Folia Parasitologica 61[1] 81-89 (2014) | DOI: 10.14411/fp.2014.005
Host specificity and metamorphosis of the glochidium of the freshwater mussel Unio tumidiformis (Bivalvia: Unionidae)
- 1 Universidade de Lisboa, Faculdade de Ciências, Centro de Biologia Ambiental, Lisboa, Portugal;
- 2 Instituto Português de Malacologia, Zoomarine, Albufeira, Portugal;
- 3 Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, Madrid, Spain
The glochidium larvae of freshwater mussels of the family Unionidae need to find suitable hosts to attach themselves and metamorphose into free-living juveniles. The specificity of the host-parasite relationship was investigated for the Iberian Unio tumidiformis Castro, 1885 by means of experimental infections and also by analyzing naturally infected fish. The process of encapsulation of glochidia was studied using scanning electron microscopy. Unio tumidiformis has proven to be an unusual host-specific unionid mussel, apparently parasitizing only fish of the genus Squalius Bonaparte, 1837. Successful encapsulation or complete metamorphosis was observed in five fish taxa: S. aradensis (Coelho, Bogutskaya, Rodrigues et Collares-Pereira), S. caroliterti (Doadrio), S. pyrenaicus (Günther), S. torgalensis (Coelho, Bogutskaya, Rodrigues et Collares-Pereira) and S. alburnoides (Steindachner) complex (only for the nuclear hybrids with at least one copy of the S. pyrenaicus genome). Complete metamorphose was achieved in 6 to 14 days at mean temperatures ranging from 21.8 to 26.1°C. The current study provides support for cell migration being the main force of cyst formation and shows the influence of potential host's genome in response to the infection process to determine the success of the metamorphosis.
Keywords: Mollusca, larvae, encapsulation, juvenile, temperature, Iberian Squalius
Received: January 17, 2013; Accepted: June 24, 2013; Prepublished online: January 10, 2014; Published: January 11, 2014 Show citation
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References
- Araujo R., Bragado D., Ramos M.-A. 2001: Identification of the river blenny, Salaria fluviatilis, as a host to the glochidia of Margaritifera auricularia. J. Mollusc. Stud. 67: 128-129
Go to original source... - Araujo R., Camara N., Ramos M.-A. 2002: Glochidium metamorphosis in the endangered freshwater mussel Margaritifera auricularia (Spengler, 1793): a histological and scanning electron microscopy study. J. Morphol. 254: 259-265
Go to original source...
Go to PubMed... - Araujo R., Gomez I., Machordom A. 2005: The identity and biology of Unio mancus Lamarck, 1819 (= U. elongatulus) (Bi
- valvia: Unionidae) in the Iberian Peninsula. J. Mollusc. Stud. 71: 25-31
- Araujo R., Reis J., Machordom A., Toledo C. Madeira M.J., Gomez I., Velasco J.C., Morales J., Barea J.M., Ondina P., Ayala I. 2009: Las nayades de la peninsula Iberica. Iberus, 27: 7-72
- Arey L.B. 1932: Certain basic principles of wound healing. Anat. Rec. 51: 299-313
Go to original source... - Barfield M.L., Watters G.T. 1998: Non-parasitic life cycle in the green floater, Lasmigona subviridus (Conrad, 1835). Triannual Unionid Rep. 16: 22
- Barnhart M.C., Haag W.R., Roston W.N. 2008: Adaptations to host infection and larval parasitism in Unionoida. J. N. Am. Benthol. Soc. 27: 370-394
Go to original source... - Berrie A., Boize B. 1985: The fish hosts of Unio glochidia in the River Thames. Verh. Int. Verein. Limnol. 22: 2712-2716
Go to original source... - Blazek R., Gelnar M. 2006: Temporal and spatial distribution of glochidial larval stages of European unionid mussels (Mollusca: Unionidae) on host fishes. Folia Parasitol. 53: 98-106
Go to original source...
Go to PubMed... - Collares-Pereira M.J., Coelho M.M. 2010: Reconfirming the hybrid origin and generic status of the Iberian cyprinid complex Squalius alburnoides. J. Fish Biol. 76: 707-715
Go to original source...
Go to PubMed... - Crespo-Lopez M.E., Duarte T., Dowling T.E., Coelho M.M. 2006: Modes of reproduction of the hybridogenetic fish Squalius alburnoides in the Tejo and Guadiana rivers: an approach with microsatellites. Zoology 109: 277-286
Go to original source...
Go to PubMed... - Dartnall H.J.G., Walkey M. 1979: The distribution of glochidia of the Swan mussel, Anodonta cygnea (Mollusca), on the three-spined stickleback Gasterosteus aculeatus (Pisces). J. Zool. 89: 31-37
Go to original source... - Douda K., Horky P., Bily M. 2012: Host limitation of the thick-shelled river mussel: identifying the threats to declining affiliate species. Anim. Conserv. 15: 536-544
Go to original source...
