on th abdominae l appendages of larvae of trichoptera ... · on th abdominae l appendages of larvae...

On the Abdominal Appendages of Larvae ofTrichoptera, 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 appendagesof a primitive Trichopteran, Rhyacophila sp., correspond muscle by muscle withthose of Corydalus. The terminal appendages of the larvae of typical members of otherfamilies of Trichoptera are compared with those of Rhyacophila; although there isgreat variety of form, the same muscles can be traced in all. Similarities between thelarvae of Neuroptera and Lepidoptera are not so close; the resemblances are in generalfeatures which are shared with other soft blood-filled appendages such as those ofTardigrada or Onychophora. Finally the general mechanical principles governing thebending of limbs are discussed. Soft turgid appendages such as the abdominal legsof caterpillars depend on a mechanism quite unlike that of the hard, jointed limbs ofother 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 ofTrichopteran larvae, and intermediate stages are described which suggest a way inwhich the change may have come about in true appendages.

CONTENTSPAGE

I N T R O D U C T I O N . . . . . . . . . . . 3 5 1

A B D O M I N A L A P P E N D A G E S O F N E U R O P T E R A . . . . . . . 3 5 2

T E R M r N A L A P P E N D A G E S O F C O R Y D A L U S . . . . . . . - 3 5 4

T R I C H O P T E R A : T E R M I N A L A P P E N D A G E S O F R H Y A C O P H I L A . . . . - 3 5 6

V A R I A T I O N S W I T H I N T H E F A M I L Y R H Y A C O P H I L I D A B 3 6 0

C A S E - B U I L D I N G F A M I L I E S 3 6 2

F A M I L Y P O L Y C E N T R O P I D A E . . . . . . . . . . . 3 6 5

F A M I L Y P S Y C H O M Y I D A E . . . . . . . . . . . 3 6 8

F A M I L Y P H I L O P O T A M I D A E . . . . . . . . . . . 3 7 0

F A M I L Y H Y D R O P S Y C H I D A E . . . . . . . . . . . 3 7 1

G E N E R A L C O N C L U S I O N S O N T H E T R I C H O P T E R A . . . . . . . 3 7 2

T H E E V O L U T I O N O F J O I N T E D L I M B S . . . . . . . . . 3 7 4

L E P I D O P T E R A . . . . . . . . . . . . . . 3 7 s

INTRODUCTION

THE larvae of Trichoptera have a pair of movable appendages at therear 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 notbuild cases there is a great variety of form and function within the order.The muscular mechanisms are interesting in themselves because they seemto depend on mechanical principles rather different from those on whichtypical jointed limbs operate. A comparative study of different families brings[Quarterly Journal of Microscopical Science, Vol. 92, part 4, pp. 351-76, Dec. 1951.]

J421.20 B b

352 Pryor—On the Abdominal Appendages of Larvae of Trichoptera,

out an interesting evolutionary series, in which it appears that the appendageshave been lengthened by including in their bases part of the tip of theabdomen. The extreme expression of this tendency is found in larvae of thefamily Polycentropidae, in which the tenth abdominal segment is completelydivided into two lateral halves with no direct communication between them.

The homology of these appendages is obscure. From a comparison of themusculature, Snodgrass (1938) claims that they do not correspond to theabdominal legs of caterpillars, as one might expect, or to the terminal appen-dages of the larvae of Neuroptera; on the other hand he traces a relation betweenthe abdominal appendages of caterpillars and the terminal appendages ofsome Neuropteran larvae. These suggestions seem to be based on an incom-plete description of the muscles of both Trichoptera and Neuroptera; a fullerinvestigation shows that there is a close resemblance between Trichopteraand some Neuroptera, but that the relation with Lepidoptera is doubtful.

