Development of the hair mechanosensilla on the pupal labial palp of the butterfly, Pieris rapae L. (Lepidoptera : Pieridae)

Int. J. InsectMorphol. & Emhrxol., Vol. 16, No. 5/6, pp. 343 354, 1987 Printed in Great Britain

DEVELOPMENT ON THE

PIERIS

PUPAL

RAPAE

0020 7322/87$3.[111+ ,00 © 1987Pergamc,n JournalsLtd.

OF THE

HAIR

LABIAL

PALP

MECHANOSENSILLA OF THE

L. ( L E P I D O P T E R A

BUTTERFLY,

: PIERIDAE)

JONG-KYOO L E E Institut ffir Zoologie, Universitht Regensburg, D-8400 Regensburg, Federal Republic of G e r m a n y

(Accepted 6 July 1987)

Abstrac=t--Structure and ontogeny of the hair mechanosensilla on the distal segment of the pupal labial palp of Pieris rapae (Lepidoptera : Pieridae) were investigated in 7 succcssiee stages between 28 hr after pupation and emergence of the imago. There are 7-8 mechanosensilla in the distal region of each palp in both sexes. These sensilla house a single sensory cell characterized by a tubular body, and 3 enveloping cells. At 28 hr after pupation, the anlagen of the hair mechanosensila arc visible. Consecutive steps in the formation of the sensilla arc: (1) elongation of the outer dendritic segment and of the dendritic sheath; (2) outgrowth of the trichogen cell and cuticle deposition; (3) increase in the diameter of the dendritic outer segment and in the n u m b e r of microtubules within it; (4) reduction of the distal part of the dendritic outer segment and formation of the tubalar body; (5) folding of the m e m b r a n e of the dcndritic outer segment and appearance of the receptor lymph cavity. The tubular body is formed during a period of about 80 hr. Its earliest appearance comprises groups of 3-4 microtubules, which are connected by electron-dense material. T h e final dense tubular body develops via microtubules linked together by electron-densc materia. Index descriptors (in addition to those in title): Mechanorcccption, development, sensilla, tubular body, insect labial palps.

INTRODUCTION

ALTHOUGH insect hair mechanosensilla show considerable structural variation (for reviews see Keil and Steinbrccht, 1984; Mclver, 1985), there are some common basic characteristics. Mechanosensitive hair sensilla have no pores. In contrast to hygro- and thermoreceptive sensilla, they possess a flexible socket ('no pore sensilla with flexible socket'; Altner, 1977). They are usually innervated by one sensory cell characterized by the presence of a tubular body in the distal region of the dendritic outer segment (Thurm, 1964). The region of the tubular body is most likely the site of mechanosensory transduction (Thurm, 1964, 1965, 1984; Gaffal et al., 1975; Rice, 1975; Gaffal and Theiss, 1978; Matsumoto and Farley, 1978; French and Sanders, 1979, 1981; Gnatzy and Tautz, 1980; Altner and Bauer, 1982; Erler, 1983). Cones integrated within the cell membrane and filamentous strands between the dendritic membrane and the microtubules of the body are thought to play a key role in this process (Thurm, 1984). Despite its tunctional significance, the ontogenetic development of the tubular body 343

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has n o t b e e n s t u d i e d so far. Thus, a study o f the o n t o g e n y of the hair m e c h a n o s e n s i l a was s t a r t e d . S u r p r i s i n g l y , it was f o u n d that the t u b u l a r b o d y d e v e l o p s stepwise and that i n t e r m e d i a t e stages, which r e s e m b l e the loosely p a c k e d t u b u l a r b o d i e s in certain m e c h a n o r e c e p t i v e sensilla in s o m e o t h e r a r t h r o p o d species, occur.

