Some Notes on the Mucous and Skin Glands
of Arion ater.
By
H. Aileen Barr, M.Sc,
Assistant Keeper in Zoology, Manchester Museum.
With Plates 38-9 and 5 Text-figures.
INTRODUCTION.
THE skin of the Pulmonates consists of an outer layer of epithelial cells which, in sonie regions of the body, bear cilia, and
beneath this a loose layer of connective tissue and muscular
fibres, interspersed with blood lacunae and containing a large
number of unicellular glands.
These glands are of three kinds :
(1) Cells which produce a globule of mucus : unicellular
mucous glands.
(2) Cells which secrete calcareous granules : calcic glands.
(3) Cells which produce granules of colouring matter : pigmentary glands.
In A r i o n a t e r var. C a s t a g n e a , the subject of this
paper, there are two types of pigment present :
(1) Black pigment granules, contained in small chromatophores.
(2) Red pigment which does not occur in definite cells, but
is found in the dermal mucous cells.
Most Pulmonates have in addition to these unicellular glands
an internal aggregation of cells which secrete mucus, which is
known as the supra-pedal gland. For a bibliography of papers
dealing with this organ, I refer to my paper (2) on the pedal
gland of M i 1 a x.
Certain families of Pulmonates, in particular the Arionidae
and Zonitidae, possess also an external mucus-secreting structure on the posterior end of the body, which is known as the
caudal gland.
504
E. AILEBN BARE,
This gland was first described.in 1852 by St. Simon (21). He
did not, however, study the histology of the organ. Andre (1)
in 1898 again described the caudal gland, but without figures of
its histological details.
With regard to the integumentary glands, the pigmentation
of slugs has been discussed theoretically in a number of papers.
Simroth, in his paper on the slugs of Germany (23), puts for
ward a number of theories to which I shall refer later. Eisig
(on the Oapitellidae), Carnot (3), Solger (23), Andre (1), and
others have discussed the theories of colouring both for Vertebrates and Invertebrates, and examples have been taken from
the Mollusca. Distaso (7) writes an interesting paper on the
connexion between the pigmentation of the mantle and shell in
H e l i x , a problem to be noticed also in reference to those
animals which have lost their shell, such as the Arionidae.
I propose in this paper to describe the aggregations of mucous
cells known as the pedal and caudal glands in A r i o n a t e r ,
and to discuss some aspects of the inter-relation of the mucous,
calcic, and pigmentary cells of the skin in A r i o n a t e r var.
Castagnea.
MATERIAL AND METHODS.
Most of the animals used for this work were the variety
C a s t a g n e a of A r i o n a t e r , which were bred in captivity
from animals collected at Chapel-en-le-Frith. Some specimens
of var. A t r a from Manchester and Buxton were also used,
but the var. C a s t a g n e a was found to be more satisfactory
for a study of the integument because the cells are less obscured
by black pigment. The var. C a s t a g n e a was also chosen
because there is red pigment in its foot-fringe.
METHODS.
The animals were killed by drowning them in water acidified
with acetic acid, or by plunging them into fixative or alcohol.
The material was fixed with Bouin's fluid, or for the preservation of the red pigment especially, by corrosive sublimate without
acetic acid.
GLANDS OF ARION
505
Sections were stained with aqueous iron alum haematoxylin
and with Delafield's haematoxylin, and with an alcoholic solution of eosin. To demonstrate mucous cells, sections were
stained for 24 hours in weak acid fuchsin (a few drops of concentrated solution of fuchsin acid in 70 per cent, alcohol to a
watch-glass full of water), and then for a few minutes in a concentrated solution of methylene blue. By this method the
mucous cells appear purple with red nuclei, the calcic cells dark
purple, the other tissues pale blue. Sections were also stained
with a weak aqueous solution of methylene blue for about
12 hours. I have not found either of these stains to be permanent in balsam. I obtained the best differentiation of the glandular cells by staining sections from 12 to 24 hours in a weak
acidified solution of toluodin blue eosin (a few drops of HC1
acid added to a weak alcoholic solution of the stain), by which
method the mucous cells stain purplish with blue nuclei, the
lime-cells (if not decalcified) deep blue, and muscle and connective tissue pink.
SUPRA-PEDAL GLAND.
The pedal gland in A r i o n a t e r extends from the anterior
end of the foot to three-quarters of the way down the body.
It lies on the internal surface of the foot below the organs of
the body, and pours out its secretion by an opening at the
anterior end.
The gland is never entirely free from the foot as it is in
M i l a x . In position and structure the pedal gland of A r i o n
occupies a place midway between that of L i m a x and that of
M i l a x : in L i m a x the gland is completely buried in the
tissues of the foot, in M i l a x it is entirely free. In A r i o n it
is level with the surface of the foot at the anterior end, then
rises out of the muscular tissue without becoming detached from
it for about one-third of its length, and finally sinks down
beneath the foot surface at the posterior end.
