<oologicalJournal of the I.innean Socie!v (1982), 76: 19-28. With 12 figures
Sensory structures at the surface of
fish skin. 11. Lateralis System
E. B. LANE
AND
M. WHITEAR*
Department of ,Zoology, University College, Gower Street,
London W U E fiB 7
Recehied May 19881, Accepted for publication October 1981
Scanning electron microscopy shows the form of the cupulae offree neuromasts in two species of teleost
fish, and gives information about the organization of the free neuromasts in teleosts and lampreys. In
lampreys some neuromasts were found to lack the surrounding moat and the flanking hillocks
characteristic of the lateral line organs previously described in these fish. In all cases, the sensory cells
had the kinocilium aligned with respect to the stereocilia on the longer axis of the neuromast surface,
thus enabling the direction of erective stimulation of the free neuromasts to be deduced from their
morphological arrangement.
KEY WORDS:-Scanning
electron microscopy
~
lateralis system
~
neuromasts.
CONTENTS
Introduction . . . . . . .
Materials and methods.
. . . .
Observations . . . . . . .
Free neuromasts of Phoxinus phowinus
Free neuromasts of Rarbus sophore .
Neuromasts of Lampetra
. . .
Discussion . . . . . . . .
Acknowledgements. . . . . .
References.
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INTRODUCTION
Lampreys and aquatic amphibians have the mechanoreceptive neuromast
organs of the lateral line system situated in the epidermis of the skin. In most bony
fishes the principal part of the lateralis system is in the sensory canals, but free
neuromasts still occur in the skin. Some modified neuromasts are electroreceptors.
The structure and function of these sensory systems are described or reviewed by
Dijkgraaf (1963))Flock (1965, 1971)) Cahn (1967), Fessard (1974) and Russell
(1976). Normally, all sensory cells in a neuromast have the same plane of
* Please send reprint requests to Dr Whitear. Dr Lane’s present address is: Imperial Cancer Research Fund,
Lincoln’s Inn Fields, London WCPA 3PX, U.K.
19
+
do24-4082/82/0900l9 lOrSOU.OOj0
0 1982 The Linnean
Society of London
20
E. B. LANE AND M. WHITEAR
stimulation, but the direction of stimulation is opposite in alternating cells. The
direction is defined by the position of the kinocilium with respect to the group of SOcalled stereocilia, which are microvilli containing actin filaments (Tilney et UL.,
1980). In life, the apical processes of the sensory cells are embedded in a cupula,
secreted by the supporting cells (Hama, 1965; Petraitis, 1966; Iwai, 1967) and
consisting of glycoprotein, either neutral (SatG, 1962) or acidic (Thomopoulos,
1957; Guarnieri & Cavicchioli, 1968). The cupulae of the canal organs may be
flattened structures extending across the lumen of the canal, as in Perca Juuiatilis
(Woellwarth, 1933) and Rhynchocyrnba nystromi (Katsuki et al., 1951), or may be
dome-shaped as in Lota lota (Flock, 1965;Jakubowski, 1965). Reports of the shape
of the free neuromasts of teleosts describe them as flattened and ribbon-like
(Emery, 1880; Denny, 1937; Satb, 1962; van Bergeijk & Alexander, 1962;
Jakubowski, 1966a). The neuromast cupulae of amphibians have a similar
flattened form (Dijkgraaf, 1963; Flock & Jsrgensen, 1974). It is generally agreed
that the cupulae of free neuromasts may become broken or detached during
normal life and are continuously secreted (Sat6, 1962;Jakubowski, 1966b) ; the rate
of growth is reported as 15--30pm h-' in .N"ecturusmaculatus (Frischkopf & Oman,
1972).
The present paper reports observations on the cupulae of free neuromasts in two
species of cyprinoids, and on the sensory surface of neuromasts in lampreys, made
during a survey of the skin by scanning electron microscopy (SEM) with the object
of locating chemoreceptors (Lane & Whitear, 1982).
MATERIALS AND METHODS
The species examined were Phoxinus phoxinus (Linnaeus), Barbus sophore
(Hamilton Buchanan), Lampetra Juuiatilis (Linnaeus) anadromous adult and
I,ampetra planeri (Bloch) adult and ammocoete. The methods for electron
microscopy were as described in Lane & Whitear (1982). In addition, Ranvier
silver nitrate preparations were made of the skin of Lampetra planeri adult and
ammocoete.
