Postembryonic development of the lateral protocerebral lobes, corpora pedunculata, deutocerebrum and tritocerebrum of Phormia regina meigen (diptera: calliphoridae)

Int. J. Insect Atorphol. & Embryol.. 7 (5/6): 467 to 477. ~.~ Pergamon Press Ltd. 1978. Printed in Great Britain.

0020-7322/78/1201-0467502.00/0

POSTEMBRYONIC DEVELOPMENT OF THE LATERAL PROTOCEREBRAL LOBES, CORPORA PEDUNCULATA, DEUTOCEREBRUM A N D TRITOCEREBRUM OF P H O R M I A REGINA MEIGEN (DIPTERA: CALLIPHORIDAE)*t Ross W. GUNDERSEN+ and JOSEPH R. LARSEN Department of Entomology, 320 Morrill Hall, University of Illinois, Urbana, IL 61801, U.S.A. (Accepted 15 June 1978)

Abstract--The postembryonic development of the corpora pedunculata, deutocerebrum and tritocerebrum of Phormia reghra Meigen was studied using reduced silver stains to provide detailed observations and determine the relationships between larval and imaginal neurones. The imaginal ganglion cells of these areas are formed from isolated neuroblasts by a series of asymmetric and symmetric divisions. The imaginal corpora pedunculata are formed by 10 isolated neuroblasts located dorsal to the larval calyces. The imaginal antennal ganglia are formed by 2 isolated neuroblasts. These ganglia lie dorsal to the larval antennal ganglia which degenerate during the late larval and early pupal stages. The glomerular structure of the imaginal ganglia develops during the pupal stage after receiving antennal sensory fibers. The tritocerebrum of the imaginal brain is formed by isolated neuroblasts. The cellular and neuropilar components of the larval brain degenerate during the late larval and early pupal stages. The degenerating larval ganglion cells are characterized by pycnotic nuclei and the neuropile by a ragged, darkly stained appearance. The larval and adult brains of Phormia are discrete morphological entities as revealed by the degeneration of the larval brain, concomitant with its replacement by corresponding imaginal elements. Index descriptors (in addition to those in title): Antennal ganglia, neural degeneration, neuroblasts. INTRODUCTION STUDIES on the changes a c c o m p a n y i n g the postembryo,lic brain development of endopterygote insects are numerous. However, few attthors provide detailed observations with precise aging (e.g. Gieryng, 1965; N o r l a n d e r and Edwards, 1970). The m a j o r question arising from studies of postembryonic brain development is whether or not larval neurones are incorporated into the adult brain. This study considers the postembryonic development of the lateral protocerebral lobes, corpora pedunculata, d e u t o c e r e b r u m a n d tritocerebrum of Phormia with precise aging a n d the relationship between larval and adult neurones. F o r a more complete u n d e r s t a n d i n g of this work, consult Larsen et al. (1976) on the adult brain of Phormia. * Part of a thesis submitted by the senior author in partial fulfilment of the requirements for the Ph.D. degree in the Department of Entomology and the Graduate College, University of Illinois, Urbana, IL 61801, U.S.A. 1"Third in a series of 3 papers describing the postembryonic brain development of P. regina. Present address: University of Miami School of Medicine, Department of Physiology and Biophysics, Box 520875, Biscayne Annex, Miami, Florida 33152, U.S.A. 467

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Ross W. GUNDERSENand JOSEPH R. LARSEN M A T E R I A L S AND M E T H O D S

The Phornda larvae and pupae used in this study were synchronized in order to obtain uniform rates of development. Larvae were fixed in a modified Carnoy's fluid containing formaldehyde. Pupae were fixed in Brasil's fluid. Specimens were embedded in Paraplast. Rowell's (1963) silver impregnation was used to stain the pupal brain. The larval brains were stained utilizing Rowell's second impregnation solution followed by Blest's high temperature reduction. The cortical cells of the larval brain were stained with Delafield's hematoxylin and eosin Y. For detailed information concerning materials and methods see Gundersen and Larsen 0978). RESULTS

Formation of hnaghlal ganglioo cells The imaginal ganglion cells forming the cortex of the lateral protocerebral lobes, corpora pedunculata, deutocerebrum a n d tritocerebrum are produced by isolated neuroblasts located in the peripheral cortex of the larval brain. The neuroblasts are larger and more basophilic than larval ganglion cells (Fig. 4). These neuroblasts undergo the same n u m b e r a n d symmetry of divisions as those found in the optic lobes ( G u n d e r s e n a n d Larsen, 1978). Neuroblasts repeatedly divide asymmetrically to form daughter neuroblasts a n d small ganglion mother cells. The ganglion mother cell then divides symmetrically to form imaginal ganglion cells. Imaginal ganglion ceils are smaller a n d more basophilic t h a n larval ganglion cells (Fig. 4). Symmetric divisions of neuroblasts, which form daughter neuroblasts, were not observed.