Go to PubMed... - Engel H., Waechtler K. 1989: Some peculiarities in developmental biology of two forms of the freshwater bivalve Unio crassus in northern Germany. Arch. Hydrobiol. 115: 441-450
Go to original source... - Filipe A.F., Marques T., Seabra S., Tiago P., Ribeiro F., Moreira Da Costa L., Cowx I.G., Collares-Pereira M.J. 2004: Selection of priority areas for fish conservation in Guadiana River Basin, Iberian Peninsula. Conserv. Biol. 18: 189-200
Go to original source... - Graf D.L., Cummings K.S. 2006: Palaeoheterodont diversity (Mollusca: Trigonoida + Unionoida): what we know and what we wish we knew about freshwater mussel evolution. Zool. J. Linnean Soc. 148: 343-394
Go to original source... - Haag W.R., Warren Jr. M.L. 1997: Host fishes and reproductive biology of 6 freshwater mussel species from the Mobile basin, USA. J. N. Am. Benthol. Soc. 16: 576-585
Go to original source... - Haas F. 1940: A tentative classification of the Paleartic unionids. Field Mus. Nat. Hist., Zool. Ser. 24: 115-141
Go to original source... - Haas F. 1969: Superfamilia Unionacea. Das Tierreich 88: 1-663
- Hochwald S., Bauer G. 1990: Untersuchungen zur Populations-oekologie und Fortpfanzungsbiologie der Bachmuschel Unio crassus (Phil.) 1788. Schrift. Bayer. Landesamt Umweltschutz 97: 31-49
- Hoggarth M.A., Gaunt A.S. 1988: Mechanics of glochidial attachment (Mollusca: Bivalvia: Unionidae). J. Morphol. 198: 71-81
Go to original source...
Go to PubMed... - Kat P.W. 1984: Parasitism and the Unionacea (Bivalvia). Biol. Rev. 59: 189-207
Go to original source... - Lefevre G., Curtis W. 1912: Reproduction and parasitism in the Unionidae. J. Exp. Zool. 9: 79-115
Go to original source... - Leunda P., Elvira B., Ribeiro F., Miranda R., Oscoz J., Alves M.J., Collares-Pereira M.J. 2009: International standardization of common names for Iberian endemic freshwater fishes. Limnetica 28: 189-202
Go to original source... - Lima P., Kovitvadhi U., Kovitvadhi S., Machado J. 2006: In vitro culture of glochidia from the freshwater mussel Anodonta cygnea. Invert. Biol. 125: 34-44
Go to original source... - Nezlin L.P., Cunjak R.A., Zotin A.A., Ziuganov V.V. 1993: Glochidium morphology of the freshwater pearl mussel (Margaritifera margaritifera) and glochidiosis of the Atlantic salmon (Salmo salar): a study by scanning electron microscopy. Can. J. Zool. 72: 15-21
Go to original source... - Pekkarinen M., Englund V.P. 1995: Description of unionacean glochidia in Finland, with a table aiding in their identification. Arch. Hydrobiol. 134: 515-531
Go to original source... - Perez-Quintero J.C., Bech Taberner M., Huertas Dionisio J.L. 2004: Los moluscos de las aguas continentales de la provincia de Huelva (SO Espana). Iberus 22: 19-31
- Ramos M.-A. 1998: Implementing the habitats directive for mollusc species in Spain. J. Conchol., Spec. Public. 2: 125-132
- Reis J. 2006: Atlas dos Bivalves de Agua Doce de Portugal Continental. Instituto da Conservacao da Natureza, Lisboa, 130 pp
- Reis J., Araujo R. 2009: Redescription of Unio tumidiformis Castro, 1885 (Bivalvia, Unionidae), an endemism from the south-western Iberian Peninsula. J. Nat. Hist. 43: 1929-1945
Go to original source... - Ribeiro F., Beldade R., Dix M., Bochechas J. 2007: Carta piscicola nacional. Direccao Geral dos Recursos Florestais-Fluviatilis, Lda. World Wide Web electronic publication, www.cartapiscicola.org, 09/2007
- Ribeiro F., Collares-Pereira M.J., Moyle P.B. 2009: Non-native fish in the fresh waters of Portugal, Azores and Madeira Islands: a growing threat to aquatic biodiversity. Fish. Manag. Ecol. 16: 255-264
Go to original source... - Robalo J.I., Almada V.C., Levy A., Doadrio I. 2007: Re-examination and phylogeny of the genus Chondrostoma based on mitochondrial and nuclear data and the definition of 5 new genera. Mol. Phylogenet. Evol. 42: 362-272
Go to original source...
Go to PubMed... - Robalo J.I., Santos C.S., Levy A., Almada V.C. 2006: Molecular insights on the taxonomic position of the paternal ancestor of the Squalius alburnoides hybridogenetic complex. Mol. Phylogenet. Evol. 30: 276-281
Go to original source...
Go to PubMed... - Rogers-Lowery C.L., Dimock Jr R.V. 2006: Encapsulation of attached ectoparasitic glochidia larvae of freshwater mussels by epithelial tissue on fins of naive and resistant host fish. Biol. Bull. 210: 51-63
Go to original source...
Go to PubMed... - Taeubert J.E., Gum B., Geist J. 2012a: Host-specifity of the endangered thick-shelled river mussel (Unio crassus Philipsson 1788) and implications for conservation. Aquat. Conserv. Mar. Freshwat. Ecosyst. 22: 36-46
Go to original source... - Taeubert J.E., Martinez A.M.P, Gum B., Geist J. 2012b: The relationship between endangered thick-shelled river mussel (Unio crassus) and its host fishes. Biol. Conserv. 155: 94-103
Go to original source... - Watters G.T., O'Dee S.H. 1998: Metamorphosis of the freshwater mussel glochidia (Bivalvia: Unionidae) on amphibians and exotic fishes. Am. Midl. Nat. 139: 49-57
Go to original source...