Comparison of the appendages of different orders of insects leads to aconsideration of the muscular mechanism of soft turgid appendages in general,and to the question of how the typical arthropod limb has evolved. As ageneral rule the flexor muscles of soft appendages operate by kinking the wallnear the point of insertion, the muscle itself being wholly contained within asingle segment of the appendage. This is essentially unlike the system ofrigid levers by means of which a jointed limb is moved; here the muscle mustbe attached by means of a tendon to the hard parts of the next segment, sothat the tendon runs across the joint, and contraction of the muscle causes onesegment to pivot about the end of the next. It is not easy to see how onesystem can have evolved from the other without loss of function at anystage, and as far as thoracic limbs are concerned we have no fossil evidenceand no surviving intermediate stages. A comparative study of the terminalappendages of Trichoptera does, however, offer a clue to one possible solution,because they seem to have undergone a parallel evolution, and several inter-mediate stages have survived.

ABDOMINAL APPENDAGES OF NEUROPTERA

The terminal appendages of the larvae of Neuroptera, Trichoptera, andLepidoptera are a specialized form of the appendages sometimes found in theother abdominal segments, and their homologies can only be understood byreference to those of abdominal appendages in general. I shall begin thereforeby discussing the homologies of the abdominal appendages of the larvae ofNeuroptera.

The most complete set of appendages is found in the larvae of Corydalusand Chauliodes (Sialidae), which have been described by Snodgrass (1931).The first eight abdominal segments of the larvae of Corydalus bear taperingfleshy filaments at the sides; below and slightly behind the filaments there aretufts of tracheal gills arising from a trilobed tubercle (fig. 1). Both filaments andgill tufts arise from a common base, a lateral lobe of the body-wall. The fila-ments 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'sfigure 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-wallof the same segment. Beside these direct muscles, the lateral (dorso-ventral)muscles of the body-wall come to be associated with the appendages to someextent. There are two sets of lateral muscles; external laterals lying outside

trach. ext latV2 VI I dorsal. uscle

gill tubercle

FIG. 1 FIG. 2

FIG. 1. Right side of an abdominal segment of Corydalus, from below. Vi , V2, ventralmuscles of filament. Dorsal, dorsal muscle of filament.

FIG. 2. Abdominal segment of Sialis lutaria, from the left side. Vi , V2, ventral muscles offilament. Trach., trachea. Ext. lat., external lateral muscles.

the main tracheal trunk, and internal laterals lying inside it. The externallaterals are in three groups; a single muscle at the front and rear of eachsegment 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 cornersof each segment.

The anatomy of Sialis is like that of Corydalus, except that there are no gilltufts, and the filaments are jointed. The muscles of the filaments are similar(fig. 2), except that the dorsal muscle arises farther forward. The externallateral muscles (ext. lat., fig. 2) form a continuous palisade of narrow bandsseparating the cavity of the lateral lobes from the general body cavity.

Snodgrass has suggested that the filaments and gill tufts of Corydalus arehomologous with the styli and eversible vesicles of Thysanura, basing hisargument on the similarity of the musculature. This is an interesting idea, andon general grounds probable enough, but there are several details of themusculature that do not agree. As Snodgrass himself has pointed out, the


retractor muscles of the vesicles arise from the ventral plates, while those ofthe gill tufts arise from the dorso-lateral body-wall; the styli have only twobasal muscles, which arise from the extreme base, while the filaments havethree, two of which arise from the distal end of the first segment.

If the filaments of Corydalus are homologous with styli it seems unlikelythat 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

segment10

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 Sialisresemble thoracic legs in having internal muscles in the first three segments.In this he is mistaken, however; only basal muscles are present. A paper byHeymons (1896), quoted by Snodgrass, seems to refer to the distal parts ofthe ventral muscles rather than to true internal muscles. Seitz (1940) claimsthat the basal muscles of the filaments can be compared in detail with thecoxal muscles of a thoracic leg, but this is founded on a false interpretationof the arrangement of the muscles of the filaments. Ochse (1944) points outthe errors of Seitz, but has himself mistaken some of the external laterals formuscles 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 areno gill tufts on the ninth and tenth abdominal segments of Corydalus. On thetenth 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. Filamentsare absent on the ninth segment, but are present in a reduced form on the


tenth. The muscles of these terminal appendages are shown in fig. 5, in whichthe appendage of one side is represented as split open by a vertical longi-tudinal cut a little to the outside of the mid-line (along AB in fig. 3). Detailsof 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. Formuscles see text. Internal lateral muscles of segment 9 omitted.

of the appendage, and arising from the median face of the appendagejust 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 fromthe anterior dorsal margin of segment 9.

