functional morphology of the pretarsus in larval thysanoptera

Functional morphology of the pretarsus in larval Thysanoptera

B. S . HEMING Department of Entomology, University of Alberta, Edmonton, Alberta

Received January 31, 1972

HEMING, B. S. 1972. Functional morphology of the pretarsus in larval Thysanoptera. Can. J. 2001. 50: 751-766.

Legs of larval thrips differ in form and function from those of the adults. The tarsal depressor muscle and tibia1 gland of the adult are absent, the trochanter and tarsus are fused to the femur and tibia, respectively, and the relative sizes and shapes of the remaining parts differ.

Contraction of the pretarsal depressor muscle elevates and flattens the unguitractor plate and flexes the ungues laterally and downward. Extenders associated with the bases of the ungues rotate outward and pull out and spread the arolium. This subsequently inflates with blood pressure. When the depressor muscle relaxes, the recoil of two stretched restraining tendons originating on the tibiotarsal walls and inserting proximally into the unguitractor apodeme returns the unguitractor plate to its resting position. The ungues approach each other anteriorly and the extenders flip back into the pretarsus, pulling the arolium within the unguitractor plate as the latter rolls up longitudinally. Minor differences in pretarsal function existing between larvae of the two suborders are indicated.

Repla,cement of the first- by the second-instar pretarsus is described and an explanation is offered for the origm of the divergence between larval and imaginal mechanisms.

HEMING, B. S. 1972. Functional morphology of the pretarsus in larval Thysanoptera. Can. J. Zool. 50: 751-766.

Chez les Thysanopteres, les pattes de la lawe different de celles de l'adulte tant par leur forme que par leur fonction. Le muscle depresseur du tarse et la glande tibiale de l'adulte sont absents chez la lame, le trochanter est fusionnk au femur et le tarse au tibia; les autres parties de la patte larvaire different de celles de la patte adulte par leur forme et leurs proportions relatives.

En se contractant, le muscle depresseur du prktarse eleve et Ctend la plaque unguitractrice en m6me temps qu'il flkchit les griffes lateralement et vers le bas. Des extenseurs, associks a la base des griffes, font une rotation vers l'exterieur de fagon a faire sortir l'arolium et B I'6tendre. Par la suite, celui-ci se gon- flera sous I'effet de la pression sanguine. La detente du muscle dbpresseur amene le reliichement de deux tendons de retien, partant des parois tibio-tarsales pour s'inskrer a la base de I'apodeme unguitracteur, ce qui permet la plaque unguitractrice de retourner A sa position de repos. Les griffes se rapprochent l'une de l'autre anterieurement et les extenseurs retournent dans le pretarse, retirant ainsi I'arolium A I'interieur de la plaque unguitractrice pendant que celle-ci s'enroule sur elle-mgme, dans le sens longitudinal. La fonction du pretarse varie lkgerement chez les larves des deux sous-ordres.

On d&t de quelle fagon le prktarse du second stade remplace celui du premier stade; on tente aussi d'expliquer quels phknomenes sont a l'origine des divergences de fonctionnement chez la larve et chez I'adulte.

Introduction prepared. Sections were stained in Delafield's or Harris' hematoxylin and eosin, or in Gomori's trichrome

In larval and adult Th~sano~tera each 1% (Humason 1967). Fixation caused some shrinkage and terminates in a protrusible, bladder-like arolium. this accounts for the se~aration of the evidermis from I have 'described the function of the imaginal pretarsus and discussed previous work and terminology (Heming 1971). I describe here the functional morphology of the pretarsus in the two larval stages and the molt between them, point out errors made by previous workers, and suggest an explanation for the origin of the divergence between larval and imaginal mechanisms.

Methods Cleared and uncleared whole mounts (Heming 1969)

and serial sections (Heming 1970, 1971) of male and female first- and second-stage larvae of Frankliniella fusca (Hinds) (Terebrantia: Thripidae) and Haplothrips verbasei (Osborn) (Tubulifera: Phlaeothripidae) were

the cuticle shown in rn&y of the illustrations. Whole mounts in Canada balsam or Hoyer's medium

of larvae of the following species were examined by conventional and phase microscopy : Aeolothrips sp. (Aeolo- thripidae), Heterothrips arisaemae Hood (Heterothrip- idae), Merothrips morgani Hood (Merothripidae), Ana- phothrips secticornis (Trybom) (Thripidae), Chirothrips sp. (Thripidae), Taeniothrips simplex (Morison) (Thrip- idae), Amphibolothrips sp. (Phlaeothripidae), Cephalo- thrips monilicornis (Reuter) (Phlaeothripidae), Haplo- thrips halophilus Hood (Phlaeothripidae), Haplothrips (Leptothrips) sp. (Phlaeothripidae), and Oedaleothrips yosemitae Moulton (Phlaeothripidae).

Living and alcohol-fixed larvae of H. verbasci were frozen in liquid nitrogen, which was vacuum-evaporated in an Edwards Pearse tissue dryer model E.P.D. 2. The larvae were mounted venter upwards on a specimen stub with double-sided adhesive tape, and coated evenly with 150 A of gold. The legs were then observed from various

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752 CANADIAN JOURNAL OF ZOOLOGY. VOL. 50, 1972

angles and at various magnifications with a Cambridge Mark I1 Stereoscan. The problem of charging, caused by the long setae of the larvae preventing them from estab- lishing adequate contact with the surface of the stub, was solved by surrounding each specimen with a drop of conductive silver paint. This filled the space between larva and stub.

Living larvae of H. verbasci were observed with a Leitz stereoscopic microscope as they scrambled over the branched hairs of their host plant, Verbascum thapsus L. (Scrophulariaceae) and walked on various substrates. For detailed study of how the pretarsus works, larvae were mounted alive on a rnicroswpe slide and examined with a Wild M-20 microscope. The larva to be observed was picked up with an insect pin previously dipped in water and transferred face-down into a drop of water on a 12-mm coverslip. The coverslip was then picked up between thumb and forefinger, inverted, and placed on a second drop of water on a microswpe slide. The larva was then studied with conventional, phase, and polarizing optics at X 500 and X 625. As the thrips had its pretarsi against the wverslip, movements of the various parts, as the arolia expanded and retracted, wuld be observed. Distances traversed by the unguitractor plate and changes in length of the restraining tendons were measured with a calibrated ocular micrometer. A water-filled eye dropper was kept handy to replace water lost from under the coverslip through evaporation. Larvae and adults observed in this way for more than 4 h were still alive when returned to their host plant.