MATERIALS AND METHODS Adult males and females of P. rapae were collected from local populations and kept in the laboratory to deposit eggs on cabbage leaves. The larvae were reared at 26.5 +_ I°C in a 16 hr light and 8 hr dark cycle. Under these conditions, the animals had no pupal diapause. The imagines emerged about 160 hr after pupation (gee and Altner, 1985). Anlagen of the labial palps were excised from 23 pupae at 28 hr (n = 6), 411hr (n = 5), 64 hr (n = 7), 81) hr (n = 6), 90 hr (n = 8) and 120 hr (n = 8) after pupation, and from imagines (n = 9). Fixation was performed by immersion of the palps in the following 2 fixatives: (1) Karnovsky's glutaraldehyde-paraformaldehydemixture in 0.1 M Na-cacodylate buffer (pH 7.3; buffer 185 mosmol; cf. Glauert, 1974) for 4-18 hr at 20-26°C, followed by post fixation with 2% OsO4 in the same buffer; (2) 2.5% or 5% glutaraldehyde in 0.1 M phosphate buffer (pH 7.3; buffer 226 mosmol) for 4-18 hr at 20-26°C, followed by postfixation with 2% OsO~ in the same buffer. After dehydration, the specimens were embedded in Durcupan (Fluka, Buchs, Switzerland) and sectioned with a diamond knife on an LKB Ultrotome Ill or Reichert Ultracut microtome. The sections were stained with uranyl acetate and lead citrate and viewed with a Siemens 101 or Zeiss 10 CR electron microscope. For scanning electron microscopy, specimens were anesthetized with CO2 and the labial palps were fixed as for transmission electron microscopy. The scales were removed by a needle and ultrasonically prior to airdrying after the propylene oxide stage. After coating with gold in a sputter coater (Hummer II, Technics Inc., Alexandria, Virginia, U.S.A.), the palps were examined in a Cambridge Stereoscan $4-I0 scanning electron microscope. RESULTS

Structure o f the hair mechanosensilla in the imago T h e labial p a l p o f P. rapae consist of 3 s e g m e n t s , with the distal s e g m e n t b e i n g a b o u t l m m long. T h e tip of the distal s e g m e n t has a pit, which is f o r m e d d u r i n g p u p a l life ( K i m , 1961). This h o u s e s a b o u t 80 sensilla, which p r e s u m a b l y react to CO2 a n d a r e c h e m o s e n s i t i v e in a d d i t i o n ( L e e et al., 1985; B o g n e r et al., 1986). N o hair m e c h a n o s e n s i l l a in the pit, but 7 - 8 p o r e l e s s sensilla are p r e s e n t o u t s i d e the pit in the apical r e g i o n of t h e distal s e g m e n t within a b o u t 50 Ixm from its tip. Five to six of these sensilla a r e l o c a t e d on the v e n t r a l face o f the palp, the r e m a i n i n g 2 on the d o r s a l face (Fig. 1). T h e shaft o f t h e s e hair sensilla is a b o u t 50 ixm long, with a basal d i a m e t e r of 2.5 Ixm (Fig. 2). It has 9-13 l o n g i t u d i n a l cuticular ridges. In the s o c k e t r e g i o n , a j o i n t m e m b r a n e and s u s p e n s i o n fibers are visible. E l e c t r o n - d e n s e s t r a n d s e x t e n d f r o m the hair shaft b e t w e e n the s u s p e n s i o n fibers. A l l these sensilla a r e o f the s a m e s t r u c t u r a l t y p e a n d are c h a r a c t e r i z e d by the p r e s e n c e o f single s e n s o r y cell a n d 3 e n v e l o p i n g cells. T h e d e n d r i t i c o u t e r s e g m e n t of the s e n s o r y cell consists o f a ciliary section a n d a v o l u m i n o u s distal section. T h e t o t a l length o f the d e n d r i t i c o u t e r s e g m e n t is a b o u t 4 Ixm. T h e ciliary section is c h a r a c t e r i z e d by the typical 9 × 2 + 0 p a t t e r n of m i c r o t u b u l e d o u b l e t s . It lies within the i n n e r r e c e p t o r l y m p h cavity that is s u r r o u n d e d by the i n n e r m o s t e n v e l o p i n g cell ( t h e c o g e n cell). T h e d i a m e t e r of the i n n e r r e c e p t o r l y m p h cavity a r o u n d the ciliary section is a b o u t 1 Ixm. A typical 2.3 Ixm long t u b u l a r b o d y is l o c a t e d within the tip of the distal section (Fig. 3). D e l i c a t e s t r a n d s c o n n e c t the d e n d r i t i c m e m b r a n e to the o u t e r m o s t m i c r o t u b u l e s of the t u b u l a r b o d y (Fig. 4). A b o u t 1 Ixm b e n e a t h the tip of the t u b u l a r b o d y , it c o m p r i s e s a b o u t 600 m i c r o t u b u l e s , a n d the d e n d r i t i c o u t e r s e g m e n t is a b o u t 1.3 Ixm in d i a m e t e r .

