Soft Scale Insects - Their Biology, Natural Enemies and Control
Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.
18.104.22.168 Embryonic Development; Oviparity and Viviparity ERMENEGILDO TREMBLAY
EMBRYONIC DEVELOPMENT The mature oocyte in members of the family Coccidae is very similar to that noted in the Diaspididae (Koteja, 1990). Indeed, even the so-called "Krassilstschick cell', which was considered to be typical of the pedicel of diaspidid ovarioles, has also now been shown to be present in the Coccidae. The spermathecae are usually well developed (De Marzo et al., 1990) and, in Sphaerolecanium prunastri (Fonscolombe), were found to contain sperm bundles and free spermatozoa (Tremblay, 1961). Oogenesis, the production of polar bodies and fertilization were also studied in this species and were found not to differ from those known for diaspidoids. The first synchronic and asynchronic divisions of the zygotic nucleus and its derivatives (cleavage nuclei) lead to the formation of the blastoderm and vitelline or yolk nuclei (Fig. 22.214.171.124.1,A). The latter are cleavage nuclei, which are surrounded by a dense cytoplasm, and which remain in the yolk mass when the cleavage nuclei migrate towards the periphery of the egg to give rise to the blastoderm. At the same time, some cells at the posterior egg pole tend to form a group rather than arranging themselves in the single blastoderm layer. These cells are the first "germ cells" which appear in coccids (as in the diaspidids) at the posterior egg pole when the invagination, which gives rise to the embryo, starts. Once the germ cells, i.e. the primordial gonads, have appeared, they show some peculiar characters which allow them to be easily distinguished from blastoderm cells. In species of Pulvinaria, Saissetia, Coccus and Parthenolecanium, Teodoro (1916, 1921) observed the first germ cells as round cells with a chromatin-rich nucleus in the caudal tract of the invaginating germ band, although in S. prunastri, Tremblay (1961) observed them in the early blastoderm stage, even before the start of polar proliferation which precedes the invagination process, when they appeared as larger and less chromophilous cells than the blastoderm cells. This dissimilarity between the observations of Teodoro and Tremblay in the apparent structure of the germ cells is probably due to the different histological procedures; this may also account for the difference in the time of their detection in early embryos. Circumstantial evidence, however, is in favour of their very precocious appearance, which should closely coincide with blastoderm formation. The differentiation of the germ band, which leads to the first appearance of the embryo proper and of the amnion and superficial extraembryonic envelope (serosa), starts with a cellular proliferation which takes place in the blastoderm wall, located at the posterior egg pole. This proliferation produces a polycellular layer which corresponds to the wellknown "ventral plate" of the classical embryonic scheme, whose name is indicative of its typical ventral position. This original position is found in margarodids (e.g., Icerya
Section 126.96.36.199 references, p. 260
spp.) and diaspidoids (e.g., species of Quadraspidiotus and Pseudaulacaspis) but not in those Coccidae so far examined, in which the cellular proliferation starts in a position clearly polar (Fig. 188.8.131.52.1, B,C). The invagination process (anatrepsis) which follows proceeds towards the anterior egg pole and produces the usual bilayered band (Fig. 184.108.40.206.1,D).
Fig. 220.127.116.11.1. A - T h e blastoderm stage ofPulvinaria v/t/s (L.): b, blastoderm; y, yolk; vu, vitelline nuclei. B, C - Two consecutive stages of the invagination process in P. v/t/s, leading to the formation of the germ band. D - An early embryo of Saissetia oleae (Olivier): a, amnion; g, germ band: s, serosa. E - An embryo of Coccus hesperidum L. showing the amniotic cavity (ar in which sections of antennal, buccal and locomotory rudiments are visible. In none of the sections shown in this figure are germ cells represented (atier Teodoro, 1916, 1921).
At first, the two cellular layers of this invagination appear identical in histological sections, but they quickly evolve into a thicker layer (the germ band) and a thinner layer (the amnion). The distinction between the two layers becomes more evident as the invagination proceeds because, in contrast to the active proliferation of the cells of the germ band, the amniotic cells rapidly become flattened due to their less intensive division. The same flattening process occurs in the superficial extraembryonic
Embryonic development; oviparity and viviparity
blastoderm which, thus, evolves into the outer serosal membrane enveloping the yolk, surrounded by its vitelline membrane and the invaginating band. The germ band represents the early embryo (Fig. 18.104.22.168.1,E), which is thus formed with its cephalic parts downwards or, in other words, emerging from the polar blastoderm, and with its abdominal region directed towards the anterior egg pole. As anatrepsis proceeds, the embryo undergoes a torsion which is typical of all Coccoidea and which makes it difficult to obtain a complete view in histological sections as compared with complete preparations. With the evolution of the germ band into the segmented embryo and of the amnion as an internal membrane facing its ventral side, the thin fissure separating the two original layers becomes the amniotic cavity. The first description of the differentiation of the mesoderm as a thin layer all along the germ band was given by Teodoro (1916) for Pulvinaria vitis (L.). The mesoderm layer is produced when anatrepsis has completed the first curve, soon after the germ band has reached the anterior egg pole. In sections, it rapidly looses its linear aspect and evolves into a dozen groups or masses of cells, as in other insects. At this stage, groups of degenerating nuclei, named "paracytes", were described by Strindberg (1919) in front of the invaginating germ band before it reached the anterior egg pole. The cells to which these nuclei belonged were considered to be derivatives of the amniotic layer but no suggestions were made as to their significance. Anatrepsis finishes with the formation of segments and appendages (metamerization) and the appearance of stomodeal and proctodeal invaginations. This stage is then followed by katatrepsis, i.e. in which the growth of the embryo rapidly changes direction, with its cephalic parts moving towards the anterior egg pole. In this def'mitive position, the ventral side of the embryo with its appendages comes into contact with the chorion, while the dorsal region becomes exposed to the yolk mass. This process is interpreted as an embryonic movement which facilitates the embryogenesis of internal tissues and organs. The studies referred to above were all done prior to the 1960's and since then there has been no further research on soft scale embryogeny and further work in this field is urgently neeAed.
