~ o o l o g i c a journal
l
of !he I.innean Society (1982), 75: 141 151. With 26 figures
Sensory structures at the surface of fish skin
I. Putative chemoreceptors
E. B. LANE*
AND
M. WHITEART
Department of <oology, University College, Gower Street, London IVClE 6B 7
.Icreptedfor publication August 1981
Fish skin contains solitary epidermal sensory cells which, on evidence from their cytology, are believed
t o he chemosensory. ‘l’hr external appearance of thr ‘ipical sensory processes of these cells. as seen hy
scanning electron microscopy, is shown in four species of ostariophysan teleosts, and is compared with
the morphology of the pores ofexternal taste buds. The apical processes of the gustatory cells are simple
in Form in all cases so far investigated in gnathostome fishes, but in some cases the solitary sensory cells
have apical processes divided distally into a number ofsmaller processes. In the dipnoan fish Protopterur
amphibiur, external taste buds have simple blunt gustatory processes protruding through a cap of mucus
that coven the taste bud pore. Solitary sensory cells in this species have a bulbous undivided apical
process. In the lampreys, the ‘end buds’ have an apical morpholo,gy different from the taste bud pores
of teleost fish. Lamprey epidermis has numerous solitary sensory cells each bearing a number of
microvilli.
KEY WORDS:-Scanning
electron microscopy
fish skin
sensory structures.
CONTENTS
Introduction . .
Material and methods
Obsenations . .
Discussion . . .
Acknowledgements.
References. . .
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1NTKODUC;’I’ION
Chemical sensiti\ity is highly developed in aquatic vertebrates, a s is to be
expected from the solvent properties of their eniironment. Olfactory sensory cells
are limited to the nasal epithelium but the gustatory system is more widespread,
with taste buds occurring on the body and fin surfaces of some species as well as in
the oral and pharyngeal epithelia. For general reviews of the chemosensory
systems, see Bardach & Atema (1971) and Hara (1971).
Scanning electron micrographs (SEM) of taste buds on the hagfish Myxine
glutino.ra have been published by Georgieva et al. (1979).SEM of teleost taste buds
* Present address: 1mperi;il Cancer Research Fund, P.O. Box 123, 1,incoln’s Inn Fields, London WCYA 3 PX.
t Plmse send reprint requests t o D r Whitear.
0024 ,4082/82/06014I
+ 1 I $OS.CX)/O
I4I
c) 1982 The Linnean Society of I.ondon
142
E. B. LANE AND M. WHITEAR
have been published by Graziadei (1969), Reutter & Breipohl (1975), Ovalle &
Shinn (1977), Reutter (1978), Ono (1980) and Meyer-Rochow (1981). Reutter et
al. (1974) showed, besides taste buds, SEM of a solitary sensory cell apex with a
single microvillus on the tongue of Xiphophorus helleri; this corresponds to the type
described by Whitear (1952, 1965, 1971) in external and oral epidermis ofvarious
teleosts. The present results are from a survey of the surface of four species of
teleost, a dipnoan and two species of lamprey, to demonstrate the external
morphology of these, or similar, cell types which are assumed on cytological
grounds to be chemoreceptive.
MATERIAL AND METHODS
The species used were: the minnow, Phoxinus phoxinus (Linnaeus) and an Indian
barb, Barbus sophore (Hamilton Buchanan) (both cyprinoids), the black bullhead,
Ictalurus melas (Rafinesque) and the peppered catfish, C'orydoras paleatus Uenyns)
(both siluroids), the lungfish Protopterus amphibius (Peters) (dipnoan), and the river
and brook lampreys, Lampetra Juviatilis (Linnaeus) adult and 1,. planeri (Bloch)
adult and ammocoete (cyclostomes).
