Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T05:08:35.612Z Has data issue: false hasContentIssue false

Monorchis parvus and Gymnophallus choledochus: two trematode species infecting cockles as first and second intermediate host

Published online by Cambridge University Press:  04 March 2020

Luísa Magalhães*
Affiliation:
CESAM - Centre for Environmental and Marine Studies, Departamento de Biologia, Universidade de Aveiro, 3810-193 Aveiro, Portugal
Guillemine Daffe
Affiliation:
Université de Bordeaux, CNRS, Observatoire Aquitain des Sciences de l'Univers, UMS 2567 POREA, F-33615, Pessac, France
Rosa Freitas
Affiliation:
CESAM - Centre for Environmental and Marine Studies, Departamento de Biologia, Universidade de Aveiro, 3810-193 Aveiro, Portugal
Xavier de Montaudouin
Affiliation:
Université de Bordeaux, CNRS, UMR EPOC, Station Marine, 2, rue du Pr Jolyet, F-33120, Arcachon, France
*
Author for correspondence: Luísa Magalhães, E-mail: [email protected]

Abstract

The most deleterious stage of a trematode life cycle occurs in the first intermediate host where the parasite penetrates as a miracidium and asexually multiplicates in sporocysts or rediae. When infection advances, other organs can be occupied with severe effects on host individual health and population dynamics. Existing studies focused on these host/parasite systems are still scarce due to the usual low prevalence in ecosystems. Using cockles (Cerastoderma spp.) and two trematode species (Monorchis parvus and Gymnophallus choledochus) infecting these bivalves as first and second intermediate host, the present work aimed to (1) summarize the most relevant literature and (2) provide new information regarding this host/parasite system, taking advantage of a 21-year monthly database from Banc d'Arguin (France). This long-term monitoring showed that different trematode species display varying host size range preference (6–38 and 31–36 mm for M. parvus and G. choledochus, respectively). The occurrence of coinfection was lower than expected, raising some questions related to parasite interspecific competition. This review improved our understanding of the processes shaping the prevalence and distribution of parasitism. This study highlighted that beyond constant trematode assemblage monitoring, there is a need to identify the main predictors of rediae/sporocysts infection, such as the definitive host dynamics and miracidium infection processes, for future better management of host severe disease and mortality episodes.

Type
Review Article
Copyright
Copyright © The Author(s), 2020. Published by 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

Antar, R and Ben Abdallah, LG (2013) Trematodes in fishes of the genus Diplodus (Teleostei, Sparidae) from Bizerte Lagoon (Northern coast of Tunisia). Bulletin of the European Association of Fish Pathologists 33, 4452.Google Scholar
Baiocchi, T, Lee, G, Choe, DH and Dillman, AR (2017) Host seeking parasitic nematodes use specific odors to assess host resources. Scientific Reports 7, 113.CrossRefGoogle ScholarPubMed
Bartoli, P (1971) Recherches sur les gymnophallidae f. n. morozov, 1955 (digenea), parasites d'oiseaux des cotes de camargue: systematique, biologie et ecologie (PhD thesis). Aix Marseille 3, France.Google Scholar
Bartoli, P (1974) Competitive exclusion case among trematodes: elimination of Gymnophallus choledochus T. Odhner, 1900 by Gymnophallus nereicola J. Rebecq and G. Prevot, 1962 in Camargue (France) (Digenea, Gymnophallidae). Bulletin de La Societe Zoologique De France-Evolution Et Zoologie 99, 551559.Google Scholar
Bartoli, P (1981) Démographie et phénomène de compétition intraspécifique des Gymnophallidae Morozov, 1955 chez les deuxièmes hôtes intermédiaires. Annales de Parasitologie 56, 3344.CrossRefGoogle Scholar
Bartoli, P (1984) Distomatoses des Lamellibranches marins sur le littoral mediterraneen français. Haliotis 14, 98107.Google Scholar
Bartoli, P and Combes, C (1986) Stratégies de dissémination des cercaires de trématodes dans un écosystème marin littoral. Acta Oecologica 7, 101114.Google Scholar