4. External lateral muscle of segment 10. Small isolated strands whichfrom their position spanning the base of the filament seem to corre-spond to the central group of external lateral muscles in a normalabdominal segment.

5. Internal lateral muscles of segment 10. The posterior set of internallaterals are reduced to two strands running from the ventral wall of theappendage backwards and upwards to the external dorsal wall (5a).There are also a few strands (56) which pass under the retractors of theclaws and pass up median to them.


6. Ventral longitudinal muscles of segment 10. From their function theymay be called the intrinsic flexors of the claws.

7. Extrinsic flexor of claws. Inserted with 6 above, but runs forwardthrough 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 anteriormargin 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 lateralmuscles of a typical segment. Although it seems probable that the terminalappendages are serially homologous with gill tufts, as Snodgrass suggests,the positive evidence is weak. The most important muscle concerned is theretractor, and it is not quite similar in the two cases; that of the gill tuftarising in the same segment and that of the appendage on the anterior marginof the segment in front.

TRICHOPTERA: TERMINAL APPENDAGES OF RHYACOPHILA

The terminal appendages of the larvae of typical case-building Trichopteraare reduced and modified, and their musculature can only be understood by


comparing it with that of free-living larvae; the type that most nearly re-sembles Corydalus is found in the family Rhyacophilidae.

The terminal appendages of the larva of a typical species of Rhyacophilaare shown in figs. 6-9. At the posterior end are strong movable claws, andoutside them a pair of slender, curved fixed hooks. On the anterior ventralregion 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, buthave no muscles attached. The inner faces of the appendages are membran-ous; the outer faces are heavily sclerotized, and are further stiffened by asclerotized internal ridge, the oblique suture (fig. 8), which runs from the baseof the anterior hooks forward and up to the dorsal surface, immediately in frontof the base of the fixed hook. The fixed hooks correspond in position to thefilaments of Corydalus, and their relation to the external lateral muscles ofsegment 10 confirms that they are in fact truly homologous. The anteriorhooks seem to be a new, cuticular structure and are peculiar to Rhyacophilidae.The muscles, which have been numbered to correspond with those of Cory-dalus, are as follows.


fixed hook

FIG. 8. Left terminal appendage of Rhyacophila sp. with the muscles as seenby transparency.

FIG. 9. Right terminal appendage of Rhyacophila sp.


1. Dorsal longitudinal muscle. In tracing homologies I have assumed thatthis muscle is lost in Trichoptera, but it is possible that as a result of theextreme reduction of the dorsal wall of the appendage proper, it hasacquired a connexion with the claw, and is represented by one of thetwo intrinsic retractors of the claw (2a, zb).

2. Intrinsic retractor of claw. Divides into two muscles, which arise fromthe upper anterior margin of the claw itself and are inserted on theanterior outer wall of segment 10, one above the other (za, zb).

3. Extrinsic retractor of claw. Like 2 above divided into two. They are notdirectly connected to the claw, but run from the posterior dorsal wall ofthe appendage at the base of the claw to the anterior dorsal wall ofsegment 9, crossing over one another in the mid-line (3a, 36).

4. External lateral muscle of segment 10. This muscle becomes one of themost important flexors of the claw, and from its position in Trichopterawill be called the external flexor of the claw. It arises from a smallsclerotized 'sole' (sole 1, figs. 7 and 8), and runs forwards and upwardsto the base of the fixed hook.

