On the Abdominal Appendages of Larvae of
Trichoptera, Neuroptera, and Lepidoptera, and the Origins
of Jointed Limbs
By M. G. M. PRYOR
(Fellow of Trinity College, Cambridge)
SUMMARY
The musculature of the abdominal appendages of the larvae of Sialis and Corydalus
(Neuroptera) is described, and their homologies discussed. The terminal appendages
of a primitive Trichopteran, Rhyacophila sp., correspond muscle by muscle with
those of Corydalus. The terminal appendages of the larvae of typical members of other
families of Trichoptera are compared with those of Rhyacophila; although there is
great variety of form, the same muscles can be traced in all. Similarities between the
larvae of Neuroptera and Lepidoptera are not so close; the resemblances are in general
features which are shared with other soft blood-filled appendages such as those of
Tardigrada or Onychophora. Finally the general mechanical principles governing the
bending of limbs are discussed. Soft turgid appendages such as the abdominal legs
of caterpillars depend on a mechanism quite unlike that of the hard, jointed limbs of
other arthropods, and it is difficult to see how the one'can have evolved from the other.
It is suggested that a parallel evolution has taken place in the terminal appendages of
Trichopteran larvae, and intermediate stages are described which suggest a way in
which the change may have come about in true appendages.
CONTENTS
PAGE
INTRODUCTION
A B D O M I N A L
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APPENDAGES
TERMrNAL APPENDAGES
TRICHOPTERA:
VARIATIONS
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CASE-BUILDING
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3 5 1
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3 5 2
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OF NEUROPTERA
OF C O R Y D A L U S
T E R M I N A L
W I T H I N
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APPENDAGES
OF R H Y A C O P H I L A
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3
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3
THE FAMILY RHYACOPHILIDAB
5
4
5
6
3 6 0
FAMILIES
3 6 2
F A M I L Y
POLYCENTROPIDAE
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3 6 5
F A M I L Y
PSYCHOMYIDAE
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3 6 8
F A M I L Y
PHILOPOTAMIDAE
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3 7 0
F A M I L Y
HYDROPSYCHIDAE
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3 7 1
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3 7 2
G E N E R A L
T H E
CONCLUSIONS
EVOLUTION
LEPIDOPTERA
O N THE TRICHOPTERA
OF JOINTED
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L I M B S
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3 7 4
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3 7 s
INTRODUCTION
T
HE larvae of Trichoptera have a pair of movable appendages at the
rear end which may be used either as accessory walking legs or as hooks to
grip the sides of the case; particularly among predaceous larvae which do not
build cases there is a great variety of form and function within the order.
The muscular mechanisms are interesting in themselves because they seem
to depend on mechanical principles rather different from those on which
typical jointed limbs operate. A comparative study of different families brings
[Quarterly Journal of Microscopical Science, Vol. 9 2 , part 4, pp. 351-76, Dec. 1951.]
J421.20
Bb
352 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
out an interesting evolutionary series, in which it appears that the appendages
have been lengthened by including in their bases part of the tip of the
abdomen. The extreme expression of this tendency is found in larvae of the
family Polycentropidae, in which the tenth abdominal segment is completely
divided into two lateral halves with no direct communication between them.
The homology of these appendages is obscure. From a comparison of the
musculature, Snodgrass (1938) claims that they do not correspond to the
abdominal legs of caterpillars, as one might expect, or to the terminal appendages of the larvae of Neuroptera; on the other hand he traces a relation between
the abdominal appendages of caterpillars and the terminal appendages of
some Neuropteran larvae. These suggestions seem to be based on an incomplete description of the muscles of both Trichoptera and Neuroptera; a fuller
investigation shows that there is a close resemblance between Trichoptera
and some Neuroptera, but that the relation with Lepidoptera is doubtful.
Comparison of the appendages of different orders of insects leads to a
consideration of the muscular mechanism of soft turgid appendages in general,
and to the question of how the typical arthropod limb has evolved. As a
general rule the flexor muscles of soft appendages operate by kinking the wall
near the point of insertion, the muscle itself being wholly contained within a
single segment of the appendage. This is essentially unlike the system of
rigid levers by means of which a jointed limb is moved; here the muscle must
be attached by means of a tendon to the hard parts of the next segment, so
that the tendon runs across the joint, and contraction of the muscle causes one
segment to pivot about the end of the next. It is not easy to see how one
system can have evolved from the other without loss of function at any
stage, and as far as thoracic limbs are concerned we have no fossil evidence
and no surviving intermediate stages. A comparative study of the terminal
appendages of Trichoptera does, however, offer a clue to one possible solution,
because they seem to have undergone a parallel evolution, and several intermediate stages have survived.
ABDOMINAL APPENDAGES OF NEUROPTERA
The terminal appendages of the larvae of Neuroptera, Trichoptera, and
Lepidoptera are a specialized form of the appendages sometimes found in the
other abdominal segments, and their homologies can only be understood by
reference to those of abdominal appendages in general. I shall begin therefore
by discussing the homologies of the abdominal appendages of the larvae of
Neuroptera.
The most complete set of appendages is found in the larvae of Corydalus
and Chauliodes (Sialidae), which have been described by Snodgrass (1931).
