsuccessful
final drops of the sculpin were observed if the source of
oscillations was located immediately in front of the fish
(sector 20). When the sculpin moved in short darts to
the source of oscillations, its location in the most sensitive
place at the side was retained. Whenever the fish
turned one side to the source of oscillations all the time,
the movement trajectory represents an arch. Fish canapproach the
source perceiving it with left or right side
receptored in an alternating manner (Coombs and Conley,
1997).
To discover prey in darkness, pelagic planktivores
often use the so-called saltation search when periods of
active swimming are interchanged with short-term
stops. The prey is detected in the moment when the fish
is immobile and the ratio between the hydrodynamic
noise and the useful signal is the most optimal. The distance
of the prey detection and directed drop usually
does not exceed one body length of the predator
(Norton, 1991; Norton and Brainerd, 1993).
Fish living in stagnant or slowly moving water environments
are relatively inactive. Many deep-sea and
bathypelagic fish use free neuromasts to detect active
prey or approaching predators. This is possible due to
several structural and physiological adaptations reducing
the level of low-frequency hydrodynamic noises
affecting the receptors. These adaptations include high
laterally compressed cupules of neuromasts, the large
size of neuromasts, dermal tubercles and papillae positing
neuromasts outside the immobile borderline layer,
the inactivity of the fish and low level of their metabolism.
Many deep-sea fish have very wide and shallow
canals of the lateral line on the head, which in the functional
respect (spectral sensitivity) are not very different
from free neuromasts. Many deep sea fish have an
eellike body and swimming pattern causing a much
lower level of oscillations in the environment. This
reduces the unfavorable hydrodynamic noises and
makes the fish less conspicuous to predators and prey.
It was recently found that the lateral line, along with
the auditory reception, is involved in the search of
active objects not only in water, but also in the bottom
substrate. Sculpins C. bairdi can easily find a 10 Hz
vibration, imitating the moving ground benthos organisms
(Nereis and Lumbriculus). The response to the
vibration is observed only if the fish is placed on thebottom, the
fish touches the surface of the substrate
with its lower jaw, and holds its breathing movements
for more than 1 s. If it receives the signal in this
moment, it rapidly turns to the source of the stimulus.
A series of short darts towards the vibration occurs after
this. It is very important that the fish touches the substrate
with its lower jaw after each dart. The response
terminates by a precise directed strike at the ground in
the place of the oscillation source. The fish can respond
at the distance up to 30 cm, i.e., four–five body lengths.
If the vibration is not contacting the ground, the
response distance is lower, 1–2 cm. The treatment of
mandibular neuromasts at the lower surface of the
lower jaw in large fish with streptomycin or cobalt salt
brings about partial or complete disturbance of the
response: the fish touched the substrate with the lower
jaw but did not dart toward the oscillation source
(Fig. 37) (Janssen, 1990). Most probably, many bottom
fish feeding on infauna can use the lateral line together
with the auditory reception to catch hidden prey objects
from the bottom substrate.
In fish specializing on feeding on fallen insects, the
lateral line provides for not only the information about
the prey, but also allows the fish to determine the distance
to it. The mechanism of the precise detection is
associated with the distribution of the surface waves
evoked by the insect and the ability of the fish to perceive
and analyze these oscillations. There are several
important differences between the surface waves and
the waves distributed in water. In particular, the lowfrequency
components of surface waves distribute at
higher speeds than the high-frequency, whereas the
reverse is characteristic of shift waves. On the whole,
the speed of surface waves is more than 1000 times
lower than waves distributing in the water column.
They hardly penetrate into the water column, therefore
the fish specializing feeding on fallen insects usually
stay at the surface.
The detection of the surface waves is based on canal
and free neuromasts located on the head and is well
developed in such fish as Pantodon buchholzi (Pantodontidae),
Galaxias fasciatus (Galaxiidae, Osmeriformes),
Fundulus notatus (Cyprinodontidae) or
Aplocheilus lineatus (Cyprinodontidae) (Schwartz,
1965; Hoin-Radkovsky et al., 1984). The direction of
the prey is determined due to the difference in the time
and the amplitude of the waves coming to symmetrical
neuromasts on both sides of the fish head (Schwartz,
1965; Schwartz and Hasler, 1966). The distance to the
source is determined due to the well-developed ability
of these fish to analyze the spectral composition of surface
waves coming from the prey and its dynamics. An
insect fluttering in water generates oscillations in a
wide frequency range, much wider than the baseline
oscillations of the water surface evoked by the wind or
the fish itself (Fig. 38). But after a short time after the
signal dispersed a small distance, its spectrum changed
because of the much faster attenuation of high-frequency
components and their slower distribution. The
oscillation amplitude significantly reduces with the distance
from the source (Fig. 39).
Analyzing the frequency, time, and amplitude
parameters of the signal reaching the receptors on both
sides of the body, fish can easily determine the distance
to the prey. The deviation error in the drop is
about 5(. The response distance
in fish reaches 50–60 cm in Fundulus and up to
1 m in Aplocheilus. The response latency is usually
only 0.038 s (Schwartz, 1967). It is quite enough if the
A. lineatus detects only the first eight–ten wave oscillations
to localize the source (Bleckmann and Schwartz,
1981). If the fish are experimentally presented with a
signal, similar in its spectral and frequency parameters usuallyto the
signal from a larger distance, the fish make an
error and perform a more distant drop (Bleckmann,
1993). Fish retain the capability to orient and catch
fallen insects even if they lack almost all neuromasts
(Bleckmann and Schwartz, 1982), but loose this ability
if the artificial source generates a monofrequency rather
than a polyfrequency signal

Defensive Behavior
Large active objects evoke relatively strong, highamplitude,
and low-frequency oscillations, which can
distribute far in water and can be easily perceived by
lateral line receptors, primarily, by free neuromasts.
Large fish are usually the sources of such signals. The
behavioral response to such stimulus expressed in
active escape or hiding, allowing to avoid predators,
especially at night and in twilight hours, when the danger
cannot be so easily detected with other sense
organs. The defensive response to high-amplitude, lowfrequency
oscillations is innate and appears early in the
fish ontogeny, after the first appearance of free neuromasts
in larvae before the beginning of exogenous feeding
or at the beginning of the larval period (Disler,
1960). The involvement of the lateral line in the realization
of the active escape response is supported by the
links between the Mauthner cells (involved in the active
escape response) and lateral line nerves