The corpora pethtnculata All the c o m p o n e n t s of the corpora p e d u n c u l a t a (calyx, stalk, anterior a n d median roots) are present at hatching. Development is accomplished by an increase in size without major morphological modifications. Fibers directly responsible for the development of the corpora p e d u n c u l a t a are derived front imaginal ganglion cells proliferated by 10 isolated neuroblasts. These neurobl:~sts are

FIG. 1. Sagittal section through lateral protocerebral lobe (LPL) at pupariation. Neuropile of larval calyx of corpus pedunculatum (LCA) and lateral protocerebral lobe exhibiting darkly stained ragged appearance characteristic of degenerating larval neuropile. FIG. 2. Sagittal section through lateral protocerebral lobe (LPL) 18 hr after pupariation. Note absence of degenerating neuropile in imaginal calyx of corpus pedunculatum (ICA) and lateral protocerebral lobe. Also note that imaginal calyx is smaller than larval calyx (Fig. l). FIG. 3. Frontal section through imaginal calyx of corpus pedunculatum, 120 hr after hatching. Three of 5 neuroblasts (NB) and associated imaginal ganglion cells (IGC) responsible for forming cortex of imaginal calyx are observed. FIG. 4. Frontal section through protocerebral cortex, 72 hr after hatching (hematoxylin and eosin). Cortex contains 3 types of cells: neuroblasts (NB), larval ganglion cells (LGC) and imaginal ganglion cells (IGC). Lateral protocerebral lobe (LPL). FIG. 5. Frontal section through imaginal calyx of corpus pedunculatum (ICA) 120 hr after hatching. Note pyramidal shape of calyx and imaginal ganglion cells (IGC) of its cortex. FIG. 6. Dorso-ventral section through larval calyx of corpus pedunculatum (LCA), 120 hr after hatching. Note 4 of 5 fiber bundles (arrows) ;,vhich form imaginal calyx. FIG. 7. Dorso-ventral section through larval antennal ganglion (LAG), 120 hr after hatching. Note degenerating larval ganglion cells (LGC). FIG. 8. Dorso-ventral section through larval cortex of corpus pedunculatum, 120 hr after hatching. Note 3 degenerating larval ganglion cells (arrows) which exhibit condensed chromatin material of pycnotic nuclei. FIG. 9. Frontal section through median roots of larval corpora pedunculata (MR), 96 hr after hatching. Note prominent trilobed structure of median roots characteristic of larva.

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divided into 2 groups of 5, 1 group for each pedunculate body. Each group of neuroblasts is positioned in a semicircle dorsal to the larval calyx (Fig. 3). lmaginal ganglion cells derived front these neuroblasts remain in 5 groups dorsal to each calyx (Fig. 3). The fibers of these imaginal ganglion cells coalesce into 5 bundles which are seen in dorso-ventral sections (Fig. 6). The 5 fiber bundles proceed ventrally along the posterior surface of the larval calyx and enter the stalk (Fig. 6). These fiber bundles form the imaginal calyx, a pyramidal area of lightly stained fine fibers lying posterior to the larval calyx (Figs. 5, 12). Between 18 and 72 hr after pupariation, no morphological changes in the corpora pedunculata were observed. During this period the corpora pedunculata reach their imaginal size.

The lateral protocerebral lobes The lateral protocerebral lobes increase in size from hatching until 72 hr after pupariation. This increase in size results from the production of imaginal ganglion cells from neuroblasts present in the larval cortex (Fig. 19). The imaginal ganglion cells add their fibers to the lateral protocerebral neuropile increasing its size. The median bundle, which arises from the lateral protocerebral lobes, is present throughout development and is unaffected by the degeneration of the larval lateral protocerebral lobes. During the first 72 hr after pupariation, the bipartate median bundle, characteristic of the larva (Fig. 17), assumes the imaginal morphology. Each half of the median bundle shifts medially, and at 72 hr after pupariation the 2 halves meet and form the single adult median bundle which bifurcates around the esophagus (Fig. 15).

