Biol. J . Linn. SOC.,4: 147-168. With 7 plates and 2 figures
June 1 9 7 2
On the structure and function of the mouthparts
of the soil-inhabiting collembolan Folsomia
candidn
H. E. GOTO, F.L.S.
Department o f Zoology and Applied Entomology,
Imperial College, L ondon
Accepted for publication June 1972
The fine structure of the mouthparts of the collembolan Folsomiu cundidu is described, largely
o n the basis of a study with the scanning electron microscope. The structure of the maxilla and
of the mandibular molar plate is clarified and its interpretation corrected. The grinding
function, usually attributed t o the collembolan molar plate is disputed. This possible change in
function of the mouthparts may also mean that these insects play a slightly different role than
hitherto believed in the breakdown of the litter and humus in the soil.
An alternative method to replace freeze-drying in the preparation of Collembola, and
possibly other small arthropods for scanning electron microscope studies is described.
CONTENTS
Introduction
. . .
. . . . . . .
Materials and methods
. . . . . . . . .
Outline topography of the mouthparts
. . . .
External morphology in the region of the "mouth"
.
The labrum
. . . . . . . . . .
The maxilla outer lobe
. . . . . . .
The labium
. . . . . . . . . .
The mandible . . . . . . . . . . . .
The apical region . . . . . . . . .
The molar region . . . . . . . . .
The basal region
. . . . . . . . .
The maxilla
. . . . . . . . . . . .
The maxilla head . . . . . . . . .
The function of the maxilla
. . . . .
The hypopharynx
. . . . . . . . . .
Conclusion
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Summary
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Acknowledgements
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References
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INTRODUCTION
In recent years considerable attention has been paid to the food and feeding
habits of soil-inhabiting Collembola in relation to the problem of soil formation
and the long-term effect of some persistent pesticides on the soil fauna. The
study of the mouthparts of Collembola has largely been confined t o those of
147
148
H. E. GOT0
the surface-dwelling species. Folsomia candida is a common and widely
distributed soil-inhabiting species in Europe that appears to play an important
part in the breakdown of litter and the formation of humus. I t was partly for
this reason and partly because of the ease with which specimens can be
maintained in breeding cultures that they were selected for study.
A number of papers have been published on the structure and, to a lesser
extent, on the function of the mouthparts of the Collembola. Notable among
them are those of Stummer-Traunfels (1891), Folsom (1899 & 1900), Willem
(1900), Hoffmann (1905 & 1908), Borner (1908 & 1909), Denis (19281,
Schaller & Wolter (1962), Wolter (1963) and Manton (1964). FranGois (1971)
has recently restudied the endoskeletal components of the head capsule of
some Collembola. With regard to the food material, apart from some isolated
references, there has been relatively little published, vide Macnamara ( 1924),
Poole (1959), Singh (1969) and Massoud (1971).
The Collembola or springtails constitute one of the two entognathous orders
of apterygote insects. I t is partially on account of this entognathous or
enclosed condition of the mandibles and the main part of the maxillae that so
few studies have been made of the detailed structure of the mouthparts and of
their functions. Not only are they enclosed within the head but they are also,
in the majority of the Collembola, of minute size and frequently of
considerable complexity. For this reason studies have been very largely
restricted to the mouthparts of those species that are of comparatively large
size, e.g. to those of some species of Tomocerus Nicolet, 1841 and of
Orchesella Templeton, 1835, or to those of species of smaller size but in which
the structure is not of a very complicated nature, as in Anurida maritima
(Guerin-Meneville, 1836). I t is especially in the structure of the so-called
maxilla head that great complexity frequently exists. This complexity has been
known for many years but in the majority of relevant publications no attempt
has been made to provide any interpretation beyond the vaguest of statements.
The notable exception is to be found in Borner’s (1908) paper in which he
records the results of his investigation of the structure of the maxilla head of
Tomocerus (Pogonognathellus) longicornis (Muller, 1776) under the name
Tomocerus plumbeus (L.). This is one of the largest of the Collembola and one
with very complex maxilla heads. Borner (1908) also compared the maxilla
head of this species with some smaller but simpler collembolan maxillae. Other
studies have been concerned not so much with the detailed structure of the
heads of the mandibles and maxillae but rather with the outline morphology,
function, development and homologies of the entire complex of the
entognathous mouthparts. The difficulty of morphological interpretation
resides very largely in the structure of certain appendages, mostly known as
lamellae, arising from the maxilla head. These structures are often provided
with fringes of tapering, finger-like or tooth-like outgrowths that may be very
numerous and frequently of only about one micron in thickness. They often lie
superimposed one upon another and are, in many cases, virtually impossible to
interpret with any degree of certainty by means of conventional or
phase-contrast light microscopy, even with squash-preparations or when the
mandibles and maxillae can be removed from within the head by
microdissection. Serial sectioning has not proved to be of much help.
In spite of the uncertainty of any interpretation of the morphology of the
MOUTHPARTS OF FOLSOMIA CANDIDA
149
maxilla head and its appendages in the majority of species, these structures
have been used on a number of occasions as the basis of a taxonomic revision,
e.g. Poinsot’s (1965) revision of the genus Archisotoma Linnaniemi, 1912 and
Massoud’s (1967) monographic study of the Neanuridae. In other cases, where
the maxillae are smaller, as for example in the species of the genus Anurida
Laboulbene, 1865, the comparative lengths of the lamellae and of the main
body of the maxilla head have been used as taxonomic criteria both in
descriptions and in keys (e.g. Gisin, 1960: 95). Even the precise number of the
maxillary appendages to be found in some species of Collembola is still in
dispute. In others, e.g. those of the genus Fofsomia Willem, 1902, the
morphology of the mouthparts has been very little or not at all used to provide
taxonomic characters, almost certainly on account of their small size and
complexity ; neither the mandibles nor the maxillae are mentioned in Folsom’s
(1937) monograph on the nearctic Isolomidae or in the otherwise very full
descriptions of the genus Folsomia and its species given by Stach in his
monograph on the family Isotomidae (1947). Similarly no use was made of the
structure of the mouthparts in Gisin’s (1960) key to the species of Fofsomia in
his work on the European Collembola. Some of the most commonly used
characters for separating the 50 or so species of the genus Fofsomia have been
known for some years to be applicable only in the case of fully developed
specimens (Goto, 1956a); the application of these key characters leads to
misidentification of juveniles and on more than one occasion has resulted in the
erection of new species or even genera on the basis of juvenile specimens (e.g.
Goto, 1956b). This study of the fine structure of the mouthparts of Fofsomia
candida formed the preliminary part of an investigation to find new taxonomic
characters that would be valid in the case of early as well as late instars. The use
of structures that are not fully understood has already led to some confusion in
the systematics of the Collembola, and any vague interpretation based on
inadequate understanding can be very dangerous. Lawrence (1968) has given a
warning of the possibility of misinterpretation of such complex structures as
those found on the collembolan maxilla. This is entirely supported by my own
investigations on the mouthparts of Fofsomia and other springtails.
