Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-22T17:36:28.258Z Has data issue: false hasContentIssue false
  • English
  • Français

Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline

Published online by Cambridge University Press:  26 March 2009

Xavier de Montaudouin ,
David W. Thieltges ,
Mériame Gam ,
Manuela Krakau ,
Suzana Pina ,
Hocein Bazairi ,
Laurent Dabouineau ,
Fernanda Russell-Pinto  and
K. Thomas Jensen
Xavier de Montaudouin*
Affiliation:
Université de Bordeaux, UMR EPOC 5805, Station Marine d'Arcachon, 2 rue du Pr Jolyet, F-33120 Arcachon, France
David W. Thieltges
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
Mériame Gam
Affiliation:
Université Hassan II Aïn Chock, Faculté des Sciences Aïn Chock, Départment de Biologie, Km 8 Route El Jadida, BP 5366 Maârif, 20100 CasablancaMorocco
Manuela Krakau
Affiliation:
Foundation Alfred Wegener Institute for Polar and Marine Research, Wadden Sea Station Sylt, Hafenstraße 43, 25992 List/Sylt, Germany
Suzana Pina
Affiliation:
Laboratory of Aquatic Zoology, Department of Aquatic Production, ICBAS, Abel Salazar Institute for Biomedical SciencesLg. Prof. Abel Salazar 2, 4009-003 Porto, Portugal
Hocein Bazairi
Affiliation:
Université Hassan II Aïn Chock, Faculté des Sciences Aïn Chock, Départment de Biologie, Km 8 Route El Jadida, BP 5366 Maârif, 20100 CasablancaMorocco
Laurent Dabouineau
Affiliation:
Campus de la Tour d'Auvergne BP 90431, Université UCO Bretagne Nord, 22 204 Guingamp, France
Fernanda Russell-Pinto
Affiliation:
Laboratory of Aquatic Zoology, Department of Aquatic Production, ICBAS, Abel Salazar Institute for Biomedical SciencesLg. Prof. Abel Salazar 2, 4009-003 Porto, Portugal
K. Thomas Jensen
Affiliation:
Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Finlandsgade 14, DK-8200 Aarhus, Denmark
*
Correspondence should be addressed to: X. de Montaudouin, Université de Bordeaux, UMR EPOC 5805, Station Marine d'Arcachon 2 rue du Pr Jolyet, F-33120 Arcachon, France email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We describe the digenean fauna of one of the dominant intertidal hosts, the common cockle Cerastoderma edule, in terms of biomass, off north-eastern Atlantic shores. Using published and unpublished literature we have prepared an identification key and provide an up-date of the large-scale distributional patterns of digenean species of the common cockle. At least sixteen digenean species, belonging to seven families, use cockles as intermediate host. Among these species two utilize cockles as first intermediate host only, whereas two species utilize cockles as both first and second intermediate host. The remaining eleven species have cockles as their second intermediate host. Water birds and fish are the definitive hosts to twelve and four species, respectively.

Cockles are infected with digeneans along the latitudinal gradient from southern Morocco to the western region of the Barents Sea often with high infection levels. Whereas some of these digenean species occur along most of the latitudinal gradient others show a more restricted northern or southern distribution mostly caused by an underlying latitudinal gradient of host species.

Knowledge of digenean species and their large-scale distribution pattern may serve as a baseline for future studies dealing with the effects of climate change on parasite–host systems. For such studies the cockle and its digenean community could be an ideal model system.