The deutocerebrum The postembryonic development of the deutocerebrum, or antennal ganglia, begins ill the larva 72 hr after hatching by the addition of imaginal neuropile to each larval antennal ganglion. This neuropile forms the imaginal antennal ganglia. Each of the imaginal antennal ganglia is formed by the fibers of imaginal ganglion cells produced by a neuroblast lying latero-ventral to each ganglion (Fig. 18). In sagittal and frontal sections the imaginal antennal ganglia form a cap of lightly stained fibers resting on the dorsum of the larval antennal ganglia (Figs. 16, 18). Growth of the imaginal antennal ganglia continues until 60 hr after pupariation even though the 2 neuroblasts are absent at pupariation.

FIG. 10. Sagittal section through tritocerebrum (T) at pupariation. Note ragged, darkly stained appearance of tritocerebrum characteristic of degenerating neuropile. Lateral protocerebral lobe (LPL). FIG. I 1. Sagittal section through brain 18 hr after pupariation. Note lack of degenerating neur0pile. Also note that remaining neuropile is composed of fine, lightly stained fibers. Imaginal antennal ganglion (IAG), larval antennal ganglion (LAG), lateral protocerebral lobes (LPL), tritocerebrum (T). FIG. 12. Sagittal section through brain, 120 hr after hatching. Larval and imaginal fibers of olfactorio globularis (LFOG, IFOG) are seen joining to form composite larval and imaginal olfactorio globularis. Central complex (CC), imaginal calyx of corpus pedunculatum (ICA), larval calyx of the corpus pedunculatum (LCA), median root of corpus pedunculatum (MR), larval antennal ganglion (LAG). FXG.13. Frontal section through larval calyx of corpus pedunculatum (LCA), 120 hr after hatching. Larval fibers of olfactorio globularis (LFOG) are observed entering larval calyx. FIG. 14. Frontal section through imaginal calyx of corpus pedunculatum (ICA), 120 hr after hatching, lmaginal fibers of olfactorio globularis (IFOG) are observed entering imaginal calyx.

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A portion of the neuropilar growth of the imaginal antennal ganglia after the disappearance of the neuroblasts, can be accounted for by the acquisition of sensory fibers from the developing antenna between 36 and 48 hr after pupariation. The antennal sensory fibers reach the imaginal antennal ganglia by following the pupal antennal nerve. The pupal antennal nerve is first observed at 18 hr after pupariation and is formed by the fibers of a transient group of ganglion cells located at the base of the imaginal antennal disc (Fig. 21). The fibers of these transient ganglion cells follow the larval antennal nerve to the imaginal antennal ganglion (Fig. 21). Between 18 and 24 hr after pupariation, the larval antennal nerve degenerates, the imaginal antennal disc everts and only the pupal antennal nerve is observed connecting the antenna to the imaginal antennal ganglion. The antennal sensory fibers develop and follow the pupal antennal nerve to the imaginal antennal ganglion to form the imaginal antennal nerve (Fig. 22). Between 48 and 60 hr after pupariation the pupal nerve degenerates, leaving the imaginal antennal nerve intact. During the period from 60 to 72 hr after pupariation, the glomerular structure of the imaginal antennal ganglia develops (Fig. 20). Earlier than 60 hr after pupariation, the ganglia are homogeneous. Therefore, the glomerular structure develops after the acquisition of the antennal sensory fibers. The olfactorio globularis is present throughout larval and pupal development and connects the antennal ganglia to the calyces of the corpora pedunculata (Figs. 13, 14, 17). At 120 hr after hatching, the olfactorio globularis is a composite of larval and imaginal fibers (Fig. 12). Fibers from the imaginal antennal ganglia fbllow the larval fibers of the olfactorio globularis to the calyces of the corpora pedunculata (Fig. 14). The larval fibers enter the larval calyx and the imaginal fibers enter the imaginal calyx (Fig. 13).

The tritocerebrum The tritocerebrum increases in size from hatching until 72 hr after pupariation. The fibers responsible for this increase in size are formed by imaginal ganglion cells produced by isolated neuroblasts located in the larval tritocerebral cortex (Fig. 19). These neuroblasts are absent at pupariation.

