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JOURNAL OF MORPHOLOGY 236:139149 (1998)

The Stomatogastric Nervous System of the Honey Bee (Apis mellifera) in a Critical Phase of Caste Development
ISABEL C. BOLELI1*, ZILA LUZ PAULINO SIMOES1, AND KLAUS HARTFELDER2 1Depto. Biologia, Faculdade de Filosoa, Ciencias e Letras de Ribeirao Preto, Universidade de Sao Paulo, 14040-901 Ribeirao Preto, SP, Brazil 2Zoologisches Institut, Universitat Tubingen, D-72076 Tubingen, Germany *Correspondence to: Isabel C. Boleli, Depto. Biologia, Faculdade de Filosoa Ciencias e Letras de Ribeirao Preto, USP, Av. Bandeirantes 3900, 14040-901 Ribeirao Preto, SP, Brazil; E-mail: zlpsimoe@usp.br

ABSTRACT Progress in our understanding of polymorphic differentiation of female honey bee larvae into queens and workers required a re-evaluation of neuronal pathways potentially involved in transmitting information on food quality. This study presents new data on the anatomy of one of these pathways, the stomatogastric nervous system (SNS) of honey bee larvae and pupae. Scanning electron microscopy preparations demonstrated not only developmental changes in frontal ganglion structure, but also provided rm evidence for a hypocerebral ganglion in the honey SNS. In addition to previously described SNS nerves, the frontal, recurrent and esophageal nerves, and the frontal connectives, we observed three new nerves that connect the SNS to the central nervous system and the foregut. The rst one is an unpaired connective nerve of the frontal ganglion to the anteromedial protocerebrum. The second consists of paired lateral branches of the recurrent nerve, and the third is a plexus of ne nervous branches associated with the pharynx. Lateral extensions of the newly described hypocerebral ganglion also make contact with the pharynx. Similar but smaller branches were also observed to originate from the esophageal nerves as they run along the foregut. The exact anatomical localization of the cardiostomatogastric nerves, which connect the SNS with the retrocerebral complex, could also be detected. The description of such new nervous connections will serve as a database for functional analyses on the role of the SNS in differential feeding responses of the honey bee larvae, representing the initial step in caste differentiation. J. 1998 Wiley-Liss, Inc. Morphol. 236:139-149, 1998. The polymorphic phenotypes observed in most highly social insects do not result from caste-specic, distinct genetic programs, but rather represent hormonally controlled differences in morphogenetic growth. The rst and inductive step leading to social insect caste differentiation has been conceptualized as a nutritional switch (Wheeler, 86). In the honey bee, Apis mellifera, such a nutritional switch is well known and consists of the differential feeding of queen and worker larvae in the late larval stages with either royal jelly or a mixed diet of glandular secretions, pollen and honey (Shuel and Dixon, 59; Rembold et al., 74). Such external stimuli generally will require perception and processing systems in order to transmit
1998 WILEY-LISS, INC.

appropriate information to the endocrine system. The presence of chemical and mechanical receptors for food quality on mouthparts of honey bee larvae has been demonstrated (Goewie, 78). Any further pathways involved in transmission and transformation of such information relevant to honey bee caste differentiation, however, still remain obscure, and only the nal element in such a hypothetical axis, the neuroendocrine tract, has received more attention (Ulrich and

Contract grant sponsor: CAPES; Contract grant sponsor: DAAD. *Correspondence to: Isabel C. Boleli, Depto. Biologia, Faculdade de Filosoa Ciencias e Letras de Ribeirao Preto, USP, Av. Bandeirantes 3900, 14040-901 Ribeirao Preto SP, Brazil.