Observations A. STRUCTURE

(a) Legs The legs of first-instar larvae are the same as

those of the second except for their smaller size. They are lightly sclerotized in both stages and

each consists of coxa (cx.), femur (fm.), tibiotarsus (tib.), and pretarsus (ptar.) (Fig. I), the trochanter and tarsus being fused to the femur and tibia, respectively. All three pairs of legs are similar but the hind legs are slightly longer. In Chirothrips sp. the legs are much smaller relative to body size than they are in other species but they are identical in structure.

The intrinsic musculature of the midleg in a first-instar larva of F. fusca is illustrated in Fig. 1 and the origins, insertions, and functions of these muscles are given in Table 1 where muscles marked with an asterisk function in the pretarsal mechanism. I refer to the muscles moving the femur as trochanteral muscles since they are carried through to the adult and function there as such.

The muscles of the fore- and hind-legs are about the same except that in the foreleg the furcal extracoxal depressor of the femur is replaced by a pleural muscle. The size and number of fibers comprising each muscle vary far less in larval than in adult legs because of the absence of sexual dimorphism and polymorphism present particularly in adult Tubulifera (see reference by Ananthakrishnan 1969).

There are fewer femoral campaniform sensilla (Fig. 1, c.s.) than in the adult (Heming 197 1, Fig. 1). They occupy the position of the future tro- chantero-femoral junction. The femoral chordotonal organ of the larval stages is similar to that of the adult and in both F. fusca and H. verbasci

ar. aroliurn ar. L. II second-instar arolium ax. auxilia C.S. campaniform sensilla cx. coxa dep. ptar. pretarsal depressor muscle. dep. ptar. J. b. femoral branch of dep. ptar. dep. tib. ti biotarsal depressor muscle dep. tr. femoral (trochanteral) depressor

eb. el. c.

muscle elastic cuticle of unguitractor plate tibiotarsal elastic cuticle

e. rn. ecdysial membrane ex. tr. f. furcal extracoxal depressor muscle of

femur ext. extenders f. fulcrum fern. femur fem. gl. femoral gland fil. filament to arolium d ~

h. I. lev. tib.

hinge overlapping extension of unguis tibiotarsal levator muscle

lev. tr. mt. n. ptar. d. ptar. cl. res. td. SO. tar. I tar. 2 tib. rib. c. o. rib. gl. t.3. ugf. ugf: L. II un. un. L. II utr. utr. L. I1 utr. ap. ulr. ap. L. I utr. ap. L. II

femoral (trochanteral) levator muscle microtrichia nerve innervating dep. ptar. pretarsal scolopidia pretarsal claw restraining tendons socket first tarsomere second tarsomere tibibtarsus tibiotarsal chordotonal organ tibia1 gland terminal seta unguifer second-instar unguifer ungu~s second-instar ungues unguitractor plate second-instar unguitractor plate unguitractor apodeme first-instar unguitractor apodeme second-instar unguitractor apodeme

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HEMING: PRETARSAL MORPHOLOGY IN THYSANOPTERA LARVAE

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FIG. 1. Frankliniella fusca Hinds (Thripidae) larva I. Midleg, anterior aspect, showing musculature. FIG. 2. Aeolothrips sp. (Aeolothripidae) larva 11. Foreleg. A, lateral aspect, arolium retracted; B, frontal aspect. arolium partially expanded. FIG. 3. HeterothripS arisaemae Hood (Heterothripidae) larva 11. Mldleg, frontal aspect showing partially expanded arolium. Arrows indicate movements. FIG. 4. Merothrips morgani Hood (Merothripidae) larva I. Midleg, posterolateral aspect. FIG. 5. Haplothrips verbasci (Osborn) (Phlaeothripidae) larva I. Foreleg, lateral aspect. FIG. 6. H. verbasci larva 11. A, foreleg, posterior aspect, showing fully expanded arolium; B, midleg, anterior aspect, showing partially expanded arolium.

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contains the same number of scolopidia (seven). in the larval one but a thin (2.0 p) "sponge" is However, it is shorter because of the smaller present in at least some larvae of both F. ffusca femur of these stages. and H. verbasci.

(b) Pretarsal Mechanism Superficially, the larval thysanopteran pre-

tarsus more closely resembles that of other insects than does that of the adult. Some idea of the uniformity of this structure throughout the order can be gained by a study of Figs. 1 to 6. These show the pretarsi of representative species of the five families. These figures also show some differences in tibiotarsal chaetotaxy and micro- sculpture existing between the families.

( i ) Arolium (ar.) The arolium in larval Thysanoptera is a

delicate, membranous sac continuous laterally and distally with the margins of the unguitractor plate (utr.) and folded within it when retracted (Fig. 2B; Fig. 3; Fig. 6A, B; Fig. 7 I-K; Fig. 8 A, K, L; Fig. 10B; Fig. 11H). Anteriorly and proximally the wall of the arolium is continuous also with the mesial margin of each unguis (un.) (Fig. 71; Fig. 8 1, J). In phlaeothripid larvae, this portion of the arolium is sclerotized on either side to form a pair of triangular sclerites which I call extenders (ext.) because they aid in expansion and retraction of the arolium (Fig. 6B; Fig. 8 A, J; Fig. 9A; Fig. 10 A, B; Fig. 11G). These sclerites are sometimes visible in terebrantian larvae too, particularly in mero- thripids, but they are usually weakly developed (Fig. 7A). The "cuff", and surface sclerites of the imaginal arolium (Heming 1971) are absent

(ii) Ungues (un.) The ungues of larval thrips are claw-like,

particularly in the family Phlaeothripidae, and are therefore similar to those of many other insects (Figs. 1-6; Fig. 7 G-I, K, L; Fig. 8 A, H-K; Fig. 9A, B, D; Fig. 10A, B; Fig. 11 A, F, G). They are more or less sclerotized, particularly at their apices and, at least in H. verbasci, are delicately fluted in their long axes (Fig. 9D). Proximally and laterally they are continuous with the auxiliae (ax.), lightly-sclerotized lateral . -

extensions of the unguitractor plate (utr.) (Figs. 1-3; Fig. 5; Fig. 6A; Fig. 7 G, H ; Fig. 8 H, I; Fig. 9 A, B; Fig. 10 A, B). In phlaeothripid larvae a diagonal hinge (h.) of flexible cuticle separates unguis and auxilia of each side (Fig. 5 ; Fig. 8 H, I ; Fig. 9 A, B; Fig. 10A; Fig. 11A). Thus, when the pretarsal depressor muscle contracts, each unguis is able to flex laterally (Fig. 10 A, B).

