Ontogenesis of pleuropodia in different species of Blattaria (Insecta): A comparative study

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Ontogenesis of pleuropodia in different species of Blattaria (Insecta): A comparative study a

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Simonetta Lambiase , Aldo Grigolo & Patrizia Morbini

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Dipartimento di Biologia Animale , Università di Pavia , Piazza Botta 9, Pavia, I‐27100, Italy b

Servizio di Anatomia Patologica ‐ IRCCS Policlinico S. Matteo , Viale Forlanini 14, Pavía, I‐27100, Italy Published online: 28 Jan 2009.

To cite this article: Simonetta Lambiase , Aldo Grigolo & Patrizia Morbini (2003) Ontogenesis of pleuropodia in different species of Blattaria (Insecta): A comparative study, Italian Journal of Zoology, 70:3, 205-212, DOI: 10.1080/11250000309356518 To link to this article: http://dx.doi.org/10.1080/11250000309356518

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Ital. J. Zool., 7ft 205-212 (2003)

Ontogenesis of pleuropodia in different species of Blattaria (Insecta): a comparative study SIMONETTA LAMBIASE ALDO GRIGOLO Dipartimento di Biologia Animale, Università di Pavia, Piazza Botta 9, I-27100 Pavia (Italy)

PATRIZIA MORBINI

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Servizio di Anatomia Patologica - IRCCS Policlinico S. Matteo, Viale Forlanini 14, I-27100 Pavía (Italy)

ABSTRACT The embryonic development of several insects is characterized by the formation of a pair of pleuropodial appendages on the first abdominal segment. The present paper describes the comparative ontogenesis, morphology, and structure of the pleuropodia of a few species of Blattaria belonging to their three differe/it families: Blattidae, Blattellidae, and Blaberidae. The pleuropodia appear when the first abdominal coelomic cavities begin to disintegrate; then they develop quickly, and regress when the dorsal closure of the embryo occurs. A slow process of degeneration leads, in some species, to the formation of a pair of small flaps; in others, the pleuropodial morphology is retained although the organ loses its secretory functions. In all species, the pleuropodia are cast off at embryonic eclosion, together with the first cuticle produced during an intraoothecal moult. The pleuropodia can be bulbiform, filiform, or caliciform. A relationship is suggested between pleuropodial morphology and the modality of reproduction of the cockroaches. In fact, the oviparous and most ancestral false ovoviviparous species have a bulbiform pleuropodium, while the phyletically younger false ovoviviparous and the false viviparous species have an elongated pleuropodium. Finally, the hypotheses so far proposed about the functions of these structures in Blattaria are discussed. KEY WORDS: Pleuropodia - Cockroaches - Embryology. ACKNOWLEDGEMENTS This research was supported by a grant from the Italian Ministero Istruzione Università e Ricerca. The Authors are grateful to Mr. C. Mottini for his technical assistance. (Received 23 December 2002 - Accepted 3 April 2003)

INTRODUCTION The pleuropodia (Rathke, 1844; Patten, 1884; Wheeler, 1890), a pair of embryonic organs that appear on the first abdominal segment, are clearly derived from an ancestral pair of abdominal limbs (Anderson, 1972). They have been identified in many taxa of insects (Grasse, 1977). So far, the pleuropodia of six species of Blattaria have been described. In this order of insects, the serial homology of pleuropodia with legs was evidenced by studies carried out on the "notched" sternite mutant (si) of Blattella germánica (Ross, 1986); therefore, the pleuropodia must be considered as modified abdominal legs. Other pleuropodia-like appendages, such as the adenopodia of the 9 th segment, showing a semi-evaginated morphology, may develop from the pleural surface of the Blattaria abdomen (Stay, 1976). Several functions have been tentatively proposed for insect pleuropodia, and circumstantial evidence on the functions of these organs in Blattaria has been published. The data collected by Engelmann (1957) provided strong proof that an enzymatic secretion is involved in nymph hatching; moreover, on the basis of Stay's data (1976), an osmoregulatory function between embryonic haemolymph and extra-embryonic fluids seems to be highly probable. In the present paper, we describe the ontogenesis, development, and degeneration of pleuropodia of six species of cockroaches from the following families and subfamilies, named according to the systematics proposed by Me Kittrick (1964): Blattidae (Blattinae), Blattellidae (Plectopterinae, Blattellinae) and Blaberidae (Pycnoscelinae, Oxyhaloinae). In addition, the morphology of pleuropodia in a further species of Blaberidae belonging to the Blaberinae subfamily is described. MATERIALS AND METHODS The experiments were carried out on the following species: Periplaneta americana (Linnaeus 1758), Blatta Orientalis Linnaeus 1758, Blattella germánica (Linnaeus 1767), Supella supellectilium (Serville 1839), Pycnoscelus surinamensis (Linnaeus 1767), Leucophaea maderae (Fabricius 1781), Naupboeta cinérea (Olivier 1789), Blaberus craniifer Burmeister 1838. The species belonging to the Blattidae (P. americana and B. orientalis) and to the Blattellidae {B. germánica and S. supellectilium) are oviparous, whereas those belonging to the Blaberidae (P. surinamensis, L. maderae, N. cinérea, and B. craniifer) are false ovoviviparous (Roth & Willis, 1958). Newly emerged females of the experimental species were isolated from the mass culture, reared in glass jars and after a week paired for breeding; the newly emerged adult females of P. surinamensis (a parthenogenetic population brought from Surinam to Pavia in 1938 by C. Jucci) were scored for oothecal extrusion. The day of extrusion of the oothecae was considered the first day of embryonic development in both the oviparous and false ovoviviparous species. The oothecae from oviparous species and females of false ovoviviparous species with oothecae were kept in a thermostat (28 °C, 80% r.h.). The insects were fed a mixture of fresh lettuce and bread crumbs, and received water ad libitum. The embryos were collected by opening the released oothecae starting from the keel, in the case of oviparous species, or gently