Degeneration of larval elements during postembryogeny Between 120 hr after hatching and 18 hr after pupariation, the larval ganglion cells and neuropile of the corpora pedunculata, lateral protocerebral lobes, deutocerebrum and tritocerebrum degenerate. The degenerating larval ganglion cells have eccentric nuclei with extremely condensed chromatin material which is characteristic of the pycnotic nuclei of degenerating cells (Figs. 7, 8). The degenerating neuropile is darkly stained and ragged in appearance (Figs. 1, 10, 16). After degeneration of the larval elements, the remaining neuropile is formed of lightly stained imaginal fibers interspersed with a few darker stained fibers (Figs. 2, 11). The larval fibers of the olfactorio globularis also degenerate during the late larval and early pupal stages. Only 2 differences in morphology were produced by the degeneration of larval elements. These are localized to the corpora pedunculata. The first is that the median roots lack the 3 larval protuberances which were visible in frontal sections (Fig. 9). Secondly, the imaginal calyx is smaller and pyramidal rather than spherical (Fig. 2).

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IGC

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F~c. 15. Frontal section through lateral protocerebml lobes (LPL), 72 hr after pupariation. Note median bundle (MB) as it bifurcates around the esophagus (E). Anterior root of the corpus pedunculatum (ARk),median root of the corpus pedunculatum (MR). FIc. 16. Sagittal section through antennal ganglia and lateral protocerebral lobe (LPL), at pupariation. Note ragged, darkly stained neuropile of larval antennal ganglion (LAG) and lateral protocerebral lobe, characteristic of degeneration. Imaginal antennal ganglion (IAG). Fic. 17. Frontal section through brain, 24 hr after hatching. Note bi~artate median bundle (MB). Accessory protocerebral lobe (APL), anterior root of the corpus pedunculatum (AR), esophagus (E), larval antennal ganglion (LAG), lateral protocerebral lobe (LPL), olfactorio globularis (OG), tritocerebrum (T). FIo. 18. Frontal section through larval and imaginal antennal ganglia (LAG, IAG), 120 hr after hatching. Imaginal antermal ganglion forms a cap of fine lightly stained fibers dorsal to larval ganglion. Ventro-lateral to imaginal ganglion lies its associated neuroblast (NB) and imaginal ganglion cells (IGC).

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Ross W. GUNDERSENand JOSEPHR. LARSEN DISCUSSION

The corpora pedunculata The corpora pedunculata of Phormia (calyx, stalk and roots) are present at hatching. This is similar to the following endopterygote insects: Myrmeleon europaeus (LuchtBertram, 1962), C,dex pipiens (Hinke, 1961) and Apis mellifera (Lucht-Bertram, 1962). Most endopterygote insects studied differ from Phormia in that the corpora pedunculata are absent at hatching and develop during the larval stage (Gieryng, 1965; Satija and Kaur, 1967; Ali, 1974). The isolated neuroblasts responsible for the development of the corpora pedunculata in Phormia are also observed in Danaus plexippus in close association with the calyces (Norlander and Edwards, 1970). Phormia's differs from Hymenoptera and Coleoptera in that neuroblast aggregates, not isolated neuroblasts, are responsible for the development of the corpora pedunculata in these 2 orders (Panov, 1966). In Phormia the fibres of imaginal ganglion cells form the separate imaginal calyx of the corpora pedunculata, differing from Danaus (Norlander and Edwards, 1970) in which the fibers are added to the larval calyx and a separate imaginal calyx was not observed. The corpora pedunculata of Ephestia kuhniella (Schrader, 1938) and Danaus (Norlander and Edwards, 1970), unlike Phormia, undergo development which is delayed until the pupal stage, or accelerates during the late larval stage respectively. The deutocerebrum The larval antennal ganglia of most endopterygote insects studied are homogeneous (e.g. Gieryng, 1965; Satija and Aggarwal, 1967; Satija and Sharma, 1968), similar to Phormia. Tenebrio molitor (Panov, 1961) and Danaus plexippus (Norlander and Edwards, 1970) possess glomerular structure in the larval antennal ganglia, unlike Phormia. The isolated neuroblasts responsible for the development of the antennal ganglia are also observed in Danaus (Norlander and Edwards, 1970), Tenebrio (Panov, 1961) and Apis mellifera (Panov, 1961). In these insects, the fibers of the ganglion cells produced by these neuroblasts are added to the larval antennal ganglia to form the imaginal antennal ganglia. In Phormia, the larval and imaginal antennal ganglia are distinct structures, and postembryonic development occurs only in the imaginal ganglia. The glomerular structure of the imaginal antennal ganglia develops during the pupal stage in all endopterygote insects studied (e.g. Panov, 1961 ; Gieryng, 1965; Norlander and Edwards, 1970), identical to observations on Phormia. Titschack (1928) determined that