At their proximal ends, the ungues are flexibly joined to the inner end of the unguifer (ugf.) on which they rotate (at point f. in Fig. IOA). In larval Terebrantia, the proximal, mesial angle of one unguis (the right one in a right leg, the left one in a left) is produced into an extension (1.) which overlaps and fits into a socket (so.) of the corresponding angle of the other unguis (Fig. 2B; Fig. 3; Fig. 7 G, L). The apex of this lobe is continued into the center of the pretarsus as a filament (fil.) which joins the apex

TABLE 1 Principal intrinsic muscles in the rnidleg of a first-instar larva of F. fusca

Muscle Oriein Insertion Function

Lev. tr. Ex. tr. f.

Anterolateral part of coxa Right mesofurcal fold

Dep. tr. Medial surface of coxa Lev. tib. Dorsolateral wall of

proximal 213's of femur Dep. tib. Lateroventral walls of

femur *Dep. ptar. f. b. Dorsal wall of apex of . .

femur *Dep. ptar. Proximal dorsal wall of

tibiotarsus *Res. td. (paired, not a Posterolateral wall of

muscle but an elastic tibiotarsus tendon)

*Muscles functioning in the pretarsal mechanism (see text).

Dorsal femoral margin Ventral femoral margin

Ventral femoral margin Dorsal tibiotarsal apodeme

Ventral tibiotarsal apodeme

Apex of unguitractor apodeme

Unguitractor apodeme

Apex of unguitractor apodeme

Levator of femur Extracoxal depressor of

femur Depressor of femur Levator of tibiotarsus

Depressor of tibiotarsus

Flexor of ungues

Flexor of ungues

Antagonizes action of dep. ptar. and dep. ptar. f. b.

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HEMING: PRETARSAL MORPHOLOGY IN THYSANOPTERA LARVAE

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FIG. 7. F. fusca larva I1 9 , foreleg. A, median sagittal section; B-J, transverse sections at points and angles indicated by arrows in A. B, through base of tibiotarsus; C, through tibiotarsus just below insertion of restraining tendons into unguitractor apodeme; D, through tibiotarsal chordotonal organ; E, through unguitractor apodeme; F, through unguifer, and unguitractor plate; G, through unguitractor plate and bases of ungues; H, same, just distal to G; I, through pretarsus, showing fusion of arolium to margins of ungues; J, through apex of pretarsus. K-L, Frontal sections at points indicated by arrows in A. K, slightly oblique at level of origins of restraining tendons; L, through unguifer, showing overlapping bases of ungues.

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CANADIAN JOURNAL OF ZOOLOGY. VOL. 50. 1972

fern. t ib.

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HEMING: PRETARSAL MORPHOLOGY IN THYSANOPTERA LARVAE 757

of the inflexed anterior wall of the arolium (ar.) (Fig. 7 A, G, H, L). The extension of the unguis just described is absent from larval phlaeothripids, probably because of the development of the extenders.

In the larva of Merothrips morgani the ungues of each leg are each subdivided into an apical claw (ptar. cl.) and a proximal part (Fig. 4). This subdivision is present also in the adult of this species (Heming 1971, Fig. 5).

(iii) Unguifer ( u d ) (= patella, Priesner 1960) In larval Thysanoptera the unguifer is almost

identical throughout the order (Fig. 1 ; Fig. 2A; Fig. 4; Fig. 5; Fig. 7A, F, L; Fig. 8A, H; Fig. 10A, B; Fig. 11A). It is a triangular, sclerotized thickening borne by the inner side of the anterior wall of the tibiotarsal apex, which extends inwards and somewhat distally to a point (f.) which joins flexibly to the bases of the ungues (un.)

The unguitractor apodeme (utr. ap.) in larval Thysanoptera continues distally as a strengthen- ing, sclerotized ridge for some distance down the middle of the unguitractor plate (Fig. 6A; Fig. 10 A, B). Just distal to its attachment to the apodeme, the proximal margin of the plate is thickened into two lateral ridges. These extend on either side as the proximal margins of the auxiliae to the bases of the ungues (Fig. 6A; Fig. 7G; Fig. 10 A, B) and are probably comparable to the ringvormige Beugel mentioned by Doeksen (1941) and earlier workers (Jordan 1888; Uzel 1895; Hinds 1902).

The apex of the unguitractor plate in H. verbasci and probably in other phlaeothripids is quite thick (Fig. 9A) and contains a transverse band (e.b.) of flexible cuticle staining red in Gomori's trichrome (Figs. 5 4 A ; Fig. 8 A, L). The band is coiled when the arolium is retracted and this is apparently its natural state.

In vhlaeothri~id larvae three fine lines (ptar. (iv) Unguitractor Plate (utr.) d.) exiend longkudinally down the unguitractor The unguitractor plate of larval thrips is a plate and project slightly beyond its distal end

large, flexible, spatulate plate continuous distally (Fig. 5; Fig. 6A; Fig. 9 A-C; Fig. 11A). In and laterally with the walls of the arolium (ar.) transverse sections (Fig. 8 H-K; Fig. 11 F-H) (Fig. 1; Fig. 2A; Fig. 4; Fig. 5; Fig. 6A; Fig. these lines are shown to be tubular structures 7 A, F-I; Fig. 8 A, H-L; Fig. 9 B, C ; Fig. 11 A, staining red in Gomori's trichrome. They are F-H). When the latter is retracted, the ungui- probably the scolopidia of three sense organs, tractor plate is rolled up longitudinally so that since a nerve staining blue in Gomori's trichrome its lateral margins approach each other, hiding enters each one proximally. For most of their the enfolded arolium from view (Fig. 9A; Fig. length these structures are within the lumen of 10A). Proximally, the unguitractor plate is con- the pretarsus, running along the inner face of the tinuous on either side with the pretarsal auxiliae unguitractor plate. Only distally do they actually (ax.) but more distally is separated from them by penetrate the plate, passing external to the triangular areas of membranous cuticle (covered elastic band (e.b.) of cuticle mentioned above by numerous, fine microtrichia in Aeolothrips (Fig. 11H). These three structures are found also (Fig. 2 A, B)). In H. verbasci the posterior in larval Terebrantia (Fig. 2B; Fig. 3; Fig. 7 A, surface of the plate is longitudinally grooved and J, K) but are poorly defined, remaining free of ridged (Fig. 9C). The apex of the unguitractor the unguitractor plate throughout their length plate in Aeolothrips larvae is produced into and terminating in the wall of the arolium. They numerous microtrichia (Fig. 2A, mt.). In larvae are remarkably similar in position and appear- of all families a characteristic pair of setae is ance to the tibia1 gland ducts (d. tib. gl.) that situated laterally in the plate behind the tips of I described in adults (Heming 1971) even though the ungues. this gland is not present in larvae.