Development of Hair Mechanosensilla

/

1'

i •

345

•

]

•

o

A

B

FIG. 1. Distal distribution of hair mechanosensilla on terminal segment of labial palps of P. rapae; pattern is a composite drawn from 4 palps (different symbols). A. dorsal face. B. ventral face of the palp. Pit organ is indicated by broken line.

The dendritic outer segment, together with its sheath, shows longitudinal folds in this region. There are about 8 folds, each 0.2~0.3 Ixm broad (Fig. 3). More distally at the level of the hair base, the dendritic outer segment tapers to 0.5 pom in diameter and the tubular body contains only about 70 microtubules. A conspicuous feature of the dendritic outer segment beneath the tubular body is electron-dense bodies that are attached to the microtubular doublets. These bodies are located at the: centrally directed surface of the doublets. Each dense body is 40-60 nm in diameter, but has no distinct outline (Fig. 5). The distal end of the dendritic outer segment together with the dendrite sheath is attached to the cuticle of the hair at the molting pore. This pore lies about 1 ~xm above the hair base

Development of the dendritic outer segment and hair At 28 hr after pupation, the anlagen of the hair sensilla are clearly visible. They consist of a single sensory cell and 3 enveloping cells. The distal regions of the enveloping cells bear microvilti. A dendritic outer segment, 3.5 ixm in length and 170-250 nm in diameter, projects into the space beyond the epidermal surface (Figs 6-8; 10). Proximally, it is surrounded by a sheath of curled filaments that are electron-dense. More distalb, however, the sheath shows a widemeshed hose structure and does not completely enclose the dendritic outer segment (Fig. 8). Desmosomes occur between the innermost enveloping cell (thecogen cell) and the dendritic inner segment. In some cases, the latter shows a finger-like process, which extends into an invagination of the thecogen cell and is up to 0.7 txm long (Fig. 9).

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FIG. 2. Scanning electron micrograph of tip of labial palp. Numerous scales have been removed to make mechanosensilla (arrowheads) visible. Several scales (s) have been left at tip. × 900. FIGS 3-5. Sections of dendritic outer segment of labial palp hair mechannsensilla in adult P. rapae. FIG. 3,Transverse section through dendritic outer segment at level of tubular body. Dendrite sheath (arrows) and membrane of dendritic nuter segment are folded × 34~000. FIG. 4. Longitudinal section through tubular body (tb) showing filamentous connections between a peripheral microtubu[e and membrane of dendritic outer segment (arrow). x 90,000. F1G. 5. Transverse section through dendritic outer segment at a level near ciliary section. Electron dense-bodies (arrows) are attached to micrtubule doublets, x 64,000.

D e v e l o p m e n t of Hair Mechanosensilla

F1GS 6--9. Anlage of hair mechanosensillum at 28 hr after pupation. Flo. 6. Deladritic outer s e g m e n t surrounded by dendrite sheath (arrowhead), thecogen cell (the), trichogen cell (tri) and tormogen cell (tot). × 36,000, F1G. 7. Dendritic outer segment projects above epidermal surface. It is enclosed within dendrite sheath (arrow). x 36,(100. FIG. 8. Tip of dendritic outer segment covered by meshwork of dendrite sheath (arrows). × 36,000. Fl~. 9. Transverse section through dendritic inner segment (d). A finger-like process of dendrite (arrowheads) extends into an invagination of the thecogen cell (the). x 60,00(I.