Bartoli, P and Gibson, DI (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History 41, 15531570.CrossRefGoogle Scholar
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, 479489.CrossRefGoogle ScholarPubMed
Bartoli, P, Gibson, DI and Bray, RA (2005) Digenean species diversity in teleost fish from a nature reserve off Corsica, France (Western Mediterranean), and a comparison with other Mediterranean regions. Journal of Natural History 39, 4770.CrossRefGoogle Scholar
Basch, PF, Lie, KJ and Heyneman, D (1969) Antagonistic interaction between Strigeid and Schistosome sporocysts within a snail host. Journal of Parasitology 55, 753758.CrossRefGoogle ScholarPubMed
Bauchot, ML (1987) Sparidae. In Fischer, W, Bauchot, ML and Schneider, M (eds), Fiches FAO d'Indentification des espèces pour les Besoins de la Pêche (Revison 1), Méditerranée et Mer Noire. Zones de pechê 37, vol. II (Vertébrés). Rome: FAO-CEE, pp. 7611530.Google Scholar
Baudrimont, M, de Montaudouin, X and Palvadeau, A (2003) Bivalve vulnerability is enhanced by parasites through the deficit of metallothionein synthesis: a field monitoring on cockles (Cerastoderma edule). Journal de Physique IV 107, 131134.Google Scholar
Binning, SA, Shaw, AK and Roche, DG (2017) Parasites and host performance: incorporating infection into our understanding of animal movement. Integrative and Comparative Biology 57, 267280.CrossRefGoogle ScholarPubMed
Bojko, J, Grahame, JW and Dunn, AM (2017) Periwinkles and parasites: the occurrence and phenotypic effects of parasites in Littorina saxatilis and L. arcana in Northeastern England. Journal of Molluscan Studies 83, 6978.CrossRefGoogle Scholar
Bowers, EA (1965) Studies on some parasites of sea birds and molluscs (PhD thesis). University College of Swansea, Swansea.Google Scholar
Bowers, EA (1969) Cercaria Bucephalopsis Haimeana (Lacaze-Duthiers, 1854) (Digenea: Bucephalidae) in cockle, Cardium edule L. in south Wales. Journal of Natural History 3, 409422.CrossRefGoogle Scholar
Bowers, EA and James, BL (1967) Studies on morphology, ecology and life-cycle of Meiogymnophallus minutus (Cobbold 1859) com. nov. (Trematoda-Gymnophallidae). Parasitology 57, 281300.CrossRefGoogle Scholar
Bowers, EA, Bartoli, P, Russell-Pinto, F and James, BL (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, 505510.CrossRefGoogle Scholar
Boyden, CR (1970) Comparative studies on Cerastoderma edule (L.) and Cerastoderma glaucum (Poiret) (PhD thesis). Queen Mary College, London.Google Scholar
Bozhkov, DK and Odening, K (1979) Problem of variable numbers of hosts in the life-cycles of Helminths. Folia Parasitologica 26, 1519.Google ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al Revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cheng, TC (1967) Marine Molluscs as hosts for symbioses – with a review of known parasites of commercially important species. In Russell, FS (ed.), Advances in Marine Biology, Book 5, pp. 226. Plymouth, UK: Elsevier.Google Scholar
Ching, HL (1995) Evaluation of characters of the digenean family Gymnophallidae Morozov, 1955. Canadian Journal of Fisheries and Aquatic Sciences 52, 7883.CrossRefGoogle Scholar
COCKLES Project (2017–2020) Co-operation for restoring CocKle SheLlfisheries & its ecosystem-services in the Atlantic Area, EAPA_458/2016.Google Scholar
Correia, S, Magalhães, L, Freitas, R, Bazairi, H, Gam, M and de Montaudouin, X (2020) Large scale patterns of trematode parasite communities infecting Cerastoderma edule along the Atlantic coast from Portugal to Morocco. Estuarine, Coastal and Shelf Science 233, 106546.CrossRefGoogle Scholar
Cremonte, F, Gilardoni, C, Pina, S, Rodrigues, P and Ituarte, C (2015) Revision of the family Gymnophallidae Odhner, 1905 (Digenea) based on morphological and molecular data. Parasitology International 64, 202210.CrossRefGoogle ScholarPubMed
Cribb, TH, Bray, RA, Olson, PD and Littlewood, DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197254.CrossRefGoogle ScholarPubMed