5a. Internal lateral muscles of segment 10. These also become flexors ofthe claw, and will be called the internal flexors. They arise from acentral 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 fibresmedian to the retractors of the claw. There are usually three groups offibres in Rhyacophila, but only two in most other Trichoptera.

6. Ventral longitudinal muscle of segment 10. This muscle becomes theanterior flexor of the claw in Trichoptera.

7. Extrinsic flexor of the claw. As in Corydalus.

8. Transverse muscles. These probably represent the ventral transversemuscles of segment 10. They run from the anterior outer cornerof segment 10 to the soft median wall of the appendage just behindthe anus.

Comparing Rhyacophila with Corydalus, the most striking difference is thereduction of the appendage proper until nothing remains but the claw itselfand the ventral 'sole' to which the flexor muscles are attached. The anteriorattachment of the intrinsic retractors (za, zb), which in Corydalus seems tomark the anterior limit of the appendage proper, has moved forward until itnearly coincides with the anterior limit of segment 10.

The terminal appendages of Rhyacophila are an extremely effective devicefor keeping a foothold in fast-flowing streams. In the Slovenian Alps I haveseen a larva of the Rhyacophila glareosa group walk out over flat rock under avery 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 isolatedoccurrence, remains of blepharocerid larvae occurring mixed with headcapsules of chironomid larvae, which form the main food of the Rhyacophila.The larva of Rhyacophila may perhaps be considered as the most highlyevolved of those animals which keep their foothold by means of hooks andgrapples; it is interesting to find it preying on blepharocerid larvae, which arecertainly the leading exponents of the vacuum-sucker method.

To grip the rock the claws and the anterior hooks act as the two jaws ofwide pincers, their tips being brought together by the action of the dorso-ventral flexor muscles (4, 5, 6, 7), which tend to arch the whole appendage byraising the ventral surface. Off the ground, contraction of the flexors archesthe appendage until the tip of the claw nearly touches the tip of the anteriorhook. The anterior hook has no muscles of its own, but it may be moved tosome extent by the buckling of the sclerite to which it is attached. When theflexors contract they will bend the sclerotized anterior dorsal wall of theappendage inwards and downwards, and so cause the external wall to bulgeoutwards, carrying with it the base of the anterior hook. This will cause thetip of the hook to move inward and slightly backwards, pivoting about itsattachment to the end of the oblique suture. The extent of this movement issmall, but the elaborate structure of the hinge about which the anterior hookpivots suggests that the movement may play an important part in grippingthe rock.

The function of the fixed hook becomes clear when the appendage is con-sidered in its natural position, with the tip of the fixed hook touching theground. The rigid arch of the fixed hook will then serve to brace the uppersurface of the appendage against the pull of the external flexor, and it willprevent any downward movement of the dorsal attachments of the flexormuscles. The importance of this function is shown by the condition of amutilated specimen in which the fixed hook had been broken off short andhealed; the stump had rotated until the tip again reached the ground.

The development of the lateral muscles of the tenth segment as the mainflexors of the claw has resulted in the loss of the inner claw found in Cory-dalus, which is remote from the muscle attachments. The action of theappendage in gripping small irregularities of the substrate is assisted by theelasticity of the claw itself. About half-way down on the ventral surfacethe claw has a distinct line of weakness along which it is not sclerotized. Thereis a slight fold in the cuticle over the unsclerotized part, and the dorsal wallabove is thickened; the function of the whole arrangement being apparentlyto allow of increased elastic deformation of the claw.

VARIATIONS WITHIN THE FAMILY RHYACOPHILIDAE

The family Rhyacophilidae is divided into two sub-families, Rhyacophilinaeand Glossosomatinae. The larvae of the Rhyacophilinae, or such of them ashave been described, can be divided again into three groups, of which the


typical species are Rh. septentrionis, glareosa, and tristis. Larvae of theseptentrionis and glareosa groups are much alike as regards their terminalappendages, differing only in the relative size and hardness of the parts, butthe larvae of the tristis group lack the fixed hook. They are small larvae, withrelatively small abdomens, living among stones in fast streams. The muscula-ture remains much the same, and so does the general shape of the appendage

sole 2oblique suture

FIG. 10. Terminal appendages of Rhyacophila larva of group tristis. From below and to theleft.