The first eight abdominal segments of the larvae of Corydalus bear tapering
fleshy filaments at the sides; below and slightly behind the filaments there are
tufts of tracheal gills arising from a trilobed tubercle (fig. 1). Both filaments and
gill tufts arise from a common base, a lateral lobe of the body-wall. The filaments have no internal muscles, but they can be moved by three basal muscles,
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
353
a ventral pair arising well.inside the base of the filaments (Vi; V2, fig. 1),
and a single muscle (dorsal, fig. 1) attached to the dorsal rim. Snodgrass's
figure is incorrect in showing all three muscles arising from the extreme base.
The gill tuft has a retractor muscle inserted on the dorso-lateral body-wall
of the same segment. Beside these direct muscles, the lateral (dorso-ventral)
muscles of the body-wall come to be associated with the appendages to some
extent. There are two sets of lateral muscles; external laterals lying outside
trach.
V2
VI
ext lat
I dorsal. uscle
gill tubercle
FIG.
1
FIG.
2
FIG. 1. Right side of an abdominal segment of Corydalus, from below. V i , V2, ventral
muscles of filament. Dorsal, dorsal muscle of filament.
FIG. 2. Abdominal segment of Sialis lutaria, from the left side. V i , V2, ventral muscles of
filament. Trach., trachea. Ext. lat., external lateral muscles.
the main tracheal trunk, and internal laterals lying inside it. The external
laterals are in three groups; a single muscle at the front and rear of each
segment and two together in the middle, spanning the base of the lateral lobe.
Internal lateral muscles occur as massive bundles at the front and rear corners
of each segment.
The anatomy of Sialis is like that of Corydalus, except that there are no gill
tufts, and the filaments are jointed. The muscles of the filaments are similar
(fig. 2), except that the dorsal muscle arises farther forward. The external
lateral muscles (ext. lat., fig. 2) form a continuous palisade of narrow bands
separating the cavity of the lateral lobes from the general body cavity.
Snodgrass has suggested that the filaments and gill tufts of Corydalus are
homologous with the styli and eversible vesicles of Thysanura, basing his
argument on the similarity of the musculature. This is an interesting idea, and
on general grounds probable enough, but there are several details of the
musculature that do not agree. As Snodgrass himself has pointed out, the
354 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
retractor muscles of the vesicles arise from the ventral plates, while those of
the gill tufts arise from the dorso-lateral body-wall; the styli have only two
basal muscles, which arise from the extreme base, while the filaments have
three, two of which arise from the distal end of the first segment.
If the filaments of Corydalus are homologous with styli it seems unlikely
that those of Sialis can be telopodites, as Snodgrass (19315.1935) and Seitz
(1940) have claimed; in fact this theory seems to be founded on errors about
appendaoe
segment
10
FIG. 3
FIG. 4
FIG. 3. Tip of abdomen of Corydalus from above, AB, line of section in fig. 5.
FIG. 4. Tip of abdomen of Corydalus from below. Hairs omitted.
the anatomy of Sialis. Snodgrass (1931) claims that the filaments of Sialis
resemble thoracic legs in having internal muscles in the first three segments.
In this he is mistaken, however; only basal muscles are present. A paper by
Heymons (1896), quoted by Snodgrass, seems to refer to the distal parts of
the ventral muscles rather than to true internal muscles. Seitz (1940) claims
that the basal muscles of the filaments can be compared in detail with the
coxal muscles of a thoracic leg, but this is founded on a false interpretation
of the arrangement of the muscles of the filaments. Ochse (1944) points out
the errors of Seitz, but has himself mistaken some of the external laterals for
muscles attached directly to the base of the filament.
THE TERMINAL APPENDAGES OF CORYDALUS
We may now turn to a consideration of the terminal appendages. There are
no gill tufts on the ninth and tenth abdominal segments of Corydalus. On the
tenth segment gill tufts are replaced by a pair of short, soft-walled appendages
(figs. 3 and 4), each bearing a pair of large curved claws at the tip. Filaments
are absent on the ninth segment, but are present in a reduced form on the
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
355
tenth. The muscles of these terminal appendages are shown in fig. 5, in which
the appendage of one side is represented as split open by a vertical longitudinal cut a little to the outside of the mid-line (along AB in fig. 3). Details
of the muscles are as follows:
1. Dorsal longitudinal muscle of segment 10.
2. Intrinsic retractor of the claws. Inserted on the dorsal wall of the
appendage between the claws, slightly to the middle of the mid-line
1mm
FIG. 5. Tip of abdomen of Corydalus, represented as split open along line AB of fig. 3. For
muscles see text. Internal lateral muscles of segment 9 omitted.
of the appendage, and arising from the median face of the appendage
just behind the first joint (i.e. near the posterior margin of segment 10).
3. Extrinsic retractor of the claws. Inserted with z above, and arising from
the anterior dorsal margin of segment 9.
4. External lateral muscle of segment 10. Small isolated strands which
from their position spanning the base of the filament seem to correspond to the central group of external lateral muscles in a normal
abdominal segment.