These studies were largely carried out with the scanning electron microscope
which provides not only a useful magnification of up to about ~ 3 0 , 0 0 0but also
a resolution of 200 A or better and a depth of focus at least 300 times better
than that available with light microscopy at comparable magnifications. This
has enabled the detailed structure to be observed and has revealed an even
greater degree of complexity in the structure of both the mandibles and of the
maxillae than was previously suspected. The structure, and probably also the
function, of the mandibular molar plate has been found to be other than is
usually thought.
MATERIALS A N D METHODS
Cultures of Folsomia candida Willem, 1902 were maintained in the
laboratory by methods essentially similar to those previously described (Goto,
1961) but with less water in the plaster and with stabilized wheat germ
(Bemax) provided for food in addition to dried yeast pellets. As the stocks have
been in culture for a number of years in my laboratory, checks were made with
150
H. E. GOT0
wild populations from Imperial College Field Station, Sunninghill, Berkshire
but no differences were found between the structure of the mouthparts of the
latter and those of the individuals in culture.
The early treatment of the specimens destined, on the one hand, for
examination of the external features of the “mouth” region of the head and,
on the other, for detailed study of the entognathous components of the feeding
apparatus was different.
(a) Those specimens ultimately to be used for the examination of the
external features were first freeze-dried en musse from life and stored in a
stoppered tube placed in a desiccator until required for further treatment. The
latter consisted of the fixing of the specimen to a standard Cambridge
Instrument Company Stereoscan stub, at first with Durofix or double-sided
Sellotape but subsequently with colloidal silver in iso-butyl methyl ketone
(Acheson’s ‘dag’ 915) directly on the stub or as an addition to Sellotape to
provide better mechanical fixation and conductivity. The specimens were then
coated with pure gold. Aluminium and gold/palladium alloy were both used in
early trials but with less effective results.
The freeze-drying process was necessary because without this treatment the
head capsule (and the rest of the body) shrivelled to a greater or lesser extent
but nearly always sufficiently to obscure some of the surface details of the
labrum, “mouth”, labium and the external lobe of the maxilla.
Through the courtesy of Mr A. D. Greenwood and the help of Miss J. Fillery
I was able, in the latter stages of this work, to make use of the critical point
drying apparatus made by Mr Greenwood in the Botany Department, Imperial
College. This proved to be a satisfactory and very convenient substitute for
freeze-drying. The apparatus is essentially as described by Boyde & Wood
(1969). In this method the specimens were dehydrated in successive grades of
alcohol and transferred to amyl acetate for three days, or longer, after which
the specimens were placed in the critical point drying apparatus where the amyl
acetate was replaced by liquid carbon dioxide. The temperature of the carbon
dioxide was then raised to its critical point and the pressure released. The
specimens were then ready for vacuum coating and examination.
In some work done jointly with Dr K. Boratynski on certain cuticular
structures in Coccoidea (Hemiptera) it was noticed (by K.B.) that, following
the same procedure as mentioned above, the specimens showed very little sign
of distortion when allowed to dry in the air after reaching the third day in amyl
acetate. These observations were repeated with Folsomia candida and other
small Collembola with the same results. Although there were some signs of
distortion they were no more evident than was sometimes seen after
freeze-drying and occasionally after critical point drying. This method may
prove to be of more general application.
(b) Examination of the mandibles, maxillae, hypopharynx and associated
posterior tentorial apodemes required the complete removal of these structures
from the head capsule. This proved to be very difficult in freeze-dried and
critical point-dried specimens and the process was, in fact, found to be
unnecessary as comparatively little or no distortion was observed in the
structure of the mandibles and maxillae, even of the very delicate maxillary
lamellae, prepared with preliminary freeze-drying. This was not true for parts
of the hypopharynx (see p. 164). Softening of the more delicate components
MOUTH PARTS 0F FOL SOMIA C ANDIDA
151
of the mouthparts did, however, result from the subsequent maceration process
and this gave rise to a small amount of distortion. The removal of the
entognathous components of the mouthparts was greatly facilitated by the
following treatment: specimens were killed in ethyl acetate vapour and placed
in a mixture of lactophenol and chlorazol black E (Goto, 1964), covered and
maintained at 60” C until all but the cuticular parts were completely macerated.
At this stage the cranial cuticle, posterior parts of the mandibles, stipites,
cardines, hypopharynx and posterior arms of the tentorium were grey-black,
but transparent, and the heads of the mandibles and maxillae were dark, almost
black. The specimens were then thoroughly washed in 70% ethyl alcohol and
placed on a cavity slide in 50% alcohol. The mandibles and maxillae, being
clearly visible owing to the staining with chlorazol black, could then be
removed with comparative ease from the head capsule by dividing the left and
right halves of the ventral surface of the head along the longitudinal labial
suture and the linea ventralis with a pair of fine-pointed needles. The latter
were also used to pull out the mouthparts and associated structures. In about
one-quarter of the specimens treated in this way, both the mandibles and the
maxillae everted, at least partially, through the “mouth” during the process of
maceration in the lactophenol/chlorazol black mixture. These were the easiest
of the specimens to use for the removal of the mouthparts. Using this
technique, not only the mandibles and maxillae (including the outer lobes of
the latter) but also the hypopharynx, superlinguae and posterior arms of the
tentorium could be removed as a single unit, the latter being attached to the
maxillary cardines. The whole complex could then be transferred t o the
Stereoscan stub and orientated in the required position by partially embedding
them in a very fine film of colloidal silver. Thin films were more easily obtained
by diluting the silver ‘dag’ with further iso-butyl methyl ketone. The handling
of these structures as a complete unit proved to be much simpler than was the
case when isolated mandibles or maxillae were used. This was largely a question
of size, an individual maxilla head, for example, measures about 0.03 to
0.04 mm in length by about 0.02 mm across; the whole maxilla including the
delicate stipital and cardinal regions is approximately 0.3 mm in length.
The examination of the apical portions of the mandibles, maxillae and
hypopharynx could be made to some extent in situ by widening the “mouth”.
This was done by making small lateral incisions at the sides of the “mouth” and
raising the lowering the labrum and labium respectively This operation was
most easily carried out after embedding the head in silver ‘dag’ on the stub
leaving only the “mouth” region exposed.
All observations with light microscopy were by means of Wild
phase-contrast, in most cases after mounting in polyvinyl lactophenol with or
without chlorazol black.
For most of the observations a Cambridge Instrument Company Mark I1
Stereoscan scanning electron microscope was used at various magnifications
and accelerating voltages (as indicated in the legends accompanying the plates)
for the more detailed observations. Some of the observations and
photomicrographs of external and mandibular structures were made with a
JEOL JSM-S1 scanning microscope. This gave excellent results at lower
magnifications. The majority of the stereoscan photomicrographs were taken
on 35 mm Ilford Pan F film.
