Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T14:14:49.851Z Has data issue: false hasContentIssue false
  • English
  • Français

Three unrelated species, 3 sites, same host – monogenean parasites of the southern fiddler ray, Trygonorrhina fasciata, in South Australia: egg hatching strategies and larval behaviour

Published online by Cambridge University Press:  27 March 2006

V. GLENNON ,
L. A. CHISHOLM  and
I. D. WHITTINGTON
V. GLENNON
Affiliation:
Marine Parasitology Laboratory, School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, South Australia 5005, Australia
L. A. CHISHOLM
Affiliation:
Marine Parasitology Laboratory, School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, South Australia 5005, Australia
I. D. WHITTINGTON
Affiliation:
Marine Parasitology Laboratory, School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, South Australia 5005, Australia Monogenean Research Laboratory, Parasitology Section, The South Australian Museum, North Terrace, South Australia 5000, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

The southern fiddler ray, Trygonorrhina fasciata (Rhinobatidae), is parasitized by 3 monogenean (platyhelminth) species from 3 families on 3 different sites of the host: Calicotyle australis (Monocotylidae) from the cloaca, Pseudoleptobothrium aptychotremae (Microbothriidae) from the skin and Branchotenthes octohamatus (Hexabothriidae) from the gills. Cues that promote egg hatching were investigated for each species and the behaviour of their larvae was also documented. Eggs were laid by parasites in vivo and maintained at 22 °C. Three different egg hatching and host finding strategies were discovered. Calicotyle australis eggs hatched spontaneously with a strong diurnal rhythm that is likely to be under circadian control. The larva is ciliated, photo-responsive and can survive for up to 24 h at 22 °C after hatching. Pseudoleptobothrium aptychotremae may have a ‘bet-hedging’ strategy. Some eggs hatched spontaneously and rhythmically. However, since the hatching success was low, it is possible that other eggs require a different cue provided by the host. The larva is also ciliated but shows no photo-response and was observed to remain active for <4 h at 22 °C after hatching. Branchotenthes octohamatus has a ‘sit-and-wait’ strategy that depends on mechanical disturbance to stimulate hatching. The larva is unciliated, shows no photo-response but may survive for more than 2 days at 22 °C after hatching. The implications of hatching strategy, larval behaviour and morphology in the goal to find a host are discussed for each species.

Keywords

MonogeneaMonocotylidaeMicrobothriidaeHexabothriidaeegg hatchinglarval behaviourTrygonorrhina fasciata
Type
Research Article
Information
Parasitology , Volume 133 , Issue 1 , July 2006 , pp. 55 - 66
Copyright
2006 Cambridge University Press