Schooling Behavior
There is not much data pointing to the possible
involvement of the lateral line organs in schooling
behavior in fish. For example, in observations of a blind
Anchoviella individual, it always joined the school and
repeated all schooling maneuvers (Moulton, 1960). In
experiments with the tuna Euthynnus affinis, the tested
fish separated by a transparent partition were located
with respect to each other differently than when they
were in a single school, pointing to the possible role of
the lateral line in the within-school pattern (Cahn,
1972). Blinded individuals of pollack Pollachius virens
retained the within-school contacts but lost them after
the lateral line nerve was cut (Pitcher et al., 1976; Partridge
and Pitcher, 1980). Unfortunately, many of these
experiments did not control well the completeness of
the deprivation during the whole experiment. The
attempts to associate the transition to schooling with
massive formation of neuromasts in juvenile fish (Blaxter,
1987) are not convincing The examples indicating that the lateral line
is not
important in schooling behavior of fish are much more
abundant (Pavlov and Kasumyan, 2000), when the
retention of the lateral line but exclusion of vision
caused the complete destruction of the school and complete
loss of schooling behavior. It is most likely that
the lateral line plays only a secondary role in the realization
of schooling behavior and provides for precise
coordination during rapid maneuvers, along with
vision, when the distance between schooling partners is
very short (Gray and Denton, 1991). However, as is
supported by many authors, even in compact schools
the involvement of the lateral line seems not completely
convincing because, for example, herrings (Clupeidae)
with very well-developed schooling behavior, have no
lateral line canals on the sides of the body (Sand, 1984;
Popper and Platt, 1993). It was hypothesized (Chubukov
et al., 1987) that in Clupeidae, Carangidae,
Scombridae, and Istiophoridae, the complex network of
canals on the head is primarily used for mutual control
of the swimming speed in the school.
Spawning and Parental Behavior
The complex organization of spawning behavior, characteristic
of many fishes, is often accompanied by displays,
shifts, dances, vibrations, and other specific behavioral
patterns. Obviously, the low-frequency oscillations
may bear very important information and can help in the
synchronization of spawning behavior and spawning. The
efficiency of such signalization depends on a small distance
between the partners, usually less than one body
length, i.e., in the near acoustic field.
The involvement of the lateral line in spawning
behavior has long bee only hypothesized (Tinbergen,
1951; Keenleyside, 1979). Experimental data supporting
this have been obtained only recently in sockeye
salmon Oncorchynchus nerka (Satou et al., 1994a,
1994b). The spawning behavior of males and females
of these fish represents an array of displays: sharp
bends of the body of the female in the nest make the
male somewhat downstream move rapidly towards the
female and a characteristic quivering (vibration) causing,
in turn, a quivering response of the female, signal its readiness
for spawning. In response, the male approaches the
female, quivers, opens its mouth, and releases the sperm.
This releases the female’s response: quivering and release
of eggs. During the body bending and quivering, the fish
cause oscillations with the frequency from 2 to 37 Hz, and
the myograms in males and females at various stages of
spawning behavior are different.
To analyze the role of the low-frequency oscillations
in spawning behavior of these fish, the responses of
dwarf sockeye salmon males to plastic models of a ripe
female (the length of the model 24 cm, depth 6 cm, and
width 4 cm) were observed. The model, vibrating
in the vertical hyperplane with the frequency 2–32 Hz
and the amplitude 1.7–2.5 mm brought about all the
spawning repertoire including the release of the sperm
in males located in a basin with a gravel substrate
(142 42 45 cm, current speed 5–6 cm/s). Depending
on the frequency of quivering, males performed from
2–4 to 7–10 spawning cycles during two minutes of the
experiment. Characteristics of the model coloration
(black or white or models with black upper or lower
parts) did not affect the behavior of the male significantly.
The efficiency of an opaque quivering model
was significantly weaker. The spawning behavior was
not observed in the absence of quivering, when the
vibrating model was shielded by a glass partition, or if
visual and hydrodynamic models were separated from
each other. Interestingly, the dart and quivering of the
male were best stimulated by the model oscillations
with the frequency 2 Hz, whereas opening the mouth
and sperm release, with the frequency of 5 and 21 Hz,
which agreed with the frequency of the quivering performed
by female sat the respective stages of the
spawning behavior (Fig. 40).
Signals perceived with the lateral line receptors may
be very important in parental behavior of certain fishes.
Males of the fighting fish Betta splendens use such signals
to rapidly attract the juvenile offspring swimming
near the surface at a distance from the nest in case of
danger. In such cases, the male takes an oblique posture,
touches the water surface, and makes fluttering
movements with its pectoral fins. This evokes a surface
wave, which can be perceived by the young at a distance
up to 40 cm, and which rapidly causes directed
movement to the source of the oscillations. The
response is observed both in light and in darkness. It
can be easily released in response to an artificial signal
with the optimal frequency 8–10 Hz and amplitude,
13 m. The efficiency of such signalization is quite
high, about 70% of the brood approaches the nest after 1–2 min

Orientation in Space
and the Response to the Current
Many fish species experience water currents. The
ability to determine its presence, strength, direction, and the structure
is extremely important for the survival
and most behavioral forms: defensive, territorial,
spawning, schooling, migration, etc. (Pavlov, 1979,
1980, 1986). This ability is especially important for the
species living under conditions of turbulence or in darkness,
or who are active at night. Orientation against the
current is necessary to the fish feeding on drift because
it allows them to obtain olfactory information about the
approaching prey, for energetically more efficient resistance
to the current, for migrations or redistribution
within the same habitat, as in nearshore marine fishes of
the tidal zone, and to retain their position within the
current and so on.
The perception of the current by the fish is possible
due to free neuromasts, the cupules of which are
directly affected by the pressure of the water passing
along the fish body (Engelmann et al., 2000). Removal
of free neuromasts causes the same increase of the fish
response threshold to the current as the simultaneous
removal of all types of neuromasts (Cheimarrichthys
fosteri, Pagothaenia borchgrevinki, blind form of Astyanax
fasciatus). Blocking of only intra-canal neuromasts
does not cause any significant deviations in the
fish sensitivity to the current. When food scent appears
in water, the sensitivity of the fish to the water current
significantly increases
Removal of free neuromasts significantly interferes
with the rheoreaction in marine cartilaginous fishes, as
has been shown in the shark Heterodontus portusjacksoni
Due to the lateral line, fish can orient in the environment
in complete darkness and detect obstacles. It has
been hypothesized first by Dijkgraaf (1963), and
experimentally
corroborated by Campenhausen et al. (1981
etc.) in cave fish. Cave fish constantly perform hydrodynamic
monitoring of their environment, specific
hydrodynamic location, comparable with the echolocation
of bats (Chiroptera) and Noctuidae butterflies
(Lepidoptera) or the active electrolocation of weakly
electric fishes (Lapshin et al., 1993; Lapshin, 1995;
Moller, 1995). As a result of this location, the fish create
a three-dimensional “hydrodynamic representation”
or “hydrodynamic image” of the environment (Hassan,
1989). And this makes their orientation in darkness
possible. Moving forward by inertia, i.e., without their
own active movements, the fish induces wave oscillations
and creates a hydrodynamic field, which is disturbed
by any objects in proximity reflecting these
waves (Fig. 42). The pattern of the field disturbance
depends on the size and shape of the object, the speed
of its movement, the pattern of swimming, etc.
The use of the lateral line to avoid encounters with
obstacles in darkness was experimentally shown in
other fish species: intact dace Leuciscus leuciscus with
the length of 4–5 cm could successfully avoid encounters
with a plate placed into the water current with the
speed gradient from 0.3 to 2.0 cm/s/cm at the distance
not more than 20 cm (Pavlov and Tyuryukov, 1993,
1995). The reception of oscillations, reflected by large
underwater objects, allows fish to use these objects as
stationary landmarks, which is very important for territorial
fishes, such as juvenile salmons, retaining their
position not only in the light but also in the dark part of
the day, and successfully resist the current. After the
nerves enervating neuromasts on one side of the body,
the fish can retain orientation with respect to such
objects due to receptors on the intact side

