Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T06:16:45.697Z Has data issue: false hasContentIssue false
  • English
  • Français

Recent advances in our understanding of pentastomid reproductive biology

Published online by Cambridge University Press:  06 April 2009

J. Riley
J. Riley
Affiliation:
Department of Biological Sciences, The University, Dundee DD1 4HN, Scotland
Get access Rights & Permissions [Opens in a new window]

Summary

Pentastomids are arthropod parasites which attain maturity in the respiratory tracts of vertebrates. All pentastomids exhibit an obvious sexual dimorphism in that fully mature females are invariably much bigger than males. Unusually though, copulation, which happens only once in the lifetime of females, occurs when both sexes are approximately the same size and the uterus of the female is undeveloped. This is because sperm is stored in spermathecae which, being positioned at the junction of the oviduct and uterus, become more remote from the vagina as the uterus elongates during development. The provision of spermathecae for sperm storage allows oocytes, shed continuously from the ovary, to be fertilized from time to time. What renders this process quite remarkable, and possibly unique, is the extreme length of the patent period. In one species this can extend up to an estimated 10 years and is associated with an egg production of about 106 eggs/female/year. Spermathecal structure provides some clues as to how prolonged sperm storage and the continuous fertilization of oocytes is accomplished. The upper region of the access duct is a narrow, chitinized tube which tapers to as little as 3 μm diameter at the point of entry into the spermatheca. The chitinous (?) lining of the spermatheca is relatively impermeable and apparently functions to totally isolate sperm from external influences: stored sperm are arranged in bundles and whorls and remain totally quiescent and inactive during the storage period. The entire spermatheca is invested by muscle fibres, the contraction of which will express small numbers of sperms through the narrow access duct. These are then reactivated by secretions from the female reproductive tract: the extreme narrowness of the spermathecal duct provides the fine adjustment of the system. The narrowness of the duct also creates problems during the process of insemination, since sperm discharged directly into the female reproductive tract would be unlikely to find the spermatheca through such a structure. Accordingly, the male cirrus is much modified to directly penetrate the spermathecal duct during copulation. Sperms, stored in the male seminal vesicle, are apparently activated prior to sperm transfer, and swim along the cirrus to be guided directly into the spermathecal lumen. Some unusual variations on the normal pentastomid life-cycle are discussed.

Type
Research Article
Information
Parasitology , Volume 86 , Issue 4 , April 1983 , pp. 59 - 83
Copyright
Copyright © Cambridge University Press 1983

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

Ali, J. H. & Riley, J. (1983). Experimental life-cycle studies of Raillietiella gehyrae Bovien, 1927 and Raillietiella frenatus Ali, Riley & Self, 1981: pentastomid parasites of geckos utilizing insects as intermediate hosts. Parasitology 86, 147–60.CrossRefGoogle Scholar
Ali, J. H., Riley, J. & Self, J. T. (1981). A revision of the taxonomy of the blunt-hooked Raillietiella, pentastomid parasites of African, South East Asian and Indonesian lizards, with a description of a new species. Systematic Parasitology 3, 193–207.CrossRefGoogle Scholar