The pedal gland consists of a mass of white cells of irregular
shape, which secrete mucus. These cells are separated, especially on the lower surface of the gland, by intercellular spaces
506
R. AILBEN BARE
and muscle-fibres, so that the whole organ is considerably less
compact than it is in M i 1 a x . This mass of secreting cells is
traversed, through its entire length, by a ciliated tube, the
excretory canal, which receives and discharges to the exterior
the secretion from the gland-cells. Two blood-vessels run along
the gland, one on either side of it. At the anterior end they are
loosely attached to the lateral walls. Towards the posterior end
they sink down and become slits among the secreting cells and
muscular tissue.
SECRETORY CELLS.
The gland-cells are large, and irregular or more or less oval
in shape. They contain large nuclei, which in the actively
secreting phase of the cell show darkly staining chromatin and
usually a clearly marked nucleolus. The cells are either full of
a granular substance, or very much vacuolated owing to the
expulsion of their mucous secretion. The cells discharge their
mucus into the intercellular spaces, especially into those that
are situated just below the canal (see fig. 2, PI. 38). From there
the mucus passes out into the lumen of the canal. This process
is probably assisted by contraction of the muscles which are
found between the cells. Some of the glandular cells (i. e. those
in the roof of the canal, and round its dorsal half) discharge
their contents directly into the canal.
In the anterior and middle parts of the gland the cells form
a fairly compact mass ; in the posterior part, when the gland
has sunk down into the tissues of the foot, the secreting cells
become separated in groups from each other, by muscular
and connective tissue (see Text-fig. 1). The gland does not
therefore end abruptly, but gradually disappears among the
other elements of the foot.
CANAL.
The excretory canal which traverses the pedal gland does not
project beyond the secretory cells at the posterior end, as it does
in M i 1 a x, but gradually diminishes until it becomes a slit in
the muscular tissue of the foot. The mucous cells and inter-
GLANDS OF ARION
507
cellular spaces containing mucus, discharge their contents into
the lumen of the canal.
The floor of the canal is ciliated, especially on two projecting
ridges which run the whole length of the canal, and are composed of small cells each of which bears a tuft of short cilia.
Between these ciliated humps lies a groove, at first shallow,
but gradually becoming deep and narrow towards the posterior
end of the body. The cells lining the groove are generally much
vacuolated and often split away from each other, where mucus
has been discharged. They each bear a few long cilia which
drive the secretion from the cells to the anterior end of the canal
(see fig. 1, PI. 38).
TEXT-FIG. 1.
Transverse section of (A) middle and (B) posterior regions of pedal
gland, to show position of blood-vessels, ex c, excretory canal;
b v, blood-vessel.
The roof of the canal is not composed of a single layer of cells
as it is in M i l a x , but of an irregular layer of connective tissue
and muscle-fibres, with a few glandular cells. Towards the
posterior end of the canal the muscular layer on the roof becomes much thicker, and at the same time the secreting cells
increase in number and form an irregular projection from the
roof into the lumen of the canal. In some parts of the gland
this projection consists entirely of mucous cells, but in others
it is composed chiefly of connective tissue.
The main excretory canal in A r i o n does not form the
secondary ones which are found in M i l a x .
BLOOD-VESSELS.
Embedded among the secretory cells, on the sides of the pedal
gland, are two blood-vessels. These sink more deeply into the
508
R. AILEBN BARR
substance of the foot, as the gland becomes more deeply embedded, and appear at the posterior end as slits in the tissues
(see Text-fig. 1).
'
There are also a number of blood lacunae present between the
connective-tissue cells, but I have not observed in A r i o n the
two constant blood channels which run beneath the ciliated
humps in M i 1 a x and L i m a x .
SECRETION.
The slime secreted by the pedal gland is clear and sticky and
contains neither pigment nor lime granules. There do not appear
to be any crystalline concretions formed in the canal, sach as are
present in the blind posterior end of the canal in Mil a x .
This is probably due to the fact that in A r i o n the posterior
end of the tube is embedded in muscular tissue, whose constant
contractions and expansions (i. e. as the animal moves along)
prevent any accumulation of waste matter.
The slime is driven out from the aperture of the gland partly
by the action of the cilia lining the canal, partly by the contraction of the muscles between the mucous cells, and also probably by the movements of the foot itself, which will especially
influence that part of the gland which is embedded in the tissue
of the foot.
The secretion from the pedal gland is used to form a locomotory track on which the mollusc can move, and in the young
stages of the animal it is used, together with the caudal-gland
mucus, to form a slime string by means of which the slugs can
descend from trees. It plays no part in copulation, as it does
in L i m a x , because the Arions do not copulate in the same
curious suspended manner.
CAUDAL GLAND.
P o s i t i o n . — T h e caudal gland occurs in the Arionidae and
Zonitidae. It is a triangular patch of epithelium at the posterior
end of the body, which contains a great concentration of unicellular mucous and calcic glands, which discharge their secretion into the hollowed ' floor ' of the gland : this floor, in a con-
GLANDS OP ARION
509
tracted specimen, is practically covered by a flap of skin which
extends down from the body-wall. Andre (1) calls it the ' fossette
triangulaire caudale ', a much more descriptive name than
' caudal gland '.
In connexion with the caudal gland are the p e r i p o d i a l
g r o o v e s , open ciliated channels, which run one on either side
of the body, between the upper body-wall and the foot-fringe.