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Rembold, 83). The earliest caste-specic endocrine response is elevated levels of juvenile hormone synthesis by the corpora allata of fourth and early-fth instar queen larvae (Rachinsky and Hartfelder, 90). The structure of the neuroendocrine tract (brain/corpora cardiaca/corpora allata) and its function in the regulation of synthesis and secretion of morphogenetic hormones were elaborated and are now well understood for a few lepidopteran species only, in particular Manduca sexta (Gilbert 89; Westbrook et al., 91) and Bombyx mori (Mizoguchi et al., 90). Attempts to functionally characterize the neuroendocrine axis in the larval and pupal stages of honey bee permitted us to identify specic sets of brain neurosecretory cells that positively stained for a Bombyx prothoracicotropic-hormone-like peptide (Paulino Simoes et al., 97). No immunoreac tivity against this peptide, however, was detectable in any of the axons. Similar indications of an incompletely developed neuronal architecture in larval honey bees were also obtained for the serotonergic system (Boleli et al., 95). Serotonin, however has been demonstrated to stimulate juvenile hormone synthesis in vitro (Rachinsky, (94). These observations led us to conclude that the classically proposed neuroendocrine axis controlling insect metamorphosis may not be fully functional in the honey bee larva, and that an additional neuronal axis, the stomatogastric nervous system (SNS), could be involved in transmitting information on food quality to the endocrine system of the honey bee larva. Turning to the SNS as a potential candidate in the regulation of caste differentiation was encouraged by this systems well established role in the coordination of food intake in insects and food transport through the foregut (Hill et al., 66; Dogra and Ewen, 71; Verret and Mills, 76; Cooper and He, 94; Miles and Booker, 94). Connections of the SNS with the brain as well as with the endocrine complex have been reported in many insects (Willey, 61; Gundel and Penzlin, 78; Kirby et al., 84; Dai et al., 87; Moore and Loher, 88; Jagota and Habibulla, 92). For the honey bee, anatomical studies of the SNS date back over fty years (Rehm, 40; Bickley, 42; Schaller, 50; Ritcey and Dixon; 69, Wirtz, 73). Despite all these accounts, however, the exact anatomical organization of the honey bee SNS remains unclear and contradictory, and many details concerning gut innervation, as well as connections of

the SNS with the brain and the retrocerebral endocrine complex, have not been resolved. We, therefore, considered a detailed analysis of anatomical organization as a prerequisite for any further investigations into the SNSs physiological role in caste differentiation. The purpose of this study was to re-evaluate the gross morphology of the larval SNS in honey bee queen and worker larvae by means of scanning electron microscopy.
MATERIALS AND METHODS

Larvae and pupae of the honey bee (Apis mellifera L.) were obtained from colonies kept under natural conditions at the Department of Genetics, University of Sao Paulo at Ribeirao Preto, and the Department of Zool ogy, Tubingen University, Germany. Queen larvae and pupae were reared by grafting rst instar larvae as in standard apicultural practice. Denition of substages in the critical fth larval instar was according to Rembold et al. (80) and Rachinsky and Hartfelder (90). The SNS was exposed by an incision in the cuticle on the back of the head, extending through the neck region and thoracic segments. Once opened, the preparation was ushed with phosphate-buffered saline (PBS), 0.1 M pH 7.4; NaCl 0.9%), and the tracheae and muscles surrounding the stomatogastric complex were carefully removed. Subsequently, PBS was replaced by cold xative (1% glutaraldehyde, 0.6% paraformaldehyde, 0.25% DMSO in 0.12 M cacodylate buffer at pH 7.2). The in situ-xed brain, SNS, foregut, and retrocerebral complex were then carefully dissected out of the head and thoracic carcass, and xed in fresh xative for an additional 2 hr at 4C. After rinsing in cacodylate buffer, the preparations were dehydrated in a graded alcohol series up to absolute ethanol. Subsequently, they were submitted to critical point drying and, after sputter-coating with palladium gold, they were examined and photographed using Cambridge 250KM2 and Jeol JSM 5200 scanning electron microscopes.
RESULTS

The frontal ganglion and its nerves The stomatogastric nervous system of honey bee female larvae and pupae is composed of two ganglia, the frontal and the hypocerebral ganglion. The frontal ganglion is situated on the pharynx close to the fron-