Keywords

parasitismlatitudinal patternsCerastoderma eduleidentification key
Type
Review
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 3 , May 2009 , pp. 543 - 556
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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

Bartoli, P., Jousson, O. and Russell-Pinto, F. (2000) The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. Journal of Parasitology 86, 479–489.CrossRefGoogle ScholarPubMed
Baudrimont, M., de Montaudouin, X. and Palvadeau, A. (2006) Impact of digenean parasites infection on metallothionein synthesis by the cockle (Cerastoderma edule): a multivariate field monitoring. Marine Pollution Bulletin 52, 494–502.Google Scholar
Bowers, E.A. (1969) Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Digenea: Bucephalidae) in the cockle, Cardium edule L. in South Wales. Journal of Natural History 3, 409–422.Google Scholar
Bowers, E.A. and James, B.L. (1967) Studies on the morphology, ecology and life-cycle of Meiogymnophallus minutus (Cobbold, 1859) comb. nov. (Trematoda: Gymnophallidae). Parasitology 57, 281–300.CrossRefGoogle ScholarPubMed
Bowers, E.A., Bartoli, P. and James, B.L. (1990) A demonstration of allopatric sibling species within the Gymnophallidae (Digenea). Systematic Parasitology 17, 143–152.Google Scholar
Bowers, E.A., Bartoli, P., Russell-Pinto, F. and James, B.L. (1996) The metacercariae of sibling species of Meiogymnophallus, including M. rebecqui comb. nov. (Digenea: Gymnophallidae), and their effects on closely related Cerastoderma host species (Mollusca: Bivalvia). Parasitology Research 82, 505–510.CrossRefGoogle ScholarPubMed
Boyden, C.R. (1971) A comparative study of the reproductive cycles of the cockles Cerastoderma edule and C. glaucum. Journal of the Marine Biological Association of the United Kingdom 51, 605–622.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
de Montaudouin, X., Wegeberg, A.M., Jensen, K.T. and Sauriau, P.G. (1998) Infection characteristics of Himasthla elongata cercaria in cockles as a function of water current. Diseases of Aquatic Organisms 34, 63–70.CrossRefGoogle Scholar
de Montaudouin, X., Kisielewski, I., Bachelet, G. and Desclaux, C. (2000) A census of macroparasites in an intertidal bivalve community, Arcachon Bay, France. Oceanologica Acta 23, 453–468.Google Scholar
de Montaudouin, X., Jensen, K.T., Desclaux, C., Wegeberg, A.M. and Sajus, M.C. (2005) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of Himasthla quissetensis (Echinostomatidae: Trematoda). Journal of the Marine Biological Association of the United Kingdom 85, 809–812.Google Scholar
Deltreil, J.P. and His, E. (1972) Evolution d'un gisement de Cardium edule LMK dans le Bassin d'Arcachon. Revue des Travaux de l'Institut des Pêches Maritimes 36, 301–308.Google Scholar
Desclaux, C. (2003) Interactions hôtes–parasites: diversité, mécanismes d'infestation et impact des trématodes digènes sur les coques Cerastoderma edule (mollusque bivalve) en milieu lagunaire macrotidal. PhD thesis. University Bordeaux 1.Google Scholar
Desclaux, C., de Montaudouin, X. and Bachelet, G. (2002) Cockle emergence at the sediment surface: ‘favourization’ mechanism by digenean parasites? Diseases of Aquatic Organisms 52, 137–149.Google Scholar
Desclaux, C., de Montaudouin, X. and Bachelet, G. (2004) Cockle (Cerastoderma edule) population mortality: the role of the digenean parasite Himasthla quissetensis. Marine Ecology Progress Series 279, 141–150.Google Scholar
Desclaux, C., Russell-Pinto, F., de Montaudouin, X. and Bachelet, G. (2006) First record and description of metacercariae of Curcuteria arguinae n. sp. (Digenea: Echinostomatidae), parasite of cockles Cerastoderma edule (Mollusca: Bivalvia) in Arcachon Bay, France. Journal of Parasitology 92, 578–587.Google Scholar
Evans, N.A. (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269–275.Google Scholar
