Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-23T11:58:26.422Z Has data issue: false hasContentIssue false
  • English
  • Français

Trematode fauna of Hydrobia ulvae (Gastropoda: Prosobranchia) in a eutrophic temperate estuary

Published online by Cambridge University Press:  15 December 2010

M.D. Bordalo ,
S.M. Ferreira ,
K.T. Jensen  and
M.A. Pardal
M.D. Bordalo*
Affiliation:
CFE—Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Apartamento 3046, 3001-401 Coimbra, Portugal
S.M. Ferreira
Affiliation:
CFE—Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Apartamento 3046, 3001-401 Coimbra, Portugal GIRM—School of Tourism and Maritime Technology, Marine Resources Research Group, Polytechnic Institute of Leiria, 2520-641 Peniche, Portugal
K.T. Jensen
Affiliation:
Marine Ecology, Department of Biological Sciences, University of Aarhus, Ole Worms Allé 1, Building 1135, DK-8000 Aarhus C, Denmark
M.A. Pardal
Affiliation:
CFE—Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Apartamento 3046, 3001-401 Coimbra, Portugal
*
Correspondence should be addressed to: M.D. Bordalo, CFE—Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Apartamento 3046, 3001-401 Coimbra, Portugal email: mbordalo@ci.uc.pt
Get access Rights & Permissions [Opens in a new window]

Abstract

Digenean trematodes infecting the mud snail Hydrobia ulvae were studied at two key sites of the Mondego Estuary (Portugal), from January 1993 to September 1995: a mud flat covered by the seagrass Zostera noltii, and a bare sand flat where seasonal macroalgal blooms occurred as a result of eutrophication. Digeneans belonging to Microphallidae, Notocotylidae, Haploporidae and Heterophyidae were recorded in snails from both sites whereas representatives from Echinostomatidae were only found in snails from the seagrass bed. The density of infected snails was higher at the seagrass bed than at the eutrophic area partly reflecting the difference in population structure of H. ulvae between sites. The Zostera noltii bed supports an abundant and well-structured mud snail population, with all size-classes represented, in contrast to a less abundant and juvenile dominated population in the eutrophic area. In the Z. noltii bed no clear seasonal and interannual patterns emerged in the infection densities. In the eutrophic area, the density of infected individuals increased in the presence of algae, and decreased during the occurrence of occasional flood events. Small scale spatial and temporal patterns in the prevalence of digenean trematodes in mud snails were therefore demonstrated within the Mondego Estuary that has experienced a mixture of anthropogenic impact and climate instability.

Keywords

Hydrobia ulvaedigenean trematodesparasitismMondego Estuaryeutrophication
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 4 , June 2011 , pp. 913 - 921
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