5. Internal lateral muscles of segment 10. The posterior set of internal
laterals are reduced to two strands running from the ventral wall of the
appendage backwards and upwards to the external dorsal wall (5a).
There are also a few strands (56) which pass under the retractors of the
claws and pass up median to them.
356 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
6. Ventral longitudinal muscles of segment 10. From their function they
may be called the intrinsic flexors of the claws.
7. Extrinsic flexor of claws. Inserted with 6 above, but runs forward
through segment 10 to attach to the ventral body-wall of segment 9.
9. Anterior-set of internal lateral muscles belonging to segment 10.
10. Dorsal longitudinal muscle of segment 9.
11. Ventral longitudinal muscle of segment 9.
0-5mm.
FIG. 6. Tip of abdomen of Rhyacophila sp. from above. For muscles see text.
The flexors of the claws exert their effect through the thick tendinous 'sole'
which forms the floor of the anterior part of the appendage. At the anterior
margin of segment 10 there is a set of internal lateral muscles to correspond to.
the posterior group; they run more obliquely than do the internal lateral
muscles of a typical segment. Although it seems probable that the terminal
appendages are serially homologous with gill tufts, as Snodgrass suggests,
the positive evidence is weak. The most important muscle concerned is the
retractor, and it is not quite similar in the two cases; that of the gill tuft
arising in the same segment and that of the appendage on the anterior margin
of the segment in front.
TRICHOPTERA: TERMINAL APPENDAGES OF
RHYACOPHILA
The terminal appendages of the larvae of typical case-building Trichoptera
are reduced and modified, and their musculature can only be understood by
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs 357
comparing it with that of free-living larvae; the type that most nearly resembles Corydalus is found in the family Rhyacophilidae.
The terminal appendages of the larva of a typical species of Rhyacophila
are shown in figs. 6-9. At the posterior end are strong movable claws, and
outside them a pair of slender, curved fixed hooks. On the anterior ventral
region of segment 10 is a pair of small anterior hooks (figs. 7, 8), which are
FIG. 7. Tip of abdomen of Rhyacophila sp. from below.
opposed to the claws. The anterior hooks are to some extent movable, but
have no muscles attached. The inner faces of the appendages are membranous; the outer faces are heavily sclerotized, and are further stiffened by a
sclerotized internal ridge, the oblique suture (fig. 8), which runs from the base
of the anterior hooks forward and up to the dorsal surface, immediately in front
of the base of the fixed hook. The fixed hooks correspond in position to the
filaments of Corydalus, and their relation to the external lateral muscles of
segment 10 confirms that they are in fact truly homologous. The anterior
hooks seem to be a new, cuticular structure and are peculiar to Rhyacophilidae.
The muscles, which have been numbered to correspond with those of Corydalus, are as follows.
358 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
fixed hook
FIG. 8. Left terminal appendage of Rhyacophila sp. with the muscles as seen
by transparency.
FIG. 9. Right terminal appendage of Rhyacophila sp.
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs 359
1. Dorsal longitudinal muscle. In tracing homologies I have assumed that
this muscle is lost in Trichoptera, but it is possible that as a result of the
extreme reduction of the dorsal wall of the appendage proper, it has
acquired a connexion with the claw, and is represented by one of the
two intrinsic retractors of the claw (2a, zb).
2. Intrinsic retractor of claw. Divides into two muscles, which arise from
the upper anterior margin of the claw itself and are inserted on the
anterior outer wall of segment 10, one above the other (za, zb).
3. Extrinsic retractor of claw. Like 2 above divided into two. They are not
directly connected to the claw, but run from the posterior dorsal wall of
the appendage at the base of the claw to the anterior dorsal wall of
segment 9, crossing over one another in the mid-line (3a, 36).
4. External lateral muscle of segment 10. This muscle becomes one of the
most important flexors of the claw, and from its position in Trichoptera
will be called the external flexor of the claw. It arises from a small
sclerotized 'sole' (sole 1, figs. 7 and 8), and runs forwards and upwards
to the base of the fixed hook.
5a. Internal lateral muscles of segment 10. These also become flexors of
the claw, and will be called the internal flexors. They arise from a
central sclerotized 'sole' at the base of the claw (sole 2, figs. 7 and 8)
and attach to the anterior dorsal wall of segment 10. There are no fibres
median to the retractors of the claw. There are usually three groups of
fibres in Rhyacophila, but only two in most other Trichoptera.
6. Ventral longitudinal muscle of segment 10. This muscle becomes the
anterior flexor of the claw in Trichoptera.
7. Extrinsic flexor of the claw. As in Corydalus.
8. Transverse muscles. These probably represent the ventral transverse
muscles of segment 10. They run from the anterior outer corner
of segment 10 to the soft median wall of the appendage just behind
the anus.
Comparing Rhyacophila with Corydalus, the most striking difference is the
reduction of the appendage proper until nothing remains but the claw itself
and the ventral 'sole' to which the flexor muscles are attached. The anterior
attachment of the intrinsic retractors (za, zb), which in Corydalus seems to
mark the anterior limit of the appendage proper, has moved forward until it
nearly coincides with the anterior limit of segment 10.