Ferrell, D.L., Negovetich, N.J. and Wetzel, E.J. (2001) Effect of temperature on the infectivity of metacercariae of Zygocotyle lunata (Digenea: Paramphistomidae). Journal of Parasitology 87, 10–13.CrossRefGoogle ScholarPubMed
Gam, M., Bazaïri, H., Jensen, K.T. and de Montaudouin, X. (2008) Metazoan parasites in an intermediate host population near its southern border: the common cockle (Cerastoderma edule) and its trematodes in a Moroccan coastal lagoon (Merja Zerga). Journal of the Marine Biological Association of the United Kingdom 88, 357–364.CrossRefGoogle Scholar
Goater, C.P. (1993) Population biology of Meiogymnophallus minutus (Trematoda: Gymnophallidae) in cockles from the Exe Estuary. Journal of the Marine Biological Association of the United Kingdom 73, 163–177.Google Scholar
Goater, C.P. (1995) Population dynamics of two species of intestinal helminth in oystercatchers (Haematopus ostralegus). Canadian Journal of Zoology 73, 296–300.Google Scholar
Hakalahti, T., Karvonen, A. and Valtonen, E.T. (2006) Climate warming and disease risks in temperate regions—Argulus coegoni and Diplostomum spathaceum as case studies. Journal of Helminthology 80, 93–98.Google Scholar
Hancock, D.A. and Urquhart, A.E. (1965) The determination of natural mortality and its causes in an exploited population of cockles (Cardium edule L.). Fishery Investigations 24, 1–40.Google Scholar
Hayes, M.L., Bonaventura, J., Mitchell, T.P., Prospero, J.M., Shinn, E.A., Van Dolah, F. and Barber, R.T. (2001) How are climate and marine biological outbreaks functionally linked? Hydrobiologia 460, 213–220.Google Scholar
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 272, 1059–1066.Google Scholar
Hechinger, R.F., Lafferty, K.D., Huspeni, T.C., Brooks, A.J. and Kuris, A.M. (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 82–92.Google Scholar
Hudson, P.J., Dobson, A.P. and Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.CrossRefGoogle Scholar
James, B.L. and Bowers, E.A. (1967) Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae). Parasitology 57, 607–625.Google Scholar
James, B.L., Sannia, A. and Bowers, E.A. (1977) Parasites of birds and shellfish. In Nelson-Smith, A. and Bridges, E.M. (eds) Problems of a small estuary. Swansea: Publication of the Institute of Marine Studies and Quadrant Press, pp. 1–16.Google Scholar
Jensen, K.T., Latama, G. and Mouritsen, K.N. (1996) The effect of larval trematodes on the survival rates of two species of mud snails (Hydrobiidae) experimentally exposed to desiccation, freezing and anoxia. Helgoländer Meeresuntersuchungen 50, 327–335.CrossRefGoogle Scholar
Jensen, K.T., Fernández Castro, N. 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.Google Scholar
Jonsson, P.R. and André, C. (1992) Mass mortality of the bivalve Cerastoderma edule on the Swedish west coast caused by infestation with the digenean trematode Cercaria cerastodermae I. Ophelia 36, 151–157.Google Scholar
Kesting, V., Gollasch, S. and Zander, C.D. (1996) Parasite communities of the Schlei Fjord (Baltic coast of northern Germany). Helgoländer Meeresuntersuchungen 40, 477–496.Google Scholar
Krakau, M., Thieltges, D.W. and Reise, K. (2006) Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919–925.CrossRefGoogle Scholar
Kutz, S.J., Hoberg, E.P., Polley, L. and Jenkins, E.J. (2005) Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society B 272, 2571–2576.Google Scholar
Lassalle, G., de Montaudouin, X., Soudant, P. and Paillard, C. (2007) Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient. Aquatic Living Resource 20, 33–42.Google Scholar
Lauckner, G. (1971) Zur Trematodenfauna der Herzmuscheln Cardium edule und Cardium lamarcki. Helgoländer Wissenchaft Meeresuntersuchungen 22, 377–400.Google Scholar
Lauckner, G. (1983) Diseases of Mollusca: Bivalvia. In Kinne, O. (ed.) Diseases of marine animals. Hamburg: Biologische Anstalt Helgoland, pp. 477–961.Google Scholar