Blanchet, E., de Montaudouin, X., Lucas, A. and Chardy, P. (2004) Heterogeneity of macrozoobenthic assemblages within a Zostera noltii seagrass bed: diversity, abundance, biomass and structuring factors. Estuarine, Coastal and Shelf Science 61, 111–123.CrossRefGoogle Scholar
Cardoso, P.G., Lillebø, A.I., Pardal, M.A., Ferreira, S.M. and Marques, J.C. (2002) The effect of different primary producers on Hydrobia ulvae population dynamics: a case study in a temperate intertidal estuary. Journal of Experimental Marine Biology and Ecology 277, 173–195.CrossRefGoogle Scholar
Cardoso, P.G., Brandão, A., Pardal, M.A., Raffaelli, D. and Marques, J.C. (2005) The resilience of Hydrobia ulvae populations to anthropogenic and natural disturbances. Marine Ecology Progress Series 289, 191–199.CrossRefGoogle Scholar
Clarke, K.R. and Warwick, R.M. (2001) Change in marine communities. An approach to statistical analysis and interpretation. 2nd edition. Plymouth: Primer-E Ltd.Google Scholar
Deblock, S. (1980) Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranchies) dés côtes de France. Parassitologia 22, 1–105.Google Scholar
Dolbeth, M., Cardoso, P.G., Ferreira, S.M., Verdelhos, T., Raffaelli, D. and Pardal, M.A. (2007) Anthropogenic and natural disturbance effects on a macrobenthic estuarine community over a 10-year period. Marine Pollution Bulletin 54, 576–585.CrossRefGoogle ScholarPubMed
Esch, G.W., Curtis, L.A. and Barger, M.A. (2001) A perspective on the ecology of trematode communities in snails. Parasitology 12, S57–S75.CrossRefGoogle Scholar
Ferreira, S.M., Jensen, K.T., Martins, P., Sousa, S.F., Marques, J.C. and Pardal, M.A. (2005) Impact of microphallid trematodes on the survivorship, growth and reproduction of an isopod (Cyathura carinata). Journal of Experimental Marine Biology and Ecology 318, 191–199.CrossRefGoogle Scholar
Ferreira, S.M., Brandão, A., Baeta, A., Neto, J.M., Lillebø, A.I., Jensen, K.T. and Pardal, M.A. (2007) Effects of restoration management on the estuarine isopod Cyathura carinata: mediation by trematodes and habitat change. Marine Biology 151, 109–118.CrossRefGoogle Scholar
Field, L.C. and Irwin, S.W.B. (1999) Digenean larvae in Hydrobia ulvae from Belfast Lough (Northern Ireland) and the Ythan Estuary (north-east Scotland). Journal of the Marine Biological Association of the United Kingdom 79, 431–435.CrossRefGoogle Scholar
Fish, J.D. and Fish, S. (1974) The breeding cycle and growth of Hydrobia ulvae in the Dovey Estuary. Journal of the Marine Biological Association of the United Kingdom 54, 685–697.CrossRefGoogle Scholar
Fredensborg, B.L., Mouritsen, K.N. and Poulin, R. (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.CrossRefGoogle Scholar
Fredensborg, B.L., Mouritsen, K.N. and Poulin, R. (2006) Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail—from small to large scale. Marine Biology 149, 275–283.CrossRefGoogle Scholar
Gorbushin, A.M. (1997) Field evidence of trematodes-induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom 77, 785–800.CrossRefGoogle Scholar
Graham, A.L. (2003) Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. Journal of Parasitology 89, 458–463.CrossRefGoogle ScholarPubMed
Hechinger, R.F. and Lafferty, K.D. (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B 27, 1059–1066.Google Scholar
Huxham, M., Raffaelli, D. and Pike, A.W. (1993) The influence of Cryptocotyle lingua (Digenea: Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prodobranchia): an ecological approach. Journal of Experimental Marine Biology and Ecology 168, 223–238.CrossRefGoogle Scholar
Huxham, M., Raffaelli, D. and Pike, A.W. (1995) The effect of larvae trematodes on the growth and burrowing behaviour of Hydrobia ulvae (Gastropoda: Prosobranchia) in the Ythan Estuary, north-east Scotland. Journal of Experimental Marine Biology and Ecology 185, 1–17.CrossRefGoogle Scholar
Jensen, K.T., Latama, G. and Mouritsen, K.N. (1996) The effect of larval trematodes on the survival rate of two species of mud-snails (Hydrobiidae) experimentally exposed to desiccation, freezing and anoxia. Helgoländer Meeresuntersuchungen 5, 327–335.CrossRefGoogle Scholar
Jensen, K.T. and Mouritsen, K.N. (1992) Mass mortality in 2 common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator—the possible role of trematodes. Helgoländer Meeresuntersuchungen 46, 329–339.CrossRefGoogle Scholar
Jensen, K.T., Ferreira, S.M. and Pardal, M.A. (2004) Trematodes in a Cyathura carinata population from a temperate intertidal estuary: infection patterns and impact on host. Journal of the Marine Biological Association of the United Kingdom 84, 1151–1158.CrossRefGoogle Scholar
Kesting, V., Gollasch, S. and Zander, C.D. (1996) Parasite communities of the Schlei Fjord (Baltic coast of northern Germany). Helgoländer Meeresuntersuchungen 50, 447–496.CrossRefGoogle Scholar