The terminal appendages of Rhyacophila are an extremely effective device
for keeping a foothold in fast-flowing streams. In the Slovenian Alps I have
seen a larva of the Rhyacophila glareosa group walk out over flat rock under a
very fast current to seize a larva of the blepharocerid Hapalothrix lugubris.
360 Pryor—On the Abdominizl Appendages of Larvae of Trichoptera,
Examination of gut contents showed that this was not an entirely isolated
occurrence, remains of blepharocerid larvae occurring mixed with head
capsules of chironomid larvae, which form the main food of the Rhyacophila.
The larva of Rhyacophila may perhaps be considered as the most highly
evolved of those animals which keep their foothold by means of hooks and
grapples; it is interesting to find it preying on blepharocerid larvae, which are
certainly the leading exponents of the vacuum-sucker method.
To grip the rock the claws and the anterior hooks act as the two jaws of
wide pincers, their tips being brought together by the action of the dorsoventral flexor muscles (4, 5, 6, 7), which tend to arch the whole appendage by
raising the ventral surface. Off the ground, contraction of the flexors arches
the appendage until the tip of the claw nearly touches the tip of the anterior
hook. The anterior hook has no muscles of its own, but it may be moved to
some extent by the buckling of the sclerite to which it is attached. When the
flexors contract they will bend the sclerotized anterior dorsal wall of the
appendage inwards and downwards, and so cause the external wall to bulge
outwards, carrying with it the base of the anterior hook. This will cause the
tip of the hook to move inward and slightly backwards, pivoting about its
attachment to the end of the oblique suture. The extent of this movement is
small, but the elaborate structure of the hinge about which the anterior hook
pivots suggests that the movement may play an important part in gripping
the rock.
The function of the fixed hook becomes clear when the appendage is considered in its natural position, with the tip of the fixed hook touching the
ground. The rigid arch of the fixed hook will then serve to brace the upper
surface of the appendage against the pull of the external flexor, and it will
prevent any downward movement of the dorsal attachments of the flexor
muscles. The importance of this function is shown by the condition of a
mutilated specimen in which the fixed hook had been broken off short and
healed; the stump had rotated until the tip again reached the ground.
The development of the lateral muscles of the tenth segment as the main
flexors of the claw has resulted in the loss of the inner claw found in Corydalus, which is remote from the muscle attachments. The action of the
appendage in gripping small irregularities of the substrate is assisted by the
elasticity of the claw itself. About half-way down on the ventral surface
the claw has a distinct line of weakness along which it is not sclerotized. There
is a slight fold in the cuticle over the unsclerotized part, and the dorsal wall
above is thickened; the function of the whole arrangement being apparently
to allow of increased elastic deformation of the claw.
VARIATIONS WITHIN THE FAMILY RHYACOPHILIDAE
The family Rhyacophilidae is divided into two sub-families, Rhyacophilinae
and Glossosomatinae. The larvae of the Rhyacophilinae, or such of them as
have been described, can be divided again into three groups, of which the
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
361
typical species are Rh. septentrionis, glareosa, and tristis. Larvae of the
septentrionis and glareosa groups are much alike as regards their terminal
appendages, differing only in the relative size and hardness of the parts, but
the larvae of the tristis group lack the fixed hook. They are small larvae, with
relatively small abdomens, living among stones in fast streams. The musculature remains much the same, and so does the general shape of the appendage
sole 2
oblique suture
FIG. 10. Terminal appendages of Rhyacophila larva of group tristis. From below and to the
left.
(figs. 10 and 11). The anterior hook is retained in a simplified form, but in one
species examined (from Lake Ohrid, Yugoslavia) the oblique suture was
reduced at its lower end until it scarcely reached the anterior hook. The
external flexor is well developed, and the 'sole' or sclerite at its origin (sole 2,
fig. 10) is sharply defined. The anterior attachments of both external and
internal flexors are well forward, so that the muscles lie more nearly horizontal than in other groups. The structure of the anterior hook is simpler than
in the other groups; there is no separate hinge-piece, and the whole base of
the hook is continuous with the ventro-lateral wall of segment 10.
The larvae of the Glossosomatinae are small, and build clumsy houses of
stones which they carry about with them; they use their terminal appendages
to grip the sides of the house. The house is not made to fit the larva at all
closely, so that the terminal appendages remain relatively large, and are
intermediate in structure between the appendages of free-living Rhyacophilinae and those of typical 'caddis worms'.
362 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
The terminal appendages of Agapetus fuscipes (fig. 12) will be taken as
typical of Glossosomatinae. Compared with Rhyacophilinae there is an
extension of the ventral region of the appendage proper, which has resulted
in a forward displacement of the ventral attachments of the flexor muscles
relative to the retractors. The expanded ventral 'sole' of the appendage is
FIG. I I . Terminal appendages of Rhyacophila larva of group tristis from above, r, region of
attachment of the intrinsic retractor muscles, f, region of attachment of intrinsic flexor
muscles.
heavily sclerotized and is attached to the claw over a wide base. The action of
the flexors is to rotate the appendage as a whole about the anterior dorsal
margin of the tenth segment. The musculature only differs from that of the
Rhyacophilinae in that one of the extrinsic retractors (36) seems to be absent.