OVIPARITY AND VIVIPARITY
There has been much discussion with regard to the definition of ovoviviparity versus oviparity and viviparity. Koteja (1990) mentions the rather lengthy report by Hagan (1951) on the 19th-century controversy as to whether Coccus hesperidum L. is oviparous or viviparous. In the opinion of the present author, this controversy has been caused by inadequate evaluations as to whether the egg shell (chorion) was present or absent. In fact, the delicate membrane which envelopes the nymphs of some ovoviviparous species when they emerge from the vulva orifice has often been considered an amniotic membrane or even a possible derivative of the serosa (Koteja, 1990). It is here agreeA with Koteja that this thin involucre is not of amniotic origin, since the amnion disappears during early embryogenesis. On the other hand, it is not here accepted that this membrane could be a serosal derivative or some other structure different from a true chorion. On the basis of what is known in other animals, it appears that only in viviparous insects will the chorion be totally lacking as a result of changes associated with this reproductive adaptation. This complete loss happens both when adenotrophic structures have evolved for the nourishment of the embryo and when they are absent (e.g., in viviparous aphids). In contrast, the chorion is always present in oviparous animals, where there is a continuous range of structure, from a robust egg shell to a delicate chorionic membrane. This view, therefore, considers that ovoviviparity is a
Section 22.214.171.124 references, p. 260
form of oviparity because, even when nymphs emerge from the vulva orifice by their own means, the empty egg envelopes remain in the maternal oviduct. In some cases even environmental conditions can induce oviparous females to retain their eggs in the oviduct and thus to shift toward ovoviviparity. In the genus Coccus, the eggs laid by C. pseudomagnoliarum (Kuwana) can hatch after only a few hours but may take up to 3 days (Quayle, 1915; Barbagallo, 1970), while the nymphs of Coccus hesperidum hatch at most 4 hours (usually 2-5 minutes) after deposition (Annecke, 1966). In this latter species, naked nymphs have been seen emerging from the vulva orifice but thin egg shells have been shown to remain in the female genital tract (see Hagan, 1951, for a synthesis of old data). Saakyan-Baranova (1964) reported that the slightest mechanical damage to the eggs, such as by dissecting the sexually mature females of C. hesperidum, caused the egg shells (improperly defined as ovisac by Saakyan-Baranova, 1964) to peel off caudally, leaving the nymph bare. Other known cases of "crawler producing" females in coccids have been reported for two species of Toumeyella, namely T. pinicola Ferris (Kattoulas and Koehler, 1965) and T. liriodendri (Gmelin) (Bums and Douley, 1970), both of which are oviparous but in which this is as close to ovoviviparity as in Coccus hesperidum. In Coccoidea in general, it seems that freshly laid eggs of oviparous species always contain at least a germ band. In this sense, all scale insects are oviparous but with a tendency towards ovoviviparity. Further work, however, is needed to confirm this assumption.
REFERENCES Annecke, D.P., 1966. Biologicalstudies on the immature stages of the soft brown scale, Coccushesperidum Linnaeus (Homoptera Coccidae). South African Journal of Agricultural Science, 9: 205- 228. Barbagallo, S., 1970. Notizie sulla presnza in Sicilia di una nuova Cocciniglia degli agrumi, Coccus pseudomagnoliarum (Kuwana). Entomologica, 10: 121-139. Burns, D.P. and Douley, D.E., 1970. Biology of the tulip tree Scale, Toumeyella liriodendri Gmel. (Homoptera). Annals of the Entomological Society of America, 63: 228-235. De Matzo, L., Romano, V. and Tranfaglia, A., 1990. Types of the female reproductive system in some scale insects (Homoptera: Coccoidea). Proceedingsof the VI InternationalSymposium of Scale linsects Studies, Krakow, Poland, August 1990, 2: 41-46. Hagan, H.R., 1951. Embryology of Viviparous Insects. Ronald Press, New York, 472 pp. Kattoulas, M.E. and Koehler, C.S., 1965. Studies on the biology of the irregular pine scale, Toumeyella pinicola Fen'is. Journal of Economic Entomology, 58: 727-730. Koteja, J., 1990. Embryonic development, ovipary and vivipary. In: D. Rosen (Editor), Armored Scale Insects their Biology, Natural Enemies and Control. Elsevier, Amsterdam, pp. 233- 242. Quayle, H.J., 1915. The citricola scale. University of California Agricultural Experiment Station Bulletin 255: 405-421. Saakyan-Baranova, A.A., 1964. On the biology of the soR scale Coccus hesperidum L. (Homoptera Coccoidea). EntomologicalReview, 43: 135-147. Strindberg, H., 1919. Zur Entwicklungsgeschichte der oviparen Cocciden. Zoologischer Anzeiger 50:113-139. Teodoro, G., 1916. Osservazioni sulla ecologia delle Cocciniglie con speciale riguardo alia morfologia e alia fisiologia di questi insetti. Redia, 11: 129-209. Teodoro, G., 1921. Sulla embriologia delle Cocciniglie. Redia, 14: 137-141. Tremblay, E., 1961. Osservazionisulla cariologia e sulla simbiosi endocellularedi alcuni Coccini. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 19: 215-260.