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tal margin of the brain, between the pharynx elevator muscles (Fig. 1). It is pear shaped, and its tip points anteriorly (Fig. 2). When comparing queens and workers of the honey bee, we noted not only characteristic caste-specic differences but also changes in the shape of the frontal ganglion during the larval-pupal transition. In honey bee workers, the frontal ganglion has a typical pyriform shape in the last larval stage, and becomes a more rounded structure in the pupal phase, whereas the frontal ganglion of queen pupae is dorsoventrally compressed, giving it an ellipsoidal appearance (Fig. 3). Five nerves exit the frontal ganglion: the unpaired frontal, recurrent and connective nerves, and the paired frontal connectives (Figs. 16, 17). The frontal nerve originates from the median anterior margin of the frontal ganglion. It is an unbranched ne and fragile nerve approximately 100 m in length, and runs forward along the dorsal midline of the pharynx toward the labrum (Figs. 2, 3). The frontal connectives are approximately 125 m in length and 15 m in diameter. They emerge from the posterolateral margins of the frontal ganglion, and travel to the anteroventral region of the tritocerebrum, just beneath the antennal lobes (Figs. 13). Before entering the tritocerebrum, each frontal connective merges with the ipsilateral labral nerve to form a short labrofrontal nerve (Fig. 4). The labral nerve itself innervates the maxilla and labium. The connective nerve arises from the medioposterior margin of the frontal ganglion, jointly with the recurrent nerve (Figs. 5, 16A). Over a short distance, it remains fused with the recurent nerve before the ne connective nerve separates from the dorsal surface of the stout recurrent nerve (Fig. 6). It was not possible to trace the complete path of the connective nerve up to the position where it enters the protocerebrum because it is a very fragile structure that easily ruptures during dissection. The much stouter recurrent nerve is approximately 45 m in diameter. It leaves the extreme posterior margin of the frontal ganglion between the two posterior pharyngeal muscles and travels posteriorly along the midline of the pharynx (Figs. 3, 5) before it enters the aorta and nally reaches the hypocerebral ganglion. In all specimens examined, the recurrent nerve gives off two pairs of large lateral branches that are symmetric in origin (Figs. 810). One of them forms a

peculiar ganglionic structure (Figs. 7, 9, arrows). In the same position on the dorsal pharyngeal surface, we observed many peripheral neurons that are quite variable in their distribution patterns. The ne processes of these nerves anastomose and form a complex nervous plexus that is linked to recurrent nerve (Figs. 79, arrowheads). In the posterior part of the recurrent nerve, where it enters the anterior region of the hypocerebral ganglion, a pair of short and stout nerves emerges. These nerves correspond to the cardiostomatogastric nerves that connect the SNS with the retrocerebral endocrine complex (Figs. 10, 11). The hypocerebral ganglion and its nerves Being situated just beneath the brain and surrounded by the retrocerebral system, the hypocerebral ganglion is not easily recognized. For clear demonstration of this important SNS element, it was thus necessary to carefully remove the dorsal region of the brain and the retrocerebral complex in order to expose and fully dissect this ganglion (Fig. 10). The hypocerebral ganglion of the preimaginal honey bee then appears as an elongated and attened structure, closely apposed to the dorsal surface of the pharynx. In diameter it is similar to the recurrent nerve (Figs. 11, 12). Characteristic for the larval hypocerebral ganglion are broad, n-like nerve branches extending laterally over the pharynx (Figs. 12, 13). The hypocerebral ganglion thus is not only anatomically positioned closely over the subretrocerebral foregut, but also appears to be functionally connected to this region. Interestingly, this functional association seems to be less intense in the pupal phase, when width and density of such lateral extensions are much reduced (Fig. 11). Two large nerves, generally described as esophageal nerves, arise from the posterior region of the hypocerebral ganglion (Figs. 13, 14). After traveling a short distance along the dorsal surface of the esophagus, these nerves descend and run laterally on either side of the esophagus and crop (Fig. 14). Along its projection path, each esophageal nerve sends off numerous tenuous branchesthat establish connections with the surface of the posterior foregut region (Fig. 13). The esophageal nerves terminate in ve digitlike branches over the lateral surface of the crop (Fig. 15).

Figures 16 Fig. 1. Apis mellifera. Frontal view of the brain and frontal ganglion of worker pupae, showing the localization of the frontal ganglion between the pharynx elevator muscles (asterisk). BR, brain; FG, frontal ganglion; LC, lateral connectives. Scale bar 50 m. Fig. 2. Apis mellifera. Dorsal view of the frontal ganglion of a worker larvae. FG, frontal ganglion; LC, lateral connectives, Ph, pharynx. Scale bar 50 m. Fig. 3. Apis mellifera. Dorsal view of the frontal ganglion of a queen pupae. FG, frontal ganglion; FN, frontal nerve; LC, lateral connectives; Ph, pharynx; RN, recurrent nerve. Scale bar 40 m. Fig. 4. Apis mellifera. Lateral view of the frontal