CASE-BUILDING FAMILIES
All the case-building larvae have rather similar terminal appendages, whose
structure can be derived from that of the Glossosomatinae. The sole of the
appendage is not relatively quite so large, and both extrinsic retractors (3a,
36) are present, but otherwise the mechanism is the same. The larvae of the
Phryganeidae approach the Rhyacophilid type more nearly than do those of
most other families. Phryganea sp. (fig. 13) has a tenth abdominal segment
which is almost as large as the ninth, but has the tergal plate divided into two;
the segment retains a pair of lateral dermal glands like those of other abdominal
segments (Martynow, 1901). The appendages project at the posterior corners
of the abdomen with the points of their claws directed outwards; the sole is
a distinct sclerite articulating with the claw over a wide base. The muscles
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
363
are like those of Glossosomatinae with a few minor differences; the lower
branch of the intrinsic retractor (2b) divides into three, and both extrinsic
retractors are present. It does not seem to be possible to distinguish between
external and internal flexors. The extrinsic retractors are widely separated
3A
FIG. 12. A, left terminal appendage of Agapetus fuscipes. B, terminal appendages of Agapetus
fuscipes from below. On the right side the retractors are represented, on the left the flexors.
from one another, and the upper one (3a) arises not from the base of the claw
but from the posterior wall of the appendage, near the two conspicuous black
bristles which I have called the apical bristles; above, both extrinsic retractors
attach to the intersegmental membrane behind the tergite of the ninth
abdominal segment. The upper intrinsic retractor (za) runs parallel with the
lower extrinsic retractor (36) over most of its length.
The appendages of a typical eruciform larva of the family Limnophilidae
(Stenophylax sp., figs. 14 and 15) only differ from those of Phryganea in the
relative size of the parts. The appendages are smaller relatively to the body,
and give the impression of having been pushed apart by the development of
364 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
,1mm.
i
FIG. 13. Tip of the abdomen of Phryganea sp. from right and above.
tergum of
segment 9
sole plabe
segment 10
1mm.
FIG. 14. Tip of abdomen of Stenophylax sp.
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
365
tumid, papillose 'buttocks' at the sides of the anus. The tergum of the tenth
segment is reduced to a narrow rim in front of the base of the appendage. In
both Phryganeidae and Limnophilidae lateral muscles are present, but are
divided into a large number of fine strands which arise in two groups from
apica bristles
FIG. 15. Left terminal appendage of Stenophylax sp.
the anterior edge of the tenth segment and attach to the wall of the anus;
functionally they are connected with the retraction of the 'buttocks' rather
than with movement of the claws.
FAMILY POLYCENTROPIDAE (figs. 16-18)
The larvae of the Polycentropidae build relatively large fixed webs in still
or gently flowing water. Some genera build snares with a definite shape, but
others, e.g. Plectrocnemia, just spread sheets of web over the bottom, with a
tubular retreat somewhere in the middle from which they rush out to attack
small animals that become entangled. They are all active, predaceous creatures,
366 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
FIG. 16. A, left and B, right terminal appendage of immature larva of Plectrocnemia sp.
apical
bristles
hinge rod
FIG. 17. Tip of terminal appendage of Plectrocnemia. Left appendage, from above and to
the right.
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
367
with soft muscular bodies and long mobile terminal appendages ending in
slender curved claws. The appendages are made longer by the inclusion of
a basal segment derived from the ninth abdominal segment. The musculature
of the terminal segments remains recognizably the same as in Rhyacophilidae,
but there is no fixed hook or anterior hook, and by a shift in the proportions
of the dorsal and ventral walls, the external flexor (4, fig. 16) comes to run
upward and backward from its ventral attachment rather than upward and
forward as in Rhyacophila. The two extrinsic retractors of the claw (3a, 36,
fig. 16 B) become widely separated from one
another in the vertical plane.
In this and all succeeding families there is
some elaboration of the posterior terminal face apical
of the appendage. The claw articulates by two bristle
hinge
condyles at its upper outer corners, and from rod
the articulations sclerotized rods, which I
shall call hinge-rods (figs. 17 and 18), run 0-5mm
upwards to the posterior dorsal edge of the
appendage. The hinge-rods usually join across
the mid-line just short of the top. At their
upper extremities arise two large black bristles,
which I shall call the apical bristles. This
arrangement can be traced in a distorted form
in the Rhyacophilinae; the inner hinge-rod
is a broad black band of heavily sclerotized
cuticle and is longer than the outer hingerod, so that the apical bristles lie asymmetriTerminal appendages of
cally. In case-building larvae the hinge-rods FIG. 18. Polycentropus
sp.
have disappeared altogether, but the apical
bristles are still recognizable. Typical hinge-rods are free to bend at their
upper ends, and by rotating about their upper attachments they permit of
movement of the condyles of the claw forward or backward. This movement is
controlled by the extrinsic retractors (3a, 36) which are attached to the inner
hinge-rod. In the Polycentropidae movement of the hinge-rods is slight, and
the extrinsic retractors, which are comparatively small, probably function
mainly as levators of the appendages as a whole.
