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The life cycle of Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Palaeacanthocephala: Rhadinorhynchidae) in amphipod and fish hosts from the Red Sea

Published online by Cambridge University Press:  25 February 2014

M.O. Al-Jahdali*
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh21911, Saudi Arabia
R.M. El-Said Hassanine
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh21911, Saudi Arabia
H. El-S. Touliabah
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh21911, Saudi Arabia

Abstract

The rhadinorhynchid Sclerocollum saudii Al-Jahdali, 2010 was found in the intestine of its type host, Siganusrivulatus Forsskål & Niebuhr, 1775, a siganid fish permanently resident in a lagoon within the mangrove swamps found on the Egyptian coast of the Gulf of Aqaba (between 28°7′N and 28°18′N). Larval forms of this acanthocephalan (acanthors, acanthellae and cystacanths) were only found in Megaluropus agilis Hoek, 1889 (Crustacea: Gammaridae), a benthic amphipod abundant on algae and seagrasses in the lagoon. So, this life cycle of S. saudii was elucidated under semi-natural conditions: embryonated eggs of S. saudii were directly ingested by the amphipod and hatched in its intestine; the released acanthor penetrated the intestinal epithelium in 12–18 h to reach the connective tissue serosa, where it remained for about 3 days, then penetrated the intestinal wall and remained attached to its outer surface for 4 days. It then detached and dropped free in the amphipod haemocoel and transformed into an oval acanthella, growing for 16 days to reach the cystacanth stage. The cystacanth at 46 days post-infection was infective to fish (excysted in its intestine as an active juvenile). Male and female juveniles reached maturity 17 and 23 days post-infection. Recently copulated females first appeared 26 days post-infection and all females seemed to be copulated at 28 days post-infection; partially and fully gravid females first appeared 31 and 35 days post-infection. Mature males and fully gravid females started to die off naturally 31 and 43 days post-infection and were totally expelled from the fish intestine by 42 and 52 days post-infection. The cycle was completed in 89 days and is similar to other known palaeacanthocephalan life cycles, but has its own characteristics.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Abele, L.G. & Gilchrist, S. (1977) Homosexual rape and sexual selection in acanthocephalan worms. Science 197, 8183.CrossRefGoogle ScholarPubMed
Al-Jahdali, M.O. (2010) Helminth parasites from Red Sea fishes: Neowardula brayi gen. nov. sp. nov. (Trematoda: Mesometridae Poche, 1926) and Sclerocollum saudii sp. nov. (Acanthocephala: Cavisomidae Meyer, 1932). Zootaxa 2681, 5765.CrossRefGoogle Scholar
Al-Jahdali, M.O. & Hassanine, R.M. (2012) Infrapopulations of Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Cavisomidae) in the rabbitfish Siganus rivulatus (Teleostei, Siganidae) from the Saudi coast of the Red Sea. Journal of Helminthology 86, 8594.CrossRefGoogle ScholarPubMed
Amin, O.M. (1982) Description of larval Acanthocephalus parksidei Amin, 1975 (Acanthocephala: Echinorhynchidae) from its isopod intermediate host. Proceedings of the Helminthological Society of Washington 49, 235245.Google Scholar
Amin, O.M. (1987) Acanthocephala from lake fishes in Wisconsin: ecology and host relationships of Pomphorhynchus bulbocolli (Pomphorhynchidae). Journal of Parasitology 73, 278289.CrossRefGoogle ScholarPubMed
Amin, O.M. (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273305.CrossRefGoogle ScholarPubMed
Amin, O.M., Burns, L.A. & Redlin, M.J. (1980) The ecology of Acanthocephalus parksidei (Acanthocephala: Echinorhynchidae) in its isopod intermediate host. Proceedings of the Helminthological Society of Washington 47, 3746.Google Scholar
Amin, O.M., Heckmann, R.A. & Van Ha, N. (2004) On the immature stages of Pallisentis (Pallisentis) celatus (Acanthocephala: Quadrigyridae) from occasional fish hosts in Vietnam. The Raffles Bulletin of Zoology 52, 593598.Google Scholar
Andersson, M. (1994) Sexual selection. Princeton, New Jersey, USA, Princeton University Press.CrossRefGoogle Scholar
Awachie, J.B. (1965) The ecology of Echinorhynchus truttae Schrank, 1788 (Acanthocephala) in a trout stream in North Wales. Parasitology 55, 747762.CrossRefGoogle Scholar
Awachie, J.B. (1966) The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology 40, 1132.CrossRefGoogle ScholarPubMed