(figs. 10 and 11). The anterior hook is retained in a simplified form, but in onespecies examined (from Lake Ohrid, Yugoslavia) the oblique suture wasreduced at its lower end until it scarcely reached the anterior hook. Theexternal 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 andinternal flexors are well forward, so that the muscles lie more nearly hori-zontal than in other groups. The structure of the anterior hook is simpler thanin the other groups; there is no separate hinge-piece, and the whole base ofthe hook is continuous with the ventro-lateral wall of segment 10.

The larvae of the Glossosomatinae are small, and build clumsy houses ofstones which they carry about with them; they use their terminal appendagesto grip the sides of the house. The house is not made to fit the larva at allclosely, so that the terminal appendages remain relatively large, and areintermediate in structure between the appendages of free-living Rhyaco-philinae and those of typical 'caddis worms'.


The terminal appendages of Agapetus fuscipes (fig. 12) will be taken astypical of Glossosomatinae. Compared with Rhyacophilinae there is anextension of the ventral region of the appendage proper, which has resultedin a forward displacement of the ventral attachments of the flexor musclesrelative 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 ofattachment of the intrinsic retractor muscles, f, region of attachment of intrinsic flexormuscles.

heavily sclerotized and is attached to the claw over a wide base. The action ofthe flexors is to rotate the appendage as a whole about the anterior dorsalmargin of the tenth segment. The musculature only differs from that of theRhyacophilinae 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, whosestructure can be derived from that of the Glossosomatinae. The sole of theappendage is not relatively quite so large, and both extrinsic retractors (3a,36) are present, but otherwise the mechanism is the same. The larvae of thePhryganeidae approach the Rhyacophilid type more nearly than do those ofmost other families. Phryganea sp. (fig. 13) has a tenth abdominal segmentwhich 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 abdominalsegments (Martynow, 1901). The appendages project at the posterior cornersof the abdomen with the points of their claws directed outwards; the sole isa distinct sclerite articulating with the claw over a wide base. The muscles


are like those of Glossosomatinae with a few minor differences; the lowerbranch of the intrinsic retractor (2b) divides into three, and both extrinsicretractors are present. It does not seem to be possible to distinguish betweenexternal and internal flexors. The extrinsic retractors are widely separated

3A

FIG. 12. A, left terminal appendage of Agapetus fuscipes. B, terminal appendages of Agapetusfuscipes 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 clawbut from the posterior wall of the appendage, near the two conspicuous blackbristles which I have called the apical bristles; above, both extrinsic retractorsattach to the intersegmental membrane behind the tergite of the ninthabdominal segment. The upper intrinsic retractor (za) runs parallel with thelower 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 therelative 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


,1mm. i

FIG. 13. Tip of the abdomen of Phryganea sp. from right and above.

tergum ofsegment 9

1mm.

sole plabe

segment 10

FIG. 14. Tip of abdomen of Stenophylax sp.


tumid, papillose 'buttocks' at the sides of the anus. The tergum of the tenthsegment is reduced to a narrow rim in front of the base of the appendage. Inboth Phryganeidae and Limnophilidae lateral muscles are present, but aredivided 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' ratherthan with movement of the claws.