They open into the caudal gland, and conduct the slime from the
integumentary glands, and from the glands of the foot-fringe,
to the mucus secreted by the cells of the caudal gland.
TEXT-FIG. 2.
ped gl
caud gl
Diagram of A r i o n to show position of pedal and caudal glands.
ped gl, pedal gland ; caud gl, caudal gland ; mu, mucus.
STRUCTURE OF G L A N D .
The caudal gland consists of a dorsal flap of the skin of the
back, which is plentifully supplied with mucous glands, with
some calcic cells among them, and a triangular cavity, lined
with slime glands, which passes imperceptibly into the footfringe. The gland itself does not, however, possess the pigment
cells which are found in the foot-fringe.
Secretion occurs chiefly in the floor of the gland, which is
composed of a mass of mucous cells. I cannot agree with
Andre's figure (1), which shows mucous glands on the upper
flap only and calcic cells on the lower portion. I have found
slime-secreting cells abundantly in both regions, and especially
on the floor of the gland, lime-cells being scattered between them.
In an animal which is not sexually active, the epithelium of
the floor of the gland is thrown up into high ridges. In an
animal which is about to copulate, and in which the caudal
gland is in an actively secreting condition, the mucous cells of
510
R. AILEEN BABR
the gland are greatly swollen and full of mucus, so that the
folds between the ridges are pushed up and the floor of the
gland becomes more or less convex.
The actively secreting cells are much enlarged and contain,
usually at the end of the cell farthest from the floor of the gland;
a large nucleus surrounded by a small quantity of granular
protoplasm, while the rest of the cell is occupied by a large
globule of mucus, or by a vacuole from which mucus has been
ejected (see fig. 3, PI. 38). Below the epithelium there are a
great many layers of these cells, interspersed with intercellular
TEXT-FIG. 3.
Diagram of caudal gland of A r i o n. A, in an immature animal;
B, in a sexually mature animal, to show great development of
mucous glands.
spaces and occasional lime-cells, but containing no pigment
masses.
The epithelial cells of the posterior part of the gland, where
it impinges on the foot-fringe, bear tufts of cilia, whichprobably
aid the animal to get rid of the large globule of mucus which
accumulates in the gland cavity.
In the dorsal portion of the gland the calcic cells appear more
numerous and pour out their secretion along with that of the
mucous glands (see fig. 4, PI. 38).
SECBETION.
The mucus from the caudal gland-cells is very thick and
sticky, and colourless or milky from the presence of lime
granules. It is not coloured by pigment as is the body slime.
It is removed from the surface of the gland by ciliary action,
and by its adhesion to foreign bodies.
GLANDS OF ARION
'
511
FUNCTION OF THE CAUDAL GLAND.
In young and half-grown animals the slime from the caudal
gland is certainly used, together with that of the pedal gland,
to form slime strings, by means of which the animals can descend
from trees, &c. I have not observed this taking place in any
adult. It is, indeed, very doubtful whether a slime string could
support such a heavy animal. The adults, however, when they
crawl, will often leave behind a definite mucous string from the
caudal 'gland, which is distinct from the ordinary foot-track.
I have seen one of these strings stretching a distance of 6 inches
from the caudal gland of the animal to the side of the tank in
which it lived. The presence of the foot-track also, however,
showed clearly that the animal had not descended by the slime
string, but more probably used it as a safety-line to check a
sudden fall.
Andre considers that the caudal gland is simply a reservoir
for the body mucus. Moquin Tandon calls the gland a sexual
organ, because of the part it plays in copulation : two slugs
about to copulate, first of all eat each other's caudal-gland
mucus. But since young animals with undeveloped genitalia
have a functional caudal gland, it cannot rightly be called a
sexual organ.
As the genital organs develop the animal grows very quickly,
and it is probable that the increased metabolism of the body
associated with this growth stimulates the caudal gland and
causes it to swell up and secrete abundant mucus.
The animals may devour each other's mucus simply because it
is rich in lime, all slugs being very greedy for lime before laying
their eggs. It is also possible that this secretion may contain
some substance which functions as a sexual stimulant, in place
of the stimulating ' d a r t ' of the Helicidae. Certainly this habit
of eating the caudal-gland mucus seems to be a definite part of
copulation. I observed in the case of a slug which had been
entirely isolated, that before laying its eggs it curled round and
devoured the mucous secretion from its own caudal gland.
I have also noticed a sexually active slug kept with others
512
R. AILBEN BARR
in a tank, exploring the caudal glands of the others until it
reached one which was also bearing a large globule of mucus on
the caudal gland. This it at once began to eat, and in a short
time the animals copulated. It appears possible, therefore, that
this secretion may serve as a recognition mark between animals
which are sexually mature.
The caudal gland must be considered as a patch of skin which
is especially modified, containing a very large number of mucous
and calcic glands. The growth and activity of the gland is
strongly affected by the sexual activity of the animal. In young
animals the gland functions as an accessory organ of locomotion;
but in the adults it plays a definite part in copulation, possibly
as a recognition mark between two sexually active animals.
Mucous GLANDS.