Bakker, T.C.M., Mazzi, D. & Zala, S. (1997) Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.CrossRefGoogle Scholar
Barrett, J. & Butterworth, P.E. (1968) The carotenoids of Polymorphus minutes (Acanthocephala) and its intermediate host, Gammarus pulex . Comparative Biochemistry and Physiology 27, 575581.CrossRefGoogle Scholar
Barrett, J. & Butterworth, P.E. (1973) The carotenoid pigments of six species of adult acanthocephala. Experientia 29, 651653.CrossRefGoogle ScholarPubMed
Benesh, D.P. (2007) Larval life history, transmission strategies, and the evolution of intermediate host exploitation by complex life-cycle parasites. Jyväskylä Studies in Biological and Environmental Science 182, 132.Google Scholar
Benesh, D.P. & Valtonen, E.T. (2007) Sexual differences in larval life history traits of acanthocephalan cystacanths. International Journal for Parasitology 37, 191198.CrossRefGoogle ScholarPubMed
Cable, R.M. & Dill, W.T. (1967) The morphology and life history of Paulisentis fractus Van Cleave and Bangham, 1949 (Acanthocephala: Neoechinorhynchidae). Journal of Parasitology 37, 810817.CrossRefGoogle Scholar
Chubb, J.C. (1982) Seasonal occurrence of helminths in freshwater fishes. Part IV. Adult Cestoda, Nematoda and Acanthocephala. Advances in Parasitology 20, 1292.CrossRefGoogle ScholarPubMed
Crompton, D.W.T. (1974) Experiment on insemination in Moniliformis dubius (Acanthocephala). Parasitology 68, 229238.CrossRefGoogle ScholarPubMed
Crompton, D.W.T. & Nickol, B.B. (1985) Biology of Acanthocephala. Cambridge, UK, Cambridge University Press.Google Scholar
Dezfuli, B.S. & Giari, L. (1999) Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host–parasite interface. Folia Parasitologica 46, 117122.Google Scholar
Dezfuli, B.S., Simoni, E., Duclos, L. & Rossetti, E. (2008) Crustacean–acanthocephalan interaction and host cell-mediated immunity: parasite encapsulation and melanization. Folia Parasitologica 55, 5359.CrossRefGoogle ScholarPubMed
Froese, R., Pauly, D. (2012) FishBase. World Wide Web electronic publication. Available at website www.fishbase.org (accessed accessed April 2012).Google Scholar
Ghiselin, M.T. (1974) The economy of nature and the evolution of sex. 2nd edn. 346 pp. Berkeley, California, University of California Press.Google Scholar
Gleason, L.N. (1989) Movement of Pomphorhynchus bulbocolli larvae from the hemocoel to the peripheral circulation of Gammarus pseudolimnaeus . Journal of Parasitology 75, 982985.CrossRefGoogle Scholar
Graff, D.J. & Kitzman, W.B. (1965) Factors influencing the activation of acanthocephalan cystacanths. Journal of Parasitology 51, 424429.CrossRefGoogle ScholarPubMed
Hassanine, R.M. (2006) Acanthocephalans from Red Sea fishes. Family Cavisomidae Meyer, 1932: The seasonal cycle of Diplosentis nudus (Harada, 1938) Pichelin et Cribb, 2001 in a definitive fish host, and a comment on Sclerocollum Schmidt et Paperna, 1978. Acta Parasitologica 51, 123129.CrossRefGoogle Scholar
Hine, P.M. & Kennedy, C.R. (1974) The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon. Journal of Fish Biology 6, 665679.CrossRefGoogle Scholar
Holt, R.H. (1989) Hymenolepis diminuta utilizes the envelope surrounding Moniliformis moniliformis in order to survive in the cockroach host. Journal of Parasitology 75, 160162.CrossRefGoogle ScholarPubMed
Kaldonski, N., Perrot-Minnot, M.-J., Dodet, R., Martinaud, G. & Cezilly, F. (2009) Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proceedings of the Royal Society B 276, 169176.CrossRefGoogle ScholarPubMed
Kennedy, C.R. (2006) Ecology of the Acanthocephala. 1st edn. 249 pp. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Kennedy, C.R., Broughton, P.F. & Hine, P.M. (1978) The status of brown trout and rainbow trout Salmo trutta and Salmo gairdneri as hosts of the acanthocephalan Pomphorhynchus laevis . Journal of Fish Biology 13, 265275.CrossRefGoogle Scholar
Kennedy, E.R. (1985) Regulation and dynamics of acanthocephalan populations. pp. 385416 in Crompton, D.W.T. & Nickol, B.B. (Eds) Biology of the Acanthocephala. Cambridge, UK, Cambridge University Press.Google Scholar
Khanna, D.R. (2004) Biology of helminthes. 1st edn. 456 pp. New Delhi, India, Discovery Publishing House.Google Scholar
Kopp, D.A., Elke, D.A., Caddigan, S.C., Raj, A., Rodriguez, L., Young, M.K. & Sparkes, T.C. (2011) Dispersal in the Acanthocephalan Acanthocephalus dirus . Journal of Parasitology 97, 11011105.CrossRefGoogle ScholarPubMed
Lackie, A.M. (1974) The activation of cystacanths of Polymorphus minutus (Acanthocephala) in vitro. Parasitology 68, 135146.CrossRefGoogle ScholarPubMed