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FIG. 10. Diagram of ontogeny of hair mechanosensilla on palp of labial terminal segment in Pier& rapae between 28 hr after pupation and emergence of imago at 160 hr; cut = cuticle; d = dendritic inner segment; dos = dendritic outer segment; ds = dendrite sheath; e = epidermal cell; rlc = receptor lymph cavity; the = thecogen cell; tor = tormogen cell; tri = trichogen cell.

At 40 hr after pupation, the trichogen cell has started to develop the trichogen process. In this stage, it is 1.5 ixm long. It encloses the dendritic outer segment only basally (Fig. 10). This segment and the dendrite sheath extend about 40 ixm beyond the epidermal surface. The trichogen cell is surrounded by the tormogen cell and envelops the thecogen cell; the latter encloses the inner receptor lymph cavity, which is 1.2 Ixm in diameter. At 64 hr after pupation, the trichogen process has further elongated. It is now 20 Ixm long and extends parallel to the dendritic outer segment (Fig. 10). The length of the dendritic outer segment and its sheath have not changed. About 1 txm beneath the hair base, the outer segment is approximately 250 nm in diameter and contains about 20 microtubules (Fig. 11). At the ciliary region, the inner receptor lymph cavity is 0.8 txm mt/d 60(1

"A

400

20C

/

jo

B

J

0

28 4 0

64

80 90

120

160~imago h after pupation

FIG. 11. Numbers of microtubules within dendritic outer segments of labial palp hair mechanosensilla between 28 hr after pupation and emergence of imago at 160 hr at a level about middle (A) and tip (B) of tubular body; mt = microtubules; d = dendrite.

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in diameter. The trichogen cell has begun to withdraw from the thecogen cell; it remains only partly attached to it; the tormogen cell envelops both the trichogen and the thecogen cells (Fig. 10). The cuticle is already being secreted at the surface of the sensillum and is about 20 nm thick. At 80 hr after pupation, the trichogen process has reached its final length of about 50 p~m. It contains a layer of longitudinally arranged fine filaments beneath the surface membrane, a great number of longitudinally arranged microtubules centrally within it, and many electron-dense vesicles (Fig. 12). These vesicles are about 90 nm in diameter and are more numerous in the basal part of the sensillum. The distal part of the dendritic outer segment appears to degenerate (Fig. 13). First signs of tubular body formation are visible at about 1 ~m beneath the hair base (Fig. 14). At this level, the dendritic outer segment has a diameter of 0.7 ~m and contains about 70 microtubules (Fig. 11). There are up to 4 groups, each with 3-4 microtubules, which are connected by electron-dense material. These microtubular complexes lie in the marginal region of the dendritic outer segment. More proximally, the dendritic outer segment has started to develop folds. At 90 hr after pupation, the cuticular layer at the surface of the trichogen process is already 0.8 ~m thick. Suspension fibers and other socket structures are nearly completely C{eveloped at the hair base (Fig. 10). The diameter of the dendritic outer segment has increased to 0.8 ~m and its folds are more pronounced than in the 80 hr stage. The number of microtubules in the dendritic outer segment about I ~m below the hair base has increased to about 200 (Fig. 11). A tubular body is clearly recognizable (Fig. 15). However, it is different in appearance from that in the fully developed sensillum. The density of microtubules is lower, and not all neighboring tubules are connected by electron-dense material. Instead, most microtubules are connected to only 2 neighboring tubules. Thus, curled sheets of connected microtubules are formed. Additionally, fine strands are visible between the dendritic membrane and peripheral microtubules. Electron-dense bodies, which are attached to the tubular doublets, become visible in the dendritic outer segment beneath the tubular body. At the ciliary level, the inner receptor lymph cavity has a very small diameter measuring only about 0.4 p~m. At 120 hr after pupation, i.e. 40 hr before emergence of the imago, the outer receptor lymph cavity is formed at the level of the socket septum by retraction of the tormogen cell. The trichogen cell, in contrast, fills the lumen of the hair shaft and does not show signs of retraction. At 1 ~m below the hair base, the dendritic outer segment is about 1.2 p.m in diameter and the number of microtubules within it is about 300 (Fig. 11). The tubular body has again changed its appearance. There are still sheets of microtubules as observed at 90 hr after pupation. However, these sheets are interconnected to form a spongy structure, which resembles the final structure of the tubular body (Fig. 16). The electron-dense bodies at the tubular doublets are also clearly visible. In the ciliary region, the diameter of the inner receptor lymph cavity has increased to 0.7 p~m. Thus, at this stage, the development of the hair mechanosensillum is almost completed. Main differences f':om the imago are the smaller number of microtubules within the dendritic outer segment and a smaller volume of the outer receptor lymph cavity.