FIG. 8. H. verbascilarva I1 3, midleg. A, median sagittal seaion; B-L, Transverse sections at pomts indicated by arrows in A. B, through femoro-tibiotarsal j~~nciion; C, through proximal end of tibiotarsus; D, through junction of femoral gland with unguitractor apodeme; E, through insertion of pretarsal depressor muscle into unguitractor apodeme; F, through unguitwctor apodeme distal to insertion of miraining tendons; G, through tibiotarsal chordotonal organs; H, through unyifer, ungues, and ungi~itractor plate; I, through pretarsus, showing fusion of arolium to margins of ungues; J. lhrtlugh extenders; K, through pretarsus, showing fusion of arolium to margins of unguitmctor plate; L, through elastic band of unyi- tractor plate.

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The tibiotarsal cuticle just proximal to the unguitractor plate is flexible (el. c.). On contraction and relaxation of the pretarsal depressor muscle (dep. ptar.), the unguitractor plate is pulled in and out of the distal end of the tibiotarsus (Fig. 10 A, B). At maximum contraction a portion of the apical tibiotarsal cuticle is pulled in as well. In all tubuliferous larvae I have observed there are two pairs of campaniform sensilla (c.s.) situated posterolaterally at the tibiotarsal apex (Fig. 5; Fig. 6A; Fig. 8G; Fig. 9C; Fig. 11E). In H. verbasci larvae only the lateral sensilla of each pair is innervated, the mesial one lacking a scolopale. These sensilla undoubtedly are stimulated by cuticle bending when the depressor muscle is maximally con- tracted (Fig. 10B). No such sensilla are found in larval Terebrantia (Figs. 1 4 ) where their posi- tions are often occupied by additional setae.

Because of its median rib of sclerotized cuticle, the proximal third of the unguitractor plate maintains its shape when pulled upon by the pretarsal depressor muscle. The distal portion in its length is broader and because it lacks the rib is more flexible. Because of structural relationships existing between unguitractor plate, ungues, and unguifer, this flexible portion unrolls at maximum contraction of the depressor muscle and actually becomes slightly concave (Fig. 10B).

(v) Unguitractor Apodeme (utr. up.) The unguitractor apodeme of larval Thysanop-

tera is an unpigmented, sclerotized rod, staining red in Gomori's trichrome, and extending from the proximal end of the unguitractor plate well into the tibiotarsus (Fig. 1; Fig. 2A; Fig. 4; Fig. 5 ; Fig. 7 A, C-E, K ; Fig. 8 A, E-G ; Fig. 10 A, B; Fig. 11 A-E). Into its proximal half are inserted the fibers of the pretarsal depressor muscle (dep. ptar.). Four fibers of this muscle originate on the dorsal wall of the proximal third of the tibiotarsus. In H. verbasci an additional fiber (dep. ptar. f.b.) continues into the distal end of the femur (fem.) where it fuses to the latter's apex (Fig. 8 C, D ; Fig. 10 A, B; Fig. 1 1A). In larvae of F. fusca, Taeniothrips simplex, and Merothrips morgani there are two femoral branches to this muscle (Fig. 1; Fig. 7 A, B). Uncleared whole mounts of aeolothripid and heterothripid larvae must be observed to decide whether this difference in the number of femoral branches is a characteristic of each suborder.

The nerve innervating the pretarsal depressor

muscle branches in the femur with a branch (n.) going to each fiber (Fig. 7A; Fig. 8 A, B). Each fiber thus has its own end plate.

Two slender restraining tendons (res. td.) originating posterolaterally on the walls of the tibiotarsus run mesially and proximally and insert into the unguitractor apodeme at the same level as the depressor fibers (Fig. 1 ; Fig. 7 C, K; Fig. 8F; Fig. 10 A, B). These are refringent when viewed with phase contrast or polarized light; they stain bluish-grey in hematoxylin and eosin, and turquoise in Gomori's trichrome. They are much easier to see in whole mounts of larvae than in those of adults even though more delicate, because they are not obscured by thick, pigmented cuticle. They are elastic, antagonize the action of the pretarsal depressor muscle, and function in retracting the arolium (Fig. 10B) just as they do in adult thrips (Heming 1971). When a thrips is macerated in cold 10% NaOH, the tendons lose their refringence and disappear at the same rate as the muscle fibers.

A long, slender femoral gland (fem. gl.), originating at the base of the femur in phlaeothripid larvae, continues distally into the tibiotarsus where it joins the apex of the unguitractor apodeme (Fig. 8 A-D). In some specimens of H. verbasci the apodeme is hollow for at least part of its length, with its lumen opening distally to the exterior just above the unguitractor plate (utr.) (Fig. 8A). If this lumen were continuous with the duct of the femoral gland it could serve as a passageway to the exterior for the product of this gland. In live first- and second-instar larvae of H. verbasci viewed at X 500 with ordinary or phase optics, the femoral gland shows up clearly because it contains large, refringent globules of material. When the pretarsal depressor muscle contracts and relaxes, the femoral gland moves a corresponding distance proximally and distally within the femur. This gland is present also in adults of H. verbasci where its path is much more convoluted (Heming 1971), but it does not seem to be present in larvae or adults of F. fusca and T. simplex.

The tibia1 gland, unguitractor apodeme sheath, unguitractor apodeme gland (Terebrantia), and "eyelets" (Tubulifera) of adult Thysanoptera (Heming 1971) are absent in larvae.