Lauckner, G. (1984) Impact of trematode parasitism on the fauna of a North Sea tidal flat. Helgoländer Meeresuntersuchungen 37, 185–199.CrossRefGoogle Scholar
Lebour, M.V. (1911) A review of the British marine cercariae. Parasitology 4, 416–456.Google Scholar
Littlewood, D.T.J. (2005) Marine parasites and the tree of life. In Rohde, K. (eds) Marine parasitology. Oxford: CABI Publishing, pp. 6–10.Google 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
Loos-Frank, B. (1968) Der Entwicklungszyklus von Psilostomum brevicolle (Creplin, 1829) [Syn.: P. platyurum (Mühling, 1896)] (Trematoda, Psilostomatidae). Zeitschrift für Parasitenkunde 31, 122–131.Google Scholar
Loos-Frank, B. (1969) Zur Kenntis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativ-Zyklen von Gymnophallus choledochus Odhner 1900. Zeitschrift für Parasitenkunde 32, 135–156.Google Scholar
Loos-Frank, B. (1971) Zur Kenntis der gymnophalliden Trematoden des Nordseeraumes. III. Gymnophallus gibberosus n. sp. und seine Metacercarie. Zeitschrift für Parasitenkunde 35, 270–281.Google Scholar
Maillard, C. (1976) Distomatoses de poissons en milieu lagunaire. PhD thesis. University Sciences et Techniques du Languedoc.Google Scholar
Malek, M. (2001) Effects of the digenean parasites Labratrema minimus and Cryptocotyle concavum on the growth parameters of Pomatoschistus microps and P. minutus from Southwest Wales. Parasitology Research 87, 349–355.Google Scholar
Markowski, S. (1936) Über die Trematodenfauna der baltischen Mollusken aus der Umgebung der Halbinsel Hel. Bulletin International de l'Académie Polonaise des Sciences et Lettres 1936, 285–317.Google Scholar
Mouritsen, K.N. (2002) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124, 521–528.Google 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. and Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystem. Parasitology 124, 101–117.Google Scholar
Mouritsen, K.N., Tompkins, D.M. and Poulin, R. (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146, 476–483.Google Scholar
Pelseneer, P. (1906) Parasites de mollusques marins. Bulletin Scientifique de la France et de la Belgique 40, 161–186.Google Scholar
Pina, S., Barandela, T., Santos, M.J., Russell-Pinto, F. and Rodrigues, P. (in press) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological and molecular data. Journal of Parasitology.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 Morand, S. (2000) The diversity of parasites. Quarterly Review of Biology 75, 277–293.Google Scholar
Poulin, R. and Mouritsen, K.N. (2006) Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80, 183–191.Google Scholar
Prévot, G. (1966) Sur deux trématodes larvaires d'Antedon mediterranea Lmk. (Echinoderme): Metacercaria sp. (Monorchiidae Odhner, 1911), et métacercaire de Diphterostomum brusinae Stoss., 1904 (Zoogonidae Odhner, 1911). Annales de Parasitologie 41, 233–242.Google Scholar
Reimer, L.W. (1970) Digene Trematoden und Cestoden der Ostseefische als natürliche Fischmarken. Parasitologische Schriftenreihe 20, 1–144.Google Scholar
Reimer, L.W. (1973) Das Auftreten eines Fischtrematoden der Gattung Asymphylodora Looss, 1899, bei Nereis diversicolor O.F. Müller als Beispiel für einen Alternativzyklus. Zoologischer Anzeiger 191, 187–196.Google Scholar
Russell-Pinto, F. (1990) Differences in infestation intensity and prevalence of hinge and mantle margin Meiogymnophallus minutus metacercariae (Gymnophallidae) in Cerastoderma edule (Bivalvia): possible species coexistence in Ria de Aveiro. Journal of Parasitology 76, 653–659.Google Scholar
Russell-Pinto, F. (1993) Espécies de digenea que infectam Cerastoderma edule (n.v. berbigão) em Portugal. Caracterização da resposta do hospedeiro à infestação. PhD thesis. University of Porto, Portugal.Google Scholar
Russell-Pinto, F. and Bartoli, P. (1992) Sympatric distribution of Meiogymnophallus minutus and M. fossarum (Digenea: Gymnophallidae) in Cerastoderma edule in the Ria de Aveiro estuary in Portugal. Parasitology Research 78, 617–618.Google Scholar