152
H. E. G O T 0
OUTLINE TOPOGRAPHY OF THE MOUTHPARTS
During the embryonic development of the mouthparts of the Collembola,
the mandibles become totally enclosed and the maxillae almost completely so
by the downgrowth of a pair of lateral folds at the sides of the head, the plicae
orales (p. 0.)or pleural folds. These fuse with the labrum (1.) above and with
the labium below forming a secondary mouth-opening leading into a pair of
gnathal pouches, one on either side of the hypopharynx. The secondary mouth
is here termed the “mouth”. Within the gnathal pouches on either side of the
head lie the mandibles above (morphologically anterior) and the maxillae
below. Contrary to the opinion of Snodgrass (1950), there is no mandibular
rod but the mandibles are loosely attached to the lateral walls of the gnathal
pouches by a strip of pliable cuticle representing the limb base (Denis, 1928
and Manton, 1964) and known as the mandibular suspension (m.s.). The
suspension is inserted at the extreme proximal end of the mandible. When at
rest, the mandibular molar plates (m.m.p.) (pars molaris of Massoud, 1967,
1971) lie over the hypopharynx and the apices of the mandibles (pars apicalis
or pars incisiva of Massoud, 1967, 1971) are just within the “mouth”. The
maxillae are connected via the cardines (c.) to the posterior arms of the
tentorium which converge anteriorly and lie beneath the hypopharynx and its
superlinguae. The maxilla heads lie beneath the apical mandibular cusps when
at rest. Although normally completely enclosed within the head, the distal
portions of both the mandibles and the maxillae and, t o some extent also, the
apex of the body of the hypopharynx can be protracted through the “mouth”
during the feeding movements. The relative positions of the main components
are shown in diagrammatic form in Fig. 1A. Arising from the distal end of the
stipes of each maxilla are the head, or capitulum, and above and lateral t o the
head a structure variously termed the outer lobe (o.l.m.), galea, palp (the
Maxillartaster of Schaller, 1970) or palpifer. Some authors draw a distinction
between the external lobe proper and the palp (see pp. 154-5). Massoud
(1971) follows Denis in recognizing two parts of the stipes termed coxa I and
coxa I1 at the apices of which are the internal lobe, bearing the capitulum, and
the external lobe bearing the setigerous palp respectively. The distal part of the
outer lobe lies on the surface of the head on either side of the “mouth” just
beyond the free end of the plica oralis and between the labrum and the labium
(Plate 1A). The region of the plica oralis just proximal to the point of
emergence of the outer lobe of the maxilla is distinctly defined (abgegliedertes
Stuck der Mundfalte of Hoffmann) and can easily be mistaken for a basal
segment of the outer lobe. I t bears a seta that overhangs the outer lobe of the
maxilla.
The head endoskeleton is obviously very closely related, both structurally
and functionally, to the mouthparts. Francois (1971) has studied both its
ectodermal and mesodermal derivatives in the Collembola: Anurida, Tomocerus
and Sminthurus. The significance of his work will be discussed elsewhere.
EXTERNAL MORPHOLOGY IN THE REGION OF THE “MOUTH”
The labrum
The labrum (1.) (Plate l A , D) is more or less quadrilateral in outline with the
lateral margins converging from the base to the apex and has the fronto-lateral
MOUTHPARTS OF FOLSOMIA CANDIDA
6
Oll
012 013 0 4 015 6.6 017 O h
153
6.9- 710
mm
Figure 1A. Diagrammatic representation of the mouthparts and associated structures in dorsal
view of Folsomia candida. The mandible has been removed on the right side. 19. Frontal
sclerite in ventral view. 1C. Frontal sclerite in lateral view.
154
H. E. GOT0
angles rounded. I t is bounded proximally by a deep furrow which separates it
from the fronto-clypeal region of the head. There is no obvious suture or other
superficial indication in Folsomia of a fronto-clypeal boundary but there are
some transverse depressions in this region of the head, one of which may
perhaps represent the dividing line between the frons and the clypeus. The
general tuberculation of the body cuticle (Ogel, 1965) is continued on to the
labrum except for a zone adjacent to the mouth. This is evident at the
antero-lateral angles of the labrum as a narrow strip on either side and medially
as a much broader, slightly upturned lip-like area (Plate 1B). Just proximal to
the clypeo-labral junction is a very prominent region, usually termed the
frontal sclerite (the Chitin wulste of Hoffmann), that extends laterally and some
way round the point of emergence of the outer lobe of the maxilla. The frontal
sclerite (f.s.) is very thick, particularly in the region directly above the labium,
and for this reason it is distinctly visible as a darkly stained transverse band in
preparations treated with chlorazol black (Fig. lA, B, C) (cf. Manton, 1964,
Fig. 35). The frontal sclerite provides a rigid point of origin for the labral
depressor and epipharyngeal elevator muscles (dilators of Hoffmann). From the
outer surface of the frontal sclerite there arise four setae that project forwards
and downwards over the base of the labrum. The labrum itself is provided with
three rows of strong, forwardly directed setae: a proximal row of five, a middle
row of five and a distal row of four. The setae of the basal and middle rows are
arranged one behind the other. The outer setae of all three rows are equidistant
from the lateral margins of the labrum. The two inner setae of the distal row
are situated in line with the interstices between the median and mediolateral
setae of the basal and middle rows. The strongest setae are the lateral ones of
the basal and middle rows, especially the latter which are distinctly stouter.
The setae of the middle and distal rows arise from elongate (parallel to the
main axis of the body) rather than circular shaped sockets. This would appear
to indicate a greater freedom of movement, or a restriction of movement of the
setae, in this direction. None of the labral setae appears to be specifically
modified as a sensory receptor. As some at least of them extend beyond the
free margin of the labrum and project towards the area in front of the
“mouth”, they may play some part in the collection, holding or positioning of
food before it is grasped by the apical mandibular teeth. In Folsomia cundida
no structures were found that could be comparable to the Chitinhuken
described by Hoffmann (1905: 1) arising on the epipharynx near to the tip of
the labrum at the point of insertion of the tendon of the labral depressor
muscles. The labrum is fairly mobile, being lowered by means of contractions
of the pair of depressor muscles originating on the frontal sclerite. Certain
aspects of the structure of the under side of the labrum (epipharynx) will be
discussed elsewhere.
The maxilla outer lobe
Lying on either side of the labrum and distal to the plica oralis is the outer
lobe of the maxilla (o.1.m.). Although this structure appears to form an integral
part of the wall of the head surrounding the “mouth” it is, in fact, capable of
some limited independent movement. The exposed portion of the outer lobe of
the maxilla (Fig. 1)bears seven setae. Of the seven, two are associated with one
MOUTH PARTS 0F FOL SOMIA CANDIDA
155
another: one arising from the side of a papilla (the pulpe sktigkre of Massoud
(197 1) and some earlier authors) upon which the other is apically situated. This
arrangement is reminiscent of one found on the labium that, from its structure,
would appear to be associated with chemoreception. The distal outer end of
the lobe is free of tubercles (Plate 1B).