ganglion. The frontal connective and ipsilateral labral nerve form the short labrofrontal nerve before entering the tritocerebrum. BR, brain; FC, frontal connective; FG, frontal ganglion; IN, ipsilateral labral nerve; LFN, labrofrontal nerve; Ph, pharynx; PhM, pharynx elevator muscle. Scale bar 50 m. Fig. 5. Apis mellifera. Frontal ganglion removed from the pharynx to expose its ve nerves. CN, connective nerve; FC, frontal connectives; FG, frontal ganglion; FN, frontal nerve; RN, recurrent nerve. Scale bar 50 m. Fig. 6. Apis mellifera. Detail of Figure 5 showing the connective nerve emerging from the dorsal surface of the recurrent nerve. CN, connective nerve; FG, frontal ganglion; RN, recurrent nerve. Scale bar 10 m.

Figures 711 Fig. 7. Apis mellifera.Dorsal view of the pharynx showing the recurrent nerve, its nervous branches anastomosing in a nerve plexus (arrowheads), and a peculiar ganglionic formation (arrows). Oe, esophagus; RN, recurrent nerve. Scale bar 100 m. Figs. 8 and 9. Apis mellifera. Details of the lateral branches of the recurrent nerve. Oe, esophagus; RN, recurrent nerve. Scale bar 10 m. Fig. 10. Apis mellifera. General view of the stomatogastric nervous system showing the frontal ganglion, recurrent nerve, hypocerebral ganglion and esophageal

nerve. The brain was removed leaving only the basal tritocerebrum to support the preparation. CC-A, corpora cardiacaaorta complex; FG, frontal ganglion; HCG, hypocerebral ganglion; OeN, esophageal nerve; Ph, pharynx; RN, recurrent nerve. Scale bar 50 m. Fig. 11. Apis mellifera. Detail of the recurrent nerve showing the cardiostomatogastric nerves emerging symmetrically at the junction of the recurrent nerve with the hypocerebral ganglion. CC-A, corpora cardiacaaorta complex; CSN, cardiostomatogastric nerve; HCG, hypocerebral ganglion; Oe, esophagus; RN, recurrent nerve. Scale bar 20 m.

Figures 1215

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Anatomy of the honey bee SNS Schematic reconstructions of the SNS of preimaginal honey bees depict the anatomical position of the frontal ganglion and the projection pattern of its nerves (Fig. 16A). Figure 16A shows in detail the yet undescribed connective nerve between the frontal ganglion and pars intercerebralis of the protocerebrum. The position of the newly described hypocerebral ganglion and the innervation pattern of the crop by the esophageal nerves is reconstructed and depicted in Figure 16B. A complete overview of the larval honey bee SNS (Fig. 17) shows the location of additional, newly described components of this nervous system, such as the cardiostomatogastric nerves connecting the recurrent nerve to the retrocerebral endocrine complex, as well as the nervous plexus formed by ne anastomosing nerves that exit the recurrent nerve as it passes under the tritocerebral bridge.
DISCUSSION

Comparative anatomy: newly described structures of the honey bee SNS Scanning electron microscope analysis of the SNS of honey bee larvae and pupae provided a detailed view on the organization of this nervous system. There is clear evidence for the existence of two ganglia, the already well described frontal ganglion (Rehm, 40; Bickey,42; Ritcey and Dixon, 69), and the formerly obscure hypocerebral ganglion. As the hypocerebral ganglion is an important structural element in the SNS of most insects (for review, see Penzlin, 85), its

Fig. 12. Apis mellifera. The hypocerebral ganglion of the larval SNS is a saddle-like structure connected to the esophagus by short but broad lateral extensions. HCG, hypocerebral ganglion; Oe, esophagus. Scale bar 50 m. Fig. 13. Apis mellifera.Esophageal nerve leaving the hypocerebral ganglion and projecting posteriorly along the esophagus. HCG, hypocerebral ganglion; Oe, esophagus; OeN, esophageal nerve. Scale bar 100 m. Fig. 14. Apis mellifera. Esophageal nerves descending on either side of the esophagus from a dorsal position at their root in the hypopharyngeal ganglion (top). CC-A, corpora cardiacaaorta complex; Oe esophagus; OeN, esophageal nerve. Scale bar 100 m. Fig. 15. Apis mellifera. Finger-like terminal branching of the esophageal nerve close to the crop. Oe, esophagus; OeN, esophageal nerve. Scale bar 10 m.