ONTOGENY OF THE LATERAL LINE

The first neuromasts appear in embryos under the
shell, as for example, in carp Cyprinus carpio and many
other fish species The formation of neuromasts is induced by lateral
line nerves, which develop from ganglion
cells originating from the respective placods. The
growth of nerve fibers and their branching rapidly
makes the peripheral nervous network of the lateral line
more and more complicated (Fig. 43). The first neuromasts
appear where the branching nervous fiber grows
down to the epithelium. Free neuromasts are the first to appear. In
many fish
species (Lateolabrax japonicus, Acanthopagrus
schlegeli, Kareius bicoloratus, Tridentifer obscurus,
etc.) they are conspicuous on the head even in just
emerged embryos, regardless of their small size and
rarity . In other fish (Hypomesus transpacificus,
Tribolodon hakonensis, Zacco platypus, Oryzias
latipes, etc.) neuromasts become easily visible due to
the cupula about one day after emergence (Iwai, 1972).
The size and number of free neuromasts increases rapidly
and already several days or even hours after emergence
they can be found on the body, first in its anterior
part, and then in the caudal part, and finally homogeneously
cover the body of the larvae The depth of the cupula at the moment of
neuromast
formation rapidly increases. As it was determined in
larvae of herring and cod, its growth is 1.4–4.1 m/h
(Blaxter, 1984, 1987). Due to the proliferation ability,
free neuromasts appear during the whole life of the fish
or at least during a significant period rather than in only
a limited period of early ontogeny (Disler, 1960;
O’Connel, 1981). The rate of new neuromast formation
differs in fish with a different mode of life, especially
the hydrodynamic conditions of further development.
For example, in fish laying eggs on water vegetation
(roach Rutilus rutilus, bream Abramis brama,
verkhovka Leucaspius delineatus) free neuromasts
develop faster and the recently emerged embryo have
almost two times more neuromasts per unit area of the
body than in embryos of fish spawning in mountain rivers
with a stony bottom (Diptychus maculatus,
D. dybowskii, Schizothorax pseudoksaiensis issikkuli,
Leuciscus schmidtii (Disler, 1960). The sizes of free
neuromasts in juveniles of older age groups differ less
(Fig. 45) (Wonsettler and Webb, 1997).
The formation of lateral line canals occurs significantly
later, but the vector is the same: head canals are
the first to appear, and only later, the body canal of the
lateral line. The canals development is induced by neuromasts:
separate free neuromasts first appear in places of
the canal formation. Then, their number increases, they
form even rows and continuously go down to the epidermal
groove. The roof of the canal is developed later. It
appears in the body canal in its anterior part and then distributes
in the caudal direction. The relative sizes of the
pores, leading to the canal are reduced. In larger individuals,
they could rise above the epithelium surface as
short tubes.
The canal neuromasts become larger with the
growth of the fish (Fig. 45). The number of receptor
cells in them increases, but the number of canal neuromasts
after canal formation does not change. In juveniles
of Paralichthys olivaceus (Kawamura and Ishida, 1985),
the first to develop is the mandibular canal, on the 25th
day after hatching (at the temperature 16.2–20.7C) All
canals are formed at the head to the 53th day. The formation
of the body canal occurs by the 67th day. In flatfishes,
the development of the lateral line canals on both
sides of the body is asynchronous—rapidly on the eye
side and with a delay on the blind side (Harvey et al.,
1992). In Latimeria chalumnae, lateral line canals are
formed extremely early, in embryos with a yolk sac, the
number of pores on the head approaches 300, in early
juveniles, 500, and in mature individuals, almost 3000
(Hensel and Balon, 2001).
Almost immediately after the appearance of the first
neuromasts, the lateral line becomes active and functional.
Early juveniles of fish and even prolarvae (e.g.,
keta O. keta) can respond to stimuli adequate for the lateral
line, such as currents and large underwater objects.
Very soon, later larvae and early fry exhibit responses
to weak hydrodynamic signals evoked by smaller active
objects like food organisms.
Abstract—This paper reviews the recent studies of the lateral line in
fishes. The structure of free canal neuromasts,
their receptor units, lateral line canals, vesicle of Savi, innervation,
size, and the distribution of the lateral
line organs in fishes with various life modes and systematics. The
functional parameters of the lateral line, such
as the spectral and differential sensitivity of free and canal neuromasts
are analyzed along with their functional
specialization, the nature and sources of adequate stimuli for the
receptors of the lateral line, morphological
adaptations directed to increase the sensitivity and widening the
spectrum of the stimuli perceived (the size of
the cupula, papillae, links between the lateral line canals and the
swimming bladder, intra-canal septa and narrowing
of the canals near the neuromasts zones, elastic membranes closing
the canals, etc.). The data are present
on the ability of fish to determine the source, of hydrodynamic
fluctuations located in the water column, at the
water surface or hidden within the bottom substrate, and the distance
to the source, the distance of lateral line
sensitivity in different fish species. The role of the lateral line in the
feeding, defensive, schooling, reproductive,
and parental behavior of fish is considered in detail. We also review
the responses of fish to the water current,
their orientation, and ways of hydrodynamic camouflage. The
dynamics of the neuromasts appearance during
the ontogeny is traced, along with the development of the lateral line
canals, and the development of its function
in the ontogeny, effects of pollutants on the behavior of fish, managed
by the lateral line.
STRUCTURAL ORGANIZATION
OF THE LATERAL LINE
Characteristic epidermal structures, neuromasts,
form the peripheral region of the lateral line (Fig. 1a).
Neuromasts (literally sensitive tubercles using outdated
terminology) consist of two basic cell types: hair cells
and supporting cells. Hair cells are the secondary-sensitivity
receptor cells having an epidermal origin (Fig.
1b). Each hair cell bears one high kynocyle (5–10
m)
and 30–150 shorter stereocilia (2–3
m) at its free surface.
The height of stereocilia continuously reduces
from the kynocyle, which is always located excentrically.
Such a position of the kynocyle makes the hair
cell morphologically polarized. The structure of the
kynocyle is similar to motile flagella, looking like
micro tubules (9+2). Stereocilia lack such structures
(Flock, 1965).
The number of hair cells in neuromasts depends on
its size and differs widely, from several dozen to hundreds
and thousands. The average density of hair cells
in neuromasts varies less. For example, in the common
ruffe Gymnocephalus cernuus it is about 38000 per mm2,
in neuromasts of Cotus bairdi, about 50000 per mm2,
and in neuromasts of the australian shark Mustelus antarcticus
(Triakidae), 40000–52500 per mm2 (Gray and
Best, 1989; Janssen et al., 1987; Peach and Rouse,
2000). Hair cells in neuromasts are oriented in two
opposite directions. Zones with similarly oriented
receptor cells are absent in neuromasts and, therefore
even adjacent hair cells in neuromasts may be oriented in
opposite directions. The ratio of the cells with the opposite
orientation in canal neuromasts is close to 1 : 1.
Each hair cell is surrounded by supporting cells. At
the periphery of the neuromast, where receptor cells are
absent, there are so-called cover cells, separating the
sensory field of the neuromast from the epithelium
(Münz, 1979; Coombs et al., 1988). The surface of the
sensory zone of the neuromast ranges from 40 to 80%
of the overall area of the neuromast base (Jakubowski,
1967). In the basal part, the hair cell has synaptic contacts
with afferent and efferent nerve fibers. The afferent
fibers, which transmit signals to the neural centers
of the lateral line, ramify at the base of the neuromast
and in many fish species loose their myeline cover.
Each of them contacts with several similarly oriented
hair cells. The central regulation of hair cells is via
efferent fibers (Fig. 1a).
Kynocyle and stereocilia of hair cells are submerged
into transparent and flexible cupula, vertically dominating
above the surface of the sensory epithelium and
having the shape of a cylinder hemisphere or blade. A
gel-like media, creating the cupula, is secreted by nonreceptor
cells of the neuromast: the internal part of the
cupula, by the foot cells, the outer layer, by the cover