The labium
The lateral and posterior boundaries of the labium are not very clearly
defined in mounted specimens but in living, freeze-dried and critical point-dried
material they can be located by somewhat broad and ill-defined furrows (Plate
l C , D). The furrow starts at the sides of the head just postero-ventral to the
point of emergence of the outer lobe of the maxilla, i.e. a little way in front of
the lateral limits of the clypeo-labral boundary. The furrow then runs obliquely
backwards to meet the furrow on the opposite side of the head just in front of
the point of origin of the Zinea uentralis. The labium is partially divided along
its median longitudinal line into right and left halves. Distally the separation is
clearly complete as the two halves diverge from one another. Along most of the
length of the dividing line, the two halves are totally ankylosed but still retain a
marked superficial furrow. At the base of the labium the division between the
two halves once again becomes complete. At this point there is a salivary
channel (sal.ch.) (cf. Manton, 1964; Fig. 36C, D) leading to the exterior from
h e median diverticulum of the gnathal pouch into which opens the ducts of
the labial salivary glands (Fig. 2). On either side of this median gap and
extending forwards is a pair of triangular areas (Plate 2A) of non-tuberculate
cuticle corresponding, no doubt, to the Zwickel of Hoffmann. A t is apex, the
Figure 2. Diagram of the anteromedian zone of the labium. Showing the hyuline Plurre and
salivary channel. Note the cuticular thickenings on either side at the junctions of the granular
and non-granular zones.
156
H. E. GOTO
labium bears a pair of lobes, the Klauenteil of Hoffmann or partie setigbre
(n.t.z.) of Denis. The main body of the labium (Schild of Hoffmann, kcusson or
mentum of Denis) lies posterior to and, to some extent, lateral to these lobes.
This lateral extension probably corresponds to what Willem (1900) termed the
pulpe, in my opinion, without justification. What corresponds to the true labial
palp probably exists only in some of the Sminthuridae. In Folsomia cundidu
the two apical lobes are quite separate from one another along their entire
median length. In this, and in the backward extension of the median apical gap
on to the main body of the labium, it differs, apparently, from Tornocerus
(vide Hoffmann, 1908; Fig. 8). There is no clearly defined submentum or gda,
as described by Folsom (1899) in Orchesellu Templeton, 1835. The hyaline
Plutte, described by Hoffmann in Tomocerus, is clearly visible in Plates 1B and
2B; Fig. 2 as a cuticular region devoid of epicuticular tubercles slightly
depressed from the surface; Denis referred to the hyaline Plutte as an internal
lobe of the labium, the purtie sktigbre (t.z.) being the outer one. Somewhat
similar non-tuberculated areas are also visible at the apices of the labrum and
the outer lobe of the maxilla. The homologies of the various components of the
labium in Collembola are still subject to some dispute. The setigerous lobe is
generally regarded as the homologue of the lacinia and galea, and the proximal
region as that of the mentum.
Each setigerous lobe bears a complex of five groups of papillae surmounted
by setae (Plates 1C and 2B). These are supplied with nerves from the
suboesophageal ganglion. The papillae are arranged in two rows. The proximal
row consists of two simple papillae each with one more or less plump sensory
seta arising from its apex, the median of the two setae is of the greater diameter
(about 5 : 3) and distinctly shorter (about 5 : 8). An additional seta arises from
the base of the median papilla only. This is not deeply inserted within the
papilla as is the apical one here and elsewhere as may be seen with light
microscopy. The distal row consists of three groups or clusters of associated
sensilla and acuminate setae. The median-most cluster is composed of a
broad-based, rather irregular papilla with an apical sensillum and with one
ventro-median, two outer lateral and one dorsal seta arising from the body of
the papilla. The middle of the three distal papilla-clusters is similar to the
previous one, except in details of the form of the papilla. The outer cluster is
more complex: it consists of a pair of adjacent papillae, the outer lateral one
being simple and without an apical seta-like sensillum but with a smooth,
apparently structureless, slightly expanded flat top (Plate 2C). Arising from the
ventro-median and the outer lateral aspects of the base of this papilla are too
setae. Although independent along its entire length, this papilla arises from the
outer side of the base of the adjacent main lateral papilla-cluster. The latter is
surmounted by a sensillum with four associated setae. one inserted
ventro-medianly and the other three laterally. Each of the apical sensilla is
blunt-tipped and terminates in a widely open pore (Plate 2D). On one occasion
only, whilst examining these sensilla with an acceleration voltage of 30 kV, an
apparently very delicate collar, somewhat reminiscent of those of a poriferan
choanocyte, was seen surrounding the apical pore. The collar soon disappeared
during the examination and it is not certain whether it was a true structure that
had been destroyed under the electron bombardment or if it was an artifact.
Electron beam damage to various structures was noticed on a number of
MOUTHPARTS 0F FOLSOMIA C ANDIDA
157
occasions whilst working at high magnifications and voltages. Attempts to find
such structures again were always completely unsuccessful even at electron-gun
voltages as low as 10 kV. Each of these sensilla was devoid of cuticular
tubercles but was rather faintly ringed along its entire length with irregular
annulations. These may also have been artifacts. The only obvious difference
between individual sensilla was in their lengths and diameters. Each one of the
apical sensilla arose deeply within the body of its basal papilla; this is only
visible when examined with conventional light transmission microscopy. There
is some variation in the lengths of corresponding sensilla in different
specimens-this may perhaps be due to the ability of the animal to protrude
and retract the sensilla to a limited extent-the validity of this hypothesis still
remains t o be confirmed. The apical aperture undoubtedly suggests that these
sensilla are most likely to be contact chemoreceptors, as might also be assumed
from their apical position on the labium and just below the “mouth”. In
addition to the sensilla and their associated setae just described, there are some
other acuminate, curved setae on the setigerous lobes. These consist of a basal
pair and a further pair just lateral to the outer of the two simple papillae of the
proximal row. These setae arch forwards over the papillae and their sensilla;
together with those arising from the bodies of the papillae, they undoubtedly
serve as mechanical protectors of the sensilla and may also play some part in
the feeding mechanism for sorting or impaling the food. Each half of the
mentum has one basal seta, a transverse row of three and a group of four in the
distal portion that lies alongside the setigerous lobe. None of these is obviously
modified as a sensillum. Lying close to the antero-median angle of each half of
the labium is a particularly well sclerotized strip of cuticle. These are situated
at the point of junction of the tuberculate setigerous lobe and the hyaline
plate. They are raised from the general surface of the cuticle and face inwards
and towards one another. They may correspond to the unlabelled thickenings
shown in a similar position in Hoffmann’s Fig. 8, p. 653 (1908). They appear
to differ from the latter in being more prominent. With the hyaline plate in its
normal, retracted position these strips project forwards at a slightly deeper
level. The function of these structures remains unknown.
THE MANDIBLE
The mandibles in Folsorniu cundida, as in the majority of Collembola, are of
the “biting type” (Wolter, 1963), i.e. they are provided with a well developed
molar area or plate in addition to the apical incisor teeth. The mandibles lie
above (i.e. morphologically anterior to) the maxillae and dorso-lateral to the
hypopharynx. They are attached to the lateral walls of the gnathal pouches by
thin, delicate, flexible cuticular folds that enable the mandibles to have a great
deal of freedom of movement (Manton, 1964). The mandibular muscular
systems of a few species of Collembola have been previously described, notably
by Hoffmann (1908), Denis (1928), Wolter (1963) and especially Manton
(1964). The first real understanding of the mechanisms involved in the feeding
processes in the Collembola has resulted largely from the latter work. The
muscular system was not specially studied in Folsorniu cundida but there
appear to be no marked differences between the trophic musculature of this
species and that of those that have already been studied.