de Montaudouin, X, Wegeberg, AM, Jensen, KT and Sauriau, PG (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Diseases of Aquatic Organisms 34, 6370.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, 453468.CrossRefGoogle Scholar
de Montaudouin, X, Thieltges, DW, Gam, M, Krakau, M, Pina, S, Bazairi, H, Dabouineau, L, Russell-Pinto, F and Jensen, KT (2009) Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline. Journal of the Marine Biological Association of the United Kingdom 89, 543556.CrossRefGoogle Scholar
de Montaudouin, X, Bazairi, H, Mlik, KA and Gonzalez, P (2014) Bacciger bacciger (Trematoda: Fellodistomidae) infection effects on wedge clam Donax trunculus condition. Diseases of Aquatic Organisms 111, 259267.CrossRefGoogle ScholarPubMed
Derbali, A, Jarboui, O and Ghorbel, M (2009) Reproductive biology of the cockle Cerastoderma glaucum (Mollusca: Bivalvia) from the north coast of Sfax (Gulf of Gabes, Tunisia). Ciencias Marinas 35, 141152.CrossRefGoogle 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). Université Bordeaux I, France.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, 137149CrossRefGoogle ScholarPubMed
Desclaux, C, Russell-Pinto, F, de Montaudouin, X and Bachelet, G (2006) First record and description of Metacercariae of Curtuteria arguinae n. sp. (Digenea: Echinostomatidae), parasite of cockles Cerastoderma edule (Mollusca: Bivalvia) in Arcachon Bay, France. Journal of Parasitology 92, 578587.CrossRefGoogle ScholarPubMed
Donadi, S, van der Zee, EM, van der Heide, T, Weerman, EJ, Piersma, T, de Koppel, JV, Olff, H, Bartelds, M, van Gerwen, I and Eriksson, BK (2014) The bivalve loop: intra-specific facilitation in burrowing cockles through habitat modification. Journal of Experimental Marine Biology and Ecology 461, 4452.CrossRefGoogle Scholar
Dubois, SY, Savoye, N, Sauriau, PG, Billy, I, Martinez, P and de Montaudouin, X (2009) Digenean trematodes-marine mollusc relationships: a stable isotope study. Diseases of Aquatic Organisms 84, 6577.CrossRefGoogle ScholarPubMed
Feis, ME, Thieltges, DW, Olsen, JL, de Montaudouin, X, Jensen, KT, Bazairi, H, Culloty, SC and Luttikhuizen, PC (2015) The most vagile host as the main determinant of population connectivity in marine macroparasites. Marine Ecology Progress Series 520, 8599.CrossRefGoogle Scholar
Fermer, J, Culloty, SC, Kelly, TC and O'Riordan, RM (2011) Parasitological survey of the edible cockle Cerastoderma edule (Bivalvia) on the south coast of Ireland. Journal of the Marine Biological Association of the United Kingdom 91, 923928.CrossRefGoogle Scholar
Fernandez-Reiriz, MJ, Garrido, JL and Irisarri, J (2015) Fatty acid composition in Mytilus galloprovincialis organs: trophic interactions, sexual differences and differential anatomical distribution. Marine Ecology Progress Series 528, 221234.CrossRefGoogle Scholar
Figus, V, Culurgioni, J, De Murtas, R and Canestri Trotti, G (2004) Parasites of the Lagoon cockle, Cerastoderma glaucum (Poiret, 1789) (Bivalvia: Cardiidae), from Marceddì and St. Gilla Lagoons (Sardinia, Western Mediterranean). Biologia Marina Mediterranea 11, 385388.Google Scholar
Frank, B (1969) Der bemerkenswerte Lebenszyklus des marinen Vogeltrematoden Gymnophallus choledochus. Journal fur Ornithologie 4, 471474.CrossRefGoogle Scholar
Freitas, R, Martins, R, Campino, B, Figueira, E, Soares, AMVM and Montaudouin, X (2014) Trematode communities in cockles (Cerastoderma edule) of the Ria de Aveiro (Portugal): influence of inorganic contamination. Marine Pollution Bulletin 82, 117126.CrossRefGoogle Scholar
Friesen, OC, Poulin, R and Lagrue, C (2017) Differential impacts of shared parasites on fitness components among competing hosts. Ecology and Evolution 7, 46824693.CrossRefGoogle ScholarPubMed
Galaktionov, KV and Dobrovolskij, AA (2003) The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. St. Petersburg, Russia: Kluwer Academic Publishers.CrossRefGoogle Scholar
Gam, M, Bazairi, H, Jensen, KT 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, 357364.CrossRefGoogle Scholar