There exist data that the cupula has

a certain net-like internal structure, formed from filaments
of high density (Iwai, 1967). In different species
of fish, depending on the location of the neuromast, the
depth of the cupula ranges from 0.1 to 0.7 mm and is
usually well discernible even at low magnification.
Neuromasts are supplied with blood due to a welldeveloped
network of blood capillaries.
Two types of neuromasts are usually distinguished:
free or superficial neuromasts and canal neuromasts.
Free neuromasts are located freely at the surface of the
body, their cupules are washed by the water and are
affected by environmental agents. Among the free neuromasts,
researchers usually distinguish primary or
paedomorphic neuromasts, which develop from placods,
and secondary or neomorphic neuromasts, which
either bud off from the primary neuromasts or develop
from epidermal cells due to the inducing effects of
afferent nerves (Disler, 1960; O’Connel, 1981; Coombs
et al., 1992). All canal neuromasts are primary neuromasts.
They are hidden inside epidermal or bony
canals, which are found on the body or on the head of
the fish, and open with special pores. Free and canal
neuromasts differ in structural and functional characteristics,
and the role which they play in the behavior of
the fish. Neuromasts, in various forms, can be found in
all species of fish.

Free Neuromasts
Free neuromasts are usually small. They commonly
have a cylindrical cupula and round base, the diameter
of which rarely reach 100
km (Münz, 1979; Coombs
et al., 1988). In certain species (Phrinichthys, Neoceratias,
Astyanax, Gobius) the bases of free neuromasts
are stretched and the cupula is compressed laterally,
coinciding in its section with the neuromast base
(Montgomery et al., 2001). The number of hair cells in
free neuromasts is relatively small, from several dozens
to several hundreds.
Free neuromasts can be found in lampreys
Petromyzontes (in Mixini, typical neuromasts are
absent), they are very numerous in teleost fishes Chondrichthyes
and in several bony fishes, Clupeidae, Cyprinidae,
and in certain Characinidae (Astyanax)
(Schemmel, 1967; Puzdrowski, 1989). Free neuromasts
are located openly on the head and the body of the fish,
in certain species at the caudal fin, most often at the
same level with the surface of the adjacent epithelium
(Fig. 3). Sometimes, e.g., in lampreys, free neuromasts
occur on small tubercles. In gobies Gobius, Pomatoschistus
(Gobiidae), deep-sea anglerfish Neoceratias
(Neoceratidae), Phrinichthys (Diceratiidae) and other
Ceratoidea (Lophiiformes), the tubercles, bearing free
neuromasts, are quite large and look like wide papillae
(Fig. 4) (Marshall, 1986, 1996). In Chondrichthyes and
certain other fishes (e.g., in the American pike Esox
americanus, channel catfish Ictaluridae, Amia calva,
carp larvae Cyprinus carpio, etc.), free neuromasts may
be located in depresions of the epithelium. In sharks,
rays, chimaeras, dipnoans (Lepidosiren, Neoceratodus,
and Protopterus), Polypteridae and others, neuromasts
are located on small tubercles at the bottom of epithelial
pits or depressions. Free neuromasts in these fish are
called pit organs (Webb and Northcutt, 1997; Maruska,
2001). They have earlier been erroneously considered
electroreceptor structures, but recent detailed studies of
their morphology showed that the pit organs are just
typical neuromasts (Tester and Nelson, 1969; Webb and
Northcutt, 1997; Maruska and Tricas, 1998; Peach and
Rouse, 2000). In lower sharks, chimaeras, and certain
teleosts, pit organs are located on the body in rows,
sometimes submerged in grooves. This was the basis
for the hypothesis that such rows of pit organs represent
analogues of the lateral line canals and that they
appeared during the evolution from typical canals of the
lateral line found already in primitive ancestral forms of
vertebrates (Northcutt, 1989). It is hypothesized that, in
fish, the formation of the canals is not terminated by the
development of the epidermal roof, and that the pit
organs represent modified canal neuromasts (Webb and
Northcutt, 1997). Interestingly, in the coelacanth
Latimeria chalumnae, the grooves with pit organs are
covered by a thin, skinny membrane (Hensel and
Balon, 2001).
The system of free neuromasts the blind side of the
European sole Solea vulgaris is very characteristic. The
density of neuromasts here ranges from five to ten per
mm2, they are located orderly at the same distance from
each other and surrounded by high (up to 3 mm in
adults) papillae (Fig. 5). It is considered that the papillae
rising over the relatively high (about 100
m) rhombus-
like cupula of the neuromast protect it from the disturbances
during the movement and feeding of these
bottom fish (Appelbaum and Schemmel, 1983). Similar
papillae surround free neuromasts on the blind side of
the body in New Zeland sole-like flounder Peltorhamphus
novazeelandiae (Roper, 1981). Due to the great
diversity of free neuromasts, a system for their classification
is suggested (Srivastava and Srivastava, 1968;
Coombs et al., 1988).
Free neuromasts may form groups, either short and
not connecting with each other as in gobies (Gobiidae)
or deep-sea anglers Phyrinchthys (Diceratiidae)
(Fig. 6) (Marshall, 1986). The orientation of the neuromasts
combined in the same row usually coincides and
is usually perpendicular to the row direction. On the
surface of the body and on the head of the fish, free neuromasts
are usually found in proximity to lateral line
canals (Coombs et al., 1988). In the latter case, neuromasts
are oriented parallel or perpendicularly to the
canal direction (paedomorphic or primary free neuromasts,
see Coombs et al., 1992). Free neuromasts of the
neomorphic type (secondary neuromasts) may have
very different orientation independent of the direction
of the canal (Dijkgraaf, 1963; Münz, 1979; Coombs
et al., 1988; Visher, 1989; Webb and Northcutt, 1997).
Due to the ability to proliferation, their number, especially
in early ontogeny, rapidly increases. The number
and topography of free neuromasts on the head varies
less than on the body
It was counted that in the goldfish, Carassius auratus,
the number of free neuromasts each side of the
body is about 1000, whereas the number of canal neuromasts
is significantly smaller and ranges from 52 to
60 (Puzdrowski, 1989). The number of free neuromasts
is higher than canal neuromasts in cods (Gadidae)
(Table 1). However, in many fish, the number of free
neuromasts is small or they are almost absent, as, for
example, in Siluridae and Mormyridae (Lekander,
1949; Harder, 1968), which is usually linked with the
presence of numerous ampular electroreceptors in these
freshwater fishes, which are homologous to free neuromasts
(Coombs et al., 1988). In fish living in running waters with high turbulence,
free neuromasts are usually
not numerous or almost completely absent. In fish
living in standing or slowly moving waters, free neuromasts
are usually more numerous. The life-style and the
role of the lateral line in the behavior may determine
not only the number but also many structural characteristics
of free neuromasts. For example, in the blind cave
form of Astyanax fasciatus, the capsule of free neuromasts
is two times deeper than in the nonblind form.
(earlier considered a separate species A. mexicanus)
(Teyke, 1990). Similarly, the depth of the cupula differs
in the species differently adapted to life in underground
water bodies (Poulson, 1963). In blind fish, the deepest
cupules are found on the neuromasts located on the
head (up to 300
m), they are about three times smaller
on the body, and their depth homogeneously reduces in
the rostro-caudal direction