OBSERVATIONS
Free neuromasts of Phoxinus phoxinus
The distribution of neuromasts on the head and body of this species was mapped
by Dijkgraaf (1933) and by Lekander (1949). The free neuromasts occur in groups,
some members of which share a common innervation (Whitear, 1952). The
number of organs in a particular morphological group varies from fish to fish and
even on two sides of the same individual. The orientation of individual neuromasts
in a group is in a particular direction, although some may deviate by a few degrees.
The height of the cupulae in SEM material varied from a mere stump to about
30 pm (Fig. 1) which is less than that seen in fresh material (Dijkgraaf, 1933; pers.
obs.). This depends partly on the history of the individual structure, which may
recently have been broken short, but it is probable that some shrinkage takes place
during preparation for microscopy. In SEM specimens the breadth of the cupula
might be 30 pm at the base, narrowing distally to 10 pm (Fig. 2), but some
examples were less broad (Figs 3, 4). Neuromasts sometimes occupied a slight
SEM O F FISH LATERALIS SYSTEM
21
Figures 1-4. Phoxirius phoxinus, fixed 5",, glutaraldehyde, without Mucolexx. Fig. I . Row of free
neuromasts in front of the right nostril, seen from the medial aspect; to the left, apertures of goblet
cells can be seen in the skin surface. x 150. Fig. 2. Neuromast cupula behind left nostril, bent over
towards the anterior direction; vertical striations are visible near the base (arrowed) ; some of the
epithelial cells are damaged in this region, due to preparation artefacts (c. x 1OOO). Fig. 3. Cupula
which appears to have been broken short, near that of Fig. 2 ; the flanges are less well developed.
c. x 1200. Fig. 4. Neuromast on the operculum, with cupula smaller than the preceding ones; the
surfice of the cells immediately adjacent to the cupula is covered with secretion (arrowed). x 1400.
depression in the skin surface (Figs 1, 3) ; some cupulae were bent over against the
surface.
At its base the cupula is oval in outline with flanges extending in the plane of the
long axis of the neuromast, but the flanges are of varying extent (Figs 2, 3 ) and
may be better developed on one side than on the other. In some cases the
surrounding epithelial cells reach nearly to the base of the cupula, in others a flat
surface of secreted material intervenes (Fig. 4). Vertical striations on the surface of
the cupula probably demarcate the contributions of individual supporting
(secretory) cells beneath; such columns were sometimes visible at the ragged edge
where the tip of a cupula had apparently been broken off (Figs 3,4).
In Phoxinus phoxinus, the superficial epithelial cells each show the usual
peripheral ridge (Yamada, 1968) where they abut one another; the rest of the cell
surface is papillate or covered with short, not concentric, microridges (Fig. 4). I n
some areas the external mucous layer covering the superficial epithelial cells was
still intact in the SEM specimens, concealing the microridges.
Free neuromasts of Barbus sophore
In this species the superficial epithelial cells bear well-developed microridges.
'The neuromast cupulae are smaller than in Phoxinus phoxinus and show transverse
22
E. B. LANE AND M. WHITEAR
Figures 5-8. Barbur sophore, fixed in a mixture of l",, osium tetroxide and 2.5",,glutaraldehyde, no
Mucolexx. Fig. 5. Cupula of a free neuromast on the head. x 2900. Fig. 6. As Fig. 5; the structures in
the background, and that in the foreground of Fig. 3, are apical processes of supposed chemosensory
cells (Lane & Whitear, 1982). x 3000.Fig. 7. As Figs 5 & 6; cupula lifted to show the sensory surface of
a free neuromast. x 3000. Fig. 8. Neuromast of Fig. 7 from a different angle, showing kinocilia and
short stereocilia, and the papillate surface ofthe supporting cells (p), revealed by the lifted cupula (c);
the arrow indicates the apex of a sensory cell showing the kinocilium beside the sterocilia. x 6000.
corrugations in the central part of the column, especially near the base, although
some vertical structure is also apparent (Figs 5,6,7). In Figs 5 & 6 the cupulae have
one flange which forms a frill at the side; in Fig. 7 the flanges are more
symmetrical. These cupulae are c. 7 pm in breadth.
Frequently the cupulae had been knocked off, exposing the cilia of the sensory
cells which are normally embedded in the base of the cupula. In the examples seen
the number of sensory cells was small, with 8-16 kinocilia being visible. I n Fig. 7
the cupula is displaced; in close-up (Fig. 8) it can be seen that where the
orientation of the sensory cells can be determined (by the position of the kinocilium
with respect to the stereocilia), it is along the longer axis of the neuromast surface
(broader axis of the cupula). It was not possible to see if the orientation of the
sensory cells alternated in a regular manner and on some cells the kinocilium was
not seen (perhaps it had been broken off). The diameter of a kinocilium was
c. 0.2 pm all along its length, which was usually 5 or 6 pm; some were only 2 pm
long. The number of stereocilia was small, 4-8 on each cell, and they were 1 pm
long or less. The surface of the supporting cells of the neuromast was papillate
(Fig. 8) contrasting with the microridges on the surrounding epithelial cells.