absence in the honey bee, as postulated by Rehm (40) and reported by Wirtz (73), was puzzling. In histological cross sections of the honey bee brain, the hypocerebral ganglion apparently could not be distinguished from the recurrent nerve as a separate entity. A ganglionic mass in this position, however, was suspected and discussed by LHelias (50) and Schaller (56) as constituting a true hypocerebral ganglion. Our SEM gures show that this ganglion denitely exists. Its tight association with the foregut, and its position close to the retrocerebral endocrine complex, however, may have made this structure difficult to resolve in cross sections. In other Hymenoptera, the hypocerebral ganglion is a more distinct structure (LafonCazal and Verron, 80). At the junction of the recurrent nerve with the hypocerebral ganglion we could detect a pair of nerves, the cardiostomatogastric nerves, which form a direct connection between the SNS and the retrocerebral endocrine system. This connection has already been noted by Ritcey and Dixon (69) and appears to be comparable to the ring nerve described for the ant Lasius niger (LafonCazal and Verron, 80). We have not yet been able to completely trace the paths of these nerves, and follow the projection patterns of their neurons within the endocrine system. Another nerve that may be serving an interface function between the SNS and the neuroendocrine axis is the unpaired connective nerve, a fragile nerve between the frontal ganglion and the pars intercerebralis of the larval honey bee brain. The existence of such a nerve has not previously been reported for Apis mellifera, but was reported in other insects, such as dragonies (Varma, 72), crickets (Kirby et al., 84), cockroaches (Willey, 61; Gundel and Penzlin, 78), termites (Hecker, 66) and scarab beetles (Bickley, ). In most insects, the pars intercerebralis of the protocerebrum is considered a higher-order center that controls endocrine activity. Neurosecretory material has been located in the pars intercerebralis cells of honey bee larvae by classical histology (Dogra et al., 77), and more recently also by immunocytochemical localization of an insect prothoracicotropic hormone-like peptide (Paulino Simoes et al., 97). Further more, a caste-specic timing for the development of this neuroendocrine axis has been reported (Ulrich and Rembold, (83). Based on our data, caste-specic differentia-

Fig. 16. Apis mellifera. Schematic representation of the stomatogastric nervous system of the larval and pupal honey bee. A: Frontal view. B: Hind view. AL, antennal lobe; Ao, aorta; BR, brain; CA, corpora allata; CC A, corpora cardiaca-aorta complex; CN, connective nerve; FC, frontal connective; FG, frontal ganglion; FN,

frontal nerve; HCG, hypocerebral ganglion; Mg, midgut; NCC, corpora cardiaca nerves; Oe, esophagus; OeN, esophageal nerve; Ph, pharynx; SOG, subesophageal ganglion; 1st3rd TG, prothoracic, mesothoracic, and metathoracic ganglia.

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Fig. 17. Apis mellifera. Schematic general representation of the stomatogastric nervous system and its relation to the foregut. CN, connective nerve; CSN, cardiostomatogastric nerve; F, foregut; FC, frontal connective; FG, frontal ganglion; FN, frontal nerve; HCG, hypocerebral ganglion; NP, nervous plexus; OeN, esophageal nerve.

tion is not limited to the central nervous system but also can be detected in the frontal ganglion, and these caste-specic modications may even, by their nervous connections to the CNS, affect the activity of the protocerebral centers of the neuroendocrine axis during honey bee metamorphosis. The lateral branches of the recurrent nerve and the nervous plexus formed by the anastomosis of ne nervous processes of the peripheral neurons observed on the pharynx are also an interesting and newly described feature of the honey bee SNS. Similar close associations between the SNS and pharyngeal surface were described in cockroaches (Willey, 61; Khan, 76) and in crickets (Kirby et al., 84). An even tighter association between SNS and foregut was apparent in the lateral extensions of the hypocerebral ganglion of the larval honey bee. Such intricate connections have not been previously described in other insects, and their functional role is difficult to ascertain, since the honey bee SNS has received very little attention, so far. Functional aspects Detailed structural analyses of the larval and early pupal SNS of the honey bee were sought to provide a sound anatomical basis for future functional studies, particularly on the integration of food intake regulation and endocrine activity in caste differentiation. Functional analyses of the insect SNS have generally implicated this system in the integration of food intake and crop emptying (for review see Penzlin, 85). Based on structural