FAMILY POLYCENTROPIDAE (figs. 16-18)

The larvae of the Polycentropidae build relatively large fixed webs in stillor gently flowing water. Some genera build snares with a definite shape, butothers, e.g. Plectrocnemia, just spread sheets of web over the bottom, with atubular retreat somewhere in the middle from which they rush out to attacksmall animals that become entangled. They are all active, predaceous creatures,


FIG. 16. A, left and B, right terminal appendage of immature larva of Plectrocnemia sp.

apicalbristles

hinge rod

FIG. 17. Tip of terminal appendage of Plectrocnemia. Left appendage, from above and tothe right.

apicalbristlehingerod

0-5mm


with soft muscular bodies and long mobile terminal appendages ending inslender curved claws. The appendages are made longer by the inclusion ofa basal segment derived from the ninth abdominal segment. The musculatureof 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 proportionsof the dorsal and ventral walls, the external flexor (4, fig. 16) comes to runupward and backward from its ventral attachment rather than upward andforward as in Rhyacophila. The two extrinsic retractors of the claw (3a, 36,fig. 16 B) become widely separated from oneanother in the vertical plane.

In this and all succeeding families there issome elaboration of the posterior terminal faceof the appendage. The claw articulates by twocondyles at its upper outer corners, and fromthe articulations sclerotized rods, which Ishall call hinge-rods (figs. 17 and 18), runupwards to the posterior dorsal edge of theappendage. The hinge-rods usually join acrossthe mid-line just short of the top. At theirupper extremities arise two large black bristles,which I shall call the apical bristles. Thisarrangement can be traced in a distorted formin the Rhyacophilinae; the inner hinge-rodis a broad black band of heavily sclerotizedcuticle and is longer than the outer hinge-rod, so that the apical bristles lie asymmetri-cally. In case-building larvae the hinge-rodshave disappeared altogether, but the apicalbristles are still recognizable. Typical hinge-rods are free to bend at theirupper ends, and by rotating about their upper attachments they permit ofmovement of the condyles of the claw forward or backward. This movement iscontrolled by the extrinsic retractors (3a, 36) which are attached to the innerhinge-rod. In the Polycentropidae movement of the hinge-rods is slight, andthe extrinsic retractors, which are comparatively small, probably functionmainly 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 theninth segment to its anterior outer corners. The transverse muscles of theninth 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 thelongitudinal muscles at the sides of the lobes are attached to the lateral wallabout half-way along; the effect of the contraction of these muscles is to kink

FIG. 18. Terminal appendages ofPolycentropus sp.


the lobe at the point of attachment, thus giving the appearance of a jointthere (see 'joint' in fig. 18).

FAMILY PSYCHOMYIDAE

The larvae of this family live for the most part in silken tubes attached tostones, or in burrows in rotten wood, sponges, &c, and their appendages areadapted to grip the sides of their tubes. There are two sub-families, theEcnominae and the Psychomyinae, which are not perhaps very closely relatedalthough they have similar habits; the structure of their terminal appendagesis widely different.

The appendages of the Ecnominae (figs. 19, 20) resemble those of thePolycentropidae in having long basal segments derived from the ninth seg-ment, 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 upperedge of the appendage, forming a stiff ridge to which the upper ends of theflexor muscles are attached. The lower intrinsic retractor (2b) is broaderthan the upper (2a). The extrinsic retractors (3a, 3ft) are small, and areboth attached low down near the base of the claw, suggesting that move-ment of the hinge-rod is not of much importance in the working of theclaws.

In the Psychomyinae (figs. 21, 22) the ninth segment is short, and hardlybifurcates 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 tosee 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, projectinglike a peaked gable above the claw. The gable leans slightly backwards, over-hanging 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 ventralattachment. From the mechanical point of view it is clear that reaction to thepull of the external flexor is taken by the hinge-rods.

The upper end of the inner hinge-rod is produced forward along the dorsaledge of segment 10, and provides the main attachment for the flexors (5 and6) as in Ecnominae. The sole to which the intrinsic flexors are attachedventrally is a small flat plate, bearing at its outer posterior edge an extensionfor the attachment of the external flexor. This sole is connected to the clawby a soft membrane which extends from the outer lateral and posterior edgesof the sole to the anterior ventral projection of the claw. The outer lateralwalls of the appendages, and also to a lesser extent the inner walls, are extendedat the sides into flaps which project downwards, so that the ventral surfaceof the sole comes to form the roof of a pit. The flaps also extend behind theregion of the hinge-rods, particularly on the outer side, forming a sheath intowhich the claw can be withdrawn. The dorsal part of the outer flap oftenbears a bunch of long bristles. The length and mobility of the hinge-rods andthe development of a deep heel at the base of the claw make possible a very


2A2B JA1B 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.