The mucous glands of the integument are most abundant in
the foot-fringe, the foot-sole, and the mantle margin. These
are the three most active regions of the skin, and consequently
require slime for lubrication. The foot-sole and foot-fringe are
usually ciliated, and the cilia must always have a more or less
liquid medium in which to function. This medium is supplied
by the slime. The entire skin plays an important part in respiration and must therefore be kept moist; the secretion of the
mucous cells also helps to wash away any foreign matter which
might hinder the functions of the skin.
In structure the mucous glands resemble the secreting cells
of the pedal gland. They have a large nucleus and granular
protoplasm. They open either into intercellular spaces among
the tissues which eventually lead to the surface of the body, or
discharge their contents directly to the exterior by a narrow
neck between the epithelial cells (see fig. 5, PI. 39).
The foot-fringe is especially rich in these secreting cells.
On the outer edge of the peripodial groove, in the substance
of the foot-fringe, is an aggregation of mucous cells which I
propose to call the p e r i p o d i a l g l a n d . These cells are more
or less oval, and resemble the cells of the pedal gland. They
form a compact mass below the epithelium, and appear to
GLANDS OF ABION
513
extend as a glandular ridge along the whole length of the peripodial groove. They discharge their secretion on to the surface
of the foot-fringe, between the epithelial cells, and also by intercellular spaces into the groove (see fig. 5, PI. 39).
This concentration of mucous cells probably keeps a continuous flow of slime in the ciliated peripodial channel, and also
ensures that the ciliated foot-fringe is kept moist.
CALCIC GLANDS.
The distribution of calcic cells is practically the same as that
of the mucous cells, except that calcic cells are scattered also
throughout the deeper tissues of the skin. They produce abunTEXT-FIG. 4.
Diagram of transverse section of A r i o n to show position of pedal
and peripodial glands, p gl, pedal gland ; pp gr, peripodial groove;
pp gl, peripodial gland ; / / , foot-fringe.
dant limy concretions in the connective tissue, which can be
seen, through the colourless skin of the foot-sole, as little opaque
yellowish specks. The secretion of the calcic cells is cast out
with the slime.
Some of the calcic glands, especially those in the deeper
tissues of the foot, show an irregular outline, and have a definite
darkly staining nucleus and rounded granular cell contents (see
fig. 6, PI. 39). But as a rule the nucleus is obscured by a mass of
granules which stain very darkly, and the cell wall becomes
indefinite. These glands open also between the epithelial cells,
or into spaces containing mucus. They vary very much in size
(see Text-fig. 5).
The crystalline concretions in the connective tissue of the
dermis are so numerous that they render the tissues white and
NO. 283
L 1
514
B. AILEEN BAER
opaque. In sections these concretions are seen to consist of
numerous round or oval granules lying together in a space. The
granules are clear, and the larger ones show a concentric
structure and often contain a more darkly staining speck in the
middle. They resemble closely the lime granules of the degenerate shell, but are smaller and more regular in shape. They
dissolve easily in dilute acids (seefig.7, PI. 39).
This heavy deposit of lime in the tissues is probably due to
the fact that the Arions have lost all but a vestige of their
shells, and thus have nowhere to deposit the excess lime produced in the body. A certain amount of this excess is deposited
TEXT-FIG. 5.
Section of mantle margin to show distribution of glands, cal c, calcic
cell; mu c, mucous cell; epith c, epithelial cell; ct tiss, connective
tissue ; r pig, red pigment.
on the outer walls of the blood-vessels, and the rest in the
integument.
PIGMENT.
There are two forms of pigment in the skin and sub-epithelial
tissues of Arion a t e r var. C a s t a g n e a . One is the black
pigment which is so abundant in the skin of var. A t r a , the
other is the red pigment which produces the coloured foot-fringe
characteristic of the var. C a s t a g n e a .
BLACK PIGMENT.
Occurrence in v a r . Castagnea.—The black pigment
is present in the skin of the head and tentacles, in parts of the
GLANDS OF ARION
515
mantle margin, and as black lineoles in the foot-fringe. It is
also scattered sparingly throughout the skin of the back and
sides. It is not present on the foot-sole.
In the newly hatched animal there is no sign of black pigment
except in the eyes. The young slugs usually bury themselves
and do not eat for the first day or two, during which time
they do not develop any black colouring. Then they gradually
develop a black band on the mantle, over the region of the kidney, black lineoles on the foot, and a general dusky shading on
the back which develops into lateral bands. This colouring may
persist for some time, but eventually the skin darkens and the
animal becomes more or less of one colour.
BLACK PIGMENT CELLS.
The black pigment is found in the form of minute granules
inside small chromatophores which lie in the tissues immediately below the epithelium. These chromatophores are of irregular shape, and have long processes stretching out from them.
I have not been able to identify a nucleus in the cell because of
the abundance of black pigment granules, but some of the cells
show a light opaque spot towards the centre, which may be the
nucleus (see fig. 8 b, PI. 39). Distaso (7) says that the nucleus
is visible in the chromatophores of young animals, and that as
the pigment granules are formed the nucleus becomes paler and
loses its chromatin. The light spots I have observed in some
of the cells may be due to the presence of these pale nuclei.