Garcia-Souto, D and Pasantes, JJ (2015) Molecular cytogenetics in Digenean parasites: linked and unlinked major and 5S rDNAs, B chromosomes and karyotype diversification. Cytogenetic and Genome Research 147, 195207.CrossRefGoogle ScholarPubMed
Gargouri Ben Abdallah, L and Maamouri, F (2008) Digenean fauna diversity in Sparid fish from Tunisian coasts. Bulletin of the European Association of Fish Pathologists 28, 129137.Google Scholar
Howard, C, Stephens, PA, Tobias, JA, Sheard, C, Butchart, SHM and Willis, SG (2018) Flight range, fuel load and the impact of climate change on the journeys of migrant birds. Proceedings of the Royal Society B-Biological Sciences 285, 19.CrossRefGoogle ScholarPubMed
Huet, M (1888) Note sur un parasite nouveau du Cardium edule. Bulletin de la Société Linnéenne de Normandie 1, 149152.Google Scholar
Hutton, RF (1952) Studies on the parasites of Cardium edule L.: Cercaria fulbrighti n. sp., a Gymnophallus larva with a forked tail. Journal of the Marine Biological Association of the United Kingdom 31, 317326.CrossRefGoogle Scholar
Iglesias, D (2006) Estudio patológico de las poblaciones de Berberecho Cerastoderma edule (L.) de Galicia (PhD thesis). Universidade de Santiago de Compostela, Galicia.Google Scholar
Iglesias, JIP, Navarro, E, Jorna, PA and Armentia, I (1992) Feeding, particle selection and absorption in cockles Cerastoderma edule (L.) exposed to variable conditions of food concentration and quality. Journal of Experimental Marine Biology and Ecology 162, 177198.CrossRefGoogle Scholar
Isaitchikow, JM (1924) Individual variations in Gymnophalus choledochus (Odhner,1900). Comptes Rendus des Seances de La Societe de Biologie et de Ses Filiales 91, 11871189.Google Scholar
James, BL (1964) Life cycle of Parvatrema homoeotecnum sp. nov. (Trematoda-Digenea) and a review of the family Gymnophallidae Morozov 1955. Parasitology 54, 141.CrossRefGoogle Scholar
James, BL and Bowers, EA (1967) Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma lebour, 1911 (non Müller) (Gymnophalidae). Parasitology 57, 607625.CrossRefGoogle Scholar
Johnstone, J (1905) Internal parasites and diseased conditions of fishes. Proceedings and Transactions of the Liverpool Biological Society 19, 278292.Google Scholar
Jonsson, PR 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, 151157.CrossRefGoogle Scholar
Jousson, O and Bartoli, P (2002) Species diversity among the genus Monorchis (Digenea: Monorchiidae) parasitic in marine teleosts: molecular, morphological and morphometrical studies with a description of Monorchis bleanii n. sp. Parasitology Research 88, 230241.Google ScholarPubMed
Jousson, O, Bartoli, P and Pawlowski, J (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13, 778785.CrossRefGoogle Scholar
Krakau, M, Thieltges, DW and Reise, K (2006) Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919925.CrossRefGoogle Scholar
Kuris, AM and Lafferty, KD (1994) Community structure – larval trematodes in Snail hosts. Annual Review of Ecology and Systematics 25, 189217.CrossRefGoogle Scholar
Lauckner, G (1971) Trematode fauna of cockles Cardium edule and Cardium lamarcki. Helgolander Wissenschaftliche Meeresuntersuchungen 22, 377400.CrossRefGoogle Scholar
Lauckner, G (1983) Diseases of Mollusca: Bivalvia. In Kinne, O (ed.), Diseases of Marine Animals, Book 2, 1038 pp.. Hamburg, Germany: Biologische Helgoland.Google Scholar
Lebour (1905) Notes on Northumbria trematodes. Report on the Scientific Investigations. Northumberland Sea Fisheries Committee.Google Scholar
Lebour (1907a) Fish trematodes of the Northumberland Coast. Northumberland Sea Fisheries Report. Northumberland Sea Fisheries Committee.Google Scholar
Lebour (1907b) On three mollusk-infecting Trematodes. The Annals and Magazine of Natural History 19, 102106.CrossRefGoogle Scholar
Lebour (1908) Trematodes of the Northumberland Coast. Newcastle upon Tyne, UK: Armstrong College.Google Scholar
Lebour (1912) A review of the British marine cercariae. Parasitology 4, 416456.Google Scholar
Levron, C, Ternengo, S and Marchand, B (2004) Ultrastructure of spermiogenesis and the spermatozoon of Monorchis parvus Looss, 1902 (Digenea, Monorchiidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitology Research 93, 102110.CrossRefGoogle Scholar
