Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-30T23:33:59.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Observations on the functional organization of the ovarian balls of Moniliformis and Polymorphus (Acanthocephala)

Published online by Cambridge University Press:  06 April 2009

D. W. T. Crompton  and
P. J. Whitfield
D. W. T. Crompton
Affiliation:
The Molteno Institute, University of Cambridge
P. J. Whitfield
Affiliation:
Department of Zoology, King's College, University of London
Get access Rights & Permissions [Opens in a new window]

Extract

By a variety of microscopical techniques, an initial survey has been made of the functional organization of ovarian balls from mature, inseminated female Moniliformis dubius and Polymorphus minutus. On the basis of evidence from observations made with the transmission electron microscope, we have concluded that the ovarian ball consists of three components; these are two separate, multinucleate syncytia and a cellular zone. The inner region is considered to be an oogonial syncytium from which the germ-line cells arise to form the cellular zone. The oogonial syncytium and the cellular elements are embedded in a supporting syncytium which also forms the boundary of the ovarian ball. Details of the ultrastructure of these components, observations on fertilization and a hypothesis to account for the main events occurring in an acanthocephalan ovarian ball are also presented.

Acanthocephalans are dioecious parasites which become sexually mature in the alimentary tract of vertebrates. After insemination, individual female worms begin to release embryonated eggs at rates which have been estimated to vary, on average, from 2000 per day in the case of Polymorphus minutus (Crompton & Whitfield, 1968) to 260000 per day in the case of Macracanthorhynchus hirudinaceus (Kates, 1944). Irrespective, however, of the species of acanthocephalan and the number of eggs produced, a most interesting mode of ovarian development and multiplication is believed to exist (see Bullock, 1969). Within the female worm, the primordial ovarian tissue gives rise to separate ovaries which are often termed ovarian balls. These in turn give rise to more ovarian balls and the process continues until large numbers have been formed. The ovarian balls of a mature female have no permanent attachment to the tissues of the worm. They are contained in the fluid of the body cavity either freely, or loosely constrained in large membranous chambers known as ligament sacs.

Few investigations have been made into the structure and cytology of the ovarian balls of the Acanthocephala. Early observations on the histology of the germ-line constituents of ovarian balls were made by Hamann (1891), Kaiser (1893) and Meyer (1928), each of whom suggested that some of the developing oogonial stages were arranged in a syncytial manner. In a study of the embryology of P. minutus. Nicholas & Hynes (1963) interpreted preparations of ovarian balls, which had been subjected to the Feulgen reaction, as indicative of syncytial tissue in the central region of the ball. They also recorded their uncertainty about whether an ovarian ball has a bounding membrane or not. More recently, Robinson (1964, 1965) described mitotic and meiotic divisions in oogonia and oocytes from ovarian balls of Mac. hirudinaceus and Moniliformis dubius and Stranack (1972) included an electron micrograph of part of an ovarian ball of Pomphorhynchus laevis in a description of the nature of the egg envelopes of that species. In this paper, we present a general survey, based largely on evidence obtained with the electron microscope, of the functional organization of the ovarian balls of mature M. dubius and P. minutus.

Type
Research Article
Information
Parasitology , Volume 69 , Issue 3 , December 1974 , pp. 429 - 443
Copyright
Copyright © Cambridge University Press 1974

