Ultrastructural Study of Tergal and Posterior Sternal Glands in Prorhinotermes Simplex (Isoptera: Rhinotermitidae)
Total Page：16
File Type：pdf, Size：1020Kb
Eur. J. Entomol. 102: 81–88, 2005 ISSN 1210-5759 Ultrastructural study of tergal and posterior sternal glands in Prorhinotermes simplex (Isoptera: Rhinotermitidae) JAN ŠOBOTNÍK1, FRANTIŠEK WEYDA2, ROBERT HANUS1, 3* 1Institute of Organic Chemistry and Biochemistry, Flemingovo nám. 2, CZ-166 10 Praha 6, Czech Republic; e-mail: [email protected] 2Institute of Entomology, Branišovská 31, CZ-370 05 ýeské BudČjovice, Czech Republic; e-mail: [email protected] 3Department of Zoology, Charles University, Viniþná 7, CZ-128 44 Praha 2, Czech Republic Key words. Ultrastructure, tergal gland, posterior sternal gland, secretory cell class 2, termite, Isoptera, Rhinotermitidae, Prorhinotermes simplex, imagoes Abstract. In Prorhinotermes simplex, tergal glands are present on the last three tergites (from the 8th to the 10th) in imagoes of both sexes. In addition, males possess posterior sternal glands of the same structure on sternites 8 and 9. The tergal and the posterior sternal glands consist of four cell types: class 1 and class 2 secretory cells, and class 3 cells with corresponding canal cells. The cyto- plasm of class 1 cells contains smooth endoplasmic reticulum, elongated mitochondria and numerous microtubules. Apical parts of these cells are formed by dense and long microvilli with a central ductule. Class 2 cells contain predominantly lucent vacuoles (in females) or lipid droplets (in males). The structure of class 3 cells does not differ from class 3 cells found in other body par ts. INTRODUCTION Males of several primitive genera have developed the Abdominal glands with specific sexual function occur posterior sternal glands, which occur on sternites 6 to 9 in in almost all representatives of Isoptera and Blattodea Mastotermes darwiniensis, and 8 and 9 in Porotermes (Ampion & Quennedey, 1981; Grassé, 1982; Sreng, (Hagen), Stolotermes Hagen, and Prorhinotermes. In 1984; Quennedey et al., 2004), but evidence about their Mastotermes darwiniensis, they are present also in presence in Mantodea is missing. In termites, the fol- females on sternites 6 and 7. The tergal and the posterior lowing glands were described: sternal, posterior sternal sternal glands reveal a uniform structure (Ampion & and tergal glands (Noirot, 1969; Ampion & Quennedey, Quennedey, 1981). According to observations made on 1981; Grassé, 1982). The sternal glands produce pre- females of Cornitermes bequaerti Emerson, tergal glands dominantly trail pheromones although they secrete sexual are composed of class 1, 2 and 3 cells (Bordereau et al., pheromones in the imagoes of certain species. The tergal 2002). Tergal and posterior sternal glands of unique and the posterior sternal glands (if present) are involved structure were found on sternites 6 and 7 in females of in swarming, mate attraction and courtship behaviour Macrotermes annandalei (Silvestri), formed by class 3 (Noirot, 1969; Varma, 1980; Ampion & Quennedey, cells extending to subcuticular pouches (Quennedey et al., 1981; Pasteels & Bordereau, 1998; Quennedey et al., 2004). 2004; Peppuy et al., 2004). The only identified compound produced by the tergal The tergal glands in Isoptera are usually present on last glands in termites is (3Z, 6Z, 8E)-dodeca-3,6,8-trien-1-ol, two or three tergites, but they are secondarily reduced in acting in Cornitermes bequaerti as a sexual pheromone many taxa. In Mastotermes darwiniensis Froggatt, the (Bordereau et al., 2002). The same substance is produced most primitive termite, eight glands (from the 3rd to the by the sternal gland in a number of termite species as a 10th tergite) are present, considered a plesiomorphic trail pheromone and may also act as a sexual pheromone character (Ampion & Quennedey, 1981). The tergal but in higher concentrations (for a review see Pasteels & glands occur on posterior tergites in the number from 5 to Bordereau, 1998). 8 in the genus Macrotermes Holmgren as an apomorphy The function of the tergal glands has been described (Ampion & Quennedey, 1981; Quennedey et al., 2004). more precisely in cockroaches. Female glands produce The tergal glands are present in both sexes of primitive male attractants (Sreng, 1984; 1985), while those in males Isoptera, while only appearing in females in the advanced produce two successively active chemical signals: sexual families Rhinotermitidae and Termitidae (Ampion & pheromones for attracting females and an aphrodisiac Quennedey, 1981). The genus Prorhinotermes Silvestri is involved in mating (Sreng, 1984). Female cockroaches an exception to this rule, with the glands present in both are known to feed on male tergal gland secretions; male sexes and much larger in females (Ampion & Quennedey, specific proteins serving as food for females were 1981; Šobotník & Hubert, 2003). described in Leucophaea maderae (Fabricius) (Korchi et al., 1998; Cornette et al., 2001, 2002, 2003). * Corresponding author; e-mail: [email protected]. 