The chromatophores, especially in the foot-fringe, are to be
found round the blood lacunae which arise in the connective
tissue, so that in a vertical section of the tissue the lacunae
appear to be ringed with black pigment (see fig. 8 a, PI. 39).
The black colouring matter is very stable. It is not extracted
by alcohol, xylol, or other fat solvents, nor by either weak or
strong acids.
Sirnroth (22) suggests that the black colouring stands in direct
relation to the amount of blood in the organs, and on the influence of atmospheric conditions. It seems probable that it is
directly connected with the blood, because (1) it is found in
Ll2
516
R. AILEEN BARK
close relationship to the blood lacunae; and (2) because the first
dark pigment in the young slug appears on the tentacles and
just over the kidney, both of which regions have a copious
blood supply. The fact that no black pigment appears until the
young animal has begun to feed, suggests that it may be due to
some degeneration product diffused into the blood as the result
of the metabolism of the animal body. In slugs kept in captivity, some kinds of food (i. e. lettuce) caused a darkening of the
body; but light had no apparent effect, since animals reared in
the dark developed the dark banding in the same way as did
those kept under ordinary conditions.
B E D PIGMENT.
The red pigment is distributed sparsely all over the skin and
foot-sole, and is concentrated especially in the mantle margin
and in the foot-fringe. Its distribution corresponds with that
of the integumentary mucous glands. It is found in the dermal
mucous cells, and is brought to the surface with the mucus.
The red pigment, unlike the black colouring matter, is not
contained in chromatophores. It appears, in the adult animal,
to occur chiefly in those slime glands which have passed the
granular stage and have formed a globule of mucus in the cell;
it also occurs in intercellular spaces.
It appears in the form of globules of varying sizes, and of a
bright orange-red colour. There may be several small rounded
bodies together, or a single large mass of a darker colour. These
large concretions in section show a concentric structure or appear
as a hollow sphere, often with a small granule in the middle (see
fig. 9, PI. 39). Although they have the appearance of oily drops,
they seem to be of a hard consistency, and to break into pieces
under pressure. They cause a degeneration of the cells where
they are formed, so that in vertical section the foot-fringe, for
instance, shows a great number of irregular spaces containing
red pigmentary masses which are surrounded by thin strands
of connective tissues. As Carnot (3) says, ' en grande quantite,
le pigment detruit la cellule . . . et ia fait disparaitre '.
GLANDS OF ARION
517
According to Newbigin (19), the red pigment of the Pulmonates is probably due to the presence of lipochromes. These
in the free state are soluble in oil solvents, whereas I was unable
to dissolve out the red pigment from the foot-fringe with alcohol,
xylol, or any of the reagents with which sections were treated
during mounting. However, if sections or pieces of tissue are
treated with fairly strong acid, the pigment concretions are dissolved, with the liberation of red colour into the acid. From
this fact, and from the close connexion between lime, pigment,
and mucous cells, which I shall shortly discuss, it is probable
that the red pigment forms a compound with the lime which
prevents solution of the pigment until the inorganic matter has
been dissolved. This appears to be so in shelled forms, where
lipochromes are certainly found in the shells, and where the
colouring matter and lime of the cells in the mantle margin form
coloured unsoluble compounds which are deposited to form the
shell.
RELATION BETWEEN THE SKIN GLANDS.
There is a close connexion between the mucous and calcic
glands of the skin and the red pigment. The secretion of the
lime-cells and the pigment are both passed out of the body with
the slime, and give the characteristic colour to the mucus, i.e.
in var. A t r a the slime is milky from the presence of lime
granules, in var. C a s t a g n e a it is red owing to the presence
of pigment. When this pigmented mucus is removed from the
slug's body (i. e. when the animal is scalded) the colour of the
skin is much paler. The film of mucus from the foot-fringe
shows, when it is removed, the definite pattern of patches of
red pigment and clear lines which represent the position of the
black lineoles.
As I have already indicated, the lime and pigment may be
even more closely connected, and form a definite compound
which is stored in the dermal mucous cells and gradually thrown
out of the body. This process may be comparable to the formation of skeletal structures in some Alcyonarians, where lime and
pigment combine to form coloured calcareous spicules;
518
R. AILEEN BARR
FUNCTION OF THE SKIN GLANDS.
M u c o u s Glands.—The secretion of the integumentary
mucous glands is used to keep the skin of the animal moist.
This is important because of the respiratory function of the skin
in Pulmonates. Slugs are extremely sensitive to drought and
the mucous sheath over the body helps to prevent desiccation.
The slime has also a defensive function, for many creatures will
hesitate to attack an animal with sticky slime. A slug if touched
will pour out mucus very rapidly, which makes the body
slippery and difficult to hold. The secretion also keeps the
surface of the body free from foreign matter.
C a l c i c Glands.—The calcareous concretions may be protective and render the tissues distasteful to other animals, in the
same manner as the limy or silicaceous spicules protect the
tissues of a sponge. The skin of Pulmonates, especially of those
forms which have lost the shell, contains a large amount of lime
in the form of concretions, and in A r i o n lime is found also
as a sheath round the blood-vessels. Calcic glands are numerous
in the mantle margin : it seems probable in slugs that such
glands continue to secrete lime, both on the mantle margin and
in other parts of the body, and that this lime is deposited in the
tissues. These calcic concretions, together with the degenerate
shell, may be regarded as the product of the calcic glands which
in a shelled animal would have formed the shell.