Free neuromasts at the blind surface of the head of

the European sole Solea vulgaris. (a) Individual neuromast
surrounded by numerous epidermal papillae; (b) scheme of
the free neuromast (dark circles) and epidermal papillae
positioning (light circles)
Rows of free neuromasts in fish: (a) on the head and the body of Phrynichthys
wedli (based on Marshall, 1996); (b) at the
head of Gobius niger

Examples of fish having direct mediolateral body canal of the lateral line (Salmonidae,
Clariidae, Esocidae) and fish having the
body canal shifted in the dorsal
Examples of fish having curved (Centrarchidae, Carangidae, Chaetodontidae,
Pentoceratidae, Pleuronectidae) or zigzag
(Balistidae) body canal of the lateral line

Examples of fish having broken body canal of the lateral line (Scaridae,
Cichlidae), incomplete body canal (bitterling Rhodeus
sericeus, verkhovka Leucaspius delineatus, Pomacentridae), having several
parallel body canals (Hexagrammidae), and the
fish having no body canals (Clupeidae)
Lateral line canals at the head of the common chop
Zingel zingel (a), ruffe Gymnocephalus schraetser (b), and
Hoplostethus mediterraneus (c) (from Jakubowski
Lateral line canals at the head of the common ruffe
Gymnocephalus cernuus: (1) upper temporal or frontal
commissure; (2) temporal; (3) supraorbital; (4) suborbital;
(5) preoperculo–mandibular. White ovals degignate the
positions of canal neuromasts Network of canals at the head of Sardina pilchardus

Morphological characteristics of the body lateral

line canals in fish with scales. (a) Sagittal section of the
canal: (1) neuromasts; (2) canals perforating the scales;
(3) pores of canals; (4) scale; (5) neural fibers enervating
neuromasts; (6) basic lateral line canal (based on Bond,
1979). (b) Lateral line scales of the American pike Esox
americanus: (1) neuromasts; (4) scales with grooves (based
on Merrilees and Crossman, 1973). (c) Scales of the
mediolateral body canal of Hexagrammos decagrammus,
viewed from above and from aside
Scheme of lateral line canals at the dorsal (a) and
ventral (b) side of the body in Gymnura micrura ray:
(1) supraopercular canal; (2) hyomandibular canal; (3) posterior
canals; (4) infraopercular canal; (5) hyomandibular
canal

Multiplied pore in the anterior part of the body

canal in the European sole Solea vulgaris
Lateral line canal system on the eye (a) and blind (b) sides of the body in the plaice
Pleuronectes platessa: (1) body canal;
(2) supratemporal canal; (3) temporal canal; (4) supratemporal commissure; (5) supraorbital
canal; (6) infraorbital canal; (7) preoperculo–
mandibular canal

Vesicles of Savi and the Spiracular Organ

Skates (Torpedo, Narcine, and Dasyatis) have characteristic
structures, the vesicles of Savi, which also
belong to the lateral line system. The origin and functions
of Savi vesicles still remain unclear in spite of the
fact that these structures have been described since the
middle of the nineteenth century (Savi, 1844, cit. in
Maruska, 2001). The vesicles of Savi represent closed
cavities, located at the depth 0.5–2.0 mm under the
layer of epidermis, derma, and connective tissue. They
are surrounded by a cartilaginous cover and isolated
from the external environment. The vesicles of Savi are
located in symmetrical rows at the head of skates, but
are most numerous at the ventral surface. Vesicles have
an oval shape and are oriented similarly in the same are surrounded by a
cartilaginous cover and isolated
from the external environment. The vesicles of Savi are
located in symmetrical rows at the head of skates, but
are most numerous at the ventral surface. Vesicles have
an oval shape and are oriented similarly in the same that fish can use the
vesicles of Savi to discover the
source of vibrations within the bottom substrate, to
obtain information about the character of the substrate
during touching, or touching the partner of group or
touching of prey (Nickel and Fuchs, 1974; Barry and
Bennett, 1989; Maruska and Tricas, 1998; Maruska,
2001). These hypotheses are supported by the fact that
the vesicles of Savi are more common in bottom-dwelling
fish (skates) and are absent in pelagic fish
(Maruska, 2001).
Cartilaginous and the majority of teleost fishes have
the spiracular organ. It represents an isolated cavity in
the hyoid arch zone. The morphology and the functions
of the spiracular organ are still poorly understood. It
was hypothesized that it could have proprioreceptor
functions and control the movements of the hyomandibular
apparatus in fish

INNERVATION OF THE LATERAL

LINE ORGANS
It has been considered for a long time that the innervation
of the lateral line organ involves the nervous
trigeminus (V), n. fascialis (VII), n. glossopharyngeus
(IX), and n. vagus (X). It was thought that these nerves
unite into the so-called nervous lateralis anterior, innervating
neuromasts on the head of the fish. Neuromasts
of the body and the caudal peduncle was innervated by
n. lateralis posterior, formed by branches of n. glossopharyngeus
and n. vulgaris. Some branches of the
n. lateralis posterior may also innervate neuromasts, on the body, and certain
other nerves. Ancient fossil
animals had, probably, not less than four nerves in the
lateral line, and some of them had seven nerves (Northcutt,
1989).
Central nuclei of the lateral line are situated in the
acoustic–lateral area of the medulla above the auditory
centers and close to them, as well as in eminentia granularis
of the cerebellum. Ascending pathways link
these centers with regions of the mesencephalon (torus
located in posterior regions of the head. For example,
one branch of the n. pharyngeus innervates the middle
part of the supratemporal canal and the adjacent free
neuromasts.
Recently, this scheme of innervation was rejected
(Northcutt, 1989; Coombs et al., 1992). It is thought
that teleost fishes have at least three separate nerves in
the lateral line (n. lateralis) with their own ganglia: dorsal
and ventral anterior nerves of the lateral line, innervating
free and canal neuromasts at the fish head, posterior
nerve of the lateral line, enervating neuromasts
semicircularis), and then with the thalamus and telencephalon
(McCormick, 1989). The important role of
the cerebellum in the lateral line is illustrated by the
fact that its extirpation causes the loss of previously
acquired and blocks the development of newly conditioned
reflexes to lateral line signals

Lateral line organs at the dorsal (a) and ventral (b) body
sides in a weakly electric ray Narcina brasiliensis; vesicle
of Savi is given within the border. (1) Supraopercular canal;
(2) vesicles of Savi; (3) infraorbital canal;
(4) hyomandibular canal; (5) electric organ; (6) posterior
canal; (7) peripheral neuromasts; (8) central neuromast
Hydrodynamic disturbances evoked by swimming
danio Brachydanio rerio in a media with stratified temperatures.
The visualization was based on light diffraction in a
shallow aquarium, vertical temperature gradient 2C/cm

Measures used in a study of the responses of the muskellunge Esox masquinongy to active
prey: coordinates of the prey (a)
and the locomotor response of the predator (b). , elevation, azimuth, (1) distance to the
prey, (2) ambush distance, (3) drop distance
Discovery of a source of underwater oscillations (10 Hz) imitating an active food object and hidden in the
bottom substrate
by the sculpin Cottus bairdi. (a) Target linked with a vibrator and hidden in sand ground at the depth 4 mm from
the surface;
(b) search movements of the sculpin. Silhouettes (1–9) point the subsequent alterations of the position and
orientation of the fish,
the angles between the direction of the initial orientation of the fish (before the stimulation), and the direction to
the source of oscillations
() and the direction of the fish after pre-orientation after the first drop ()