FIG. 19. Sagittal section through tritocerebrum (T) and lateral protocerebral lobe (LPL), 72 hr after hatching (hematoxylin and eosin). Note isolated neuroblasts (NB) within cortices of tritocerebrum and lateral protocerebral lobe. FIG. 20. Dorso-ventral section through imaginal antennal ganglion (IAG) 72 hr after pupariation. Note glomerular structure of ganglion (GS) and imaginal antennal nerve (IAN). FIG. 21. Dorso-ventral section through antennal part of cephalic imaginal disc (ACID), 18 hr after pupariation. Note group of transient ganglion cells (TGC). Fibers of these cells form pupal antennal nerve (PAN) which follow larval antennal nerve (LAN) to larval antennal ganglion. FIG. 22. Dorso-ventral section through base of antennae 48 hr after pupariation. Imaginal antennal nerve (IAN) is seen joining pupal antennal nerve (PAN). Transient ganglion cells tTCC).

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antennal sensory fibers are necessary for the glomerular structure of the imaginal antennal ganglia to develop. Observations on the development of this glomerular structure in Phormia are supported by this work. The glomerular structure of Phormia's imaginal antennal ganglia develops only after receiving antennal sensory fibers. Formation of the antennal nerve, olfactorio globularis and general neuropilar regions In Phormia, the imaginal antennal nerve is apparently formed by the antennal sensory fibers following the pupal antennal nerve to the imaginal antennal ganglia. A similar system is also observed in Manduca sexta (Sanes and Hildebrand, 1975). One major difference exists between Phormia and Manduca. In Manduca, the pupal antennal nerve is incorporated into the imaginal antennal nerve rather than degenerating as observed in Phormia. The olfactorio globularis is formed in a manner analogous to the antennal nerve. The imaginal fibers of the olfactorio globularis apparently follow their larval counterpart to the imaginal calyx of the corpora pedunculata. The larval olfactorio globularis then degenerates. The imaginal neuropiles of the lateral protocerebral lobes, deutocerebrum and tritocerebrum conform to the same shape as their larval counterparts after degeneration of the larval neuropile. The larval neuropile appears to serve as a template to confer a basic shape to the developing imaginal neuropile. Degeneration of larval elements during postembryogeny Degeneration of ganglion cells and neuropile has been observed in the following larval brain regions of P. reghTa: larval optic neuropile (Gundersen and Larsen, 1978), lateral protocerebral lobes, corpora pedunculata, deutocerebrum and tritocerebrum. These regions encompass the entire larval brain. The degenerating larval ganglion cells are characterized by pycnotic nuclei and the larval neuropile by a ragged, darkly stained appearance. The degeneration of the larval brain indicated that no larval brain elements are incorporated into the adult brain. The larval glomerular structure of the antennal ganglia of Danaus plexippus (Norlander and Edwards, 1970) and Tenebrio molitor (Panov, 1961) degenerate without affecting the matrix of the ganglia. Even though Phormia lack glomerular structure in the larval antennal ganglia, these observations disagree with those made on Phormia. In Phormia, both larval antennal ganglia degenerate entirely. Only one report on the degeneration of the entire larval brain was found. Tiegs (1922) observed that the entire larval brain of Nasonia mormoniella (Hymenoptera) degenerates. The degenerating larval ganglion cells contained pycnotic nuclei and the larval neuropile was ragged and discontiguous. Observations on Phormia of degeneration support those of Tiegs (1922). Most workers in the area of postembryonic brain development of endopterygote insects, describe this development as the growth of the larval brain and addition of elements to the larval brain. Therefore, it is inferred that the larval brain forms an integral part of the adult brain. This inference disagrees with this study on the postembryonic brain development of Phormia. In Phormia, the larval and adult brains are discrete morphological entities. This is revealed by the degeneration of the larval brain, concomitant with its replacement by corresponding imaginal elements. Therefore, the larval brain of Phormia is not incorporated into the adult brain, based on observations with reduced silver stains. REFERENCES Ats, F. A. 1974. Structure and metamorphis of the brain and suboesophageal ganglion ofPieris brassicae(L.) (Lepidoptera: Pieridae). Trans. R. Entomol. Soc. Lond. 125: 363-412.