158
H. E. GOTO
The apical region
The general form of the mandible is very similar to that previously described
and figured independently by Hoffmann and by Manton for Tomocerus
longicornis. The apical mandibular cusps (usually termed apical teeth (m.a.t.) in
collembolan taxonomy) are strong, smooth, well defined and more or less
conical in shape (Plate 3A). They are arranged in a single row parallel to the
long axis. The number of cusps normally varies from three to four. There are
always at least three distinct cusps on each mandible and in most cases a fourth
cusp is more or less well developed adjacent and proximal to the row of three.
Often the fourth (basal) cusp is only clearly defined on one of the two
mandibles, usually that of the right side. In such cases, on the mandible of the
opposite side the basal cusp is more often than not represented by a small, flat,
rounded swelling that merges gradually, on the proximal side, into the main
shaft of the mandible. The size of the four cusps decrease gradually from the
apical one to the basal one. In the same order, they become progressively more
blunt. Slight asymmetry allows the cusps to interdigitate during their rotary
cutting movements (Manton, 1964; 57). The degree of asymmetry between the
left and the right mandibular apical cusps is never great, as it may be in some
other Collembola, and is normally limited to a difference in the degree of
development of the fourth one. In some case, however, the body of the
mandible in this region is stouter on one than on the other appendage. I t is
usually the mandible with the better developed basal cusp that is the stouter
one; in this case the apical point is often more angular, the opposite mandible
having a more rounded appearance at the tip.
The molar region
In the molar region of the mandible there are, as in Tomocerus, some
odontoid molar cusps (mandibular molar cusps of Manton) in addition to the
so-called molar plate (m.m.p.). The odontoid molar cusps are more or less
regularly conical and lie ventral to the true molar plate. Like the apical
mandibular cusps, they gradually and progressively decrease in size from the
distal to the proximal one. They are usually rounded at their tips (Plate 3B) but
in some specimens, particularly in those prepared for conventional light
microscopy, they appear to be sharply pointed and somewhat flattened
(Plate 3C)-this may be an artifact in one or other of the methods of
preparation. There are usually from four to six odontoid molar cusps (most
commonly five) on each mandible. The number may or may not be the same
on the left and the right mandibles. At the distal end of the row, the cusps are
situated further away, i.e. more ventrally, from the main body of the molar
plate than they do at the proximal end. In the latter position they are in
contact with the molar plate and are replaced by what may be termed the
buttress rods that run back to the posterior angle of the molar plate (Plate 3D).
The buttress rods are stout and appear to form a firm but flexible
postero-ventral border to the main body of the molar plate. The more
anteriorly placed of the buttress rods sometimes seem to be divided basally into
two, or more rarely three, roots that appear to fuse at about one-third of the
distance up from their points of origin. This is an artifact as can be seen in
MOUTHPARTS OF FOLSOMIA CANDIDA
159
Plate 3C where they are separate along their entire lengths. As the posterior
margin of the molar plate is approached, the buttress rods become slightly but
progressively shorter and distinctly wider at their distal than at their proximal
ends. There are at this point a few (usually four) finger-like apical processes at
the tips of each of these buttress rods (Plate 3D). These processes are rather
variable in their orientation and to a lesser extent in their size, the former
indicating, perhaps, a somewhat more flexible nature than appears t o be
characteristic of the more basal parts of the rods. Buttress rods are absent for a
short distance before the extreme posterior tip of the molar plate (Plate 4A),
the so-called heel of the molar plate or Fersenteil of Hoffmann. At this point
there is a very large, apically rounded projection that points inwards towards
the midline of the head and slightly forwards in the direction of the apex of the
mandible.
On the opposite side of the molar plate (i.e. along its dorsal or anterior
boundary) the buttress rods are replaced by much more slender rods that taper
abruptly to a point apically (Plate 4B). Whereas the buttress rods appear t o flex
more or less uniformly along their entire length these upper molar boundary
rods flex more readily towards their apices. I t is probable that the upper molar
boundary rods, the buttress rods and perhaps also the odontoid molar cusps are
derived from the same rudiments as the individual units (molar plate cusps)
composing the main body of the molar plate. There is, in fact, very little
difference between the bounding odontoid molar cusps and the outermost
(ventral) molar plate cusps. This is especially obvious where the row of
odontoid cusps approaches the main body of the molar plate in its proximal
region (Plate 3 0 . At this point it can also be seen that the odontoid cusps are
in line with the transverse rows of the molar plate cusps. In many specimens
those molar plate cusps that lie adjacent t o the odontoid cusps appear to stand
apart from the remainder of the molar plate in their degree of development and
appear to constitute a second row of odontoid cusps. Hoffmann (1908, Plate
39, Fig. 16B) does, in fact, illustrate two such rows in Tomocerus. The
alignment of the buttress rods and the upper molar boundary rods with the
rows of molar plate cusps is not quite so obvious.
Each molar plate is an asymmetrical structure. Commencing at the distal
end, where there is a single, fine, extra-long, bristle-like cusp, the molar plate
broadens more or less symmetrically. At a point about halfway back to the
proximal end, the plate as a whole begins to turn upwards and, to some extent,
outwards providing a curved molar surface functionally very suitable for an
effective rotary/counter-rotary movement such as described by Manton in
Tornocerus.
The main body of the molar plate is very much more complex in detailed
structure than was previously envisaged and described as regular rows of minute
teeth extending from side to side of the plate. The “teeth” or cusps are, in fact,
merely the apices of rod-like structures that are not short but extend
downwards to the same level as the bases of the buttress and upper boundary
rods. They form, instead, a composite structure more akin to a brush than to a
toothed plate. The term “molar plate cusp”, although inappropriate, is
retained. The rods of the brush “pile” are not rigid but rather flexible, as can
be seen in Plate 3C. The fissures between the rows of molar plate rods and the
gaps between individual rods are never quite the same on different mandibles,
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H. E. GOTO
even in the same individual, and are clearly temporary derangements of the
“pile”. It would seem, therefore, that the molar plate, at least in this species,
may not be quite so effective a grinding surface as it was previously thought to
be. The action may be rather of a brushing, teasing and scarifying nature
adequate for separating and gently teasing the fungal hyphae on which
Folsomia feeds so frequently. There seems little doubt, however, that the
odontoid molar cusps, working together, could cut and grind the food between
them. To a small extent, however, the fissures and gaps in the pile may be
accentuated due to the softening of the cuticle during the early stages in the
preparation of the specimens (see under Methods above). Those specimens that
have been mounted for light microscopy in media that do not soften the cuticle
appreciably show less marked, but still obvious, fissuring.
In different regions of the molar plate the “pile” is composed of rods of
different types. At the extreme distal region of the plate the rods are simple
and finger-like. Just behind this region and extending back towards the
proximal end of the plate there is a large number of regular rows of
multicusped molar rods. These do not seem to be of compound origin as they
correspond to single bounding cusps or rods and their multiple condition is
only evident towards the apices of the rods. On one or more sides of the distal
region of each of these multicusped rods clusters of stumpy subsidiary cusps.