SEM OF FISH LATERALIS SYSTEM
23
Neuromasts of Lampetra
All neuromasts of lampreys occur at the skin surface. They are usually set in pits
flanked by a pair of hillocks and are arranged in rows on the head and body
(Merkel, 1880; Johnston, 1902; Razzauti, 1916; Plate, 1924; Fahrenholz, 1936).
The cupulae have not been described, nor were they present in our SEM material.
In L.Jluviatilis mucus had been removed from the skin surface; Fig. 9 is of a
neuromast of the suprabranchial line (Razzauti, 1916). The sensory area measures
48 x 10 pm, and is surrounded by cells with a papillate surface, which correspond
to the upper marginal cells of Yamada (1973). The lengths of such neuromasts,
with a moat and flanking hillocks, ranged from 155 to 32 pm, but the breadth of
the sensory surface was more constant. The moat-like pit was lined with papillate
cells resembling the marginal cells of the protuberant sensory area. Occasionally
there were two sensory protuberances within one pit.
In addition to the neuromasts flanked by hillocks, as described by previous
authors, there were smaller neuromasts, each situated on a low eminence, not
surrounded by a moat and not flanked by perceptible hillocks. This is similar to the
arrangement in the ammocoete. Those seen in the adult were in the branchial
region, and belonged to the interbranchial and suprabranchial lines of Razzauti’s
interpretation (1916), although it should be noted that the diagram in Plate (1924)
gives a more accurate idea of the distribution. The SEM specimen with these
neuromasts contained three gill apertures, and had no moated neuromasts; Fig. 9
is from the same individual but more anterior. The unmoated neuromast ofFig. 10
has a sensory surface measuring 35 x 13pm, but some were longer and some
shorter; sometimes two small sensory surfaces were adjacent. The cells surrounding
the sensory surface were papillate like the marginal cells of the moated neuromasts
and could be distinguished from the mucigenic superficial epithelial cells which
have a pitted sponge-like surface.
The neuromast of Fig. 10 has 18 kinocilia, each with a basal section c. 5 pm
long, 0.25 pm in diameter, and a terminal tapering portion bringing the total
length to 12 or 13 pm. At the base of each kinocilium there is a group of about 10
stereocilia 0.4 pm long (Figs 1 1,12). A group of smaller and less regularly arranged
microvilli occurs on the far side of the stereocilia (Fig. 12), but it is not clear if these
should also be counted as stereocilia. The rest of the apex of the sensory cell is
smooth. On many of the sensory cells the kinocilium was bent over the stereocilia
so as to obscure the view of them. The supporting cells have microvilli c. 0.6 pm
long and thicker than the stereocilia. The orientation of the sensory cells
alternated, as reported by Yamada (1973) for the moated type of neuromast; for
example, in Fig. 1 1 the sensory cell nearest to the bottom of the picture has the
stereocilia to the left (posterior) of the kinocilium and the next above it has the
stereocilia to the right. In all cases, the axis of stimulation of the sensory cells, as
shown by the orientation of the kinocilium, coincided with the longer axis of the
neuromast surface. This was usually also the long axis of the body, but some
neuromasts had an oblique orientation.
In Lampetra pfaneri prepared for SEM, the adult showed the rows of neuromasts
flanked by hillocks, for example behind the eye, but the neuromast surface was
covered by secretion and details of the sensory cell apices could not be made out.
The Ranvier method skin whole mounts showed the neuromasts well; comparison
of the two sides of a single animal showed that the number and pattern of
24
E. B. LANE AND M. WHITEAR
Figures 9- 12. I.ampetru fluviatilis, fixed 2 S U , , glutaraldehyde after 5 s Mucolexx treatment. Fig. 9.