(vi) Pretarsal Proprioceptors A pair of chordotonal organs (tib. c. o.), each

containing one scolopale, is located distally in

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FIG. 9. H. verbasci larva 11. Stereoscan micrographs of pretarsi. A, right hind pretarsus, frontal aspect; B, right fore pretarsus, lateral aspect; C, right hind pretarsus, posterior aspect; D, right fore pretarsus, showing fluting on unguis.

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HEMINO: PRETARSAL MORPHOLOGY IN THYSANOPTERA LARVAE 759

the tibiotarsi of larvae of F.fusca and H. verbasci and probably in those of other thrips (Fig. 7 A, D, K; Fig. 8G; Fig. 11B). The cap cell of each organ enters the lumen of one of the ungues and probably inserts into its wall, but the origin of its ligament proximally and the location of its sense cell could not be seen. From the alignment of both scolopidia, both organs appear to originate somewhere along the length of the unguitractor apodeme. They are probably sensitive to changes occurring in the relationship of ungues to unguitractor apodeme with contraction and relaxation of the pretarsal depressor muscle. Exact spatial relationships, origins, and insertions of these organs require further study by transmission electron microscopy.

B. FUNCTION

The mechanism of aroliar expansion (A) and retraction (B) in a phlaeothripid larva is illustrated in Fig. 10. Contraction of the pretarsal depressor muscle (dep. ptar.) elevates the unguitractor plate (utr.) and causes the ungues (un.) to flex laterally and downwards on the unguifer (ugf.) at point f. Because of greater rigidity in its

proximal third, the distal, spatulate part of the unguitractor plate unrolls and becomes slightly concave. The extenders (ext.), associated with the bases of the ungues, rotate outward and downward, pulling out, and spreading the arolium (ar.). This subsequently inflates by blood pressure. At maximum contraction of the depressor muscle, the base of the unguitractor plate is pulled into the end of the tibiotarsus, carrying some of the flexible tibiotarsal cuticle in with it. When the depressor muscle relaxes, recoil of the stretched restraining tendons (res. td.) returns the unguitractor plate to its resting position. The ungues close together again anteriorly and the extenders are flipped back into the pretarsus, pulling in the arolium behind them (Fig. 10B). The unguitractor plate rolls up longitudinally, as it resumes its resting position, because of a transverse band of elastic cuticle in its apex whose natural state is a coiled one (Fig. 5, Fig. 6A), and because of the release of tension at its base. The arolium is thus hidden from view.

The pretarsal mechanism of larval Terebrantia differs from that summarized above in the following ways (Fig. 2B; Fig. 3; Fig. 7L): When the

FIG. 10. The mechanism of expansion (A) and retraction (El) of the arolium in a phlaeothripid larva.

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ungues spread on contraction of the pretarsal depressor muscle, the mesial extension (1 .) of the overlapping unguis drops downward out of the socket (s.o.) in its mate. Since this extension is joined by a filament (fil.) to the apex of the enfolded arolium, the latter lowers as well and is expanded by blood pressure aided by the extenders in those species in which these are present. When the ungues begin to close because of the recoil of the restraining tendons, the extension of the unguis moves back up into its socket, pulling the arolium up behind it. The arolium is, at the same time, enfolded by the unguitractor plate as the latter rolls up again. The terebrantian mechanism is thus more similar

to that of the adult than is the tubuliferan one (Heming 1971, Fig. 10C; Fig. 11 A, B).

All of the movements outlined above can be followed in living larvae of H. verbasci prepared as described in "Methods." When the arolium of the foreleg in a second-stage larva is retracted, the tips of the ungues are about 10 p apart. On contraction of the pretarsal depressor muscle, the unguitractor plate moves about 8.5 p into the tibiotarsus, the femoral gland the same distance proximally in the femur, the restraining tendons increase in length from about 22 to 30 p, and the tips of the ungues diverge from each other to a maximum of about 31 p. As the depressor muscle contracts and relaxes there is a

el. c .

res. td.

'\ , ar. L.E. un L.E

FIG. 11. H. verbasci late pharate larva 11, foreleg. A, diagrammatic optical sagittal section (cross hatching represents the tibiotarsal epidermis); B-H, transverse sections at approximately the points indicated by arrows in A; B, through restraining tendons and unguitractor apodeme, showing how the second-instar apodeme forms around the first; C, through junction of second-instar tibiotarsus and pretarsus; D, through second-instar arolium and ungues, forming in apex of first-instar tibiotarsus; E, through first-instar tibiotarsal campanifom sensilla and apex of second-instar pretarsus; F, through fust-instar ungues; G, through first- instar extenders; H, through first-instar unguitractor plate and arolium.

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HEMING: PREXARSAL MORPHOLOGY IN THYSANOPTERA LARVAE 761

change in its banding pattern that is easily observed with phase contrast or under polarized light.

Some patience is required to make the measure- ments given above, since a volume of water under the coverslip sufficient to cause the legs to straighten for accurate measurement also squeezes the body of the thrips and forces blood into the arolia so that they remain expanded. If more water is added under the coverslip with an eye dropper, the coverslip lifts, the body of the larva rounds up, blood pressure is reduced in the arolia, and the restraining tendons contract, causing retraction of the arolia.

As do adults (Heming 1971), larval thrips have perfect control over the state of their arolia. Both dilation and retraction can be stopped at any time and reversed. When a larva is walking, only those legs in contact with the substrate have swollen arolia. When the larva is immobile, with all of its pretarsi on the substrate, the arolia sometimes are and sometimes are not expanded. Larvae are just as capable as adults of walking vertically and upside down on smooth surfaces. Since the larva lacks the tibia1 gland of the adult, suggested previously (Heming 1971) as being a source of adhesive material, my interpretation of the function of this gland is probably incorrect (see "Discussion").

Dilation and retraction of the arolia of each pair of legs are probably under the control of the ganglion in the thoracic segment bearing them. This control is probably mediated by the nerve innervating the pretarsal depressor muscle and modulated by co-ordinating impulses received from the tarsal and femoral proprioceptors and from elsewhere.