Russell-Pinto, F. and Bowers, E.A. (1998) Ultrastructural studies on the tegument of the metacercariae of Meiogymnophallus minutus and Meiogymnophallus fossarum (Digenea: Gymnophallidae) in Cerastoderma edule from Portugal. Journal of Parasitology 84, 715–722.CrossRefGoogle ScholarPubMed
Russell-Pinto, F., Gonçalves, J.F. and Bowers, E. (2006) Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro, Portugal. Journal of Parasitology 92, 319–332.CrossRefGoogle ScholarPubMed
Sannia, A. and James, B.L. (1978) The occurrence of Cercaria cerastodermae I Sannia, James, and Bowers, 1978 (Digenea: Monorchiidae) in populations of Cerastoderma edule (L.) from the commercial beds of the Lower Thames Estuary. Zeitschrift für Parasitenkunde 56, 1–11.Google Scholar
Sannia, A., James, B.L. and Bowers, E.A. (1978) The morphology of Cercaria cerastodermae I nom. nov. (Monorchiidae) (=Cercaria lepidapedon rachion (Cobbold, 1858) sensu Lebour, 1908) a rare digenean parasite of the cockle in Britain. Journal of Natural History 12, 487–500.Google Scholar
Sauriau, P.-G. (1992) Les mollusques benthiques du bassin de Marennes-Oléron: estimation et cartographie des stocks non cultivés, compétition spatiale et trophique, dynamique de population de Cerastoderma edule (L.). PhD thesis. University of Bretagne Occidentale.Google Scholar
Smyth, J.D. (1994) Introduction to animal parasitology, 3rd edition.Cambridge, UK: Cambridge University Press.Google Scholar
Sousa, W.P. and Gleason, M. (1989) Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia). Oecologia 80, 456–464.Google Scholar
Stunkard, H.W. (1938) The morphology and life cycle of the trematode Himasthla quissetensis (Miller and Northup, 1926). Biological Bulletin. Marine Biological Laboratory, Woods Hole 75, 145–164.Google Scholar
Thieltges, D.W. (2006) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455–461.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. (2008) Effect of host size and temporal exposure on metacercarial infection levels in the intertidal cockle Cerastoderma edule. Journal of the Marine Biological Association of the United Kingdom 88, 613–616.Google Scholar
Thieltges, D.W. and Reise, K. (2006) Metazoan parasites in intertidal cockles Cerastoderma edule from the northern Wadden Sea. Journal of Sea Research 56, 284–293.CrossRefGoogle 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. 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., 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.Google Scholar
Thieltges, D.W., Hussel, B., Hermann, J., Jensen, K.T., Krakau, M., Taraschewski, H. and Reise, K. (2008) Parasites in the northern Wadden Sea: a conservative ecosystem component over 4 decades. Helgoland Marine Research 62, 37–47.Google Scholar
Thieltges, D.W., Donas-Botto Bordalo, M., Cabalero Hernández, A., Prinz, K. and Jensen, K.T. (in press) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology.Google Scholar
Vaullegeard, A. (1894) Note sur la présence du Bucephalus haimeanus (Lacaze Duthiers) dans le Tapes ducussatus (Linné) et dans le Tapes pullastra (Montagu). Bulletin de la Société Linnéenne de Normandie 8, 8–14.Google Scholar
Wegeberg, A.M. and Jensen, K.T. (1999) Reduced survivorship of Himasthla (Trematoda, Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. Journal of Sea Research 42, 325–331.Google Scholar
Wegeberg, A.M. and Jensen, K.T. (2003) In situ growth of juvenile cockles, Cerastoderma edule, experimentally infected with larval trematodes (Himasthla interrupta). Journal of Sea Research 50, 37–43.CrossRefGoogle Scholar
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
Werding, B. (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306–333.CrossRefGoogle Scholar
Windsor, D.A. (1998) Most of the species on Earth are parasites. International Journal for Parasitology 28, 1939–1941.Google Scholar