Levron, C, Ternengo, S, Toguebaye, BS and Marchand, B (2005) Ultrastructural description of the life cycle of Nosema monorchis n. sp (Microspora, Nosematidae), hyperparasite of Monorchis parvus (Digenea, Monorchiidae), intestinal parasite of Diplodus annularis (Pisces, Teleostei). European Journal of Protistology 41, 251256.CrossRefGoogle Scholar
Loker, ES (1994) On being a parasite in an invertebrate host – a short survival course. Journal of Parasitology 80, 728747.CrossRefGoogle Scholar
Longshaw, M and Malham, SK (2013) A review of the infectious agents, parasites, pathogens and commensals of European cockles (Cerastoderma edule and C. glaucum). Journal of the Marine Biological Association of the United Kingdom 93, 227247.CrossRefGoogle Scholar
Loos-Frank, B (1969) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes I. Die Alternativ-Zyklen yon Gymnophallus Choledochus Odhner, 1900. Zeitschrift fur Parasitenkunde 32, 135156.Google Scholar
Loos-Frank, B (1971) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes IV. Übersicht über die gymnophalliden Larven aus Mollusken der Gezeitenzone. Zeitschrift fur Parasitenkunde 36, 206232.Google Scholar
Looss (1902) Zur kenntnis der trematoden-fauna des triester hafens. II. Ueber Monorchis Montic und Haplosplanchnus n.g. Centralblatt fur Bakteriologie. Parasitenkunde und Infektionskrankheiten 32, 115122.Google Scholar
Magalhães, L, Freitas, R and de Montaudouin, X (2015) Review: Bucephalus minimus, a deleterious trematode parasite of cockles Cerastoderma spp. Parasitology Research 114, 12631278.CrossRefGoogle ScholarPubMed
Magalhães, L, Freitas, R and de Montaudouin, X (2016) Cockle population dynamics: recruitment predicts adult biomass, not the inverse. Marine Biology 163, 16.CrossRefGoogle Scholar
Magalhães, L, de Montaudouin, X, Freitas, R, Daffe, G, Figueira, E and Gonzalez, P (2017) Seasonal variation of transcriptomic and biochemical parameters of cockles (Cerastoderma edule) related to their infection by trematode parasites. Journal of Invertebrate Pathology 148, 7380.CrossRefGoogle ScholarPubMed
Malham, SK, Hutchinson, TH and Longshaw, M (2012) A review of the biology of European cockles (Cerastoderma spp.). Journal of the Marine Biological Association of the United Kingdom 92, 15631577.CrossRefGoogle Scholar
Margolis, L (1973) Additional notes on polychaetes as intermediate hosts of helminth parasites of vertebrates. Journal of the Fisheries Research Board of Canada 30, 469470.CrossRefGoogle Scholar
Morgan, E, O'Riordan, RM, Kelly, TC and Culloty, SC (2012) Influence of disseminated neoplasia, trematode infections and gametogenesis on surfacing and mortality in the cockle Cerastoderma edule. Diseases of Aquatic Organisms 98, 7384.CrossRefGoogle ScholarPubMed
Morgan, E, O'Riordan, RM and Culloty, SC (2013) Climate change impacts on potential recruitment in an ecosystem engineer. Ecology and Evolution 3, 581594.CrossRefGoogle Scholar
Morley, NJ (2015) Ecology of free-living Metacercariae (Trematoda). Advances in Parasitology 89, 178.CrossRefGoogle Scholar
Morley, JW, Selden, RL, Latour, RJ, Frolicher, TL, Seagraves, RJ and Pinsky, ML (2018) Projecting shifts in thermal habitat for 686 species on the North American continental shelf. PLoS ONE 13, 128.CrossRefGoogle ScholarPubMed
Nicoll, W (1923) A reference list of the trematode parasites of British birds. Parasitology 15, 151202.CrossRefGoogle Scholar
Odhner, T (1900) Gymnophallus, eine neue Gattung von Vogeldistomen. Zentralblatt für Bakteriologie. Parasitenkunde und Infektionskrankheiten 28, 1223.Google Scholar
Odhner, T (1905) Die Trematoden des arktischen Gebietes (PhD thesis). Philosophischen Fakultät zu Upsala, Sweden.Google Scholar
Pascoe, D, Richards, RJ and James, BL (1968) Oxygen uptake metabolic rate reduced weight length and number of cercariae in starving sporocysts of Cercaria dichotoma. Experimental Parasitology 23, 171182.CrossRefGoogle ScholarPubMed