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Austin, C. R. (1965). Fertilization. Englewood Cliffs, New Jersey: Prentice-Hall, Inc.Google Scholar
Bullock, W. L. (1969). Morphological features as tools and pitfalls in acanthocephalan systematics. In Problems in Systematics of Parasites (ed. Schmidt, G. D.). Baltimore, Maryland, U.S.A. and Manchester, England: University Park Press.Google Scholar
Burton, P. R. (1967). Fine structure of the reproductive system of a frog lung fluke. II. Penetration of ovum by a spermatozoon. Journal of Parasitology 53, 994–9.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. (1970). An Ecological Approach to Acanthocephalan Physiology. Cambridge University Press.Google Scholar
Crompton, D. W. T. (1974). Experiments on insemination in Moniliformis dubius (Acanthocephala). Parasitology 68, 229–38.CrossRefGoogle ScholarPubMed
Crompton, D. W. T., Arnold, S. & Barnard, D. (1972). The patent period and production of eggs of Moniliformis dubius (Acanthocephala) in the small intestine of male rats. International Journal of Parasitology 2, 319–26.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. & Walters, D. E. (1972). An analysis of the course of infection of Moniliformis dubius (Acanthocephala) in rats. Parasitology 64, 517–23.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. & Whitfield, P. J. (1968). The course of infection and egg production of Polymorphus minutus (Acanthocephala) in domestic ducks. Parasitology 58, 231–46.CrossRefGoogle ScholarPubMed
Foor, W. E. (1967). Ultrastructural aspects of oocyte development and shell formation in Ascaris lumbricoides. Journal of Parasitology 53, 1245–61.CrossRefGoogle ScholarPubMed
Foor, W. E. (1968 a). Zygote formation in Ascaris lumbricoides (Nematoda). Journal of Cell Biology 39, 119–34.CrossRefGoogle ScholarPubMed
Foor, W. E. (1968 b). Cytoplasmic bridges in the ovary of Ascaris lumbricoides. Bulletin of the Tulane University Medical Faculty 27, 23–30.Google Scholar
Franklin, L. E. (1970). Fertilization and the role of the acrosome in non-mammals. Biology of Reproduction 2 (Suppl), 159–76.CrossRefGoogle ScholarPubMed
Golvan, Y.J. (1958). Le phylum des Acanthocephala. I. Sa place dans l'échelle zoologique. Annales de Parasitologie humaine et comparée 33, 538–602.Google Scholar
Goodey, J. B. (1957). Laboratory methods for work with plant and soil nematodes. Technical Bulletin of the Ministry of Agriculture, Fisheries and Food, no. 2. London: H.M.S.O.Google Scholar
Hamann, O. (1891). Monographie der Acanthocephalan (Echinorhynchen). Jenaische Zeitschrift für Naturwissenschaft 25, 113–232.Google Scholar
Hyman, L. H. (1951). The Invertebrates, vol. 3. New York, Toronto and London: McGraw-Hill Book Co. Inc.Google Scholar
Jessen, H., Behnke, O., Wingstrand, K. G. & Rostgaard, J. (1973). Actin-like filaments in the acrosomal apparatus of spermatozoa of a sea urchin. Experimental Cell Research 80, 47–54.CrossRefGoogle ScholarPubMed
Kaiser, J. E. (1893). Die Acanthocephalen und ihre Entwicklung. Bibliotheca Zoologica 11, Heft 7.Google Scholar
Kates, K. C. (1944). Some observations on experimental infections of pigs with the thornheaded worm, Macracanthorhynchus hirudinaceus. American Journal of Veterinary Research 5, 166–72.Google Scholar
Meyer, A. (1928). Die Furchung nebst Eibildung, Reifung und Befruchtung des Gigantorhynchus gigas. Ein Beitrag zur Morphologie der Acanthocephalen. Zoologische Jahrbucher. Anatomie und Ontogenie der Tiere 50, 117–218.Google Scholar
Meyer, A. (1933). Acanthocephala. Bronn's Klassen und Ordnungen des Tierreichs 4. Leipzig.Google Scholar
Meyer, A. (1936). Die plasmodiale Entwicklung und Formbildung des Reisenkratzers (Macracanthorhynchus hirudinaceus (Pallas)). I. Teil. Zoologische Jahrbucher. Anatomie und Ontogenie der Tiere 62, 111–72.Google Scholar
Nicholas, W. L. & Hynes, H. B. N. (1963). The embryology of Polymorphus minutus (Acanthocephala). Proceedings of the Zoological Society of London 141, 791–801.CrossRefGoogle Scholar
Pantin, C. F. A. (1964). Notes on Microscopical Technique for Zoologists. Cambridge University Press.Google Scholar
Phillips, D. M. (1970). Insect sperm: their structure and morphogenesis. Journal of Cell Biology 44, 243–77.CrossRefGoogle ScholarPubMed
Remane, A. (1963). The systematic position and phylogeny of the pseudocoelomates. In The Lower Metazoa (ed. Dougherty, E. C., Brown, Z. N., Hanson, E. D. and Hartmann, W. D.). University of California Press.Google Scholar
Robinson, E. S. (1964). Chromosome morphology and behaviour in Macracanthorhynchus hirudinaceus. Journal of Parasitology 50, 694–7.CrossRefGoogle ScholarPubMed
Robinson, E. S. (1965). The chromosomes of Moniliformis dubius (Acanthocephala). Journal of Parasitology 51, 430–2.CrossRefGoogle ScholarPubMed
Stranack, F. R. (1972). The fine structure of the acanthor shell of Pomphorhynchus laevis (Acanthocephala). Parasitology 64, 187–90.CrossRefGoogle ScholarPubMed
Whitfield, P. J. (1971 a). Spermiogenesis and spermatozoan ultrastructure in Polymorphus minutus (Acanthocephala). Parasitology 62, 415–30.CrossRefGoogle Scholar
Whitfield, P. J. (1971 b). Phylogenetic affinities of Acanthocephala: an assessment of ultrastructural evidence. Parasitology 63, 49–58.CrossRefGoogle Scholar
Whitfield, P. J. (1973). The egg envelopes of Polymorphus minutus (Acanthocephala). Parasitology 66, 387–403.CrossRefGoogle ScholarPubMed