Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T15:23:50.268Z Has data issue: false hasContentIssue false
  • English
  • Français

Factors influencing cercarial emergence and settlement in the digenean trematode Parorchis acanthus (Philophthalmidae)

Published online by Cambridge University Press:  06 July 2010

K. Prinz ,
T.C. Kelly ,
R.M. O'Riordan  and
S.C. Culloty
K. Prinz*
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
T.C. Kelly
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
R.M. O'Riordan
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
S.C. Culloty
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland Aquaculture and Fisheries Development Centre, University College Cork, Distillery Fields, North Mall, Cork, Ireland
*
Correspondence should be addressed to: K. Prinz, Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The trematode Parorchis acanthus is widely distributed and exhibits a broad host spectrum, with larval stages occurring in marine gastropods and adult flukes parasitizing on various seabird species. Unlike the majority of digeneans, its cercariae do not invade a second intermediate host but encyst on a substrate in the open. In a series of laboratory experiments, we investigated factors influencing cercarial emergence and settlement of P. acanthus. Emergence of cercariae from the gastropod intermediate host Nucella lapillus increased with increasing temperature, whereas cercarial encystment success decreased. Numbers of emerged cercariae were highest in the presence of light and water. However, although in much lower numbers, cercariae were also released from N. lapillus and successfully encysted under relatively dry conditions. Cercariae were found to settle predominantly on filtering blue mussels Mytilus edulis, suggesting that cercarial concentration on the valves is largely facilitated by the bivalve's inhalation current. After being inhaled, cercariae actively emerged from the mussels using their suckers and subsequently encysted on the shells, preferably along the rim of the valves. Barnacle epibionts Semibalanus balanoides were observed to impair cercarial settlement on mussels, by disturbing or preying on cercariae. Whilst settlement success of cercariae on M. edulis increased with increasing mussel density, intensity of encysted metacercariae decreased. Furthermore, cercariae settled more efficiently on small than on large mussels. Our findings suggest that the transmission of P. acanthus cercariae is regulated by a range of abiotic and biotic factors, with filtering activity of mussels playing a key role by enhancing accumulation of cercariae on a substrate suitable for transmission to the bird final host.

Keywords

transmissioncercariaemetacercariaeencystmentNucella lapillusMytilus edulisfiltration current
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 8 , December 2011 , pp. 1673 - 1679
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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