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

Adamson, M. L. and Caira, J. N. ( 1994). Evolutionary factors influencing the nature of parasite specificity. Parasitology 109, S85–S95.CrossRefGoogle Scholar
Chisholm, L. A., Wheeler, T. A. and Beverley-Burton, M. ( 1995). A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Systematic Parasitology 32, 159–191.CrossRefGoogle Scholar
Chisholm, L. A. and Whittington, I. D. ( 2000). Egg hatching in 3 species of monocotylid monogenean parasites from the shovelnose ray Rhinobatos typus at Heron Island, Australia. Parasitology 121, 303–313.CrossRefGoogle Scholar
Cone, D. K. and Burt, M. D. B. ( 1981). The invasion route of the gill parasite Urocleidus adspectus Mueller, 1936 (Monogenea: Ancyrocephalinae). Canadian Journal of Zoology 59, 2166–2171.CrossRefGoogle Scholar
Dunlap, J. C., Loros, J. J. and DeCoursey, P. J. ( 2004). Chronobiology: Biological Timekeeping. Sinauer Associates, Sunderland.
Ernst, I. and Whittington, I. D. ( 1996). Hatching rhythms in the capsalid monogeneans Benedenia lutjani from the skin and B. rohdei from the gills of Lutjanus carponotatus at Heron Island, Queensland, Australia. International Journal for Parasitology 26, 1191–1204.Google Scholar
Euzet, L. and Raibaut, A. ( 1960). Le développement postlarvaire de Squalonchocotyle torpedinis (Price 1942) (Monogenea, Hexabothriidae). Bulletin de la Société Neuchâteloise des Sciences Naturelles 83, 101–108.Google Scholar
Gannicott, A. M. and Tinsley, R. C. ( 1997). Egg hatching in the monogenean gill parasite Discocotyle sagittata from the rainbow trout (Oncorhynchus mykiss). Parasitology 114, 569–579.Google Scholar
Glennon, V., Chisholm, L. A. and Whittington, I. D. ( 2005). Branchotenthes octohamatus sp. n. (Monogenea: Hexabothriidae) from the gills of the southern fiddler ray, Trygonorrhina fasciata (Rhinobatidae) in South Australia: description of adult and larva. Folia Parasitologica 52, 223–230.Google Scholar
Glennon, V., Chisholm, L. A. and Whittington, I. D. ( 2006 a). A redescription of Calicotyle australis Johnston, 1934 (Monogenea: Monocotylidae) from the type-host Trygonorrhina fasciata (Rhinobatidae) off Adelaide, South Australia, including descriptions of live and silver stained larvae. Systematic Parasitology (in the Press).Google Scholar
Glennon, V., Chisholm, L. A. and Whittington, I. D. ( 2006 b). Pseudoleptobothrium aptychotremae Young, 1967 (Monogenea: Microbothriidae) redescribed from a new host, the southern fiddler ray, Trygonorrhina fasciata (Rhinobatidae) in South Australia with a description of the larva and post-larval development. Acta Parasitologica (in the Press).
Itoh, M. T. and Sumi, Y. ( 2000). Circadian clock controlling egg hatching in the cricket (Gryllus bimaculatus). Journal of Biological Rhythms 15, 241–245.CrossRefGoogle Scholar
Kearn, G. C. ( 1973). An endogenous circadian hatching rhythm in the monogenean skin parasite Entobdella soleae, and its relationship to the activity rhythm of the host (Solea solea). Parasitology 66, 101–122.CrossRefGoogle Scholar
Kearn, G. C. ( 1975). Hatching in the monogenean parasite Dictyocotyle coeliaca from the body cavity of Raja naevus. Parasitology 70, 87–93.CrossRefGoogle Scholar
Kearn, G. C. ( 1980). Light and gravity responses of the oncomiracidium of Entobdella soleae and their role in host location. Parasitology 81, 71–89.CrossRefGoogle Scholar
Kearn, G. C. ( 1982). Rapid hatching induced by light intensity reduction in the monogenean Entobdella diadema. Journal of Parasitology 68, 171–172.CrossRefGoogle Scholar
Kearn, G. C. ( 1986). Role of chemical substances from fish hosts in hatching and host-finding in monogeneans. Journal of Chemical Ecology 12, 1651–1658.CrossRefGoogle Scholar
Kearn, G. C., Ogawa, K. and Maeno, Y. ( 1992). Hatching patterns of the monogenean parasites Benedenia seriolae and Heteraxine heterocerca from the skin and gills, respectively, of the same host fish, Seriola quinqueradiata. Zoological Science 9, 451–455.Google Scholar
Ktari, M. H. and Maillard, C. ( 1972). Neonchocotyle pastinacae n.g.-n.sp. (Monogenea-Hexabothriidae) parasite de Dasyatis pastinaca dans le golfe de Tunis. Annales de Parasitologie Humaine et Comparée 47, 181–191.Google Scholar
Last, P. R. and Stevens, J. D. ( 1994). Sharks and Rays of Australia. Publication of CSIRO Division of Fisheries, Australia.
Lorenz, K. and Tinbergen, N. ( 1957). Taxis and instinct. In Instinctive Behavior; the Development of a Modern Concept ( ed. Schiller, C. H.), pp. 176–206. International Universities Press Inc., New York.
Lyons, K. M. ( 1972). Sense organs of monogeneans. Zoological Journal of the Linnean Society 51, 181–199.Google Scholar
Macdonald, S. ( 1974). Host skin mucus as a hatching stimulant in Acanthocotyle lobianchi, a monogenean from the skin of Raja spp. Parasitology 68, 331–338.CrossRefGoogle Scholar
Macdonald, S. and Combes, C. ( 1978). The hatching rhythm of Polystoma integerrimum, a monogenean from the frog Rana temporaria. Chronobiologia 5, 277–285.Google Scholar
Pike, A. W. ( 1990). Interpreting parasite host location behaviour. Parasitology Today 6, 343–344.CrossRefGoogle Scholar
Refinetti, R. ( 2000). Circadian Physiology. CRC Press, Boca Raton.
Roenneberg, T., Daan, S. and Merrow, M. ( 2003). The art of entrainment. Journal of Biological Rhythms 18, 183–194.CrossRefGoogle Scholar
Sharma, V. K. and Joshi, A. ( 2002). Clocks, genes and evolution: the evolution of circadian organisation. In Biological Rhythms ( ed. Kumar, V.), pp. 5–23. Narosa Publishing House, New Delhi.CrossRef
Sukhdeo, M. V. K. and Sukhdeo, S. C. ( 2002). Fixed behaviours and migration in parasitic flatworms. International Journal for Parasitology 32, 329–342.CrossRefGoogle Scholar
Whittington, I. D. ( 1987 a). Hatching in two monogenean parasites from the common dogfish (Scyliorhinus canicula): the polyopisthocotylean gill parasite, Hexabothrium appendiculatum and the microbothriid skin parasite, Leptocotyle minor. Journal of the Marine Biological Association of the United Kingdom 67, 729–756.Google Scholar
Whittington, I. D. ( 1987 b). Studies on the behaviour of the oncomiracidia of the monogenean parasites Hexabothrium appendiculatum and Leptocotyle minor from the common dogfish, Scyliorhinus canicula. Journal of the Marine Biological Association of the United Kingdom 67, 773–784.Google Scholar
Whittington, I. D., Chisholm, L. A. and Rohde, K. ( 2000). The larvae of Monogenea (Platyhelminthes). Advances in Parasitology 44, 139–232.Google Scholar
Whittington, I. D. and Kearn, G. C. ( 1986). Rhythmical hatching and oncomiracidial behaviour in the hexabothriid monogenean Rajonchocotyle emarginata from the gills of Raja spp. Journal of the Marine Biological Association of the United Kingdom 66, 93–111.CrossRefGoogle Scholar
Whittington, I. D. and Kearn, G. C. ( 1988). Rapid hatching of mechanically-disturbed eggs of the monogenean gill parasite Diclidophora luscae, with observations on sedimentation of egg bundles. International Journal for Parasitology 18, 847–852.CrossRefGoogle Scholar