3A

FIG. 23. Two views of the left terminal appendage of Philopotamus sp. A, seen from rightside; B, from left side.

complete retraction of the claws into the terminal sheath, an adaptation per-haps 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, whichare concealed in crevices under stones in moderately fast streams. The larvalives in a short tubular section at the end of the web, and feeds on planktonor detritus brought down by the current, so that it hardly ever has to leave the


web. Its conditions of life are not unlike those of the Psychomyidae, andthe structure of the terminal appendages in some ways resembles those of theEcnominae. There is a long basal lobe derived from the ninth segment; theclaws have a deep heel at the base; and the extrinsic flexors are relativelysmall. The hinge-rods are mobile, and there is a terminal sheath into whichthe claws can be withdrawn, although this is not as well developed as inPsychomyinae. In both Philopotamidae and Psychomyidae there is an extremedevelopment of the weak spot in the mid-ventral region of the claw describedfor Rhyacophila. Instead of a mere line of weakness the whole of the centralpart 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 ofthe claw and its projecting heel, the two being sprung apart as the claw isforced down by the contraction of the flexors, and then exerting a grip bytheir own elastic recovery.

A feature characteristic of the Philopotamidae is the asymmetry of thedorsal prolongations of the hinge-rods. As in some Psychomyidae, the innerhinge-rod is prolonged forward of the apical bristles, but instead of runningalong 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 positionto the upper part of the oblique suture of a Rhyacophilid larva; the two mayreally be homologous.

FAMILY HYDROPSYCHIDAE (figs. 25-27)

The larvae of Hydropsychidae spin a fixed net, but of a pattern entirelyunlike that of the Philopotamidae. A roughly semicircular sieve of relativelycoarse 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 moreexposed 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


insert at the anterior dorsal corner of segment 9 on the opposite side of thebody. This may be a modification connected with the use of the large bristletufts at the posterior end to clean the web, the extrinsic retractor havingacquired an additional function in bringing about lateral 'sweeping' move-ments of the appendage. Intermediates exist between this and the moreprimitive condition of ipsilateral attachment found in Corydalus; in Rhya-cophila they do cross over but not very far, and in Polycentropidae, as far as

-3AB

segments 8

1mm.FIG. 26FIG. 25

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 contri-bute to lateral sweeping movements.

The figure given by Snodgrass (1931; 1935) of the muscles of Hydropsychespecies omits the extrinsic retractors and some of the flexors; he has labelledthe ninth abdominal segment as the tenth. Haller (1948) has also given afigure of the musculature, but this too is very incomplete.

GENERAL CONCLUSIONS ON THE TRICHOPTERA

The most striking evolutionary trend in the Trichoptera is the progressivesplitting of the abdomen from behind to form paired basal lobes to theterminal appendages. In Corydalus the main part of the terminal appendage


is formed by the appendage proper; the tenth abdominal segment is onlyslightly bifurcate at its posterior end. In Rhyacophila the appendage proper isreduced until practically only the claw is left, thus making it possible for thelateral 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 Polycentropidaeand 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) con-cluded that the terminal segment of the larvae of Limnophilidae was formedby the fusion of the bases of paired appendages; in this he has been followedby Rousseau (1921), Ulmer (1925), and Betten (1934). Siltala took the Poly-centropid type as his starting-point, and considered the Limnophilid type asderived from that with the Hydropsychidae intermediate between the two.


Krafka (1924) did not agree with this view, but went too far the other way,and claimed that the terminal appendages of campodeiform larvae wereentirely formed by outgrowths from the tenth abdominal segment. None ofthese authors investigated the musculature.