The basal segment of the appendages, formed from the ninth segment,
has muscles of its own. The posterior group of internal laterals (12, fig. 16)
is present, as well as the anterior group belonging to segment 10 (9, fig. 16).
There are also dorsal and ventral longitudinal muscles (omitted in the figures)
and a pair of large ventral diagonal muscles running from the 'crutch' of the
ninth segment to its anterior outer corners. The transverse muscles of the
ninth segment occur in both the single and bifurcate parts of the segment;
in the latter they attach to the median faces of the two lobes. Some of the
longitudinal muscles at the sides of the lobes are attached to the lateral wall
about half-way along; the effect of the contraction of these muscles is to kink
368
Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
the lobe at the point of attachment, thus giving the appearance of a joint
there (see 'joint' in fig. 18).
FAMILY PSYCHOMYIDAE
The larvae of this family live for the most part in silken tubes attached to
stones, or in burrows in rotten wood, sponges, &c, and their appendages are
adapted to grip the sides of their tubes. There are two sub-families, the
Ecnominae and the Psychomyinae, which are not perhaps very closely related
although they have similar habits; the structure of their terminal appendages
is widely different.
The appendages of the Ecnominae (figs. 19, 20) resemble those of the
Polycentropidae in having long basal segments derived from the ninth segment, but the distal part, derived from the tenth segment, is relatively shorter.
The upper end of the inner hinge-rod is prolonged forward along the upper
edge of the appendage, forming a stiff ridge to which the upper ends of the
flexor muscles are attached. The lower intrinsic retractor (2b) is broader
than the upper (2a). The extrinsic retractors (3a, 3ft) are small, and are
both attached low down near the base of the claw, suggesting that movement of the hinge-rod is not of much importance in the working of the
claws.
In the Psychomyinae (figs. 21, 22) the ninth segment is short, and hardly
bifurcates at all. Both the extrinsic retractors (3a, 36) and the extrinsic flexor
(7) are large; the great width of the extrinsic retractors makes it difficult to
see whether the intrinsic retractors are present or not. The external flexor (4)
is also large.
The appendage as a whole is short and the hinge-rods are long, projecting
like a peaked gable above the claw. The gable leans slightly backwards, overhanging the base of the claw, so that the posterior edge of the external flexor,
which is attached to its apex, runs upward and backward from its ventral
attachment. From the mechanical point of view it is clear that reaction to the
pull of the external flexor is taken by the hinge-rods.
The upper end of the inner hinge-rod is produced forward along the dorsal
edge of segment 10, and provides the main attachment for the flexors (5 and
6) as in Ecnominae. The sole to which the intrinsic flexors are attached
ventrally is a small flat plate, bearing at its outer posterior edge an extension
for the attachment of the external flexor. This sole is connected to the claw
by a soft membrane which extends from the outer lateral and posterior edges
of the sole to the anterior ventral projection of the claw. The outer lateral
walls of the appendages, and also to a lesser extent the inner walls, are extended
at the sides into flaps which project downwards, so that the ventral surface
of the sole comes to form the roof of a pit. The flaps also extend behind the
region of the hinge-rods, particularly on the outer side, forming a sheath into
which the claw can be withdrawn. The dorsal part of the outer flap often
bears a bunch of long bristles. The length and mobility of the hinge-rods and
the development of a deep heel at the base of the claw make possible a very
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
2A2B JA1B
369
10
FIG. 19
05mm.
FIG. 22
FIG. 21
FIG. 19. A, right and B, left terminal appendages of Ecnomus sp.
FIG. 20. Terminal appendages of Ecnomus sp. from above.
FIG. 2 I . A, left and B, right terminal appendages of psychomyine larva; a rheophilous sp. from
S. Ireland.
FIG. 22, Tip of abdomen of a wood-boring psychomyine larva from Macedonia.
370
Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
3A
FIG. 23. Two views of the left terminal appendage of Philopotamus sp. A, seen from right
side; B, from left side.
complete retraction of the claws into the terminal sheath, an adaptation perhaps for walking over the fine silk lining of the tunnels.
FAMILY PHILOPOTAMIDAE (figs. 23, 24)
The larvae of Philopotamidae build conical webs of very fine mesh, which
are concealed in crevices under stones in moderately fast streams. The larva
lives in a short tubular section at the end of the web, and feeds on plankton
or detritus brought down by the current, so that it hardly ever has to leave the
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs 371
web. Its conditions of life are not unlike those of the Psychomyidae, and
the structure of the terminal appendages in some ways resembles those of the
Ecnominae. There is a long basal lobe derived from the ninth segment; the
claws have a deep heel at the base; and the extrinsic flexors are relatively
small. The hinge-rods are mobile, and there is a terminal sheath into which
the claws can be withdrawn, although this is not as well developed as in
Psychomyinae. In both Philopotamidae and Psychomyidae there is an extreme
development of the weak spot in the mid-ventral region of the claw described
for Rhyacophila. Instead of a mere line of weakness the whole of the central
part of the claw is thin-walled. The function of this is not clear, but it seems
FIG. 34. Tip of abdomen of Philopotamus sp. R, prolongation of hinge-rod on dorsal surface.