206 extracting the oothecae from the genital chamber from females previously anaesthetised with CO2> in the case of false ovoviviparous species. The embryonic stages of development were defined on the basis of their morphological features. The embryos were then mechanically dechorionated in Yeager (1939) solution and fixed in methanol, acetic acid (3:1) for embedding in methacrylate ester, or in glutaraldehyde for embedding in Epon. The sections, 5 urn or 2 pm thick, were stained with toluidine blue 0.1%. A few embryos with fully developed pleuropodia were stained in toto, after fixation, with basic fuchsin 0.1% to evidence the differential staining of these organs.

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RESULTS AND DISCUSSION The evaginated pleuropodium of Blattaria originates as a mammillary structure protruding into the amniotic sac, from the whole lateral surface of the first abdominal metamere, subsequent to formation of the relative coelomic cavity. Before their differentiation, the pleuropodial cells replicate with a high frequency, as do the ectodermal thoracic limb cells and, subsequently, the peripheral cells of the pleuropodial protrusion undergo a laminar shifting towards the apical region of the organ. At the end of the mitotic burst, the proximal region of the pleuropodium differentiates into a cuboidal monolayered epithelium, whereas the distal region gives rise to a simple columnar one. These processes of cellular differentiation lead to the formation of a cavity in communication with the haemocoele, inside which adipocytes and plasmatocytes, deriving from the coelomic disintegration, are observable. There are no myoblasts, which, in contrast, are identifiable in the thoracic limbs (Fig. 2C). Typical sticotropisms (Ruffini, 1925) prelude the differentiation and expansion of the distal regions and the complete morphological differentiation of pleuropodia. The morphology of the fully developed pleuropodia of a few observed species is shown in Figures 1, 3, and 5. The regression of this organ, which begins with the dehiscence of the amniotic sac, tends to be concluded before the dorsal closure of the embryo; the degenerative phenomena give rise to frequent karyorrhexes. Because the regressed pleuropodia are adherent to the exuvia deriving from the embryonic moult, they are cast off before or during embryo hatching and the new-

Fig. 1 - Blatta Orientalis: embryos in toto dated 10 (A) and 15 (B) days (x50). In (B) the embryo is stained with fuchsin. The caliciform region of the pleuropodium does not show staining. Abbreviations: a, amnion; d, deutoplasm; pi, pleuropodium.

S. LAMBÍASE, A. GRIGOIO, P. MORBINI

ly emerged nymphs do not present these structures, although cuticular marks, which disappear with the tanning processes, are evident at the sites where the pleuropodia had been. Pleuropodial shape varies considerably among the species of this order although all the pleuropodia have a basal part (stalk), which in some species dilates to form a calyx, followed by a polymorphic secretory region covered by a peculiar, thin, cuticular layer described by Stay (1976). This region can be bulbiform, filiform, or caliciform. In this respect, our data and the literature reports evidence a strong similarity in pleuropodial shape within the families of Blattidae and Blattellidae, which have bulbiform structures (Patten, 1884; Wheeler, 1890; Ross, 1986). Blaberidae, on the other hand, have profound morphological modifications of pleuropodia among the species of the different subfamilies (Hagan, 1939; Engelmann, 1957; Bullière, 1969, 1970; Ando, 1971; Aiouaz, 1974; Stay, 1976). In detail, filamentous pleuropodia seem to be specific to Diplopterinae, Oxyhaloinae, and Epilamprinae, more recent subfamilies than Blaberinae and Pycnoscelinae (Me Kittrick, 1964), which are characterized, respectively, by a caliciform and by a bulbiform pleuropodium. We have studied the sequences of pleuropodial ontogenesis in two species of Blattidae (subfamily Blattinae), B. orientalis (Figs 1-2) and P. americana, both exhibiting bulbiform pleuropodia. The first abdominal metamere, carrying the mammillary structure, elongates ventrally, as do the successive metameres, while mesoblasts surrounding the coelomic cavity differentiate. The amniotic sac is already formed. The pleuropodium differentiates rapidly into its stalk and the distal region; at this point of development, the epithelium of the stalk consists of monolayered cuboidal cells, while the bulb has highly polarized cells harbouring distally situated nuclei. Numerous mesoblasts penetrate the lumen of the stalk but no myoblasts are present; in contrast, myoblasts are clearly visible in the thoracic limbs. As the maturation of this organ becomes complete, the stalk tends to elongate: the epithelium transforms from cuboidal into squamous, partially surrounding the bulbar cells with a caliciform dilatation (Fig. 2). Adipocytes and haemocytes are now identifiable in the pleuropodial lumen. The fat body cells nearer the bulbar secretory ones show deutoplasmic inclusions different from those of the external fat bodies, because their intracellular space is homogeneously filled with a compact mass of hydrophobic substances. Towards the end of the ontogenic phases, the cells of the bulb show an inversion of tendency in cellular polarity, characterized by a nuclear migration into the luminal region of the cells (Fig. 3D-E). This stage is a prelude to the subsequent degeneration of most cells. In this period of ontogenesis, the amniotic and serosal membranes, the amniotic sac being dehiscent, are pulling towards the cephalic pole of the embryo. The degenerative processes of the pleuropodia initially give rise to a deep modi-

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PLEUROPODIA IN BLATTARIA

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