These vary in number and arrangement (Plate 4C, D). Occasionally they are
absent, the main cusp only persisting and at other times they are
indistinguishable from the main cusp. On the other hand the latter sometimes
extend well above the general level of the subsidiary cusps; this is especially
true towards the edges of the molar plate. The division of the molar plate into
two longitudinal zones, as figured for Tomocerus by Hoffmann (1908; Plate
39, Fig. 16B) was never observed in Folsomia candida.
The basal region
The remainder of the mandible, bearing the mandibular hump (Manton) or
Hocker (Hoffmann), the dorso-lateral mandibular ridge (not clearly visible in
Folsomia), and the point of articulation with the posterior mandibular
apodeme and the mandibular suspension is not nearly so well sclerotized as the
mandibular head (apical toothed and molar regions). This seems strange as this
region is the one on which are inserted some of the muscles whose contractions
result in the rotatory and counter-rotatory (as well as protraction, retraction,
adduction and abduction) movements of the mandible. These are the muscles
that are responsible for the so-called “grinding” movements of the molar plate
(Manton). The comparatively delicate nature of this posterior part of the
mandible may be associated with the pliable nature of the molar plate cusps.
The large mandibular cavity (m.c.) in which are inserted some of the
mandibular muscles is always clearly visible.
THE MAXILLA
The maxillae lie, for the most part, in the gnathal pouches just below
(posterior) to the mandibles and on either side of the hypopharynx. The
maxillae articulate basally, via the cardo (c.) and the cardo-posterior tentorial
MOUTHPARTS OF FOLSOMIA CANDIDA
161
membrane (c.t.m.), with the transverse process of the posterior tentorial
apodeme (p.t.a.) (part of Gliedfuss of Hoffmann, i.e. the sternal arms or
fulcrum of Snodgrass) as described in Tomocerus by Manton (Fig. 1). The
cardo is more or less transverse in orientation and articulates with the elongate
stipes that extends forwards to what is generally termed in taxonomic literature
the head or capitulum of the maxilla (Klauenteil of Hoffmann). Also
articulating with the stipes is the outer lobe (palp of Hoffmann, Folsom and
Manton) of the maxilla described above (p. 154). The stipes is not a slender rod
as it appears to be in, for example, Anurida maritima and Neanura muscorum
(figured in Wolter, 1963) but is more akin to that described for Tomocerus
(Hoffmann, 1908) and Orchesella (Folsom, 1899). I t consists of a much
broader structure of rather delicate cuticular material reinforced by a pair of
longitudinal thickenings (0.t.s.; i.t.s.) connected not only at their proximal and
distal points but also by a transverse connecting bar about midway along their
lengths. At the distal end arise both the outer lobe (described above) and the
inner lobe bearing the head. The latter can apparently be operated by muscles
inserted on the prominent maxillary apodeme quite independently of any
movement brought about by the musculature of the cardo and the stipes. No
special studies were made of the cardinal or stipital regions of the maxilla as
these have already been well described.
The maxilla head
The head (m.h.), capitulum, inner lobe or lacinia, as it is variously termed, is
the most complex component of the mouthparts in Folsomia candida, as it is in
many other Collembola, and for this reason a more detailed study was carried
out with the scanning electron microscope.
Borner (1908) recognized a basic type of collembolan maxilla head as having
a three-toothed ungulum (main shaft) arising from which are two dorsal and
two ventral lamellae, a median appendage attached to the inner face of the
ungulum; associated with the base of the median appendage is a smaller
subsidiary appendage. This basic type of maxilla head is found in, for example,
Tetrodontophora. Such a structure is, as Borner pointed out, very similar to the
one found in Machilis (Thysanura : Archaeognatha). Borner suggested that
where there are fewer lamellae e.g. one dorsal and one ventral in Anurida
maritima this may have been brought about by fusion. In others, all the
lamellae may be completely lost. Similarly the median appendage and its
subsidiary appendage may also be reduced or lost. In Folsomia candida
(Plate 5 ) there is a well developed ungulum with three strong teeth or cusps.
The largest tooth is the apical one; the other two are progressively reduced in
size and lie dorsal to the main axis of the ungulum. The teeth are strongly
curved medially. Projecting well beyond the apex of the ungulum is a structure
that is undoubtedly homologous with the median appendage of Borner. It
consists of two main parts: the basal shaft and the apical rake. The former
arises at about the level of the most proximal of the ungular cusps and passes
forwards and to the ventral side of the apical cusp. At this point it branches to
form the apical rake consisting of about 70-80 delicate tapering filaments
arranged in four to five rather irregular rows, the most distal row having the
most filaments and the more proximal rows bearing progressively fewer so that
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H. E. GOT0
the whole is rather fan-shaped. Each of the filaments curves inwards towards
the midline of the pre-oral cavity. In fresh material the filaments are very
regularly arranged but in specimens prepared for stereoscan photomicrography
they are apparently more limp and disarranged. The basal shaft is fairly stout
and may be derived from a fusion of the proximal stems of the filaments. Such
a fasciated bundle would be in accordance with Hoffmann’s proposition that
this structure is derived from a Gruppierung von Borsten. The basal stem is
extended proximally not as a free-standing shaft but as a ridge. Arising from
the base of the latter is a rather boat-shaped structure (Plate 6A), probably
corresponding to Borner’s basaler Nebenanhung of the median appendage (here
termed the subsidiary appendage). The concavity and edge of this appendage is
well supplied with tapering finger-like projections, for the most part
backwardly projecting. They are not arranged in very regular rows and number
about one hundred in all. Lying on either side of the median subsidiary
appendage, and arising at about the same level, is a pair of lamellae. On the
dorsal side of the ungulum the two lamellae are very different in size and,
except basally, both are distinct. These undoubtedly correspond to Borner’s
lamellae l1 and 12. As in Tetrodontophora, ll is longer than 12. In Folsomia
cundida it extends approximately to the level of the tip of the most proximal
of the ungulum teeth. The second lamella reaches only to about the middle of
the median subsidiary appendage, i.e. no more than halfway up the length of
the first lamella. The comparative lengths of both of the median appendages
and of the four lamellae, and the points to which they extend along the
ungulum cannot be given with any degree of precision as they are flexible and
the tips are frequently turned over to very different extents. I t is for this reason
that I suggest that the use of comparative lengths of these structures should no
longer be used in taxonomy unless the difference between the measurements is
very great. Both lamella 1 and lamella 2 are fringed along their entire lengths by
finger-like, tapering filaments that are distinctly longer than those lining the
cavity of the median subsidiary appendage. Along the dorsal edge of the first
lamella there is a single row of about twenty equally spaced such filaments
whereas along the inner or ventral margin there is a rather larger subapical
filament followed by a short gap and then a somewhat irregular double row of
about eight filaments followed immediately by a single row of about five.