The numbers refer to the segments.
possible that projections of the substrate may be gripped between the tip of
the claw and its projecting heel, the two being sprung apart as the claw is
forced down by the contraction of the flexors, and then exerting a grip by
their own elastic recovery.
A feature characteristic of the Philopotamidae is the asymmetry of the
dorsal prolongations of the hinge-rods. As in some Psychomyidae, the inner
hinge-rod is prolonged forward of the apical bristles, but instead of running
along the dorsal edge of the appendage, it extends over on to the outer side.
This prolongation of the inner hinge-rod (R, fig. 23) corresponds in position
to the upper part of the oblique suture of a Rhyacophilid larva; the two may
really be homologous.
FAMILY HYDROPSYCHIDAE (figs. 25-27)
The larvae of Hydropsychidae spin a fixed net, but of a pattern entirely
unlike that of the Philopotamidae. A roughly semicircular sieve of relatively
coarse mesh is supported on an outer frame of stalks or leaves spun together,
and the larva lives in a side tube. The whole is more solidly built and more
exposed to the current than the web of Philopotamidae.
The appendages are relatively long, but the ninth segment plays little part.
The hinge-rods are well developed and the external flexor (4, fig. 27) is small.
It is remarkable that the extrinsic retractors cross right over the mid-line to
372
Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
insert at the anterior dorsal corner of segment 9 on the opposite side of the
body. This may be a modification connected with the use of the large bristle
tufts at the posterior end to clean the web, the extrinsic retractor having
acquired an additional function in bringing about lateral 'sweeping' movements of the appendage. Intermediates exist between this and the more
primitive condition of ipsilateral attachment found in Corydalus; in Rhyacophila they do cross over but not very far, and in Polycentropidae, as far as
-3AB
segments 8
1mm.
FIG. 25
FIG. 26
FIG. 25. Tip of abdomen of Hydropsyche sp.
FIG. 26. Right terminal appendage of Hydropsyche seen from above.
I can make out, they do not cross over at all, although it is difficult to be sure.
The large transverse muscles of segment 10 (8, fig. 26) doubtless also contribute to lateral sweeping movements.
The figure given by Snodgrass (1931; 1935) of the muscles of Hydropsyche
species omits the extrinsic retractors and some of the flexors; he has labelled
the ninth abdominal segment as the tenth. Haller (1948) has also given a
figure of the musculature, but this too is very incomplete.
GENERAL CONCLUSIONS ON THE TRICHOPTERA
The most striking evolutionary trend in the Trichoptera is the progressive
splitting of the abdomen from behind to form paired basal lobes to the
terminal appendages. In Corydalus the main part of the terminal appendage
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
373
is formed by the appendage proper; the tenth abdominal segment is only
slightly bifurcate at its posterior end. In Rhyacophila the appendage proper is
reduced until practically only the claw is left, thus making it possible for the
lateral muscles of the tenth segment to act as flexors of the claws. The tenth
0p5mn
FIG. 27. Right terminal appendage of Hydropsyche from the left side.
segment is almost wholly cut in two, but the ninth is entire. In Polycentropidae
and Philopotamidae the tenth segment is entirely separated into two lobes,
and even the ninth is divided over about half its length.
This series has in the past usually been read backwards. Siltala (1907) concluded that the terminal segment of the larvae of Limnophilidae was formed
by the fusion of the bases of paired appendages; in this he has been followed
by Rousseau (1921), Ulmer (1925), and Betten (1934). Siltala took the Polycentropid type as his starting-point, and considered the Limnophilid type as
derived from that with the Hydropsychidae intermediate between the two.
374
Pryor—On the Abdominal Appendages of Larvae of Trichoptera,
Krafka (1924) did not agree with this view, but went too far the other way,
and claimed that the terminal appendages of campodeiform larvae were
entirely formed by outgrowths from the tenth abdominal segment. None of
these authors investigated the musculature.
THE EVOLUTION OF JOINTED LIMBS
The evolution of muscles and joints in the terminal appendages suggests
parallels with the evolution of true limbs. It seems probable that the hardjointed limbs of arthropods were derived originally from soft appendages of
FIG. Z8
planba
FIG.
20
FIG. 28. Possible stages in the evolution of a jointed limb. A, soft turgid appendage at rest;
B, the same flexed by kinking the wall; c, intermediate stage; D, jointed limb with tendon.
FIG. 29. Terminal appendage of the left side of a large caterpillar (Saturniidae), as seen from
the inside, with part of the inner wall of the appendage cut away.
the kind found in annelids, but it is not easy to imagine how the transition
came about. The mechanical principles of soft limbs extended by internal
pressure and jointed limbs of the usual arthropod pattern are entirely different, and no plausible intermediate conditions have been suggested. In the
terminal appendages of the Trichoptera, however, where a parallel evolution
from a soft-lobed appendage to something like a jointed limb has taken place,
intermediate conditions exist.