Amplitude, dynamic, and frequency parameters of surface waves, generated by fallen at water surface
flying insects (a),
fish (b), and wind
Scheme of the hydrodynamic field, generated by
the fish swimming by inertia (a), disturbance of the field by
an immobile object (b), and the scheme of the hydrodynamic
gradient at the surface of the fish body when it locates
in proximity to an immobile object

The development of the peripheral network of the anterior nerve of the lateral line in the
ontogeny of Eigenmmania sp.:
(a) juveniles at the age three days with the length 5.5 mm, neuromasts are absent on the head;
(b) juveniles at the age four days with
the length 6.25 mm, there are 17 neuromasts on the head; (c) juveniles at the age 5 days with
the length 6.5 mm, there are 23 neuromasts
on the head; (d) juveniles at the age seven days with the length 7.0 mm, there are 35
neuromasts on the head. The shadowed
zone indicates the location of the fluorescent stain injection, which spread along nervous
fibers. Arrows point to the branches of the
anterior nerve of the lateral line, simultaneously enervating neuromasts and electroreceptor
organs
The appearance of free neuromasts in early ontogeny of fish: (a) Paralichthys olivaceus, (1)
newly hatched embryos,
(2), (3), (4), (5) after 9, 21, 30 h and 9 days after hatching (Kawamura and Ishida, 1985); (b)
one-day old juveniles of Lateolabrax
japonicus; (c) one-day old juveniles of the goldfish Carassius auratus
Orientation in Space
and the Response to the Current
Many fish species experience water currents. The
ability to determine its presence, strength, direction, and the structure is
extremely important for the survival
and most behavioral forms: defensive, territorial,
spawning, schooling, migration, etc. (Pavlov, 1979,
1980, 1986). This ability is especially important for the
species living under conditions of turbulence or in darkness,
or who are active at night. Orientation against the
current is necessary to the fish feeding on drift because
it allows them to obtain olfactory information about the
approaching prey, for energetically more efficient resistance
to the current, for migrations or redistribution
within the same habitat, as in nearshore marine fishes of
the tidal zone, and to retain their position within the
current and so on. The perception of the current by the fish is possible
due to free neuromasts, the cupules of which are
directly affected by the pressure of the water passing
along the fish body (Engelmann et al., 2000). Removal
of free neuromasts causes the same increase of the fish
response threshold to the current as the simultaneous
removal of all types of neuromasts (Cheimarrichthys
fosteri, Pagothaenia borchgrevinki, blind form of Astyanax
fasciatus). Blocking of only intra-canal neuromasts
does not cause any significant deviations in the
fish sensitivity to the current. When food scent appears
in water, the sensitivity of the fish to the water current
significantly increases (Montgomery et al., 1997;
Baker and Montgomery, 1999a, 1999b) (Fig. 41).
Removal of free neuromasts significantly interferes
with the rheoreaction in marine cartilaginous fishes, as has been shown in the
shark Heterodontus portusjacksoni
(Peach, 2001).
Due to the lateral line, fish can orient in the environment
in complete darkness and detect obstacles. It has
been hypothesized first by Dijkgraaf (1963), and experimentally
corroborated by Campenhausen et al. (1981
etc.) in cave fish. Cave fish constantly perform hydrodynamic
monitoring of their environment, specific
hydrodynamic location, comparable with the echolocation
of bats (Chiroptera) and Noctuidae butterflies
(Lepidoptera) or the active electrolocation of weakly
electric fishes (Lapshin et al., 1993; Lapshin, 1995;
Moller, 1995). As a result of this location, the fish create
a three-dimensional “hydrodynamic representation”
or “hydrodynamic image” of the environment (Hassan,
1989). And this makes their orientation in darkness
possible. Moving forward by inertia, i.e., without their
own active movements, the fish induces wave oscillations
and creates a hydrodynamic field, which is disturbed
by any objects in proximity reflecting these
waves (Fig. 42). The pattern of the field disturbance
depends on the size and shape of the object, the speed
of its movement, the pattern of swimming, etc.
Observations of blind Mexican fish Astyanax fasciatus
(Characidae) indicated that when the fish locate the
space and find a novel object, it uses characteristic tactics:
approaching the object, they swim in proximity to
it by inertia. Such behavior could be repeated several
times, the fish changes the direction approaching the
object from a different side. If the fish passes above the
object, it shifts from the vertical axis so that the side
surface of the body was directed to the novel object.
The cave fish could easily discover cylindrical objects
with a diameter up to 2 mm at the distance of several
mm in water, which was determined using the conditioned
reflex methods. The fish could discriminate grids
if the distance between the vertical partitions differs by
12.5% towards its increase or decrease, e.g., grids with
the distance between the partitions 10 mm from grids
with the step 8.75 or 11.25 mm (Campenhausen et al.,
1981; Weissert and Campenhausen, 1981).
If the task is more complicated and the fish are
transferred into a completely new environment rather
than presented with novel objects, exploratory behavior
looks different. In this case it involves more rapid
swimming during the first days (Teyke, 1985). Smaller
individuals swim with relatively higher speed than
large, which is probably associated with the need to
generate more high-amplitude shift waves, i.e., for the
formation of a larger near acoustic field (Teyke, 1988).
Blocking the lateral line receptors with salts of heavy
metals brings about the compensatory increase of the
fish swimming speed. That is, the loss of sensitivity
causes the tendency to generate a stronger signal. The
hydrodynamic image of the environment (cognitive
map) is retained in the fish memory at least for several
days, because individuals returning after two days to a
familiar environment spent much less time on exploratory
behavior than if placed in a novel environment
(Teyke, 1989). Hydrodynamic location and the orientation
of cave fish involves primarily the canal neuromasts
(Abdel-Latif et al., 1990).
The use of the lateral line to avoid encounters with
obstacles in darkness was experimentally shown in
other fish species: intact dace Leuciscus leuciscus with
the length of 4–5 cm could successfully avoid encounters
with a plate placed into the water current with the
speed gradient from 0.3 to 2.0 cm/s/cm at the distance
not more than 20 cm (Pavlov and Tyuryukov, 1993,
1995). The reception of oscillations, reflected by large
underwater objects, allows fish to use these objects as
stationary landmarks, which is very important for territorial
fishes, such as juvenile salmons, retaining their
position not only in the light but also in the dark part of
the day, and successfully resist the current. After the
nerves enervating neuromasts on one side of the body,
the fish can retain orientation with respect to such
objects due to receptors on the intact side (Sutterlin and
Waddy, 1975).
Vesicles of Savi
Vesicles of Savi are found primarily on the ventral
surface of torpedinid, narcinid, and dasyatid batoids
(Norris 1932, Szabo 1958, 1968, Nickel&Fuchs 1974,
Chu & Wen 1979, Barry & Bennett 1989, Maruska &
Tricas 1998), but the function of these receptors still
remains unknown. Narcine brasiliensis has neuromasts
that are located in enclosed vesicular pouches,
which sit approximately 0.5–2.0mmbelow a relatively
compliant skin surface. Morphology of vesicles of Savi
is similar in Narcine and Torpedo where each vesicle
contains 3 neuromasts (one large central and 2 smaller
peripheral), each of which has its own cupula and
hair cells polarized parallel to the center of the neuromast
(Szabo 1968, Barry & Bennett 1989). However,
the cupula of the central neuromast in N. brasiliensis
appears more dense than the cupulae of the peripheral
neuromasts (observed in fresh tissue). Therefore,
it is possible that the cupula of the central neuromast is
weighted, and may be similar to the situation found in
the otolithic organs of teleost fishes. Therefore, these
electric rays may encode linear accelerations of the