Moated neuromast of suprabranchial row, showing sensory surface, marginal area and part of an
adjacent hillock (h). x 750. Fig. 10. Small unmoated neuromast from a row near the gill apertures
which all had their longer axes longitudinal to the body; the sensory surface shows microvilli of
supporting cells and long attenuated kinocilia, and is surrounded by a zone of papillate marginal cells
( p ) ; superficial epithelial cells appear at the top of the figure. c. x 1400. Fig. I I . Similar to Fig. 10,
showing alternation in the orientation of sensory cells; the kinocilia are deflected posteriorly and lie
over the stereocilia on those apices indicated by single arrows; the double arrows indicate a cell apex
with the stereocilia anterior to the kinocilium. c. x 5700. Fig. 12. Similar to Fig. 1 I ; microvilli of
supporting cells surrounding a sensory cell apex with the kinocilium (k) on the posterior side; the tips of
the stereocilia nearest the kinocilium are inclined together; anterior to them is a group of smaller
microvilli (arrowed) which appear to belong to the sensory cell. c. x 15500.
neuromasts was not precisely the same, even around the eye. The size of the organs
varied, some were as small as the small neuromasts seen in I,.Juviatilis. By
adjusting the focus it could be seen that flanking hillocks were present beside
nearly all the organs, for the dermis beneath rose in a shallow dome even where
there was not much change in the level of the epidermal surface. Sections of an
unmoated neuromast seen by TEM (unpub. obs.) confirmed that the epidermis at
the sides was modified; the superficial cells were less mucoid and the epithelial cells
more rounded than in normal skin. Even these hillocks, scarcely elevated,
contained numbers of Merkel cells as described by Fahrenholz (1936) in the case of
the larger, moated, neuromasts (for fine structure of the Merkel cells, see Whitear
& Lane, 1981). In SEM material of Id. planeri ammocoete some neuromasts of the
branchial region were seen; they were without obvious moat or hillocks, the largest
had a sensory surface 28 pm by 10 pm. This one bore nine tapering kinocilia
SEM OF FISH LATERALIS SYSTEM
25
c. 10 pm in total length (and probably the bases of three more), but other details
were obscured by secretion.
DISCUSSION
Reports on the structure of neuromast cupulae are scattered in the literature,
and show that there is variation between species. In the canal organs of the fish
Acerina cernua there is a ‘wall’ on either side of the cupula with physical properties
different from those of the main part Uielofet al., 1952) ;the cupulae of Percajuviatilis
have a central column with wide flanges on either side (Woellwarth, 1933). I n
amphibians the cupula has an outer sheath (Frischkopf & Oman, 1972; Cornford
& Barajas, 1980). The detailed form of the free neuromast cupulae differed in the
two cyprinoids viewed by SEM. The dimensions are in reasonable agreement with
previous reports of cupulae in Phoxinus phoxinus, although in fresh material the
cupulae are taller. It is difficult to assess the effect of shrinkage through
dehydration, b u t this is likely to have occurred. Sat6 (1962) illustrates a cupula
from a goby which, when fresh and unfixed, was 127 pm broad; in comparable
fixed and sectioned material such a cupula was only 66 pm broad, demonstrating a
considerable shrinkage effect. The basal flanges we observe in the fixed SEM
material may reflect the original in vivo extent of the cupula before dehydration.
The gobies have particularly broad, flat cupulae on the vertical rows of free
neuromasts on the flank; Merkel (1880) showed these in Gobius niger (Linnaeus).I n
whole mounts of the skin of Pomatoschistus pictus (Malm), PAS-positive cupulae of
proportions similar to those of Sato’s goby can be seen (pers. obs.). The cupula is
composed of glycoprotein and it has been suggested that, in addition to its
mechanical function, it preserves an ion-rich environment above the sensory cells
(Russell & Sellick, 1976).
In selachian fishes cupular material has been seen only rarely, and is described
as viscous rather than gelatinous in consistency (Tester & Kendal, 1968); the
position of the free neuromasts between placoid scales makes it doubtful if they
bear cupulae resembling those of teleosts. In lampreys also cupulae have not been
seen, but it is reasonable to assume that the long kinocilia normally project into
some secreted covering. Yamada (1973) found secretory vesicles in the upper
marginal cells different from those in the supporting cells and suggested that they
make a separate contribution to the cupula. In the unmoated type of neuromast,
the surface topography, and TEM of an unmoated neuromast in 1,. pfaneri, suggest
that marginal cells are present. They might be expected to secrete an outer sheath
for the cupula, which would then be thicker and more securely based when in a
moated rather than in an unmoated neuromast, but there is no positive evidence
that this is so. In the ammocoete, the burrowing habit would presumably preclude
the retention of a long and delicate cupula, especially as there are no flanking
hillocks. These hillocks are set at the sides, not in the plane of stimulation of the
neuromast. Protective prominences also occur at the sides of free neuromasts in a
flatfish (Roper, 1981).