81 Prorhinotermes is an exceptional genus among and posterior glands. Secretory cells class 1 and 2 are advanced termites because of many peculiar characters equally numerous while class 3 cells are less abundant. (for a review see Quennedey & Deligne, 1975; Štys & Secretory cell class 1 Šobotník, 1999). Among others, both sexes possess well These cells are columnar with extended apices and are developed tergal glands and posterior sternal glands are located predominantly close to the cuticle (Figs 2, 8). A only present in males. The aim of this paper is to describe few basal invaginations occur at the contact area between for the first time the fine structure of the tergal and the class 1 cells and the basement membrane. Nuclei are posterior sternal glands in swarming imagoes of both irregular, up to 12 µm in the largest dimension when flat. sexes. The cytoplasm contains a large amount of smooth MATERIAL AND METHODS endoplasmic reticulum (SER) (Figs 4, 10). It is formed by tubules about 35 nm thick. Smaller amounts of rough Imagoes of both sexes of Prorhinotermes simplex (Hagen, endoplasmic reticulum (RER) are scattered among SER 1858) originated from a colony collected by Dr. J. KĜeþek in (Fig. 4). Electron dense granules are frequently present in Soroa (Piñar del Rio, Cuba) in December 1964, and since then kept in the laboratory at 26 ± 1°C. the cytoplasm (Figs 9, 10), sometimes partially decom- Posterior dorsal parts (sternal in the case of the posterior posed into myelin figures (Fig. 9). Microvilli are dense sternal glands) of termite abdomens were fixed in a mixture of and their length varies from 1 to 4 µm. The diameter of a 2% glutaraldehyde and 2.5% formaldehyde (Polysciences, EM microvillus is about 110 nm. Microvilli are always Grade) in 0.1M phosphate buffer at laboratory temperature. equipped with a central ductule (about 40 nm in diameter; After washing in pure 0.1M phosphate buffer, tissues were post- Fig. 3). Microvilli are in direct contact with the cuticle fixed in 2% osmium tetroxide in the same buffer for 2 h, washed (Figs 2, 3, 9, 12, 15). The cytoplasm contains a moderate in bidistilled water and dehydrated in 50%, 75% and absolute amount of microtubules (Fig. 10) oriented predominantly ethanol. Subsequently tissues were embedded into Spurr resin apico-basally. Mitochondria are elongated (up to 2 µm (standard mixture). Semithin and ultrathin sections were made with a Reichert Ultracut ultramicrotome. Semithin sections were long and up to 0.5 µm thick) of a moderately dense stained with methylene blue and studied in an Axioskop Weiss matrix and flat cristae (Fig. 4). The basement membrane optical microscope (with Sony Cyber-shot digital camera). is formed by a single lamina (about 60 nm thick). Locally Ultrathin sections were stained with uranyl acetate and lead cit- it contains collagen fibres, then its thickness increases up rate (standard recipe) and studied in a Jeol 1010 transmission to 300 nm (see Fig. 16 for a similar situation in female). electron microscope. The cuticle overlying the glands reveals only a slight For the SEM study, living imagoes were placed into absolute modification. It is formed by an endocuticle (about 2 µm ethanol, dried by the critical point method, glued onto an alu- thick), an exocuticle (about 0.5 µm thick) and a thin epi- minium holder, sputter-coated with gold and observed in a Jeol cuticle (not shown). Inside the endo- and exocuticle there 6300 electron microscope. are enlarged pore canals (with a single pore canal fila- RESULTS ment), which contain fine particles of secretion (Fig. 3). The widest pore canals are in the endocuticle adjacent to Both sexes are usually equipped with three tergal exocuticle (not shown). glands situated in the anterior part of the 8th, the 9th and The connection between neighbouring cells is formed the 10th tergite. In addition, males possess two posterior by an apical desmosome followed by a long septate junc- sternal glands (on the 8th and the 9th sternite). A sur- tion (Fig. 10). Membranes are free only in the basal part. prising variability in the number of male glands occurs; in one male four tergal (on tergites 7 to 10) glands were Secretory cell class 2 observed (Fig. 1), in another one three posterior sternal Class 2 cells are oval in shape, situated among class 1 glands (on sternites 7 to 9) were found (Fig. 7). cells (Fig. 2). They do not reach the cuticle. The class 2 The surface of the cuticle covering the glands differs cells contact the basement membrane and possess from that on other body parts (based on SEM numerous shallow basal invaginations (about 0.5 µm observation). Small depressions of epicuticle are more deep). They are attached to the basement membrane by marked and numerous on the cuticle covering the glands several hemidesmosomes (Fig. 6). as well as the openings of the canals corresponding to Nuclei are rounded, situated centrally, usually about 7 class 3 cells (Fig. 14). These depressions do not corre- µm in the largest dimension. A relatively voluminous spond with the deeper structure of the cuticle.