evidence, particularly the newly described nerve plexus on the pharynx, the lateral extensions of the hypopharynx, and the nger-like branching pattern of the esophageal nerves, we would expect this to be the case in the honey bee, as well. The interesting question to ask in the honey bee, however, will be whether and how the SNS might be involved in caste differentiation, e.g., by acting as an integrating relay between different food qualities (royal jelly vs. mixed worker diet) and the endocrine system. Functionally, the SNS is best characterized for locusts and cockroaches (for review see Penzlin, 85). More recently, the sphingid moth, Manduca sexta, has been added to this list because of its eminent model character in hormonal control of metamorphosis. As demonstrated for many insects, the frontal ganglion of M. sexta larvae turned out to be a central pacemaker for neuronal activity controling buccal activity and muscle contractions in the pharynx and esophagus (Miles and Booker, 94). Caste-specic differentiation of this ganglion in the honey bee may thus be conceived as a factor affecting food intake rates in honey bee caste differentiation. Rhythmicity of foregut contractions, in turn, is expected to be modulated by sensory input resulting from gut extension. A source of such sensory input could be the newly described nerve plexus laterad of the recurrent nerve. A similar plexus in locusts consists of multipolar and bipolar neurons (Finlayson, 68; Kirby et al., 84) The axonal terminations of these neurons have been encountered between the longitudinal and circular muscles of the foregut and on the basement membrane of the gut epithelium, suggesting that the peripheral nerve plexus may be composed of both motor and sensory neurons (Kirby et al., 84). Gelperin (67) and Mohl (72) demonstrated that these multipo lar neurons are stretch receptors, and from electrophysiological tracing experiments, Tabor (76) has shown that sensory neurons of the pharynx have branches both in the recurrent nerve and the frontal connectives. Whereas the SNS is traditionally perceived as a system regulating food intake and gastrointestinal transport, its role as a potential relay between insect feeding activity and the endocrine system has recently come into focus. When tracing axons connecting the brain and retrocerebral complex in the cricket Teleogryllus commodus, Moore

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and Loher (88) discovered groups of somata in the pars intercerebralis that project to the retrocerebral complex via the esophageal nerve. Furthermore, Reichwald et al. (94) detected allatostatin-like peptides in nerve bers of the SNS of the cockroach Diploptera punctata, and Duve et al. (95) were able to inhibit contraction of the foregut by treatment with callatostatins. Serotonin, a modulatory neurotransmitter that also stimulates juvenile hormone synthesis in honey bee corpora allata (Rachinsky, 94), was not only demonstrated in SNS neurons of many insects (Klemm et al., 86; Luffy and Dorn; 91 Haeften et al., 93), but was also shown to inhibit gut contraction (Haeften et al., 93). The potential signicance in allatoregulation by serotonin-immunoreactive cells in the bridge connecting the corpora allata of the larval honey bee (Boleli et al., 95) received further support by our nding that the cardiostomatogastric nerves contact the retrocerebral complex in this region. To summarize, the larval and pupal honey bee SNS is anatomically linked to the brain, retrocerebral endocrine system, and foregut by several nerves and nervous connections. Axonal tracing and neuronal mapping carried out in other insect species disclosed complex neuronal pathways within the insect SNS and the systems it is connected with (Gundel and Penzlin, 78; Jagota and Habibulla, 92). Based on the anatomical details of the larval honey bee SNS presented in this study, it should now be feasible to determine the role of this nervous system in the honey bee as well, particularly its role in the fascinating process of caste differentiation.
ACKNOWLEDGMENTS

The authors are grateful to Prof. Dr. E. Laicine for providing access to the electron microscopy laboratory of the Faculty of Medicine, Ribeirao Preto. Special thanks are due to Horst Schoppmann, Zoological Institute in Tubingen. Maria D.S. Ferreira and Jose A. Maulin, Faculty of Medicine of Ribeirao Preto, for expert technical assistence in SEM preparations. CAPES and DAAD nancially supported this study by a doctoral fellowship and a senior researcher fellowship.
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