Peoples, RC (2013) A review of the helminth parasites using polychaetes as hosts. Parasitology Research 112, 34093421.CrossRefGoogle ScholarPubMed
Poulin, R (1999) The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology 29, 903914.CrossRefGoogle ScholarPubMed
Poulin, R and Cribb, TH (2002) Trematode life cycles: short is sweet? Trends in Parasitology 18, 176183.CrossRefGoogle ScholarPubMed
Poulin, R and Mouritsen, KN (2003) Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254, 187198.CrossRefGoogle Scholar
Prévot, G (1965) Développement expérimental d'une métacercaire de Gymnophallus (Trematoda: Digenea). Bulletin de la Société Zoologique de France 90, 451456.Google Scholar
Rakotomalala, C, Grangere, K, Ubertini, M, Foret, M and Orvain, F (2015) Modelling the effect of Cerastoderma edule bioturbation on microphytobenthos resuspension towards the planktonic food web of estuarine ecosystem. Ecological Modelling 316, 155167.CrossRefGoogle Scholar
Rangel, LF and Santos, MJ (2009) Diopatra neapolitana (Polychaeta: Onuphidae) as a second intermediate host of Gymnophallus choledochus (Digenea: Gymnophallidae) in the Aveiro Estuary (Portugal): distribution within the host and histopathology. Journal of Parasitology 95, 12331236.CrossRefGoogle ScholarPubMed
Richards, RJ, Pascoe, D and James, BL (1970) Variations in the metabolism of the daughter sporocysts of Cercaria dichotoma Lebour, 1911, containing metacercariae, during starvation in sea water and in L-glutamine and glucose solutions. Acta Parasitologica Polonica 18, 347357.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). Universidade do Porto, Portugal.Google Scholar
Russell-Pinto, F, Goncalves, JF and Bowers, E (2006) Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro, Portugal. Journal of Parasitology 92, 319332.CrossRefGoogle ScholarPubMed
Sannia, A and James, BL (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, 111.CrossRefGoogle Scholar
Sannia, A, James, BL and Bowers, EA (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, 487500.CrossRefGoogle Scholar
Schmidt, GD and Roberts, LS (2000) Trematoda: form, function, and classification of digeneans. In Janice Roerig-Blong (ed.), Foundations of Parasitology 8, pp. 219-245. New York: McGraw-Hill.Google Scholar
Scholz, T (2002) Family Gymnophallidae Odhner, 1905. In Gibson, D I (ed.), Keys to the Trematoda, Book 1, pp. 245-251. London, UK: CAB International and The Natural History Museum.CrossRefGoogle Scholar
Skirnisson, K (2015) Association of helminth infections and food consumption in common eiders Somateria mollissima in Iceland. Journal of Sea Research 104, 4150.CrossRefGoogle Scholar
Stunkard, HW and Uzmann, JR (1958) Studies on digenetic trematodes of the genera Gymnophallus and Parvatrema. Biological Bulletin 115, 276302.CrossRefGoogle Scholar
Ternengo, S, Levron, C and Marchand, B (2005) Metazoan parasites in Sparid fish in Corsica (Western Mediterranean). Bulletin of the European Association of Fish Pathologists 25, 262269.Google Scholar
Thieltges, DW (2006) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455461.CrossRefGoogle Scholar
Thieltges, DW (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, 613616.CrossRefGoogle Scholar
Thieltges, DW and Reise, K (2006) Metazoan parasites in intertidal cockles Cerastoderma edule from the northern Wadden Sea. Journal of Sea Research 56, 284293.CrossRefGoogle Scholar
Thieltges, DW, Hussel, B and Baekgaard, H (2006a) Endoparasites in common eiders Somateria mollissima from birds killed by an oil spill in the northern Wadden Sea. Journal of Sea Research 55, 301308.CrossRefGoogle Scholar
Thieltges, DW, Krakau, M, Andresen, H, Fottner, S and Reise, K (2006b) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research 60, 307316.CrossRefGoogle Scholar
Thieltges, DW, de Montaudouin, X, Fredensborg, B, Jensen, KT, Koprivnikar, J and Poulin, R (2008) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147155.CrossRefGoogle Scholar
UNEP/CMS (2014) A review of migratory bird flyways and priorities for management. UNEP/CMS Secretariat, Bonn, Germany. 164 pages. CMS Technical Series No. 27.Google Scholar