body in multiple directions because the vesicles of Savi
are arranged in rows oriented 45_ from the rostrocaudal
body axis on both the dorsal and ventral surfaces.
However, further analysis of cupular composition, hair
cell polarization, and neuromast-cupular coupling is
needed before conclusions can be made on the significance
of variation in cupular density within the vesicles
of Savi.
Vesicles of Savi in the dasyatid rays differ slightly
in morphology and distribution from Torpedo and
Narcine (Chu & Wen 1979, Maruska & Tricas 1998).
In dasyatids, vesicles of Savi are located only on the
ventral surface, contain only a single neuromast, are
contiguous with the lumen of the supraorbital canal
on the rostrum, and adjacent vesicles are connected
by tubules (Maruska & Tricas 1998). Garman (1888)
described a change in the subrostral canal of the
batoids, Potamotrygon and Paratrygon, from a tubular
structure to a row of closed rings connected by tissue,
which may represent another morphological variant of
the vesicles of Savi. Several researchers suggest that
vesicles of Savi may represent an obsolescent canal
condition, but conclusions can not be drawn until the
morphological diversity of these structures is assessed.
Also, the presence of vesicles of Savi only in the
torpediniform and dasyatid batoids suggests that these
vesicles evolved independently in these groups, but
conclusions on evolutionary relationships can not be
proposed until additional taxa are examined.
Vesicles of Savi are hypothesized to be receptors
used to detect substrate-bourne vibrations transmitted
via the skin or cartilaginous attachments in Narcine
(Barry & Bennett 1989), or serve as specialized tactile
receptors sensitive to displacement of the underlying
skin caused by contact with prey, conspecifics, or the
substrate (Nickel & Fuchs 1974, Maruska & Tricas
1998). Electrophysiological experiments in Torpedo
indicate the vesicles of Savi have a peak sensitivity
to vibrations of 150–200 Hz (Szabo 1968). Barry &
Bennett (1989) suggest the vesicles may be high frequency
vibration receptors due to their isolation and
protection of the central neuromast by an arch in
Narcine, but this remains to be experimentally tested.
The concentration of vesicles on the rostrum around
the mouth and their rostrocaudally arranged rows in
Narcine puts them in an ideal location to aid in the
localization and guidance of the mouth over prey
items. Vesicles of Savi would not respond to pressure
differences across the skin surface caused by
water movements because they are not connected to
the external environment, but should be sensitive to
direct displacement of the compliant underlying skin.
The specific orientation of the rows of vesicles (45_
to the rostrocaudal axis) in Narcine may also provide
the animal with directional information on the location
of small prey items. However, comparisons of the
morphology, distribution, and physiology of vesicles of
Savi among batoid taxa warrants further investigation
to examine the functional specialization and evolution
of these mechanoreceptors.
Feeding neuroecology of the lateral
line system
Feeding ecology and behavior can often be correlated
with the peripheral distribution of the lateral line system
70
in fishes (Dijkgraaf 1962, Hensel 1978). The batoids
examined in this study generally feed on infaunal or
epifaunal organisms that often require excavation from
the substrate and are often outside of the animal’s
visual field. The lesser electric ray, N. brasiliensis,
feeds predominantly at night on burrowing polychaete
worms with some amphipods, decapod shrimp, sipunculid
worms, and anguilliform eels also reported in
the diet (Funicelli 1975, Rudloe 1989). The clearnose
skate, R. eglanteria, is a deep-water benthic batoid
reported to feed on invertebrates such as mollusks and
small crustaceans as well as the benthic tonguefish,
Symphurus plagiusa, and other teleosts (Hildebrand &
Schroeder 1928, Fitz & Daiber 1963, Schwartz 1996).
Butterfly rays, Gymnura spp., are primarily piscivorous
feeders that actively prey on teleost fishes such
as spot, Leostomous xanthurus, and pinfish, Lagodon
rhomboides. In addition, some crustaceans, gastropods
and cephalopods were also found in the diet of smaller
Gymnura, but teleosts become more important in the
diet as the ray grows (Daiber & Booth 1960). The
Atlantic stingray, D. sabina, feeds day and night almost
exclusively on small benthic invertebrates such as
amphipods, isopods, ophiuroids and polychaetes that
they excavate from the substrate (Cook 1994, Bradley
1996). Integration of the feeding ecology and behavior
of each of these species with the morphology and
spatial distribution of the lateral line system supports
the hypothesis that the lateral line system functions in
predation in elasmobranch fishes.
Prey detection in elasmobranchs is mediated by multiple
sensory systems, but the ventral lateral line system
in batoids probably serves to locate prey and guide
the mouth over it during the final stages of prey capture.
The pored canal system on the ventral surface may
function to detect water movements generated by locomotion,
respiration, and filter-feeding activities of prey
(Montgomery&Skipworth 1997), and allowthe batoid
to reposition its body to orient the non-pored canals
and mouth directly over the prey. Non-pored canals are
often located on the ventral rostrum and around the
mouth, and may function as specialized tactile receptors
stimulated by prey contact with the skin surface
as proposed by the mechanotactile hypothesis in the
stingray (Maruska & Tricas 1998). Similarly, the vesicles
of Savi distributed around the mouth and on the
rostrum in batoids may also serve as mechanotactile
receptors involved in prey localization. The spatial separation
of vesicles of Savi would allow them to serve
as point source detectors when prey are just rostral or
lateral to the mouth.
In addition to the correlation between peripheral lateral
line organization and feeding ecology and behavior
of batoids, other evidence supports the mechanotactile
hypothesis of lateral line function. First, although the
number of lateral line pores is greater in the canals
on the dorsal surface of D. sabina, the canals on the
ventral surface often contain twice as many sensory
neuromasts. Second, the average diameter of non-pored
canals on the ventral surface is 2.5_ greater than that
of the dorsal canals in D. sabina. This indicates there
is a wide tactile receptive field on the ventral skin
surface beneath the canal that will move canal fluid
and stimulate the neuromast when it is displaced. For
any given displacement of the skin surface, fluid flow
inside a larger diameter canal will attenuate at shorter
distances from the stimulus than in a smaller diameter
canal, permitting the ray to better localize a prey
item because fewer neuromasts will be stimulated. The
compliant nature of the canal walls and dermal layers
superficial to the ventral canal would also facilitate
movement of the cupula and canal fluid in response
to skin displacement. Third, cutaneous sensory endings
(putative tactile receptors) in elasmobranchs are
stimulated by 20 _m displacements of the skin surface
(Murray 1961), but a skin displacement of less than
20 _m should stimulate the canal neuromasts of the
lateral line system, making it more sensitive to tactile
stimulation than the general cutaneous tactile system.
Therefore, these data support the hypothesis that the
non-pored canals and vesicles of Savi on the ventral
surface in the stingray and other batoids function as
mechanotactile receptors that likely play a role in the
localization and capture of prey. However, the mechanotactile
hypothesis remains to be physiologically and
behaviorally tested.
The bonnethead, S. tiburo, was used in this study to
compare the organization of the lateral line system in
batoids to a shark species with similar food habits. The
bonnethead is a small abundant coastal shark species
that feeds primarily at night on motile invertebrates
such as crabs, shrimp, bivalves, and cephalopods that
often reside in seagrass beds (Cort´es et al. 1996).
Although the bonnethead often feeds on benthic invertebrates,
it does not have the extensive non-pored canal
system or vesicles of Savi present in benthic feeding
batoids. Therefore, it is likely that prey localization
is mediated by the detection of water motions caused
by movements of prey via a pored canal system rather