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BLEST, A. D. 1961. Some modifications of Holme's silver method for insect central nervous systems. Q. J. Microsc. Sci. 102: 413-17. GIERYNG, R. 1965. Ver/inderungen der histologischen Struktur des Gehirns von Calliphora vomitoria (L.) (Diptera) w~ihrend der postembryonalen Entwicklung. Z. Wiss. Zool. 171 : 80-96. GtJNDERSEN, R. W. and J. R. LARSEN. 1978. Postembryonic development of the optic lobes of Phormia regh~a Meigen (Diptera: Calliphoridae). hit. J. htsect Morphol. Embryol. 7: 121-36. HINKE, W. 1961. Das relative postembryonale Wachstum der Hirnteile von Culex pipiens, Drosophila melanogaster und Drosophilamutanten. Z. Morphol. Oekol. Tiere 50:81-118. LARSEN, J. R., V. G. DETHIER and A. H. BROADBENT. 1976. Brain of the black blowfly, Phormia regina Meigen (Diptera: Calliphoridae). hit. J. b~sect Morphol. Embryol. 5: 79-106. LUCHT-BERTRAM, E. 1962. Das postembryonale Wachstum von Hirnteilen bei Apis mellifica L. und Myrmeleon europaeus L. Z. Morphol. Oekol. Tiere 50: 543-75. NORLANDER, R. H. and J. S. EDWARDS. 1970. Postembryonic brain development in the Monarch butterfly, Danaus plexippus plexippus L. III. Morphogenesis of centers other than the optic lobes. Wilhelm Roux' Arch. Entwickhlngsmech. Org. 164: 247-60. PANOV, A. A. 1961. The structure of the insect brain at successive stages in postembryonic development. IV. The olfactory center. Entomol. Rev. (Engl. Transl. Entomol. Obozr.). 40: 14~45. PANOV, A. A. 1966. Correlations in the ontogenetic development of the central nervous system in the house cricket Gryllus domesticus L. and the mole cricket Gryllotalpa gryllotalpa L. (Orthoptera, Grylloidae). Entomol. Rev. (Engl. Transl. Entomol. Obozr.). 45: 179-85. ROWELL,F. C. H. 1963. A general method for silvering invertebrate central nervous systems. Q. J. Microsc. Sci. 104: 81-7. SANES, J. R. and J. G. HILDEBRAND. 1975. Nerves in the antennae of pupal Manduca sexta Johanssen (Lepidoptera: Sphingidae). Will, elm Roux' Arch. Entwicklungsmech. Org. 178: 71-8. SATIJA,. R. C. and V. AGGARWAL. 1967. Histological studies on post-embryonic development of the brain of Drosophila melanogaster. Res. Bull. Panjab Univ. Sci. 18: 109-25. SATIJA, R. C. and R. P. KAUR. 1967. Brain during postembryonic life of Callosobruchus maculatus F. Res. Bull. Panjab Univ. Sci. 18: 475-89. SA'nJA, R. C. and M. L. SHARMA. 1968. Postembryonic development of the brain of Musca domestica. Res. Bull. Panjab Univ. Sci. 19: 71-80. SCHRADER, K. 1938. Untersuchungen fiber die Normalentwicklung des Gehirns und Gehirntransplantationen bei der Mehlmotte Ephestia k~hniella Zeller nebst einigen Bemerkungen fiber das Corpus allatum. Biol. Zentralbl. 58: 52-90. TIEGS,O. W. 1922. Researches on the insect metamorphosis. Part I. On the structure and post-embryonic development of a chalcid wasp, Nasonia. Trans. R. Soc. S. Aust. 46: 319-492. TITSCHACK, E. 1928. Der Fuhlernerv der Bettwanze, Cimex lectularius L., und sein zentrales Endgebiet. Zool. Jahrb. Abt. Allg. Zool. Physiol. Tiere 45: 437-62. ABBREVIATIONS ACID AR CC E GS IAG IAN ICA IFOG IGC LAG LAN LCA LGC LFOG LPL MB MR N'B PAN T TGC

USED IN FIGURES

antennal part of cephalic imaginal disc anterior root of corpus pedunculatum central complex esophagus glomerular structure of imaginal antennal ganglion imaginal antennal ganglion imaginal antennal nerve imaginal calyx of corpus pedunculatum imaginal fibers of olfactorio globularis imaginal ganglion cells larval antennal ganglion larval antennal nerve larval calyx of corpus pedunculatum larval ganglion cells larval fibers of olfactorio globularis lateral protocerebral lobe median bundle median root of corpus pedunculatum neuroblast pupal antennal nerve tritocerebrum transient ganglion cells