The calcareous granules found in the digestive gland of
H e l i x are said to be used to form the epiphragm, and may
therefore be regarded as a reserve or stored up product. This
suggests that the copious lime deposit in the tissues of naked
molluscs may lead eventually to the secondary production of
a protective shell.
PIGMENT.
The development of b l a c k p i g m e n t in the skin of slugs
is supposed by Leydig to be induced by moisture, while Simroth
suggests that a low temperature is the chief external factor
which leads to melanism. It is certainly evident that atmospheric conditions influence the colouring of slugs, since the dark
GLANDS OF ARION
519
varieties are found generally in cold damp climates, while in
drier and warmer regions the red varieties predominate. Slight
differences of temperature, however, do not appear to affect the
colouring of individual animals ; I could observe very little
difference of colouring between slugs reared out of doors, during
cold weather, and those kept indoors in as warm a situation as is
consistent with their habits. Those kept out of doors showed
more distinct colouring, both black and- red, but this was probably due simply to the fact that they were living under natural
conditions.
In addition to the external causes of the darkening of the
skin, Simroth suggests that the black pigment stands in direct
relation to the mass of blood in the organs. Andre supposes
that it may be due to some degeneration product of the blood.
As I have observed, the black pigment is clustered in small
chromatophores round the blood spaces in particular, which lends
some support to the idea that it is closely connected with the
blood supply, and may be evolved from the blood.
Carnot (3) has suggested that the deposition of black pigment
protects the skin against excessive light. This certainly appeared true of two examples of the albino form of A r i o n a t e r ,
given to me by Mr. Charles Oldham. These animals, when put
into a tank, at once buried themselves under the soil, and
appeared very uneasy when kept uncovered in the light. It is
interesting to note that in these two animals the lineoles on the
yellow foot-fringe were visible as colourless lines in the positions
of the black lines in a normally pigmented animal. I have also
observed that no black pigment is formed in the young slug
until it has left the shell, which suggests that light plays some
part in the darkening of the body ; and that it is developed as
a protection against excessive light may explain the fact that
more albino forms (i. e. forms deficient in the dark protective
pigment) are found in dull seasons.
On the other hand, if this dark pigment is a protection against
light, we should expect to find that it attains its greatest development in regions where there is the greatest amount of sunshine, in the same way as the deep pigmentation of the negro's
520
R. AILEBN BAER
skin as compared with the white man's, may be protective.
Whereas we have seen that in slugs from warm regions the black
pigment is to a large extent replaced by red pigment.
It seems probable, therefore, that the main cause of black
pigmentation lies in the internal constitution of the animal,
though possibly influenced by external causes such as moisture,
cold, &c... and that, as Simroth suggests, the pigment itself has
a direct relation to the blood, and possibly is a degeneration
product of the blood, deposited in small cells in the skin.
The r e d p i g m e n t is said to develop under the influence of
heat. Simroth calls it a warning colour, because, he says,
animals will not eat a slug with red slime.
Taylor suggests that the red pigment may have some connexion with skin respiration. He states that tissue respiration
is assisted by superficially placed colouring matter with an
affinity for oxygen. In Pelecypods the orange colouring of the
foot is said to be respiratory in function, and due to Tetronerythrine (see Taylor).
The main fact I have observed which would support this
theory is the presence of red pigment in the skin of unhatched
slugs, where it could be of great use in respiration, and could
hardly serve for any other purpose. It seems probable, however, that a pigment used in respiration would lie immediately
beneath the skin, not in the deeper dermal mucous glands, and
that it would be more widely spread in the integument. In
A r i o n a t e r var. C a s t a g n e a , for instance, it is very
sparsely scattered and veiled by dark pigment except on the
mantle margin and foot-fringe, while in var. A t r a there is
scarcely a trace of red pigment.
The red pigment develops without the direct action of light,
since it is found in the integument of unhatched slugs, inside a
shell which is opaque through the presence of lime granules.
Moreover, slugs reared in the dark show no diminution of the
bright red coloration.
Because the red pigment is cast out of the body, it seems
possible that it is a waste product. As Taylor says, ' the expulsion of colouring and other matters from the body may be
GLANDS OF ARION
521
regarded as a true excretory function'. It is interesting to note
that Tetronerythrine, the red pigment of certain birds' feathers
(see Newbigin, p. 25), which is probably the same as that of
slugs, is deposited in the feathers, which are eventually moulted,
and thus the pigment is removed from the body, although on
account of the efficient excretory organs of a bird this can hardly
be regarded as a true excretory process, as perhaps it may be
in molluscs. Certainly the presence of this pigment in the
feathers of birds argues that it does not always possess a respiratory function as it appears to do in some Pelecypods.
Sections of the foot of animals, which I injected in the bodycavity with Indian ink, showed black injected matter in the
intercellular spaces and dermal mucous glands (see fig. 10,
PI. 39). Animals injected in the same way with coloured liquid
(fuchsin acid or methylene blue) have the body slime deeply
stained. This suggests that the red pigment, which is found in
the same situations as the injected foreign matter, is a waste
product cast out of the body.