than a mechanotactile mechanism mediated by the nonpored
canals as suggested in batoids (Maruska&Tricas
1998). However, many shark species do have sections
71
of non-pored canals on the head (Garman 1888, Chu &
Wen 1979). Non-pored canals on the head of sharks
may also serve as mechanotactile receptors to facilitate
prey localization during the final stages of prey
capture and handling or during copulation, or may
help reduce stimulation of the canal system during forward
swimming movements. However, differences in
morphology and spatial distribution of the lateral line
system between batoids and sharks may also result
from different evolutionary selective pressures. Thus,
functional or phylogenetic interpretations should be
treated with caution until additional taxa are examined.
Future directions
In teleosts, the mechanosensory lateral line functions
to detect water flow across the skin surface to
facilitate prey detection (Hoekstra & Janssen 1985,
Montgomery & Saunders 1985, Montgomery et al.
1988, Montgomery 1989, Janssen et al. 1995), social
communication (Satou et al. 1991, 1994), schooling
(Partridge & Pitcher 1980), predator avoidance
(Blaxter & Fuiman 1990, Fuiman 1993), rheotaxis
(Montgomery et al. 1997), and object localization or
hydrodynamic imaging (Campenhausen et al. 1981,
Hassan 1989). Several of these functions were shown
behaviorally or physiologically to be mediated by a
specific class of mechanoreceptor organ. For example,
rheotaxis and predator avoidance in fish larvae
is mediated primarily by superficial neuromasts
(Montgomery et al. 1997, Blaxter & Fuiman 1990),
while schooling and localization of objects is often
mediated by the canal system (Partridge & Pitcher
1980, Hassan 1989). Elasmobranch lateral lines differ
from teleosts by the placement of superficial neuromasts
within grooves that enhance a bidirectional sensitivity,
and canal neuromasts that are organized as
a nearly continuous sensory epithelium with multiple
neuromasts between pores. In addition, specialized
non-pored canals are common in most species, and
vesicles of Savi are found in some rays. Thus, it cannot
be assumed that class-specific mechanoreceptormediated
behaviors in teleosts apply to elasmobranchs.
Also, the biological function of the specialized nonpored
canal system and vesicles of Savi remain
to be demonstrated. Testing of mechanoreceptorspecific
functions requires quantitative comparisons
of response properties of different mechanoreceptors
as well as direct behavioral experimentation. Several
of these mechanoreceptor-specific function hypotheses
were mentioned in previous sections and summarized
in Table 2, while a few are discussed below.
Mechanotactile hypothesis
The mechanotactile hypothesis of lateral line function
in batoids states that ventral non-pored canals
likely function as specialized tactile receptors used
to facilitate prey capture (Maruska & Tricas 1998).
Detection of weak water jets by the short-tailed
stingray, which simulated water movements generated
by prey, provided behavioral evidence for lateral
line-mediated prey detection in elasmobranch fishes
(Montgomery & Skipworth 1997). However, the relative
roles of the pored and non-pored canal systems
on the ventral surface of batoids during prey detection
and localization is unknown. The hypothesis that
non-pored canals encode displacement of the skin
can be tested by electrophysiological determination of
response properties of primary afferents that innervate
the neuromasts in these canals. Some evidence already
exists for stimulation of lateral line canals across the
skin in both teleosts and elasmobranchs, but characterization
of sensitivity and receptive field organization
remains unknown (Sand 1937, Denton & Gray 1983,
1988). Also, the question of whether or not a natural
source (e.g. prey) is able to stimulate these receptors
and elicit behaviors will require behavioral testing.
Many of the lateral line-mediated behaviors in teleosts
were demonstrated by studies that sequentially eliminated
each sensory system, including pharmacological
techniques used to block lateral line receptors (e.g.
cobalt chloride, gentamicin sulfate). However, elasmobranchs
are often large and difficult to deal with in captivity,
standard pharmacological methods (e.g. cobalt
chloride blockers) do not work in salt water, and elimination
of the lateral line system via surgical transection
of nerves without damage to the electrosensory system
is difficult. Therefore, the logistics of conducting lateral
line behavioral experiments in elasmobranch fishes
must be tediously resolved before conclusions on biological
function can be demonstrated.
Schooling hypothesis
Teleost fishes use their lateral line systems in conjunction
with vision to maintain position within a
school Individual fish
detect short-term changes in the velocity and direction
of their nearest neighbors primarily via the pored lateral
72
line canal along the trunk. Several elasmobranch
fishes are also known to form aggregations at certain
times of the year or day for reasons such as
mating and parturition, feeding, or predator avoidance.
These aggregations range from large schools
with hundreds of individuals (e.g. Sphyrna lewini and
Rhinoptera bonasus) to smaller groups of only a few
individuals (e.g. Carcharhinus amblyrhynchos). However,
relatively little is known about the organization
and function of elasmobranch schools and whether the
lateral line system plays a role in this behavior. Individuals
within a school would detect water movements
produced by swimming neighbors primarily via pored
lateral line canals along the body in sharks (i.e. posterior
lateral line canal) and on both the dorsal and
ventral pectoral fins in batoids. Therefore, it is possible
that elasmobranch species that form aggregations
have lateral line specializations such as increased
canal branching to expand the receptive field, increased
number of pores, or increased numbers of superficial
neuromasts. Morphological studies across taxa would
test the hypothesis that lateral line organization is correlated
with schooling behavior in elasmobranchs. In
addition, behavioral experiments which measure the
ability to maintain position within a school in fish with
different portions of the lateral line system ablated can
reveal the relative importance of the mechanosensory
system in elasmobranch schooling behavior.
Mechanosensory parallel processing
hypothesis
Lateral line canals on the head are innervated by the
anterior lateral line nerve complex, and those of the
body and tail by the posterior lateral line nerve. Both
branches enter the brain and terminate somatotopically
around cell plates within the medial octavolateralis
nucleus of the medulla (Bodznick & Northcutt 1980,
Puzdrowski & Leonard 1993). However, these nerves
contain neurons that innervate both superficial and
canal neuromasts. Therefore, the hypothesis that superficial
neuromasts that encode lower frequency velocity
information, and canal neuromasts that encode
higher frequency acceleration information have separate
parallel processing pathways should be tested via
neuroanatomical and neurophysiological techniques.
Central physiological and neuroanatomical studies in
elasmobranchs have shown mechanosensory lateral
line regions from the medulla to the telencephalon
(Bleckmann et al. 1987, 1989, Bleckmann & Bullock
1989, Boord & Montgomery 1989), but identification
of distinct cell populations that process velocity versus
acceleration or displacement information received
from different receptor classes has received little attention.
Also, central processing of mechanosensory information
from the distinct dorsal and ventral surfaces
of batoids requires investigation in a behavioral context.
It is currently unknown how different types of
mechanosensory information are processed and integrated
in the elasmobranch brain to elicit specific lateral
line-mediated behaviors.
The importance of the mechanosensory lateral line
system in the coordination of behaviors such as feeding,
schooling, predator avoidance, hydrodynamic imaging,
and courtship remain to be investigated in elasmobranch
fishes. However, it is only after basic questions
on lateral line structure and function are answered
that more complex questions such as how the central
nervous system processes and integrates lateral line
information with other sensory cues to elicit behaviors
can be logically approached.