Lackie, A.M. & Holt, R.H. (1988) Immunosuppression by larvae of Moniliformis moniliformis (Acanthocephala) in their cockroach host (Periplaneta americana). Parasitology 98, 307314.CrossRefGoogle Scholar
Lackie, J.M. (1972) The course of infection and growth of Moniliformis dubius (Acanthocephala) in the intermediate host Periplaneta americana . Parasitology 64, 95106.CrossRefGoogle ScholarPubMed
Ledoyer, M. (1975) Megaluropus monasteriensis (Crustacea, Amphipoda, Gammaridae) espéce nouvelle de Méditerranée comparée à M. agilis massiliensis n. sp. et à M. agilis Hoek. Bulletin du Muséum National d'Histoire Naturelle 336, 13051316.Google Scholar
Leuckart, R. (1876) Die menschlichen Parasiten und die von ihnen herruhrenden Krankheiten. 2, 3 Lief . Leipzig, Winter'sche Verlagshandlung.Google Scholar
Moore, J. (2002) Parasites and the behavior of animals. Oxford, Oxford University Press.CrossRefGoogle Scholar
Morand, S. & Hugot, J.-P. (1998) Sexual size dimorphism in parasitic oxyurid nematodes. Biological Journal of the Linnean Society 64, 397410.CrossRefGoogle Scholar
Muzzall, P.M. & Rabalais, F.C. (1975) Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). I. Seasonal periodicity and new host records. Proceedings of the Helminthological Society of Washington 42, 3134.Google Scholar
Nickol, B.B. (1985) Epizootiology. pp. 307346 in Crompton, D.W.T. & Nickol, B.B. (Eds) Biology of the Acanthocephala. Cambridge, UK, Cambridge University Press.Google Scholar
Nickol, B.B. (2003) Is postcyclic transmission underestimated as an epizootiological factor for acanthocephalans? Helminthologia 40, 9395.Google Scholar
Nickol, B.B. & Dappen, G.E. (1982) Armadillidium vulgare (Isopoda) as an intermediate host of Plagiorhynchus cylindraceus (Acanthocephala) and isopod response to infection. Journal of Parasitology 68, 570575.CrossRefGoogle Scholar
Olson, R.E. & Pratt, I. (1971) The life cycle and larval development of Echinorhynchus lageniformis Ekbaum, 1938 (Acanthocephala: Echinorhynchidae). Journal of Parasitology 57, 143149.CrossRefGoogle Scholar
Petrochenko, V.I. (1956) Acanthocephala of domestic and wild animals. Vol.1. 465 pp. Moscow, Zdatel'stvo Akademii Nauk SSSR.Google Scholar
Poulin, R. & Morand, S. (2000) Testes size, body size and male–male competition in Acanthocephalan parasites. Journal of Zoology 250, 551558.CrossRefGoogle Scholar
Randall, J.E. (1983) Red Sea reef fishes. 192 pp. London, IMMEl Publ. Co.Google Scholar
Ribas, A. & Casanova, J.C. (2006) Acanthocephalans. pp. 8189 in Morand, S., Krasnov, B. & Poulin, R. (Eds) Micro mammals and macroparasites: from evolutionary ecology to management. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Richardson, D.J., Martens, J.K. & Nickol, B.B. (1997) Copulation and sexual congress of Leptorhynchoides thecatus (Acanthocephala). Journal of Parasitology 83, 542543.CrossRefGoogle ScholarPubMed
Robinson, E.S. & Strickland, B.C. (1969) Cellular response of Periplaneta americana to acanthocephalan larvae. Experimental Parasitology 26, 384392.CrossRefGoogle ScholarPubMed
Sasal, P., Jobet, E., Faliex, E. & Morand, S. (2000) Sexual competition in an acanthocephalan parasite of fish. Parasitology 120, 6569.CrossRefGoogle Scholar
Schmidt, G.D. (1985) Development and life cycles. pp. 273305 in Crompton, D.W.T. & Nickol, B.B. (Eds) Biology of the Acanthocephala. Cambridge, UK, Cambridge University Press.Google Scholar
Schmidt, G.D. & Olsen, O.W. (1964) Life cycle and development of Prosthorhyncus formosus (Van Cleave, 1918) Travossos, 1926, an acanthocephalan parasite of birds. Journal of Parasitology 50, 721730.CrossRefGoogle Scholar
Steinauer, M.L. & Nickol, B.B. (2003) Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251254.CrossRefGoogle ScholarPubMed
Taraschewski, H. (2000) Host–parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1179.CrossRefGoogle ScholarPubMed
Uglem, G.L. (1972) The life cycle of Neoechinorhynchus cristatus Lynch, 1936 (Acanthocephala) with notes on the hatching of eggs. Journal of Parasitology 58, 10711074.CrossRefGoogle ScholarPubMed
Walker, A.O. (1904) Amphipoda Gammaridea from the Indian Ocean, British East Africa and the Red Sea. The Percy Sladen Trust Expedition to the Indian Ocean in 1905. Transactions of the Linnean Society of London, Zoology 12, 323344.CrossRefGoogle Scholar
West Eberhard, M.J. (1983) Sexual selection, social competition, and speciation. Quarterly Review of Biology 58, 155183.CrossRefGoogle Scholar