Most of these fish were anaesthetized by chilling (Mittal & Whitear, 1978) but
the lampreys were anaesthetized with MS-222. Some specimens were treated
briefly with Mucolexx (Lerner Laboratories) before fixation. Fixation was in
glutaraldehyde of various strengths, optimally 5",,, cacodylate or phosphate
buffered to pH 7.4, or in a mixture of l o , ) osmium tetroxide and 2.5",,
glutaraldehyde, cacodylate buffered. The method appropriate to the various
specimens is stated in the captions to the figures. Dehydration was either in graded
ethanol or in acidified 2,2,dimethoxypropane (Muller & Jacks, 1975). The
specimens were critical point dried (Polaron model E3000) and sputter coated
with gold (Polaron E5100 series I1 cool sputter coater) and examined in a
Cambridge S4- 10 scanning electron microscope.
Most of the specimens used were from the anterior parts of the fishes, the head
and branchial region being cut up, after fixation, into pieces of convenient size and
shape. Specimens from more posterior parts were also prepared, particularly from
the lampreys. The oral cavity of Zctalurus melas and pharynx of Phoxinus phoxinus
were examined. The dipnoan material was taken from the lips and fins.
Material of all the species concerned, prepared for transmission electron
microscopy by standard methods, was available for comparison with the SEM
results.
OBSERVATIONS
Phoxinus phoxinus: some external taste bud pores, for instance on the jaws, are
situated in a crater-like structure formed by the surrounding epithelial cells.
Others, as in Figs 1 & 2, are raised on a papilla, with the pore area usually
wrapped in a single superficial epithelial cell. In this species the epidermal cells,
especially on the head, have papillate outer surfaces rather than microvillar ridges.
In the taste bud pores the prominent microvilli, some 2 pm long by 0.3 pm thick,
are the apical processes of the gustatory cells (using the classical terminology),
while the smaller microvilli surrounding them belong to the supporting cells. All
the gustatory processes seen had simple, rather blunt, tips.
CHEMORECEFTORS IN FISH SKIN
Figures 1-4, Phoxinus phoxinus, fixed 5",, glutaraldehyde without Mucolexx. Fig. I . Taste bud pore on
the rim of the nostril. x 4760. Fig. 2. Taste bud on rim of nostril, in profile. x 7000. Fig. 3. Skin surface
in front of a nostril with some goblet cell apertures and the apical processes of solitary sensory cells.
x 1360. Fig. 4. Similar to Fig. 3, but on the operculum. x 1680.
Figures 5 8. Phoxinurphoxinus, fixed 5",, glutaraldehyde without Mucolexx. Fig. 5. Apical process o f a
sensory cell on the operculum. x 10 350. Fig. 6. Similar to Fig. 5, another sensory process. x 9975.
Figs 7, 8. Material as in Figs 5 & 6, to show short and long sensory processes. x 8580.
143
I44
E. B. LANE AND M. WHITEAR
Figure 3 is a view of the top of the head and Figs 4 & 9 of the outer surface of the
operculum, showing the apertures of goblet mucous cells and a number of
projections which are the apical processes of solitary sensory cells. These usually
reach the surface between the boundaries of superficial epithelial cells, but are
occasionally enwrapped by one.
Figures5-8 show sensory cell processes on the operculum at a higher
magnification, to illustrate the range of form in a small area of skin. In Fig. 5 the
tip is bifid, but some processes had as many as six finger-like terminal extensions.
The maximum length seen was about 4 pm (Fig. 8) but some processes were raised
only just above the epidermal surface. Diameters were about 0.5 pm. Transmission
electron microscopy (TEM) of the cell type (Whitear, 1965, 1971; Lane &
Whitear, 1977) has shown that there are tight junctions at the boundaries with the
epithelial cells, but there is no ridge at this junction, as there is at the apical
boundaries of epithelial cells. Near the mouth and on the gular region some
processes of sensory cells had undivided tips; the diameters of these processes
ranged from 0.2 to 0.5 pm, the length was between 1 and 3 pm.
Apices of solitary sensory cells were also seen by SEM in the pharyngeal
epithelium, among the taste buds on the gill arches and also on the gill filaments.
These processes were simple in form, 1-2 pm long and c. 0.2 pm in diameter, with
an undivided tip.