There are no filaments within the concavity of either of these lamellae as there
are in the case of the median subsidiary appendage. The lengths of the
individual filaments on the first lamella vary slightly; they become progressively
slightly longer from the apex of the lamella to the base. The number of
filaments on the second lamella is about twenty five. Those of the outer row
are slightly longer than those of the inner row. Unlike the filaments of the first
lamella, those of the second are arranged in a single row on both inner and
outer margins. The two rows are very close together and without a marked
concavity between them. The inner ventral face of this lamella is closely
applied to the main shaft of the ungulum and does not stand away from it
except towards the tip. In fact, from a medial examination, it appears to be a
lateral component of the ungulum shaft. In side view, however, it is seen as a
distinct lamella. In dorsal (lateral) view (Plate 6B) both lamella 1 and 2 are seen
to be broad based and markedly tapering towards the apex-they are in this
respect very similar to the figures of these lamellae in Tetrodontophora given
MOUTHPARTS OF FOLSOMIA CANDIDA
163
by Borner (p. 7, Fig. 12A). On the ventral side of the ungulum are the
remaining two lamellae. What probably corresponds to lamella 4 of Borner is
well developed and the longest of all the lamellae. The third lamella (Plate 6C),
however, is represented by a single row of about a dozen filaments arising from
a low narrow ridge extending, from the proximal extremity of the lamella,
forwards along the shaft of the ungulum and distally extending across the face
of the fourth lamella. All of the filaments of this lamella curve over the
ungulum shaft. Proximally the row arises opposite to the base of lamella 2, i.e.
close to the lateral margins of the junction of the stipes with the head. This
lamella is hardly recognizable as such and were it not for the fact that a lamella
is present in a comparable place in Tetrodontophora, for example, it might
have been interpreted as a single row of filaments forming a basal extension of
the fourth lamella.
The last maxillary lamella (lamella 4 of Borner) is the longest of all,
extending t o a point variously situated, according to the degree of apical
curvature of the lamella, somewhere between the apices of the middle and of
the most distal of the three ungular teeth. It also appears to be the most heavily
built of the lamellae and also the one with the longest and strongest filaments.
The filaments are fewer in number and much more widely spaced from one
another. As in lamellae 1 and 2, the filaments are arranged in two rows, one
along each margin with little or no concavity between them. There is a small
cluster of three to five apical filaments arranged transversely. Below and on
either side of this cluster is a gap followed by about 13 filaments in the outer
row and about nine in the inner (more distal) row.
Like the individual filaments of the lamellae and the median appendage, the
free-standing portions of each lamella as a whole is also obviously flexible as
their orientation is never quite the same and may differ considerably on
occasions; their apices may point in the same direction, either towards the
midline or to one or other side, or they may diverge, one pointing dorsally and
the other ventrally. No intrinsic musculature has been found to control the
individual movements of the lamellae and in life they presumably retain their
form and orientation merely by the elasticity of their cuticle.
The function of the maxilla
Although the mandibular mechanisms are now quite clear from
Dr S. M. Manton’s work, it is far from clear why the maxillae should have such
a complex structure. I t has been known for some time that, like the mandibles,
the maxillae (and also the hypopharynx) have the ability to be partially
exserted through the “mouth”. The function of the ungular teeth is perhaps to
supplement at least some of the functions of the apical mandibular cusps.
Wolter (1963) in the section of his paper dealing with the feeding mechanisms
in Collembola states merely that small food particles are seized by the teeth of
the mandibles and maxillae and drawn into the mouth when they are
transported t o the pharynx by the rhythmic contractions of the epipharyngeal
musculature. There is no mention of the possible function of the lamellae or
median appendages. The median filament can presumably function as a delicate
rasping or collecting organ functioning rather like a bamboo garden rake. If this
be so, it would seem that the role of Folsomia candida in the breakdown of
164
H. E. G O T 0
litter and humus of the soil in the biochemical cycle of ecosystems may be
somewhat different from that usually ascribed to it. The functions of the
remaining structures, i.e. the median subsidiary appendage and the four
lamellae, are not so clear. A study of the feeding mechanisms of Folsomia
candida using cine photography is now in process and it is hoped by this means
to elucidate the function of these structures.
THE HYPOPHARYNX
Considerable difficulty was experienced in obtaining good SEM micrographs
owing to the apparent very delicate nature of the hypopharynx, especially of
its antero-median zone. In all of the preparations for the SEM some degree of
distortion or of damage to the structure of the hypopharynx and associated
structures was suffered during their removal. The most satisfactory
preparations were those in which the dissection consisted solely of a lateral
incision on either side of the “mouth” continued posteriorly and followed by
the raising and complete removal of the upper part of the head so as to reveal
the hypopharynx in situ (Plate 7A). This dissection was carried out with the
specimen secured in silver ‘dag’, as described on p. 150.
A brief description only is given here as the morphology and function of the
hypopharynx, in relation to the other trophic components, is being made the
subject of a more extensive study, with cine as well as both transmission and
scanning electron microscopy. This will form part of the work on the
functional morphology of the feeding apparatus of Folsomia candida already
referred to above.
Superficially the hypopharyngeal apparatus is similar to that figured for
Tomocerus longicornis by Hoffmann (1908, Plate36). The median hypopharynx (glossa of Hoffmann and others) is overlaid by the pair of superlinguae
(or paraglossae auctt. ). Projecting backwards and diverging from the
hypopharynx is a pair of posterior tentorial apodemes (p.t.a.) (Manton, 1964)
or arms (lingual stalks, hypopharyngeal brachia, Glossabein, fulcrum or sternal
arms of some authors). At their posterior ends they articulate with the cardines
of the maxillae (Plate 7A, Fig. 1). Anteriorly, the two arms converge in the
body of the hypopharynx and are there joined together by a transverse bar, just
as described by Manton in Tomocerus. As suggested by Manton, the association
of the posterior tentorial apodemes with the hypopharynx is almost certainly
connected with the movement, especially the protraction and retraction, of the
latter. The importance of this movement will be dealt with elsewhere. The
dorso-median margin of the superlinguae (Plate 7B) is beset on either side with
a row of strong, medially projecting teeth. Towards the free end of the
hypopharynx, these are directed posteriorly, in the mid-region they point
towards one another and at the hind end of the row of teeth they become
much finer, more numerous and closely set. In this region the apices point
upwards and diverge somewhat from one another (Plate 7C). Between the
apices of these teeth lies a median longitudinal row of very prominent
upwardly directed tubercles. The most anterior of these is an elongate ridge
equal in length t o about three or four of the following tubercles (Plate 6C).
Behind the ridge are five tubercles each rather bluntly conical in form.
Immediately posterior to the last of these tubercles is a double row of smaller
MOUTHPARTS OF FOLSOMIA CANDIDA
165
tubercles extending back towards the region of the last of the superlingual
teeth. On either side of the large superlingual teeth, commencing in the region
of the third pair of teeth, is another, outer pair of rows of teeth. These are
much smaller and finer. They run forwards towards the tip of the
hypopharynx. In addition to these, there are other minute teeth whose
structure, distribution and function will be discussed later.
CONCLUSION
This study of the fine structure of the mouthparts of the collembolan
Folsomiu cundidu was originally undertaken to investigate the inter- and
intra-specific variation in the mouthparts of related species of Folsomiu and to
compare them with those of other, more distantly related, genera and families
of Collembola. The complexity of the task soon made it clear that the use of
these structures for taxonomic purposes would be quite impractical. However,
an extension of the study based solely on the external features of the “mouth”
region is being pursued for this purpose.