C. REPLACEMENT OF THE FIRST-INSTAR PRETARSUS BY THE SECOND

As the end of the fist stadium in F.fusca and H. verbasci approaches, the mitotic rate increases in the epidermis of the tibiotarsus and unguitractor apodeme. Apolysis then occurs except at the points of origin and insertion of the pretarsal depressor muscle and restraining tendons. The epidermis contracts away from the first- instar cuticle elsewhere, becomes quite thick, and begins to deposit a much larger and folded second-instar cuticle inside or around the first (Fig. 11). The second-instar ungues are each produced by two or three trichogen cells. In

both H. verbasci and I;. fusca the second-stage arolium is laid down in a semiexpanded state. The endocuticle of the first-instar is digested by enzymes in the molting fluid now present between the two cuticles. Only a delicate ecdysial membrane persists (Fig. 11 D, E; e.m.). A pharate second-instar larva is able to walk suc- cessfully because the pretarsal depressor muscle and restraining tendons do not detach from the first-instar cuticle until just before ecdysis. This is easily observed in living pharate second-stage larvae observed at X 500. Shortly before ecdysis, both ends of the restraining tendons detach from the first-instar cuticle. The tendons immediately contract to square blocks of material nestled between the epidermal layers of tibiotarsus and unguitractor apodeme (Fig. 11 A, B). A little later, new cuticle is elaborated over the origins and insertions of the pretarsal depressor muscle. Ecdysis occurs, the new leg being pulled out of the old as indicated by the dotted arrow in Fig. 11A. As soon as the old cuticle is shed, the larva contracts its abdominal muscles, increases the pressure of the blood in its appendages, and stretches out the new cuticle. The epidermal cells become attenuated and the restraining tendons attach to the new cuticle of tibiotarsus and unguitractor apodeme. The tibiotarsal chordontonal organs (tib. c.o.) are not replaced but, instead, detach from the first-instar cuticle and re-attach to the second (Fig. 11B). After endocuticle deposition is complete, epidermal cells producing the pretarsal cuticle become pycnotic and degenerate and their remains are withdrawn proximally out of the pretarsus. The latter is always empty of cells for most of the two larval instars.

Discussion A. Structure of the Legs

The absence of trochanter and tarsus in legs of larval thrips has been known for a long time (Priesner 1923,1928,1958,1960; Melis 1934a) in spite of reports indicating the presence of a tarsal segment (Uzel 1895; Hinds 1902; Pesson 1951b; Priesner 1958, 1960; Davies 1969; Ananthakrishnan 1969).

The larval leg musculature has been described by Davies (1969) in Limothrips cerealiwn Haliday (Thripidae). Melis (19343) and Priesner (1960) have indicated, in Liothrips oleae Costa (Phlaeothripidae), how it differs from that of the

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adult. Davies described both tarsal depressor and levator muscles and indicated that the pretarsal depressor muscle of the foreleg had both femoral and tibial branches whereas those of the mid- and hind-legs lacked a tibial branch. In fact, the principal differences between the larval and imaginal musculature, as shown in this paper and as pointed out by Melis and Priesner, are in the absence from the tibia of a tarsal depressor muscle and in a rearrangement in the fibers of the pretarsal depressor muscle (compare Fig. 1 with Fig. 1 in Heming 1971). The musculatures of the legs in F. fusca and H. verbasci are practically identical even though these species are in different suborders. Limo- thrips cerealium and F. fusca are in the same family, the Thripidae. Therefore, although I have not examined larvae of L. cerealium, I am con- vinced that Davies' account is incorrect particularly as he used serial sections exclusively in his study.

In Chirothrips falsus Priesner (= C. simplex Hood) (Thripidae) an individual thrips can complete its entire development within a single floret of black grama grass, Bouteloua eriopoda (Watts 1965). Both larval stages of this species have very small legs and are unable to walk on an exposed surface. Watts suggested that the legs were atrophied during these stages, but I have examined larvae of an unidentsed species of this genus and the legs, although relatively very small, are normal in structure. Since all species of Chirothrips live on grasses or sedges (Priesner 1960) I expect the legs in most of their larvae to be similar to those of C. simplex.

Additional differences between larval and adult legs are (i) absence of well developed meso- and meta-furcae and correlated changes in the point of origin of the extracoxal depressor of the femur (trochanter), and (ii) smaller number of femoral companiform sensilla in larvae.

B. The Pretarsal Mechanism Early attempts to explain the action of the

'bladder feet' in thrips were based primarily on study of the larvae (Jordan 1888; Uzel 1895), since the larval mechanism is less com- plicated and more easily observed than the imaginal one. Jordan's account of the mechanism in Phlaeothrips brunnea Jordan (= Hoplo- thrips pedicularis Haliday) (Phlaeothripidae) and Uzel's in Trichothrips copiosa Uzel (= Ho-

plothrips corticis DeGeer) (Phlaeothripidae) are remarkably precise and form the basis for all subsequent reports (Hinds 1902; Berlese 1909; Handlirsch 1925; Weber 1933, 1954; Pesson 1951b; Geiler 1968; Eidmann and Kuhlhorn 1970). One of Jordan's main conclusions was that the ungues were spread by pressure of blood expanding the arolium (an idea recently rein- carnated by Ananthakrishnan 1969) rather than because of contraction of the pretarsal depressor muscle. This error in interpretation was corrected by Uzel.

Unfortunately, Berlese (1909, Fig. 246A) copied one of Jordan's figures incorrectly, showing the unguitractor apodeme (e.) to be continuous rather than separate from the unguifer (c). This mistake has been perpetuated by Weber (1933, 1954) and hence by Geiler (1968) and Eidmann and Kuhlhorn (1970) even though the mechanism cannot possibly work with this arrangement.

Uzel (1895, Fig. 156) described a gland extending from the femur into the tibia of H. corticis which he suggested was the source of the fluid expanding the arolium. This gland is probably homologous with the femoral gland I have here described in H. verbasci (Fig. 8 A, C, D, fern. gl.). Since it opens into the lumen of the unguitractor apodeme rather than into that of the arolium, it cannot have this role.

The Chitinsehnen (of Jordan 1888) or Chitin- reifen (of Uzel 1895) each linking an unguis laterally and posteriorly to the unguitractor apodeme, are comparable to the ringvormige Beugel (Doeksen 1941) or "semicircularly bent rods" (Priesner 1960) described erroneously as being present in adult thrips. These "rings" are actually the inflexed, proximal margins of the unguitractor plate and auxiliae (see Fig. 6A; Fig. 7G; Fig. 10 A, B).