Bending of a soft turgid appendage is effected by the contraction of a diagonal or longitudinal muscle, which causes the appendage to kink at the
muscle attachment. The principle is well illustrated by the 'joint' in the basal
segment of the appendages of Polycentropidae. In such a mechanism the
muscle attachment is on the near side of the bend, that is to say the muscle is
wholly contained in one segment, and does not have its attachment the other
side of a joint as in a rigid articulated structure (see fig. 28). The distal segment of the appendage, and even the muscle attachment, may become
Neuroptera, and Lepidoptera, and the Origins of Jointed Limbs
375
sclerotized without affecting the mechanical principles involved. The claws
and attachments of the flexor muscles of the terminal appendages of Rhyacophila, for example, are rigid, but the mechanism is still essentially the same
as for a kink in a soft appendage. The next step is for the muscle attachment
to sink into a groove, as it has done in the Psychomyidae and Philopotamidae;
exaggerate this tendency until the sides of the groove meet underneath, and
we have a typical apodeme or tendon. On this scheme the tendon properly
belongs to the segment in which it lies, instead of being an extension from the
intersegmental membrane in front, as it is often represented.
FIG. 30. Diagram to illustrate the homologies of the terminal appendages of various larvae.
Tips of abdomen seen from above. A, Corydalus; B, Rhyacophila; c, Plectrocnemia; D,
caterpillar.
LEPIDOPTERA
Snodgrass has shown that the muscles of the terminal appendages of
caterpillars are arranged on the same general plan as those of Corydalus; the
parallel is in fact closer than appears from his description, which omits the
intrinsic retractor of Corydalus. In fig. 29 is shown a dissection of the terminal
appendage of a large saturniid caterpillar, seen from the inside with part of
the inside wall of the appendage cut away. Intrinsic and extrinsic retractor
muscles are recognizable, the planta taking the place of claws. The muscles
corresponding to the flexors of the claw are on the inside of the retractors
instead of being on the outside as in Trichoptera, but this could be explained
by the change in the relation of the appendages to the body as a whole (see
fig. 30). As the appendages are lateral rather than terminal as in Trichoptera
and Neuroptera, the retractors come to lie outside the lateral muscles. Among
the flexors are muscles which appear to correspond to both the extrinsic and
intrinsic flexors of the Neuroptera and Trichoptera, although the identity of
the rest of the flexors is not clear (in the figure they have all been labelled as
internal flexors (5)).
So far there is a general similarity between Lepidoptera and Neuroptera,
376
Pryor—Larvae of Trichoptera, Neuroptera, and Lepidoptera
but there are important discrepancies. In particular, the extrinsic retractor
of the planta arises from the dorsal body-wall of the tenth abdominal segment
instead of from the anterior margin of the ninth. The force of a general
similarity of arrangement as an argument for true homology is much weakened
if we consider the musculature of other soft, blood-filled appendages. Both
Peripatus and the Tardigrada have retractor muscles built on the same plan,
with a short intrinsic retractor inserted within the appendage and an extrinsic
retractor inserted on the dorsal body-wall of the same segment; the musculature of Peripatus has been described by Snodgrass (1938), and that of the
Tardigrada by Baumann (1921). Snodgrass (1935) bases his argument for the
homology of the abdominal appendages of caterpillars with the terminal
appendages of Neuroptera mainly on the similarity of the muscles of the planta
to the retractors of the claw, but in this respect there is in fact as much
resemblance between a caterpillar and an onychophoran or a tardigrade as
between caterpillar and Corydalus. It is safer to regard this type of double
retractor muscle as a fundamental functional requirement for this kind of
limb. Apart from the arrangement of the retractor muscles, the case for a
homology rests only on the general resemblance of the flexor muscles, and
even this is not sustained in detail, because the extrinsic flexor is inserted
dorsally on the tenth abdominal segment, instead of ventrally on the ninth as
in Neuroptera and Trichoptera. From the evidence of the musculature alone
the homology can only be pronounced as possible but not proven.
REFERENCES
BAUMANN, H., 1921. Z. wiss. Zool., ri8, 637.
BETTEN, C., 1934. N.Y. State Museum, Bull. No. 292.
HALLER, P. H., 1948. Mitt, schweiz. entom. Ges., 21, 301.
HEYMONS, R., 1896. Sitzungsber. Ges. Nat. Fr. Berlin, 6.
1896 a. Biol. Zbl., 16, 854.
KRAFKA, J:, 1924. Ann. ent. Soc. Amer., 17, 70.
MARTYNOW, A., 1901. Zool. Anz., 24, 449.
OCHSE, W., 1944. Rev. Suisse de Zool., 51, 1.
ROUSSEAU, E., 1921. LesLarvesetnymphesaquatiquesdesinsectesd'Europe. Brussels (Lebegue).
SEITZ, W., 1940. Z. Morph. u. Oek. d. Tiere, 37, 214.
SILTALA, A. J., 1907. Zool. Jhb., Suppl. 9, 21.
SNODGRASS, R. E., 1931. Morphology of the Insect Abdomen. Smithsonian Misc. Coll.,
85 (6).
I93S- Principles of Insect Morphology, 1st ed. New York (McGraw Hill).
1938. Evolution of the Annelida, Onychophora and Arthropoda. Smithsonian Misc.
Coll., 97 (6). ,
ULMER, G., 1925. 'Trichoptera', in Biologie d. Tiere Deutschlands (ed. P. Schulze). Berlin.