During the early stages of this study, the basic similarity of the mouthparts
of Folsomiu cundidu with those of other Collembola described previously soon
became apparent. There are a number of differences, some of which suggest
that, in spite of Dr S . M. Manton’s now classic work, we do not yet fully
understand some of the details of the functional morphology of the
mouthparts of Collembola. I t is this aspect that is now being investigated.
Unfortunately this may also mean that less is now known than previously
believed of the manner in which this collembolan breaks down its food
materials. Fungal hyphae and angiosperm remains have been found in the
alimentary canal but it is not known what use is made of the various
components of the food.
SUMMARY
The fine structure of the mouthparts of Folsomia cundidu (Collembola:
Isotomidae) has been investigated, very largely with the aid of the scanning
electron microscope. The general morphology of the labrum, mandibles,
maxillae, hypopharynx and labium is given in outline and some details of the
mandibles and maxillae provided. Certain comparisons are made with earlier
work.
The structure of the mandibular molar plate is described in detail and it is
suggested that its brush-like form cannot function as a very efficient grinding
mechanism as was previously believed. I t may act rather as a scarifying and
teasing organ. The details of the maxillary lamellae are described in some detail.
Their very complex nature, without intrinsic maxillary musculature, poses an
interesting problem in functional morphology, as well as possibly of having to
ascribe a different role to Folsomiu cundidu with regard to this collembolan’s
part in the breakdown of organic matter in the soil.
The interrelationships of the mandibular molar plate, maxillary lamellae,
hypopharynx, superlinguae and various epipharyngeal structures (not described
here) is one of complex and fine precision.
166
H. E. GOTO
The use of critical point drying technique to replace that of freeze-drying is
described. This enables very good results to be obtained without expensive
apparatus .
ACKNOWLEDGEMENTS
I wish t o express my gratitude to the Imperial College Departments of
Geology and of Metallurgy for the use of their scanning electron microscope,
on which the major part of this work was carried out, and especially to
Mrs M. Culpan for the many hours that she spent operating the instrument.
Some of the later work was undertaken on the Botany Department SEM and I
am grateful to Professor A. J. Rutter, Mr A. D. Greenwood and Miss J. Fillery
for making this possible.
I also wish to thank Messrs R. H. Harris and B. S. Martin, both of the
Zoology Department of the British Museum (Natural History), for their
invaluable help and advice in relation to the freeze-drying and the coating of
specimens respectively.
I should also like to express my gratitude to the Directors of JEOL (U.K.)
Ltd. for allowing me considerable time on their JSM-S1 demonstration
microscope and for the provision of an operator.
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MOUTHPARTS O F FOLSOMIA CANDIDA
167
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ABBREVIATIONS USED IN FIGURES
C
c.th.
c.t.m.
f.s.
i.t.s.
1.
m.a.
m.a.t.
m.c.
m.h.
m.m.p.
cardo
cuticular thickening of labium
cardo-posterior tentorial membrane
frontal sclerite
inner thickening of stipes
labrum
maxilla head apodeme
mandibular apical teeth
mandibular cavity
maxilla head
mandibular molar plate
m.s.
n.t.z.
o.1.m.
0.t.S.
p.0.a.
p.h.s.
p.0.
p.t.a.
sal. ch.
t.2.
mandibular suspension
non-tuberculate zone of cuticle
outer lobe of the maxilla
outer thickening of stipes
position of postantennal organ
position of hypopharynx and superlinguae
plica oralis
posterior tentorial apodeme
salivary channel
tuberculate zone of labial cuticle.
EXPLANATION O F PLATES
PLATE 1
A. Facial view of the head of Folsomia candida showing the relative positions of the labrum,
, kV).
labium, external lobe of the maxilla and the “mouth” ( ~ 3 6 0 20
B. Left side of the “mouth” showing the nongranulated zones of t h e labrum. labium and outer
lobe of the maxilla ( ~ 1 6 0 0 20
, kV).
C. Ventral view of the labium (x800, 20 kV).
D. Lateral view of the “mouth” region. Note the labrum, labium, external lobe of the maxilla,
plica oralis and frontal sclerite (x510. 20 kV).
PLATE 2
A. Salivary channel with Zwickel ( ~ 8 0 0 015
, kV).
B. Anterior part of the right side of the labium showing the distribution of sensilla and other
setae ( ~ 1 4 4 020
, kV).
C. Lateral sensillum ( 7 ) of the labium ( ~ 1 4 , 0 0 0 20
, kV).
D. Labial chemoreceptors (?). Note the darkened tips where the sensilla are believed to be
, kV).
perforated ( ~ 1 4 , 0 0 0 20
168
H. E. GOT0
PLATE 3
A. Dissection showing apex of mandibles in sltu. Note apical incisor teeth. The molar areas are
distorted ( ~ 5 2 815
, kV).
B. Mandibular molar plate. Note the odontoid molar cusps and the buttress rods (x600, 15 kV).
C. The two molar plates in partial contact. Note the flexing of the molar plate rods and the
irregular fissuring between rows ( ~ 2 0 0 020
, kV).
D. Buttress rods near the proximal end of the molar plate. Note the fimbriated tips of the
posterior buttress rods and the irregular fissuring of the plate rods ( ~ 4 0 8 020
, kV).
PLATE 4
A. Proximal extremity of the molar plate. Note the projection at the heel ( ~ 2 7 0 020
, kV).
B. The upper molar boundary rods flexing in contact with those of the opposite mandible
(x4800,20 kV).
C. Apices of molar plate rods of the middle zone showing the multicusped tips ( ~ 1 0 , 0 0 0 ,
20 kV).
D. Apices of molar plate rods from a more posterior position ( ~ 3 0 0 015
, kV).
PLATE 5
Maxilla head in approximately median view. The subsidiary appendage and the third lamella
(ventro-basal) are partially concealed ( ~ 6 0 0 020
, kV).
PLATE 6
A. Dorso-median view of the middle section of the maxilla head to show the subsidiary
appendage. Note the food (?) adhering to the apical incisor teeth ( ~ 4 6 7 520
, kV).
B. Maxilla head in dorsal view to show the bases and attachment of the two dorsal lamellae.
Note the food (?)attached to the rake ( ~ 2 0 5 020
, kV).
C. Medial view of the maxilla showing the third lamella-a single row of filaments at the base of
the fourth lamella (right hand side of the maxilla head) ( ~ 2 0 4 020
, kV).
PLATE 7
A. Dissection to show the hypopharynx, superlinguae and the posterior tentorial arms in situ
(distorted) ( ~ 3 1 51, 5 kV).
B. The superlinguae in dorsal view. Note the inwardly directed teeth and the median tubercles
( ~ 1 2 6 015
, kV).
C. Posteromedian zone of the superlinguae with the fine, upwardly directed filament-like teeth
( ~ 3 0 0 015
, kV).
D. Antero-median zone of the superlingual teeth showing the large anterior tubercles ( ~ 3 0 6 0 ,
15 kV).