Figures 9- 12. Fig. 9. Phozinusphoxinus, fixed 5",,glutaraldehyde without Mucolexx. Apical process ofa
sensory cell and a goblet cell aperture, on the operculum. x 3100. Fig. 10. Barbus sophor, fixed I"(,
osmium tetroxide mixed with 2.5",, glutaraldehyde, without Mucolexx. Epithelial cells with ridged
surfaces, on the head, and the apical processes of two sensory cells. x 2900. Fig. 1 1 . Material as in
Fig. 10 apical process of a sensory cell, in profile. x 12000. Fig. 12. Similar to Fig. 1 I but seen from
above. This process has the terminal projections bunched together. x I I 750.
CHEMORECEFTORS IN FISH SKIN
I45
Barbus sophore: on the skin of the head the superficial epithelial cells have well
developed microridges and the processes of sensory cells bear terminal projections
(Figs 1G12). T h e range of size is similar to that of the minnow, the total length of
the process in Fig. 11 being just under 3 pm and the diameter c. 0.5 pm. Some
examples had as many as 12 minor terminal projections. Simple apical processes
were not seen, but this may have been due to a restricted area of investigation.
Corydoras paleatus: Fig. 13 shows an external taste bud, which protrudes and is
wrapped in a superficial epithelial cell. Figure 14 is a view over the skin at comparable
magnification where there are three protuberances between the boundaries of the
epithelial cells; the nearest is shown at greater magnification in Fig. 15. These
structures are interpreted as the apices of solitary sensory cells, which have been
found by T E M in the same material. Some projections were a little longer, and
might have a papillate tip, but long terminal extensions were not seen. T h e
epidermis also contains ionocytes; one seen by T E M had a narrow apex, about
1 pm in diameter, but this is larger than the normal sensory cell apex, and the
ionocyte bore a few microvilli comparable in size to those on the superficial
epithelial cells. Reference to Fig. 15 shows that such papillae are smaller than the
sensory cell process. Cells similar to the ionocytes were described as secretory cells,
in this species, by Schulte & Holl (1971).
Ictalurus melas: the examples of solitary sensory cell apices in Figs 16 & 17 are
from the palatal epithelium, where they are simple. It is not known if more
Figures 13-15. Coyforas paleatus, fixed 6.25",, glutaraldehyde without Mucolexx. Fig. 13. Pore of a
taste bud on the operculum, with gustatory processes. x 2875. Fig. 14. Material as in Fig. 13 view over
the cheek with three processes ofsensory cells between the epithelial cells. x 2900. Fig. 15. Close-up of
the nearest process in Fig. 14. The superficial cpithelid cells bear papillae rather than microridges.
x 17 400.
I46
E. B. LANE A N D M. WHITEAR
Figures 16, 17. Ictalurus melus, fixed I",) osmium tetroxide mixed with 2.5",, glutaraldehyde, without
Mucolexx. Fig. 16. Processes of solitary sensory cells on the palatal epithelium. x 11300. Fig. 17.
Similar to Fig. 16 sensory process with a ragged appearance of the membrane. x 5750.
Figures 18-21. Fig. 18. Profoptem amphibiuc, fixed I",, osmium tetroxide mixed with 2.5",,
glutaraldehyde, no Mucolexx. Taste bud near the tip of a pelvic fin. T h e smooth epithelial cells
surrounding the taste bud retain a mucous layer which has come off the cells at the top of the figure
which show microvilli. x 1185. Fig. 19. Close-up of taste bud pore of Fig. 18 from a different angle.
Gustatory processes penetrate a cap of mucus borne on the microvilli of supporting cells
(arrowed). x 5850. Fig. 20. Protopfnur amphibius, fixed 6",,
glutaraldehyde after Mucolexx treatment.
Apical process ofa solitary sensory cell, bearing a plume probably ofmucus, projecting from the skin of
the lip. x 7150. Fig. 21. Material as in Fig. 20, looking down on to another sensory cell
process. x 10875.
CHEMORECEFTORS IN FISH SKIN
147
Figures 22,23. ImnpelraJuvialih, fixed 2.5",,glutaraldehyde after Mucolexx treatment. Fig. 22. Row of
end buds in latrral skin. The concavity ofthe skin and the bulging surfaces ofindividual epithelial cells
are preparation artefacts. x 198. Fig. 23. Surface of a similar organ in the ventral skin. hlultivillous
a p e x of a sensory cell; each apex occupies ii tiny depression in thr surface of the organ. x 1 I 500.
elaborate cell apices occur elsewhere. The range of size is considerable; those in
Fig. 16 are 1 pm long, that in Fig. 17 is about 4 pm and set in a small pit. The
withered appearance of this example is matched, in sections viewed by TEM, by a
corrugated plasma membrane on the apical process.