Krebs, C.J. (1999) Ecological methodology. 2nd edition. Menlo Park, CA: Addison-Wesley Educational Publishers, Inc.Google Scholar
Lafferty, K.D. and Kuris, A.M. (1999) How environmental stress affects the impact of parasites. Limnology and Oceanography 44, 925–931.CrossRefGoogle Scholar
Lauckner, G. (1980) Diseases of Mollusca: Gastropoda. In Kinne, O. (ed.) Diseases of marine animals. Volume I. General aspects, Protozoa to Gastropoda. Chichester: John Wiley & Sons, pp. 311–424.Google Scholar
Lillebø, A.I., Pardal, M.A. and Marques, J.C. (1999) Population structure, dynamics and production of Hydrobia ulvae (Pennant, 1777) (Mollusca: Prosobranchia) along an eutrophication gradient in the Mondego Estuary (Portugal). Acta Oecologica 20, 289–304.CrossRefGoogle Scholar
Lopes, R.J., Cabral, J.A., Múrias, T., Pacheco, C. and Marques, J.C. (2002) Status and habitat use of waders in the Mondego Estuary. In Pardal, M.Â., Marques, J.C. and Graça, M.A. (eds) Aquatic ecology of the Mondego River basin. Global importance of local experience. Coimbra: Imprensa da Universidade de Coimbra, pp. 219–230.Google Scholar
Martins, I., Pardal, M.A., Lillebø, A.I., Flindt, M.R. and Marques, J.C. (2001) Hydrodynamics as a major factor controlling the occurrence of green macroalgal blooms in a eutrophic estuary: a case study on the influence of precipitation and river management. Estuarine, Coastal and Shelf Science 52, 165–177.CrossRefGoogle Scholar
Meißner, K. and Bick, A. (1999) Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae)—laboratory studies. Diseases of Aquatic Organisms 35, 47–52.CrossRefGoogle Scholar
Montaudouin, X., de Blanchet, H., Kisielewski, I., Desclaux, C. and Bachelet, G. (2003) Digenean trematodes moderately alter Hydrobia ulvae population size structure. Journal of the Marine Biological Association of the United Kingdom 83, 297–305.CrossRefGoogle Scholar
Mouritsen, K.N. and Jensen, K.T. (1994) The enigma of gigantism: effect of larval trematodes on growth, fecundity, ingestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology 181, 53–56.CrossRefGoogle Scholar
Mouritsen, K.N. and Jensen, K.T. (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123–134.CrossRefGoogle Scholar
Mouritsen, K.N. (2002) 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.CrossRefGoogle ScholarPubMed
Mouritsen, K.N., Tompkins, D.N. and Poulin, R. (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146, 476–483.CrossRefGoogle Scholar
Múrias, T., Cabral, J.A., Marques, J.C. and Goss-Custard, J.D. (1996) Short-term effects on intertidal macroalgal blooms on the macrohabitat selection and feeding behaviour of wading birds in the Mondego Estuary (West Portugal). Estuarine, Coastal and Shelf Science 43, 677–688.CrossRefGoogle Scholar
Norkko, J., Bonsdorf, E. and Norkko, A. (2000) Drifting algal mats as an alternative habitat for benthic invertebrates: species specific responses to a transient resource. Journal of Experimental Marine Biology and Ecology 248, 79–104.CrossRefGoogle ScholarPubMed
Pardal, M.A., Cardoso, P.G., Sousa, J.P., Marques, J.C. and Raffaelli, D. (2004) Assessing environmental quality: a novel approach. Marine Ecology Progress Series 267, 1–8.CrossRefGoogle Scholar
Probst, S. and Kube, J. (1999) Histopathological effects of larval trematode infections in mud snails and their impact on host growth: what causes gigantism in Hydrobia ventrosa (Gastropoda: Prosobranchia)? Journal of Experimental Marine Biology and Ecology 238, 49–68.CrossRefGoogle Scholar
Rothschild, M. (1936) Gigantism and variation in Peringia ulvae Pennant (1777), caused by infection with larval trematodes. Journal of the Marine Biological Association of the United Kingdom 20, 537–546.CrossRefGoogle Scholar
Short, F., Carruthers, T., Dennison, W. and Waycott, M. (2007) Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology 350, 3–20.CrossRefGoogle Scholar
Sola, J.C. (1996) Population dynamics, reproduction, growth, and secondary production of the mud-snail Hydrobia ulvae (Pennant). Journal of Experimental Marine Biology and Ecology 205, 49–92.CrossRefGoogle Scholar
The Ramsar Convention on Wetlands (2007) What's New @ Ramsar—Portugal designates five varied Ramsar sites. Accessed 14 July 2007, at http://www.ramsar.org/wn/w.n.portugal_five.htmGoogle Scholar
Thieltges, D.W., Krakau, M., Andresen, H., Fottner, S. and Reise, K. (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research 60, 307–316.CrossRefGoogle Scholar
Zander, C.D., Reimer, L.W., Barz, K., Dietel, G. and Strohbach, U. (2000) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). II. Guild communities, with special regard to snails, benthic crustaceans and small-sized fish. Parasitology Research 86, 359–372.CrossRefGoogle ScholarPubMed
Zar, J. (1996) Biostatistical analysis. 3rd edition. Upper Saddle River, NJ: Prentice-Hall.Google Scholar