DISCUSSION The present study shows that the sensilla on the labial palp of P. rapae are typical hair

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FIG. 12. Longitudinal section through base of trichogen process of hair mechanosensillum at 80 hr after pupation. An outer filamentous layer (f) encloses a central region that contains microtubules and electron dense granules (arrows). Dendritic outer segment (asterisk) is visible at right side of process, x 36,000.

Development of Hair Mechanosensilla

FIG. 15. Transverse section through tubular body at 90 hr after pupation. Arrows indicate dendrite sheath. × 120,000. FIG. 16. Transverse section through tubular body at 120 hr after pupation. Arrows indicate dendrite sheath, x 108,000.

FIG. 13. Transverse section through degenerating distal part of dendritic outer segment at 80 hr after pupation. Residues of segment are enclosed within dendrite sheath (arrow). Segment runs parallel to trichogen process (tp). A thin cuticular layer (arrowheads) has been secreted at surface of this process, x 36,000. FIG. 14. Transverse section through dendritic outer segment at a level where tubular body is formed. Electron-dense material is visible between some groups of 2-4 microtubules, x 180,000.

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mechanosensilla. They are innervated by 1 sensory cell that contains a tubular body within its dendritic outer segment. The 600 microtubules of this body correspond well in number with the average of a few hundred by Mclver (1985). A special characteristic of the labial paip sensilla is the occurrence of electron-dense bodies at tubule doublets in the dendritic outer segment. Such bodies are not a general feature of insect hair mechanosensilla (see review by McIver, 1975, 1985; Rice, 1975; Barth and Blickan, 1984; Keil and Steinbrecht, 1984; Zacharuk, 1985). However, similar structures have been found by Miiller et al. (1978) at the outer surface of tubule doublets in companiform sensilla on the eye of Gryllus campestris. Amorphous dense bodies have been reported also by Gaffal and Bassemir (1974) in antennal olfactory sensilla of the bug, Dysdercus intermedius and by Lee and Altner (1985) in the labial palp-pit organ (LPPO) of Pieris rapae. In all these cases, the dense bodies can be assumed to enhance the mechanical stability of the dendrite in a way similar to the intertubular electrondense connections of tubular bodies or related structures (cf. Keil and Steinbrecht, 1984; Haug, 1985; Lee and Altner, 1985). There are no signs of sensory or enveloping cell degeneration in the present material, although a degeneration, which is already finished at 28 hr after pupation, the earliest stage investigated, cannot be excluded. However, within the LPPO degenerating sensory cells were clearly visible at this stage (Lee and Altner, 1985) and the labial palp scolopidia were found to degenerate at even later stages (Lee and Altner, 1986), and there is no reason for assuming that degeneration processes should not be synchronized in the same papal segment. Thus, it appears that the degeneration processes analyzed by Lee and Altner (1985, 1986) are restricted to the pit organ and the labial palp scolopidia. Despite this difference in the occurrence of degenerating sensory cells, there is a conspicuous correspondence in the sequence of events of differentiation in the palpal mechanosensilla and the sensilla of the pit organ. Both sensillar forms develop according to a common schedule, the main steps being elongation of the dendritic outer segment (cf. Lee and Altner, 1985). This developmental scheme fits nicely with other known cases of hair sensillum development in holometabolous insects (Ernst, 1972; Hansen and Hansen-Delkeskamp, 1983; De Kramer and Van Der Molen, 1984; Kuhbandner, 1984). The most interesting event during mechanosensillum differentiation is the formation of the tubular body in the tip of the dendritic outer segment. It begins about the middle of pupal life, i.e. when the distal parts of the dendritic outer segment and of the dendrite sheath that lie outside the developing hair shaft are reduced. Evidence has been presented here that the tubular body develops continuously for about 80 hr. Two main process run in parallel: (1) an increase in number of microtubules within the dendritic outer segment together with an increase in the diameter of this segment and (2) an increasing joining of parallel microtubules by electron-dense material. Additionally, a 3rd process must be assumed: the formation of the membrane cones and the filamentous structures that connect these cones with the peripheral tubules. The latter process could not be analyzed in the present material. The increase in number of microtubules is great within the distal section of the dendritic outer segment, but much less proximally. This difference is not shown by the sensilla of the LPPO (Lee and Altner, 1985). It reflects the high degree of differentiation of mechanosensitive dendritic segments as compared with chemosensitive segments. It is not known whether there is a characteristic pattern of intercalation of newly formed microtubules; however, electron-dense material does appear to connect the