Some authors have speculated that the cupulae of the free neuromasts of teleosts
project into a zone of mucus at the surface of the fish, rather than into the
boundary layer ofthe water interface (Kuiper, 1967; Walters & Lin, 1967). Ifso,
this mucus must be much diluted, for the SEM observations showed that most
26
E. B. LANE AND M. WHITEAR
goblet cells were not discharged and that the external mucoid layer, which in life
covers the microridges of the superficial epithelial cells, is only a micrometre or so
thick, negligible compared with the height of the cupulae. When seen in life, the
cupulae of free neuromasts show a swaying motion (Dijkgraaf, 1933; Denny, 1937 ;
SatG, 1962; pers. obs.) and are c. 100 pm long. Cahn & Shaw (1962) saw cupulae of
similar length flattened back against the body of a larval teleost during swimming,
and perpendicular to the body only when the fish stopped. Some of the cupulae
seen by SEM were bent over as in Fig. 2, or even nearer to the skin surface.
However, such bending does not imply stimulation of the sense organ, which
depends on displacement of the stereocilia in the plane defined by the kinocilium
(Dijkgraaf, 1963; Flock, 1965) which is usually, as in the examples we saw by
SEM, the plane of the broad axis of the cupula, i.e. the longer axis of the sensory
surface.
In lampreys, the stereocilia are shorter than the surrounding microvilli, which
led Yamada (1973) to suggest that they could play little part in reception.
Evidence from the saccular receptors of a frog shows, however, that it is the
stereocilia, not the kinocilium, which mediate transduction (Hudspeth & Jacobs,
1979). There are variations in morphology of these apical processes across the
range of acoustico-lateralis receptors considered as a whole. In the case just
mentioned, the kinocilium bears a terminal knob. I n the cochlea of the alligator
lizard (Tilney et al., 1980) some of the stereocilia are longer than the kinocilium
and nearly a hundred times as long as the stereocilia of lamprey neuromasts. Long
and tapering kinocilia also occur in a minority of the sensory cells in the labyrinth
of lampreys (Lowenstein et al., 1968). Yamada (1973) found 18-20 stereocilia per
sensory cell in his lamprey, which is close to the SEM result, but in Barbw sophore
there are only 4-8 stereocilia per cell. Roper (1981) showed 28 stereocilia on a
receptor cell of a pleuronectid free neuromast, while in the canal organs 40-50 are
reported (Flock, 1965; Yamada & Hama, 1972). Sensory cells in larval neuromasts
can have 30-40 stereocilia (Iwai, 1967).
Free neuromasts, exposed at the surface of the skin, would be expected to
respond to stimuli which would not affect the canal organs (Dijkgraaf, 1963). If the
plane of stimulation of the neuromast is always on the long axis of the sensory
surface, as seems to be the case, it should be possible to predict the sensitivity of the
fish to local water movements from maps of the orientation of the free neuromasts,
such as have already been made for several species (Moore & Burris, 1956;
Jakubowski, 1966a; Schwartz & Hasler, 1966; Merrilees & Crossman, 1973;
Roper, 1981). There are practical difficulties in studying the free neuromasts,
especially their cupulae, in any but small fish. Larval fish have naked neuromasts
which later become enclosed to form the canal system; it is not clear how far the
enclosed and the exposed systems are functionally separate. Branson & Moore
(1962) argue that all neuromasts are part of the same system and that primitive
teleosts have a well developed canal system which is simplified, or incomplete, or
replaced by lines of external neuromasts, in ‘advanced’ perciform fishes.
Uncovered neuromasts on the head of Aplocheilus lineatus (Cuvier & Valenciennes),
a cyprinodont, have been shown to form a direction-sensitive system detecting
surface waves in the water (Schwartz, 1965, 1967) but the morphology shows that
these sense organs are homologous to canal neuromasts of related fishes, and thus
secondarily exposed and not similar to the smaller and more numerous free
neuromasts found in cyprinoids such as Phoxinus phoxinus. The Japanese conger eel
SEM O F FISH LATERALIS SYSTEM
27
has a row of free neuromasts (pit organs) on the body, separate from the lateral line
canal; each organ has 50-130 sensory cells, with the orientation alternating in a
dorsoventral direction (Hama, 1978).
In lampreys all the neuromasts are uncovered although the flanking hillocks
may provide some protection especially for the closely set lines of neuromasts on
the head. The variability in the precise distribution and the small size of some of
the neuromasts found in LampetruJluviutilis suggest that the system may not be
functionally as efficient as that found in gnathostome fishes.
ACKNOWLEDGEMENTS
We thank Dr A. K. Mittal, Dr 0. S. Bamford, the Department of Biological
Sciences, University of Bath, Mrs Lyne Rolph, Messrs E. Perry and B. L. Pirie,
and the S.R.C. for the various reasons mentioned in Part I of this study.
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