The red colouring matter does not appear to be manufactured
by the mucous cells. It is found only in a few of them, and
always in those which have lost their nucleus and practically
degenerated into a globule of mucus.
If, as I have suggested, the red pigment and lime form a
compound in the tissues, this fact also gives support to the view
that the pigment is an excretion product. Durban says ' calcareous concretions and bodies of the nature of urates may give
rise to coloration; now the latter class of substances are certainly waste products '. He also says that ' pigmentation will
ensue if pigment granules are brought to the surface more
rapidly than they can be got rid of '. This explains why the
colouring of mature slugs is usually more intense than that of
immature animals.
The supposition that the red pigment of slugs is an excretory
product is supported also by the fact that molluscs with brightly
coloured shells have often dull-coloured bodies, while those
(i. e. the slugs) which have lost their shells have usually bright
colouring and definite markings. Now in the shelled forms,
522
R. AILEEN BARR
pigment and lime are deposited on the shell, which may to a
certain extent be regarded as an excretion from the animal's
body * which serves the useful purpose of protection : in those
forms which have lost the shell the lime glands are still active
and deposit calcium in the tissues. This lime, in the superficial
layers of the skin, probably combines with red colouring matter
to form concretions which are stored in the mucous cells till they
can be passed out of the body.
This excretion of red pigment from the skin is the strongest
support for the theory that the colour is a waste product. The
mucus is expelled for the definite purpose of keeping the skin
moist; but the excreted red colouring matter does not appear
to be of any definite use, except, possibly, the acquired one of
protection, as a warning colour.
The main functions of the skin glands, therefore, are :
(1) To keep the skin moist;
(2) To produce black pigment, which is probably a degeneration product of the blood and may act as a light-screen ;
(8) To manufacture lime, which is deposited in the skin
because of the suppression of the shell;
(4) To pass the red pigment with the mucus out of the body,
and to store the excess of this pigment in certain parts
of the skin.
SUMMARY.
1. The p e d a l g l a n d is an internal aggregation of mucous
cells, whose products form a locomotory slime track, and are
expelled from the gland by ciliary action in the excretory canal
of the gland, and by contractions of muscular fibres among the
cells and by the movements of the foot. The pedal gland of
A r i o n is intermediate in position and structure between that
of L i m a x and that of Mi 1 a x .
2. The c a u d a l g l a n d is an aggregation of mucous and calcic
cells at the posterior end of the body. Its secretion is used, in
the young stages, to form a slime thread for descent; during
1
Taylor says that a H e l i x can live when its organic connexion with
the shell is completely severed.
GLANDS OF ARION
528
the period of sexual activity the slime gland becomes much more
active, probably owing to the influence of the developing sexual
organs. Its secretion is devoured mutually by slugs about to
copulate.
3. There is an aggregation of unicellular mucous glands on the
outer side of the peripodial groove, which I propose to call
the p e r i p o d i a l g l a n d . This pours out its secretion on
to the foot-fringe and into the peripodial groove, an open
ciliated channel which carries the mucous secretion of the body
down to the caudal gland.
4. The skin of A r i o n contains mucous, calcic and pigmentary
glands which are most numerous on the mantle margin and
foot-fringe.
(a) The m u c o u s c e l l s provide a secretion all over the body,
especially on any ciliated region, which keeps the
integument moist.
(b) The calcic concretions are probably an excess of lime
formed by the c a l c i c c e l l s , which in a shelled
species would be employed in building up the shell.
They may exercise a protective function, as do the
spicules of sponges.
(c) The b l a c k p i g m e n t c e l l s , or chromatophores, are
minute irregular cells found just under the epithelial
layer, and are often clustered round the blood lacunae.
It is probable that the black pigment is produced as
a degeneration product of the blood.
(d) The r e d p i g m e n t is not contained in special cells but
lies in the dermal mucous glands and intercellular spaces.
It is probably a compound produced by a lipochrome
and the lime of the calcic cells, and it is stored in the
tissues in default of a shell on which it might be deposited. It is excreted, possibly as a waste product
from the body, along with the body mucus.
I should like to thank Miss E. MacGill and Dr. G. Lapage for
their helpful criticism and advice. I am also grateful to Mr. J. W.
Taylor for lending me his translation of a paper, and to every
one who has assisted me in the collection of material.
524
R. AILBEN BARE
LITERATURE.
1. Andre, E. (1898).—" La fossette triangulaire caudale de 1'Arion rufus ",
' Rev. Suisse Zool.', vol. v, p. 179.
2. Barr, R. A. (1926).—" Some observations on the pedal gland of
Milax ", ' Quart. Journ. Micr. Sci.', vol. 70, p. 647.
3. Carnot, P. (1897).—" Recherches sur le m6chanisme de la pigmentation ", ' Bull. Sci. Trance et Belgique ', xxx, ser. iv, vol. ix, p. 1.
4. Cuenot, L. (1892).—" Etudes physiologiques sur les GasWropodes Pulmones ", ' Arch. Biol.', vol. xii, p. 683.
5.