Ali, J. H., Riley, J. & Self, J. T. (1982 a). A description of a new species of Raillietiella (Pentastomida: Cephalobaenida) from Egyptian lizards with a reassessment of the taxonomic status of Raillietiella geckonis (Diesing, 1850) Sambon, 1910 and Raillietiella affinis Bovien, 1927. Systematic Parasitology 4, 169–80.CrossRefGoogle Scholar
Ali, J. H., Riley, J. & Self, J. T. (1982 b). Amphibians as definitive hosts for pentastomids: Raillietiella bufonis n.sp. from Bufo lemur in Puerto Rico and a reassessment of Raillietiella indica Gedoelst, 1921. Systematic Parasitology 4, 279–84.CrossRefGoogle Scholar
Ali, J. H., Riley, J. & Self, J. T. (1983). A revision of the taxonomy of Raillietiella boulengeri (Vaney & Sambon, 1910) Sambon, 1910, R. orientalis (Hett, 1915) Sambon, 1922 and R. agcoi Tubangui & Masiluñgan, 1956 (Pentastomida: Cephalobaenida). Systematic Parasitology (in the Press).Google Scholar
Banaja, A. A., James, J. L. & Riley, J. (1975). An experimental investigation of a direct life-cycle in Reighardia sternae (Diesing, 1864), a pentastomid parasite of the herring gull (Larus argentatus). Parasitology 71, 493–503.CrossRefGoogle ScholarPubMed
Banaja, A. A., James, J. L. & Riley, J. (1976). Some observations on egg production and autoreinfection of Reighardia sternae (Diesing, 1864), a pentastomid parasite of the herring gull. Parasitology 72, 81–91.CrossRefGoogle ScholarPubMed
Bonhag, P. F. & Wick, J. R.(1953). The functional anatomy of the male and female reproductive systems of the milkweed bug Oncopeltus fasciatus Dalls (Heteroptera: Lygaeidae). Journal of Morphology 93, 177–283.CrossRefGoogle Scholar
Blum, M. S. & Taber, S. (1965). Chemistry of the drone honey bee reproductive system III. Dehydrogenases in washed spermatozoa. Journal of Insect Physiology 11, 1489–1501.CrossRefGoogle Scholar
Cavalieri, F. (1970). Contribucion al conocimiento de Cephalobaena tetrapoda Heymons, 1922 (Linguatula: Cephalobaenida). Physis 30, 291–9.Google Scholar
Chabaud, A. G. & Choquet, M. T. (1954). Nymphes du pentastome Gigliolella (n.gen.) brumpti (Giglioli, 1922) chez un lemurien. Revista di Parassitologia 15, 331–6.Google Scholar
Chapman, R. F. (1969). The Insects, Structure and Function. English Universities Press.Google Scholar
Diamond, J. M. (1971). Standing gradient model of fluid transport in epithelia. Federation Proceedings of the Federation of the American Society of Experimental Biology 30, 6–13.Google ScholarPubMed
Deakins, D. E. (1973). Occurrence of encysted larval Raillietiella (Pentastomida) in an adult female. Transactions of the American Microscopical Society 92, 287–8.CrossRefGoogle Scholar
Doucet, J.(1965). Contribution a l'éetude anatomique, histologique et histoohemique des pentastomes (Pentastomida). Office de la Recherche Scientifique et Technique D'Outre Mer, Paris.Google Scholar
Esslinger, J. H. (1962 a). Morphology of the egg and larva of Porocephalus crotali (Pentastomida). Journal of Parasitology 48, 457–62.CrossRefGoogle ScholarPubMed
Esslinger, J. H. (1962 b). Development of Porocephalus crotali (Humboldt, 1808) (Pentastomida) in experimental intermediate hosts. Journal of Parasitology 48, 452–6.CrossRefGoogle Scholar
Esslinger, J. H. (1968). Morphology of the egg and larva of Raillietiella furcocerca (Pentastomida) from a Colombian snake (Clelia clelia). Journal of Parasitology 54, 411–16.CrossRefGoogle ScholarPubMed
Fain, A. (1961). Les pentastomides de l'Afrique centrale. Annates de Musée Royal de I'Afrique centrale, Series 8, 92, 1–115.Google Scholar