Protopterus amphibiuJ : Pfeiffer (1968) recorded taste buds from external skin of the
head of Protopterus sp., and they also occur on the fins. In SEM specimens they are
not easy to recognize, because they are usually covered by a cap of mucus
(Fig. 18). In close-up (Fig. 19) it can be seen that the mucous cap is carried on the
microvilli of supporting cells and is penetrated by the tips of a few gustatory cell
processes, each c. 0.3 pm in diameter. Solitary sensory cell processes were also
difficult to identify in the dipnoan, but Figs 20 & 21, from the skin of the lip, are
interpreted as such. The bulbous apical processes, which are c. 1 pm across near
the tip, differ from those found in teleosts, but the shape and dimensions agree with
those of the apices of cells seen in sections by TEM (unpublished observations)
which fit the criteria for chemosensory cells (Fox el al., 1980).
Lampetra jluviatilis and L. planeri: in the lampreys, groups of loosely associated
sensory cells in the skin have been called Endknospen or end buds (Merkel, 1880;
Johnston, 1902; Razzauti, 1916) on the assumption that they correspond to taste
buds. Fahrenholz (1936) pointed out many differences between these organs and
the pharyngeal taste buds, which are reinforced by the presence of bar synapses in
the receptor cells (Whitear & Lane, 1981). In fact, these organs are not taste buds,
but have been included in this section in deference to Merkel's classification; there
is considerable doubt that they are chemosensory, but their function is not known.
'The organs, at least in flank skin, occur in rows set obliquely to the axis of the
body, and appear as shallow domes with dimpled surfaces (Fig. 22). Each dimple
is occupied by a cell apex with 8&90 closely set short microvilli (Fig. 23) ; the rest
of the organ is covered by a secretion.
Fahrenholz ( 1936) distinguished several types of bipolar sensory cells in lamprey
epidermis. Apices of differentiated cells were found by SEM. The types illustrated
appear, by comparison with TEM material, to belong to chemosensory cells (Fox
et a/., 1980). Such cells may be found over most of the head and body, and in the
ammocoete particularly under the oral hood. The fringed trailing edge of the
dorsal fin of I,. planeri (Fig. 24), the site from which these cells were first described
148
E. B. LANE AND M. WHI'I'EAK
(Langerhans, 1876) has the skin surface thickly set with apices bearing microvilli
(Fig. 25). These may protrude between, or be wrapped in, the epithelial cells.
Some have longer and stouter microvilli than others (Fig. 26); it is not known if
this implies a functional distinction. The cells may be called oligovillous, as
opposed to a polyvillous type which is believed not to be sensory (Fox et al., 1980).
Figures 24 26. Lampctra planeri, fixed I", osmium tetroxide mixed with 2.5",,glutaraldehyde, without
Mucolexx. Fig. 24. Low power view of the trailing edge of the dorsal fin. x 130. Fig. 25. Closer view of
the fringed posterior edge ofthe dorsal fin, showing epithelial cell surfaces and the apices ofoligovillous
cells. x 2600. Fig. 26. Close-up of two of the oligovillous cells in Fig. 25, and the papillate surhce of
epithelial cells. x 6500.
CHEMORECEPTORS IN FISH SKIN
149
DISCUSSION
I n case the identification of the solitary sensory cells by SEM is questioned, it
should be stated that in Phoxinus phoxinus, the species in which this cell type has
been most studied, the only other differentiated cells reaching the surface of the
skin are goblet mucous cells and, very rarely, ionocytes. I n the other species we
have established, by TEM, that similar solitary sensory cells are present. In some
particular cases, we were unable to distinguish projecting cellular structures from
extruded mucus by SEM, but in other instances, such as those illustrated, there
ran be no doubt of the cellular nature of the projection and of its difference from a
mucous cell apex (Figs 3, 4 , 9 ) . The pit surrounding some apical processes from
Ictalurus melas palate (Fig. 17) is similar to the condition on swordtail tongue
illustrated by Reutter el al., (1974) but most of the projections arose from a flush
surfiice.