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m i c r o t u b u l e s in a d i s t i n c t p a t t e r n . T h i s p r o c e s s starts w i t h g r o u p s o f 3 - 4 m i c r o t u b u l e s b e i n g c o n n e c t e d , w h i c h a p p e a r to b e n u c l e i f o r f u r t h e r l i n k i n g t o g e t h e r o f m i c r o t u b u l e s . It c a n e a s i l y b e i m a g i n e d t h a t t h e a t t a c h m e n t o f m i c r o t u b u l e s f r o m 2 o r 3 d i r e c t i o n s l e a d s to t h e c u r l e d s h e e t s o f i n t e r c o n n e c t e d m i c r o t u b u l e s o b s e r v e d 90 hr a f t e r p u p a t i o n . S u c h a n a r r a n g e m e n t r e s e m b l e s t u b u l a r b o d i e s in c e r t a i n m e c h a n o r e c e p t o r s o f s p i d e r s . F o e l i x a n d C h u - W a n g (1973) d i s t i n g u i s h e d d e n s e a n d l o o s e t u b u l a r b o d i e s in s p i d e r s a n d a r g u e d t h a t a t u b u l a r b o d y s h o u l d b e d e f i n e d as a n y d e n s e a r r a n g e m e n t o f m i c r o t u b u l e s , w h i c h is r e s t r i c t e d to t h e d e n d r i t e t e r m i n a l . L o o s e t u b u l a r b o d i e s h a v e b e e n f o u n d also in i n s e c t s , e . g . in c o n t a c t c h e m o r e c e p t i v e s e n s i l l a o n t h e l a b i u m o f D y s d e r c u s i n t e r m e d i u s ( G a f f a l , 1981). I n t h e l a b i a l p a l p m e c h a n o r e c e p t o r s o f P. rapae, a l o o s e t u b u l a r b o d y is p r e s e n t f o r o n l y a b o u t 30 h r a n d is t h e n c h a n g e d i n t o a d e n s e o n e . A t 120 hr a f t e r p u p a t i o n , t h e n e t w o r k v i s i b l e in t r a n s v e r s e s e c t i o n s o f t h e t u b u l a r b o d y s h o w s a c o n s i d e r a b l y h i g h e r n u m b e r o f i n t e r c o n n e c t i o n s a n d m e s h e s t h a n at 90 h r a f t e r p u p a t i o n . F i n a l l y , t h e p e r i p h e r a l p a l i s a d e s (cf. G a f f a l a n d H a n s e n , 1972; M c l v e r , 1985) d e v e l o p at l a t e r stages. F u r t h e r i n v e s t i g a t i o n s will s h o w w h e t h e r d e n s e t u b u l a r b o d i e s g e n e r a l l y d e v e l o p via a l o o s e s t a g e . Acknowledgement:; This study was supported by the Deutsche Forschungsgemeinschaft (SFB 4: G1). 1 thank Drs B.-U. Budelmann and H. Wunderer for their helpful comments on the manuscript, and Dr J. Kien for attentive linguistic corrections. I am extremely grateful to Professor H. Altner for his constructive discussions and critical reading of the manuscript. Thanks are also due to Ms H. Hallmer and Ms R. Nowak for expert photographic assistance, and Ms R. Rochelt for typing the manuscript.