Fain, A. & Mortelmans, J. (1960). Observations sur le cycle évolutif de Sambonia lohrmanni chez le Varan. Preuve d'un développment direct chez les Pentastomida. Bulletin de la Classe des Sciences, Series 5, 46, 518–31.CrossRefGoogle Scholar
Fonseca, F. & Ruiz, J. M. (1956). Was ist eigentlich Pentastoma megastomum Diesing, 1836? (Porocephalida: Porocephalidae). Senckenbergiana Biologica 37, 469–85.Google Scholar
Gretillat, S. & Brygoo, E. R. (1959). Raillietiella chamaeleonis n.sp. première espèce de Cephalobaenidae (Pentastomida) signalée a Madagascar. Annals de Parasitologie Humaine et Comparée 34, 112–20.CrossRefGoogle Scholar
Giglioli, G. S. (1922). A new genus Alofia of the family Linguatulidae. An anatomical account of A. ginae. Journal of Tropical Medicine and Hygiene 25, 371–7.Google Scholar
Hett, M. L. (1915). On a new species of pentastomid from aN. African snake (Zamenis ravigieri). Quarterly Journal of Microscopical Science 61, 185–200.Google Scholar
Hett, M. L. (1924). On the family Linguatulidae. Proceedings of the Zoological Society of London 1924, 107–59.CrossRefGoogle Scholar
Heymons, R. (1935). Pentastomida. In Bronns Klassen und Ordnungen des Tierreiches, vol. 5. Leipzig.Google Scholar
Heymons, R. (1939). Beiträge zur Systematik der Pentastomiden II. Einige Bemerkenswerte Pentastomiden aus Lacertililiern. Zeitschrift für Parasitenkunde 10, 675–90.CrossRefGoogle Scholar
Heymons, R. (1940). Ueber die Lebenweise der in Krokodilen vorkommenden Pentastomida. Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin 1940, 253–63.Google Scholar
Hobmaier, A. & Hobmaier, M. (1940). On the life-cycle of Linguatula rhinaria. American Journal of Tropical Medicine 20, 199–210.Google Scholar
Hopps, H. C., Keegan, H. L., Price, D. L. & Self, J. T. (1971). Pentastomiasis. In Pathology of Protozoal and Helminthic Diseases ivith Clinical Correlation (ed. Marcial-Rojas, R. A.), pp. 970–89. Baltimore: Williams & Wilkins Co.Google Scholar
Keegan, H. L.(1943). Observations on the pentastomid Kiricephalus coarctatus (Diesing) Sambon, 1910. Transactions of the American Microscopical Society 62, 194–9.CrossRefGoogle Scholar
Lavoipierre, M. M. J. & Lavoipierre, M.(1965). The American cockroach Periplaneta americana as an intermediate host of the pentastomid Raillietiella hemidactyli. Medical Journal of Malaya 20, 72–3.Google Scholar
Lavoipierre, M. M. J. & Lavoipierre, M. (1966). An arthropod intermediate host of a pentastomid. Nature 210, 845–6.CrossRefGoogle ScholarPubMed
Lavoipierre, M. M. J. & Rajamanickam, C. (1973). Experimental studies on the life cycle of a lizard pentastomid. Journal of Medical Entomology 10, 301–2.CrossRefGoogle ScholarPubMed
Leuckart, R. (1860). Bau und Entwicklungeschichte der Pentastomen. Nach Untersuchungen besonders von Pent. tenoides und P. dendiculatum. G.F. Winter'sche Verlagshandlung 6, 160.Google Scholar
Lim, B. L. & Yong, H. S. (1977). Pentastomid infection in the house geckoes from Sarawak, Malaysia. Medical Journal of Malaya 32, 59–62.Google Scholar
Loher, W. (1960). The chemical acceleration of the maturation process and its hormonal control in the male desert locust. Proceedings of the Royal Society, B 153, 380–97.Google Scholar
Lohrmann, E. (1889). Untersuchungen über den anatomischen Bau der Pentastomen. Archiv. für Naturgeschichte 1, 303–37.Google Scholar
Ludwig, W. (1926). Untersuchungen über den Capulationsapparat der Baumwanzen. Zeitschrift für wissenschaftliche Zoologie 5, 291–380.Google Scholar