(1900).—" Excretion chez les Mollusques ", ibid., vol. xvi, p. 49.
6.
(1914).—"Les organes phagocytaires des Mollusques", 'Arch.
Zool. Exp. et Gen.', vol. 54, p. 267.
7. Distaso, A. (1908).—" Die Beziehung zwischen den Pigmentbandern des
Mantels und denen der Schale, &c", ' Biol. Centralbl.', vol. 28,
p. 120.
8. Durham, H. E. (1892).—" On wandering cells in Echinoderms, &c",
' Quart. Journ. Micr. Sci.', vol. 33, p. 81.
9. Florentin, R. (1897).—" Quelques experiences sur les pigments ",
' Bull. Sci. France et Belgique, xxx, ser. 4, vol. ix.
10. Franz, V. (1908).—" Die Struktur der Pigmentzelle ", ' Biol. Centralbl.', vol. xxviii, p. 536.
11. Gain, W- E. (1892).—"Some remarks on the colour changes in Arion
intermedius ", ' Conchologist'.
12. Griffiths, A. B. (1892).—' Physiology of the Invertebrata.'
13. Harmer, S. F. (1892).—"On the nature of excretory processes in
Marine Polyzoa", 'Quart. Journ. Micr. Sci.', vol. 33, p. 123.
14. Hogben, L. T. (1924).—' Pigmentary Effector System.'
15. Jones, K. H. (1895).—" Molluscan albinism, &c", ' Journ. Conch.',
vol. viii, p. 3.
16. Kowalevsky, A. (1889).—" Ein Beitrag zur Kenntnis der Excretionsorgane ", ' Biol. Centralbl.', Bd. ix, p. 65.
17. MacMunn, C. A. (1890).—" Contributions to Animal Chromatology ",
' Quart. Journ. Micr. Sci.', vol. 30, p. 51.
18. Mosely, H. N. (1877).—" On the colouring matters of various animals,
&c", ibid., vol. 17, p. 1.
19. Newbigin, M. (1898).—' Colour in Nature.'
20. Poulton, E. B. (1890).—' The Colours of Animals.'
21. St. Simon (1852).—" Observations sur la glande caudale de 1'Arion
rufus ", ' Journ. Conch. Paris ', vol. iii, p. 278.
22. Simroth, H. (1885).—" Versuch einer Naturgeschichte der deutschen
Nachtschneeken ", ' Zeitschr. wiss. Zool.', vol. 42.
GLANDS OF ARION
525
23. Solger, B. (1889).—" Zur Struktur der Pigmentzellen ", ' Zool. Anz.',
vol. xii.
24. Taylor, J. W. (1900).—' British Land and Freshwater Mollusca1,
vols. i and ii.
25. Tye, S. (1878).—" Molluscan Threads ", ' Journ. Conch.', vol. i, p. 401.
EXPLANATION OP PLATES 38 AND 39.
ABBREVIATIONS USED IN THE FIGURES.
m, muscle-fibres ; ex can, excretory canal; rf, roof of canal; mu, mucus;
cil, cilia; cil gr, ciliated groove ; cil h, ciliated hump; ct tiss, connective
tissue ; mu c, mucous cell; ep c, epithelial cell; n, nucleus ; int sp, intercellular space ; cal c, calcic cell; r pig, red pigment; du, duct; chr,
chromatophores ; lac, lacuna ; cal gr, lime granules ; cal con, calcic concretions ; vac mu c, vacuolatecl mucous cell; gr mu c, granular mucous
cell.
PLATE 38.
Fig. 1.—A, transverse section. Middle of pedal gland, showing ciliated
groove and humps of the excretory canal and muscle-fibres in the roof of
the canal. B, transverse section. Posterior end of pedal gland, showing
projection from the roof of the canal, rf, roof of canal; cil gr, ciliated
groove ; pro, projection ; cil h, ciliated humps. Approx. X 350.
Fig. 2.—Mucous cells from pedal gland, secreting mucus into intercellular
space. X 370.
Fig. 3.—Longitudinal section. Floor of caudal gland of sexually active
animal, showing enlarged mucous cells, x 370.
Fig. 4.—Longitudinal section. Dorsal part of caudal gland showing
calcic cells and mucous glands opening to the exterior. X 370.
PLATE 39.
Fig. 5.—Transverse section. Peripodial gland with mucous cells opening
into peripodial groove (pp gr). x 370.
Fig. 6.—Calcic glands in tissue of foot containing lime granules (calgr)X380.
Fig. 7.—Transverse section of dermis of foot, showing calcic concretions
(cal con) in spaces in the connective tissue. X 370.
Fig. 8.—A, vertical section of foot-fringe, showing black pigment cells
(chr) clustered round a blood lacuna, x 370. B, black pigment cells or
chromatophores. Approx. x 750.
Fig. 9.—Transverse section of foot-fringe, showing red pigment (rpig) in
dermal mucous glands, x 370.
Fig. 10.—Transverse section of foot of A r i o n injected with Indian ink,
showing the injected matter (inj) among the dermal mucous cells and in
intercellular spaces. X 370.