The hypothesis that these cells are chemosensory is based on close resemblances
between their cytoplasmic characters and those of the gustatory cells of the
corresponding species (Whitear, 1971 ; Fox et al., 1980).
Although a large number of apical processes of solitary sensory cells has been
seen in sections of Phoxinus phoxinus by T E M , the existence of the small terminal
extensions in this species had not been suspected previously. Multiple projections
at the apices have however been seen in other species, for instance in Trigla lucerna
[Whitear, 1971) and Clupea harengus (Fox et al., 1980). I n these cases, the main apex
of the cell was less protuberant. In SEM material there was considerable variation
in the length of the apical processes and in the number of terminal extensions. This
may relate to growth during the life cycle of an individual sensory cell, the form of
the process varying as new material is brought to the apex. By SEM, some of the
apices seen in Phoxinus phoxinus, and all seen in Ictalurus melas and Corydoras paleatus,
had undivided ends, and it is possible there may be regional or specific differences.
‘I’he wrinkled appearance of the membrane, commonly seen in Ictalurus melas, if not
an artefact, may also be due to a process of rapid renewal. Projecting cell apices
reported from another catfish, Ancistrzis sp. (Ono, 1980), need to be identified in
sections before i t can be ascertained if they belong to sensory cells or to some other
cell type.
The gustatory processes of taste buds in teleost fish appear always to be simple
(authors cited above, p. 142).Taste bud cells in other situations may have divided
ends, as in toads (Sagmeister et al., 1977) or mammals (Trujillo-Cen6z, 1957;
Miller & Chaudhry, 1976;Jahnke & Baur, 1979 and other authors). The function
of the receptor cell of lamprey end buds is not known, but the nature of the synapse
and the mode of innenration are different from those of taste buds (Whitear &
Lane, 1981 1. ‘The external taste buds ofMyxineglutinosa are more like those ofother
fish (Georgieva el al., 1979).
I n the dipnoan Protopierus amphibius, the taste bud pore illustrated, with a mucous
cap penetrated by gustatory cell processes, resembles those of the axolotl (Whitear,
1976). The swollen shape of the apical process of the solitary sensory cell might
ha\.e been an artehct, but was similar in sectioned material after using various
fixati\,es. Roth & Tscharntke ( 1976) found club-shaped projections on the sensory
cells of the electroreceptors in Protopterus dolloi; the swelling was not due to osmotic
efyects of the fixative, and it was suggested that it was a device to increase the area
of the receptive surface. ‘4 similar explanation can account for the swollen
I50
E. B. LANE AND M. WHITEAR
chemosensory process of the dipnoan, which would serve the same function as the
divided tip in some teleost receptors.
The scattered sensory cells seen in the lampreys (oligovillous cells, Fox et ul.,
1980) all had more than one projecting microvillus; examples seen had from two to
30. Individual microvilli had simple tips, a few were somewhat swollen. Yoshie &
Honma ( 1979) showed SEM of the apices of oligovillous cells on the oral cirrhi of a
Japanese species of lamprey, but described the processes as ciliary. The supposition
that the oligovillous cells are chemosensory is based on resemblances of their
internal fine structure to that of the teleost isolated sensory cells (Fox et ul., 1980;
Whitear & Lane, in prep.).
ACKNOWLEDGEMENTS
Dr A. K . Mittal kindly provided specimens ofBarbus sophore, Dr 0.S. Bamford of
the University of Nairobi, Protopterus amphibius, and the Department of Biological
Sciences, University of Bath, some of the lampreys. The micrographs were taken
on the University of London Board of Studies in Zoology instrument at Bedford
College and we thank Mrs Lyne Rolph for assistance. We are grateful to Messrs E.
Perry and B. L. Pirie for technical help, and to the S.R.C. for financial support
from grant no. GR/A/3740.6, 1977-1978.
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