THE EVOLUTION OF JOINTED LIMBS

The evolution of muscles and joints in the terminal appendages suggestsparallels with the evolution of true limbs. It seems probable that the hard-jointed 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 transitioncame about. The mechanical principles of soft limbs extended by internalpressure and jointed limbs of the usual arthropod pattern are entirely differ-ent, and no plausible intermediate conditions have been suggested. In theterminal appendages of the Trichoptera, however, where a parallel evolutionfrom 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 dia-gonal or longitudinal muscle, which causes the appendage to kink at themuscle attachment. The principle is well illustrated by the 'joint' in the basalsegment of the appendages of Polycentropidae. In such a mechanism themuscle attachment is on the near side of the bend, that is to say the muscle iswholly contained in one segment, and does not have its attachment the otherside of a joint as in a rigid articulated structure (see fig. 28). The distal seg-ment of the appendage, and even the muscle attachment, may become


sclerotized without affecting the mechanical principles involved. The clawsand attachments of the flexor muscles of the terminal appendages of Rhya-cophila, for example, are rigid, but the mechanism is still essentially the sameas for a kink in a soft appendage. The next step is for the muscle attachmentto sink into a groove, as it has done in the Psychomyidae and Philopotamidae;exaggerate this tendency until the sides of the groove meet underneath, andwe have a typical apodeme or tendon. On this scheme the tendon properlybelongs to the segment in which it lies, instead of being an extension from theintersegmental 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 ofcaterpillars are arranged on the same general plan as those of Corydalus; theparallel is in fact closer than appears from his description, which omits theintrinsic retractor of Corydalus. In fig. 29 is shown a dissection of the terminalappendage of a large saturniid caterpillar, seen from the inside with part ofthe inside wall of the appendage cut away. Intrinsic and extrinsic retractormuscles are recognizable, the planta taking the place of claws. The musclescorresponding to the flexors of the claw are on the inside of the retractorsinstead of being on the outside as in Trichoptera, but this could be explainedby the change in the relation of the appendages to the body as a whole (seefig. 30). As the appendages are lateral rather than terminal as in Trichopteraand Neuroptera, the retractors come to lie outside the lateral muscles. Amongthe flexors are muscles which appear to correspond to both the extrinsic andintrinsic flexors of the Neuroptera and Trichoptera, although the identity ofthe rest of the flexors is not clear (in the figure they have all been labelled asinternal 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 retractorof the planta arises from the dorsal body-wall of the tenth abdominal segmentinstead of from the anterior margin of the ninth. The force of a generalsimilarity of arrangement as an argument for true homology is much weakenedif we consider the musculature of other soft, blood-filled appendages. BothPeripatus and the Tardigrada have retractor muscles built on the same plan,with a short intrinsic retractor inserted within the appendage and an extrinsicretractor inserted on the dorsal body-wall of the same segment; the muscula-ture of Peripatus has been described by Snodgrass (1938), and that of theTardigrada by Baumann (1921). Snodgrass (1935) bases his argument for thehomology of the abdominal appendages of caterpillars with the terminalappendages of Neuroptera mainly on the similarity of the muscles of the plantato the retractors of the claw, but in this respect there is in fact as muchresemblance between a caterpillar and an onychophoran or a tardigrade asbetween caterpillar and Corydalus. It is safer to regard this type of doubleretractor muscle as a fundamental functional requirement for this kind oflimb. Apart from the arrangement of the retractor muscles, the case for ahomology rests only on the general resemblance of the flexor muscles, andeven this is not sustained in detail, because the extrinsic flexor is inserteddorsally on the tenth abdominal segment, instead of ventrally on the ninth asin Neuroptera and Trichoptera. From the evidence of the musculature alonethe homology can only be pronounced as possible but not proven.

REFERENCESBAUMANN, H., 1921. Z. wiss. Zool., r i8 , 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.

on th abdominae l appendages of larvae of trichoptera ... · on th abdominae l appendages of larvae...

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