Mahon, J. (1954). A new species of Raillietiella, a pentastomid from the bearded lizard, Amphibolurus barbatus (Cuv.). Proceedings of the Zoological Society of London 124, 509–16.CrossRefGoogle Scholar
Noc, F. & Curasson, G. (1920). Contribution á l'étude de l'éevolution biologique de Porocephalus armillatus Wyman. Bulletin de la Société de Pathologie Exotique 13, 656–9.Google Scholar
Norrevang, A. (1972). Oogenesis in Pentastomida. Acta Zoologica, Stockholm 53, 57–72.CrossRefGoogle Scholar
Osche, G. (1963). Die systematische Stellung und Phylogenie der Pentastomida. Zeitschrift für Morphologie und Ökologie der Tiere 52, 487–596.CrossRefGoogle Scholar
Penn, G. H. (1942). The life-history of Porocephalus crotali, a parasite of the Louisiana muskrat. Journal of Parasitology 28, 277–83.CrossRefGoogle Scholar
Pillers, A. W. N. (1925). Linguatula serrata Frölich 1789 in the nasal cavity of a bull bitch. Veterinary Journal 81, 126–30.Google Scholar
Riley, J. (1972). Some observations of the life-cycle of Reighardia sternae Diesing,1864 (Pentastomida). Zeitschrift für Parasitenkunde 40, 49–59.CrossRefGoogle ScholarPubMed
Riley, J. (1973). A redescription of Reighardia sternae Diesing 1864 (Pentastomida: Cephalobaenida) with some observations on the glandular systems of pentastomids. Zeitschrift für Morphologie und Ökologie der Tiere 76, 243–59.CrossRefGoogle Scholar
Riley, J. (1981). An experimental investigation of the development of Porocephalus crotali (Pentastomida: Porocephalida) in the Western Diamondback Rattlesnake (Crotalus atrox). International Journal for Parasitology 11, 127–32.CrossRefGoogle Scholar
Riley, J. (1983 a). Accessory sex glands of pentastomids. In Reproductive Biology of Invertebrates, vol. 3 (ed. Adiyodi, K. G. and Adiyodi, R. G.). Wiley.Google Scholar
Riley, J. (1983 b). Sexual differentiation and behaviour of pentastomids. In Reproductive Biology of Invertebrates, vol. 5 (ed. Adiyodi, K. G. and Adiyodi, R. G.). Wiley.Google Scholar
Riley, J. (1983 c). The reproductive strategies of pentastomids. In Reprodutive Biology of Invertebrates, vol. 6 (ed. Adiyodi, K. G. and Adiyodi, R. G.). Wiley.Google Scholar
Riley, J., Banaja, A. A. & James, J. L.(1978). The phylogenetic relationships of the Pentastomida: the case for their inclusion within the Crustacea. International Journal for Parasitology 8, 245–54.CrossRefGoogle Scholar
Riley, J., James, J. L. & Banaja, A. A. (1979). The possible role of the frontal and sub-parietal gland systems of the pentastomid Reighardia sternae (Diesing, 1864) in the evasion of the host immune response. Parasitology 78, 53–66.CrossRefGoogle ScholarPubMed
Riley, J. & Self, J. T. (1979). On the systematics of the entastomid genus Porocephalus (Humboldt, 1811) with descriptions of two new species. Systematic Parasitology 1, 25–42.CrossRefGoogle Scholar
Riley, J. & Self, J. T. (1980). On the systematics and life-cycle of the pentastomid genus Kiricephalus Sambon, 1922 with descriptions of three new species. Systematic Parasitology 1, 127–40.CrossRefGoogle Scholar
Riley, J. & Self, J. T. (1981 a). A redescription of Waddycephalus teretiusculus (Baird, 1862) Sambon, 1922 and a revision of the taxonomy of the genus Waddycephalus (Sambon, 1922), pentastomid parasites of Asian, Australian and Indonesian snakes, with descriptions of eight new species. Systematic Parasitology 3, 243–57.CrossRefGoogle Scholar
Riley, J. & Self, J. T. (1981 b). Some observations on the taxonomy and systematics of the pentastomid genus Armillifer (Sambon, 1922) in South East Asian and Australian snakes. Systematic Parasitology 2, 171–9.CrossRefGoogle Scholar