The ability of the larva to walk vertically or upside down on smooth surfaces was attributed by Uzel (1895) to a shallow depression at the apex of each pretarsus (see his Fig. 155~). When this was placed against the substrate it supposed- ly acted as a suction cup. Since this depression is present only when the arolium is retracted (Fig. 9A; Fig. 10) it cannot function in this way.

I (Heming 1971) ascribed the clinging capa- bility of the imaginal arolium to the presence of a sticky elaboration of the tibial gland on its surface. Larval thrips do not have a tibial gland

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HEMING: PRETARSAL MORPHOLOGY IN THYSANOP?ERA LARVAE 763

but are nevertheless just as successful as adults at walking on smooth surfaces. This suggests that my interpretation of the role of this gland was incorrect. Also, larvae have present in their pretarsi three fine "ducts" comparable in appearance and position to the tibial gland ducts of adults. I have already indicated that I consider these "ducts" in larvae to be the scolopidia of three sense organs. Therefore, another explanation must be found to account for the climbing ability of thrips.

Assuming that the arolia form an airtight seal with a smooth substratum, atmospheric pressure alone could account for the ability of these insects to walk inverted on smooth surfaces. This phenomenon has bcen suggested by Roth and Willis (1952) to account for the climbing ability of several species of cockroaches. The products of the femoral gland in adult and larval Tubulifera and possibly of the tibial gland in adult thrips could conceivably find their way onto the surface of the arolium, the former via the unguitractor apodeme lumen and unguitractor plate, the latter via the ducts of the tibial gland. Once there they could keep the arolium moist and supple, assuring a tight contact between arolium and substrate.

The pretarsal structures and phenomena described for the &st time here are (i) size and rolled state of the unguitractor plate and its relationship to the arolium, (ii) extenders of tubuliferous arolia, (iii) restraining tendons, (iv) mechanism of aroliar retraction, and (v) pretarsal proprioceptors.

C. Evolutionary Considerations Why do the pretarsi of larval Thysanoptera

differ from those of adults? In most insects such a divergence in form is correlated with a difference between the habits of juveniles and adults (Snodgrass 1954; Hinton 1963). Larval and adult Thysanoptera, however, seem to have similar feeding habits and often occw together on the same food plant or in the same habitat (Priesner 1960; Ananthakrishnan 1969). Thus, there appears to be little reason why the imaginal pretarsus should not serve the larvae as well.

The answer could lie in consideration of the so-called "aberrant Exopterygota," the sternor- rhynchous Psyllidae, Aleurodidae, and Coccoi- dea. All these taxa illustrate a "distinct though sporadic tendency for the young insect to

develop special characteristics of its own that are not carried over to the adult stage" (Snod- grass 1954). In addition, their mouthparts resemble those of Thysanoptera in being similar in young and adults. The life histories of these insects are summarized by Weber (1930), Pesson (1951~) and Snodgrass (1954). In all of them the first-instar form is active with well-developed legs, whereas the subsequent, feeding stages are more (Aleurodidae, Coccoidea), or less (Psylli- dae) sedentary with their legs reduced or absent. As the divergence between young and adult increases, there is a corresponding increase in the degree of metamorphosis undergone in the last one or two juvenile stages, the least amount taking place in the Psyllidae and the greatest amount in male Coccoidea. In the latter there are usually propupal and pupal stages comparable in every way to the equivalent stages of Thysanoptera (Pesson 195 1 b; Snodgrass 1954; Priesner 1960). Thus, the life histories of Thysa- noptera and male Coccoidea are very similar except that the reason for different juvenile and imaginal legs and for pupal stages is obvious in the latter but not in the former.

Although the habits of larvae and adults in present day Thysanoptera appear similar (Pries- ner 1960), there are "differences between them that are sometimes overlooked. In many species, larvae are more cryptophilous than adults (this is one reason for the paucity of larvae in collec- tions). In those Thysanoptera in which adults too are cryptophilous (most Tubulifera; grass-, bark-, and gall-dwelling Terebrantia), they are structurally specialized in the direction of the larvae (e.g., fusion of tarsomeres, secondary loss of wings, development of tarsal and tibial hooks replacing the claw-like ungues lost by the adults, see references by Stannard 1957; Priesner 1960).

Since the principle of the larval and adult pretarsal mechanisms is the same, they probably started to diverge from a common mechanism which already had the restraining tendons and a protrusible arolium fused with the margins of the ungues (Fig. 12). The probable evolutionary sequence leading to this level of development has already been discussed (Heming 1971, Fig. 13). Divergence between larval and imaginal pretarsi began when the young started to specialize for feeding and the adults for repro- duction. As the habits of larvae and adults

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764 CANADIAN JOURNAL OF ZOOLOGY. VOL. 50. 1972

became increasingly different, the pretarsi of tions indicated in Fig. 12. Fusion of the tro- the two forms changed with them in the direc- chanter with the femur and of the tarsomeres

FIG. 12. The probable evolutionary sequence in the divergence between larval and imaginal thysanopteran pretarsi.

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HEMING : PRETARSAL MORPHOI ,OGY IN THYSANOITERA LARVAE 765

to each other and to the tibia and the persistence of claw-like ungues in the larvae all provided the larvae with more traction.

Tarsal segments of imaginal legs (Fig. 12, upper right) are slightly flexible on each other and considerably so at their juncture with the tibiae (see p. 102, right column, second para- graph in Heming 1971). Within the closed con- fines of a bud or a leaf sheath, contraction of the legs' tibial depressor muscles would flex the tibiae and would result in considerable force being applied to the pretarsi and tarsomeres. This would result in their being bent at right angles to the tibiae (although contraction of the tarsal depressor muscles antagonizes this tendency, they are not as strong as the tibial depressors). As the only part of the imaginal leg capable of exerting traction (the arolium) would not be pressed against the substrate, further progress down the sheath would be impossible unless additional hooks or claws were present on the tarsis or tibiae (as they are in cryptophilous adults).

In larvae, contraction of the tibiotarsal depressors would flex the tibiotarsi. Since the tarsi are fused to the tibiae, simultaneous contraction of the pretarsal depressor muscles would result in the clawed ungues and the expanded arolia being brought against the substrate. Using these the larvae could (and do) push themselves farther into a confined space. This would enable them to crawl onto parts of their host plants previously closed to them (e.g., terminal buds, leaf sheaths of grasses and sedges etc.) which would not only provide them with more succulent food, but also offer them additional protection from predators. Eventually, a degree of structural divergence was reached which necessitated the last two immature stages assuming a transformation role similar to that suggested by Hinton (1963) for the last nymphal stage in the evolution of the endopterygote pupa.