Asanji, M.F. and Williams, M.O. (1985) Effect of age and environmental factors on the viability and excystment of metacercarial cysts of Parorchis acanthus in vivo and in vitro. Zeitschrift für Parasitenkunde 71, 595–601.Google Scholar
Bell, A.S., Sommerville, C. and Gibson, D.I. (1999) Cercarial emergence of Ichthyocotylurus erraticus (Rudolphi, 1809), I. variegatus (Creplin, 1825) and Apatemon gracilis (Rudolphi, 1819) (Digenea: Strigeidae): contrasting responses to light:dark cycling. Parasitology Research 85, 387–392.Google Scholar
Bennett, S.C., Irwin, S.W.B and Fitzpatrick, S.M. (2003) Tributyltin and copper effects on encystment and in vitro excystment of Parorchis acanthus larvae. Journal of Helminthology 77, 291–296.CrossRefGoogle ScholarPubMed
Combes, C., Fournier, A., Moné, H. and Théron, A. (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.Google Scholar
Craig, L.H. (1975) Himasthla quissetensis and Lepocreadium setiferoides: emergence patterns from their molluscan host, Nassarius obsoletus. Experimental Parasitology 38, 56–63.CrossRefGoogle ScholarPubMed
Cross, M.A., Irwin, S.W.B. and Fitzpatrick, S.M. (2001) Effects of heavy metal pollution on swimming and longevity in the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 123, 499–507.CrossRefGoogle ScholarPubMed
Davenport, J., Smith, R.J.J.W. and Packer, M. (2000) Mussels (Mytilus edulis L.): significant consumers and destroyers of mesozooplankton. Marine Ecology Progress Series 198, 131–137.Google Scholar
de Montaudouin, X., Wegeberg, A.M., Jensen, K.T. and Sauriau, P.G. (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Diseases of Aquatic Organisms 34, 63–70.CrossRefGoogle Scholar
Evans, D.W., Irwin, S.W.B. and Fitzpatrick, S.M. (1997) Metacercarial encystment and in vivo cultivation of Cercaria lebouri Stunkard 1932 (Digenea: Notocotylidae) to adults identified as Paramonostomum chabaudi van Strydonck 1965. International Journal for Parasitology 27, 1299–1304.CrossRefGoogle ScholarPubMed
Feare, C.J. (1970) Aspects of the ecology of an exposed shore population of dogwhelks Nucella lapillus (L.). Oecologia 5, 1–18.Google Scholar
Haas, W. (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109, S15–S29.Google Scholar
Haas, W. (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364.CrossRefGoogle ScholarPubMed
Haas, W., Körner, M., Hutterer, E., Wegner, M. and Haberl, B. (1995) Finding and recognition of the snail intermediate hosts by 3 species of echinostome cercariae. Parasitology 110, 133–142.CrossRefGoogle ScholarPubMed
Jensen, K.T., Castro, N.F. and Bachelet, G. (1999) Infectivity of Himasthla spp. (Trematoda) in cockle (Cerastoderma edule) spat. Journal of the Marine Biological Association of the United Kingdom 79, 265–271.CrossRefGoogle Scholar
Koprivnikar, J. and Poulin, R. (2009) Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitology Research 105, 957–965.CrossRefGoogle ScholarPubMed
Kuntz, R.E. (1947) Effect of light and temperature on emergence of Schistosoma mansoni cercariae. Transactions of the American Microscopical Society 66, 37–49.CrossRefGoogle ScholarPubMed
Lauckner, G. (1980) Diseases of Mollusca: Gastropoda. In Kinne, O. (ed.) Diseases of marine animals. Volume I. General aspects, Protozoa to Gastropoda. New York: John Wiley & Sons, pp. 311–424.Google Scholar
Lehane, C. and Davenport, J. (2002) Ingestion of mesozooplankton by three species of bivalve; Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. Journal of the Marine Biological Association of the United Kingdom 82, 615–619.Google Scholar
Lehane, C. and Davenport, J. (2004) Ingestion of bivalve larvae by Mytilus edulis: experimental and field demonstrations of larviphagy in farmed blue mussels. Marine Biology 145, 101–107.CrossRefGoogle Scholar
Lo, C.-T. and Lee, K.-M. (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347–350.Google Scholar
Lyholt, H.C.K. and Buchmann, K. (1996) Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25, 169–173.CrossRefGoogle Scholar
Morley, N.J., Crane, M. and Lewis, J.W. (2001) Toxicity of cadmium and zinc to encystment and in vitro excystment of Parorchis acanthus (Digenea: Philophthalmidae). Parasitology 122, 75–79.Google Scholar
Morley, N.J., Leung, K.M.Y., Morritt, D. and Crane, M. (2003) Toxicity of anti-fouling biocides to Parorchis acanthus (Digenea: Philophthalmidae) cercarial encystment. Diseases of Aquatic Organisms 54, 55–60.CrossRefGoogle ScholarPubMed
Mouritsen, K.N. (2002a) The Hydrobia ulvae–Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341–347.Google Scholar
Mouritsen, K.N. (2002b) The Hydrobia ulvae–Maritrema subdolum association: cercarial emergence controlled by host activity. Journal of Helminthology 76, 349–353.CrossRefGoogle ScholarPubMed
Mouritsen, K.N., McKechnie, S., Meenken, E., Toynbee, J.L. and Poulin, R. (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. Journal of the Marine Biological Association of the United Kingdom 83, 307–310.Google Scholar
Newell, R.C. (1979) Biology of intertidal animals. Faversham: Marine Ecological Surveys.Google Scholar
Olivier, L. (1951) The influence of light on the emergence of Schistosomatium douthitti cercariae from their snail host. Journal of Parasitology 37, 201–204.Google Scholar
Pechenik, J.A. and Fried, B. (1995) Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111, 373–378.Google Scholar
Pietrock, M. and Marcogliese, D.J. (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.Google Scholar
Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.Google Scholar
Poulin, R. and Cribb, T.H. (2002) Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.Google Scholar
Prinz, K., Kelly, T.C., O'Riordan, R.M. and Culloty, S.C. (2009) Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Marine Biology 156, 2303–2311.Google Scholar
Rauch, G., Kalbe, M. and Reusch, T.B.H. (2005) How a complex life cycle can improve the sex life of a parasite. Journal of Evolutionary Biology 18, 1069–1075.Google Scholar
Rees, F.G. (1937) The anatomy and encystment of Cercaria purpurae Lebour, 1911. Proceedings of the Zoological Society of London B 107, 65–73.Google Scholar
Rees, F.G. (1948) A study of the effect of light, temperature and salinity on the emergence of Cercaria purpurae Lebour from Nucella lapillus (L.). Parasitology 38, 228–242.Google Scholar
Riisgård, H.U. (2001) On measurement of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Marine Ecology Progress Series 211, 275–291.Google Scholar
Stunkard, H.W. and Shaw, C.R. (1932) The effects of dilution of seawater on the activity and longevity of certain marine cercariae, with descriptions of two new species. Biological Bulletin. Marine Biological Laboratory, Woods Hole 61, 242–271.Google Scholar
Thieltges, D.W. (2007) Habitat and transmission—effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve. Parasitology 134, 599–605.Google Scholar
Thieltges, D.W. and Reise, K. (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150, 569–581.Google Scholar
Thieltges, D.W. and Rick, J. (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google Scholar
Thieltges, D.W., Bordalo, M.D., Caballero Hernández, A., Prinz, K. and Jensen, K.T. (2008) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology 135, 1111–1116.Google Scholar
Wagenbach, G.E. and Alldredge, A.L. (1974) Effect of light on the emergence pattern of Plagiorchis micracanthos cercariae from Stagnicola exilis. Journal of Parasitology 60, 782–785.CrossRefGoogle ScholarPubMed
Wegeberg, A.M., de Montaudouin, X. and Jensen, K.T. (1999) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). Journal of Experimental Marine Biology and Ecology 238, 259–269.Google Scholar
Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. Tokyo: Keigaku Publishing.Google Scholar