Riley, J. & Self, J. T. (1982). A revision of the pentastomid genus Parasambonia Stunkard & Gandal, 1968: a new character, a description of the male and a new species. Systematic Parasitology 4, 125–33.CrossRefGoogle Scholar
Rodhain, J. & Vuylsteke, C. (1932). Contribution a l'étude des porocephales des crocodiles africains. Revue de Zoologie et de Botanique Africaines 23, 1–11.Google Scholar
Salazar, N. P. (1964). A newly reported arthropod parasite in the lungs and body cavity of some Philippine snakes. Philippine Journal of Science 93, 171–8.Google Scholar
Sambon, L. W. (1922). A synopsis of the family Linguatulidae. Journal of Tropical Medicine and Hygiene 25, 188–206.Google Scholar
Sambon, L. W. (1922). A synopsis of the family Linguatulidae. Journal of Tropical Medicine and Hygiene 25, 391–428.Google Scholar
Self, J. T.(1969). Biological relationships of the Pentastomida; a bibliography on the Pentastomida. Experimental Parasitology 24, 63–119.CrossRefGoogle ScholarPubMed
Spencer, W. B. (1892). The anatomy of Pentastomum teretiusculum (Baird). Quarterly Journal of Microscopical Science 34, 1–73.Google Scholar
Stiles, C. W. (1891). Bau und Entwicklungsgeschichte von Pentastomum proboscideum Rud. und Pentastomum subcylindricum Dies. Zeitschrift für wissenschaftlich Zoologie 52, 85–157.Google Scholar
Storch, V. & Bockeler, W. (1979). Electron microscope observations on the sensilla of the pentastomid Reighardia sternae (Diesing, 1864). Zeitschrift für Parasitenkunde 60, 77–86.CrossRefGoogle Scholar
Taber, S. & Blum, M. S. (1960). Preservation of honey bee semen. Science 131, 1734–5.CrossRefGoogle ScholarPubMed
Vargas, M. V. (1971). Hallazgo de Subtriquetra subtriquetra Sambon, 1922 (Pentastomida) en Costa Rica y su redescripción. Revista Latinoamericana de Microbiologica 13, 137–46.Google Scholar
Vargas, M. V. (1974). The biology and taxonomy of Sebekia and Subtriquetra. Proceedings of the Third International Congress of Parasitology, Munich 2, 1021.Google Scholar
Vargas, M. V. (1975). Description del huevecillo, larva y ninfa de Subtriquetra subtriquetra Sambon, 1922 (Pentastomida) y algunas observaciones sobre su ciolo de vida. Revista de Biologie Tropicale 23, 67–75.Google Scholar
von Haffner, K. (1922). Beiträge zur Kenntnis der Linguatuliden. I. Ovarium und Eibildung von Porocephalus armillatus (Wyman). Zoologischer Anzeiger 54, 162–70.Google Scholar
von Haffner, K. (1924). Beiträge zur kenntnis der Linguatuliden. III. Ueber den Hoden und die Spermatocystenbildung von Porocephalus moniliformis. Zoologischer Anzeiger 58, 285–90.Google Scholar
von Haffner, K. & Rack, G. (1965). Neues über die Entwicklung der Pentastomide Reighardia sternae (Diesing, 1864). Zoologische Jahrbücher, Abteilung für Anatomie, Ontogenie der Tiere 72, 419–44.Google Scholar
von Haffner, K., Rack, G. & Sachs, R. (1969). Verschiedene Vertreter der Familie Linguatuliadae (Pentastomida) als Parasiten von Säugetier en der Serengeti (Anatomie, Systematik, Biologie). Mitteilungen aus dent Hamburg Zoologischen Museum Institut 66, 93–144.Google Scholar
Whitfield, P. J. (1970). The egg sorting function of the uterine bell of Polymorphus minutus (Acanthocephala). Parasitology 61, 111–26.CrossRefGoogle Scholar
Wigglesworth, V. B. (1972). The Principles of Insect Physiology. London: Chapman and Hall.CrossRefGoogle Scholar
Wingstrand, K. G. (1972). Comparative spermatology of a pent&stomid Raillietiella hemidactyli and a branchiuran crustacean Argulus foliaceus with a discussion of pentastomid relationships. Biologiske Skrifter 19, 1–72.Google Scholar