In a developmental study I (Heming 1970) have intimated that complete metamorphosis is disappearing in the Tubulifera. One reason for this could be that adults in this suborder are converging towards the larvae in structure because of the widespread assumption of cryptophily by adults. Since there is progres- sively less need for pupal stages, these are being lost.

Larval Tubulifera, as a group, are more cryptophilous than larval Terebrantia. This probably accounts for the differences in pretarsi existing between the members of each suborder.

Acknowledgments B. Hocking and D. R. Whitehead read and

criticized a preliminary draft of the manuscript. A. Borkent prepared many of the whole-mount preparations and assisted with collecting, while L. J. Stannard, Jr., of the Illinois Natural History Survey, Urbana, provided me with mounted larvae of Heterothrips arisaemae. G. D. Braybrook and D. A. Craig introduced me to the intricacies of the department's stereoscan microscope and took the micrographs, while J. S. Scott assisted with the illustrations. J. BglicZk translated the pertinent sections of Uzel's monograph from the original Czech and Miss N. Daviduk typed the manuscript. I am much obliged to all of these individuals for their competent assistance. This study was supported by the National Research Council of Canada.

ANANTHAKRISHNAN, T. N. 1969. Indian Thysanoptera. 2001. Monoer. No. 1. Publ. Inf. Dir. Counc. Sci. Ind. - -

Res. New ~ i l h i . BERLESE, A. 1909. Gli insetti. Vol. 1. Embriologia e

morfologia. Societa Editrice Libraria, Milano. DAVIES, R. G. 1969. The skeletal musculature and its

metamorphosis in Limothrips cerealiwn Haliday (Thvsanootera: Thrividae). Trans. R. Entomol. Soc. . - --. - A ,

Lond. 12i: 167-233. ~ E K S E N . J. 1941. Bijdrage tot de Vergelijkende Morpho-

logie der Thysanoptera. Meded. Landbouwhoogesch. ~ageningen, 45: 1-1 14.

Emunn~, H., and F. KOHLHORN. 1970. khrbucb der En~umolome. 2nd ed. P. Parey. Hamburg and Berlh

GEILER, H. fi68. Morphologie, hatomie und Hisrologie der Insekten. In Angewandte Entomologie. Edircd hy R. Fritzschc, 1-1. Geiler, and U. Sedlag. G. Fischer, Stuttgart. pp. 23-1 18.

HANDLIRSCH, A. 1925. Systematische ubersicht. In Handbuch der Entomologie. Vol. 3. Edited by C . Schroder. G. Fischer, Jena. pp. 377-1143.

HEMING, B. S. 1969. A modified technique for mounting Thysanoptera --a --- in Canada balsam. Entomol. News, 80: 323-328. - 1970. Postembryonic development of the female reproductive system in Frankliniella fusca (Thripidae) and Haplothrips verbasci (F'hlawthripidae) (Thysanop- tera). Misc. Publ. Entomol. Soc. Am. 7(2): 197-234. - 1971. Functional morphology of the thysanopteran pretarsus. Can. J. Zool. 49: 91-108.

HINDS, W. E. 1902. Contribution to a monograph of the insects of the order Thysanoptera inhabiting North America. Proc. U.S. Nat. Mus. 26: 79-242.

HINTON, H. E. 1963. The origin and function of the pupal stage. Proc. R. Entomol. Soc. Lond. 38: 77-85.

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. J. Z

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766 CANADIAN JOURNAL OF ZOOLOGY. VOL 50, 1972

HUMASON, G. L. 1967. Animal tissue techniques. 2nd ed. W. H. Freeman and Co., San Francisco.

JORDAN, K . 1888. Anatomie und Biologie der Physapoda. Z. Wiss. Zool. 47: 541-620.

MELIS, A. 1934a. Tisanotteri italiani. Studio anatomo- morfologico e biologico del liotripide dell' olivo (Liothrips oleae Costa). Redia, 21 : 1-183.

19346. Nuove ossewazioni anatomo-istologische sui diversi stati postembrionali del Liothrips oleae Costa. Redia, 21: 263-334.

PESSON, P. 1951a. Ordre des Homoptkres. In Trait6 de zoologie. Insectes sup6rieurs et hkmiptboides. Vol. 10, Fasc. II. Edited by P. P. Grasd. Masson et Cie, Paris. pp. 1390-1656.

1951b. Ordre des Thysanoptera. In Trait6 de zoologie. Insectes sup6rieurs et hkmiptkroides. Vol. 10, Fasc. II. Edited by P. P. Grass&. Masson et Cie, Paris. pp. 1805-1869.

PRIESNER, H. 1923. Beitrage zur Morphologie der Jugendstadien der Thysanopteren (I). Sitzungsb. Akad. Wiss. Wien. 132: 1-18.

1928. Die Thysanopteren Europas. F. Wagner, Wien. . .

1958. ifber den Tarsus der Thysanopteren und

seine sogenannte Endblase. Verh. Ver. Naturwiss. Heimatforsch. Hamburg, 33: 1-3.

1960 (1964). A monograph of the Thysanoptera of the Egyptian deserts. Publ. Inst. Desert Egypt, 13: 1-540 A -7,.

ROTH, L. M., and E. R. WILLIS. 1952. Tarsal structure and climbing ability of cockroaches. J. Exp. Zool. 119: 483-517. - -. . . . - . - . .

SNODGRASS, R. E. 1954. Insect metamorphosis. Smithson. Misc. Collect. 122(9): 1-124.

STANNARD. L. J.. JR. 1957. The vhylogeny and classifica- tion of .the ~ o r t h ~rnerican-gene; of the suborder Tubulifera (Thysanoptera). a. Biol. Monogr. 25: 1-200. - -..

Urn, H . 1895. Monographie der Ordnung Thysanop- tera. Koniggratz, Bohmen.

WATTS, J. G. 1965. Chirothrips falsus on black grama grass. N. M. Agric. Exp. Sta. Bull. 499.

WEBER, H. 1930. Biologie der Hemipteren. J. Springer, Berlin.

1933. Lehrbuch der Entomologie. G. Fischer, Stuttgart.

1954. Grundriss der Jnsektenkunde, 3rd ed. G. Fischer, Stuttgart.

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