REFERENCES ACTNER, H. 1977. Insect sensillum specificity and structure: an approach to a new typology, pp. 295-3113. In J. LE MACNENand P. MACLEOD(eds) Olfaction and Taste. Vol. 6. Information Retrieval, London. ALTNER, H. and F. BAUER. 1982. Ultrastructure of specialized, thrust-sensitive, insect mechanoreceptor: stimulus-transmitting structures and sensory apparatus in the rostral horns of Noctiophilus biguttatus. Cell Tissue Res. 226: 337-54. BARTH, F. G. and R. BClCKHAN. 1984. Mechanoreception, pp. 554-582. In J. BRE~TER-HAHN, A. G. MALTOLS~and K. S. R~CHARDS(eds) Biology of the Integument. Vol. 1. Springer, Berlin, Heidelberg, New York. BOGNER, F., M. BOPPR~,, K.-D. ERNS'I and J. BOECKH. 1986. CO~ sensitive receptors on labial palps of Rhodogastria moths (Lepidoptera : Arctiidae): physiology, fine structure and central projection. J. Comp. Pk,ysiol. 158: 741-49. DE KRAMER, J. J. and L. G. VAN DER MOLEN. 1984. Development of labellar taste hairs in the blowfly, Calliphora vicina (Insecta, Diptera). Zoomorphology 104: 1-10. ERLER, G. 1983. Reduction of mechanical sensitivity in an insect mechanoreceptor correlated with destruction of its tubular body. Cell Tissue Res. 234: 451-61. ERNST, K.-D. 1972. Die Ontogenie der basiconischen Riechsensillen auf der Antenne yon Neerophorus (Coleoptera). Z. Zellforsch. 129: 217-36. FOEHX, R. F. and I.-W. CHU-WANG. 1973. The morphology of spider sensilla I. Mechanoreceptors. Tissue Cell 5 : 4 5 [ 60. FRENCH, A. S. and E. J. SANDERS. 1979. The mechanism of sensory transduction in the sensilla of the trochante=al hair plate of the cockroach, Periplaneta americana. Cell Tissue Res. 198: 159-74. FRENCH, A. S. and E. J. SANDERS. 1981. The mechanosensory apparatus of the femoral tactile spine of the cockroacl', Periplaneta americana. Cell Tissue Res. 219: 53-68. GAFI=AL,K. P. 1981. Terminal sensilla on the labium of Dysdercus intermedius Distant (Heteroptera : Pyrrhocoridae). Int. J. Insect Morphol. Embryol. 10: 16. GAFFAL, K. P. and U. BASSEMm. 1974. Vergleichende Untersuchung modifizierter Cilienstrukturen in den Dendriten mechano- und chemosensitiver Rezeptorzellen der Baumwollwanze Dysdercus und der Libelle Agrion. Protoplasma 82: 177-202. GAFFAL, K. P. aad K. HANSEN. 1972. Mechanorezeptive Strukturen der antennalen Haarsensillen der Baumwol~wanze Dysdercus intermedius Dis. Z. Zellforsch. 132: 79-94.

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