Hostname: page-component-5c6d5d7d68-thh2z Total loading time: 0 Render date: 2024-08-17T23:55:58.988Z Has data issue: false hasContentIssue false

Morphology and molecular analysis of life-cycle stages of Proctoeces maculatus (Looss, 1901) (Digenea: Fellodistomidae) in the Bizerte Lagoon, Tunisia

Published online by Cambridge University Press:  23 December 2015

R. Antar*
Affiliation:
Unité de Recherche: Bio-Ecologie Animale et Systématique Evolutive, Faculté des Sciences de Tunis, Université de Tunis El Manar, 2092, Tunis, Tunisie
L. Gargouri
Affiliation:
Unité de Recherche: Bio-Ecologie Animale et Systématique Evolutive, Faculté des Sciences de Tunis, Université de Tunis El Manar, 2092, Tunis, Tunisie

Abstract

The life cycle of Proctoeces maculatus (Looss, 1901) (Digenea, Fellodistomidae) was studied in Bizerte Lagoon (Tunisia). Three sequential hosts appear to be involved: the Mediterranean mussel Mytilus galloprovincialis Lamarck, 1819 (Mytilidae) as the first intermediate host; the polychaete Sabella pavonina Savigny, 1822 (Sabellidae), as the second intermediate host; and fishes (Lithognathus mormyrus (Linnaeus, 1758) (Sparidae), Trachinotus ovatus (Linnaeus, 1758) (Carangidae) and Sparus aurata Linnaeus, 1758 (Sparidae) as the definitive hosts. It should be noted that S. pavonina was recorded as second intermediate host for P. maculatus for the first time. Molecular confirmation of the morphological identification of the life-cycle stages of this digenean was obtained using partial 28S rDNA sequences. Comparative sequences revealed that the sporocysts and the metacercariae are conspecific but they diverged by 0.3% from the adults. The present results raised the possibility of the existence of cryptic species within the different developmental stages. However, all the present isolates differed from material from Archosargus probatocephalus in the Gulf of Mexico identified as P. maculatus.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

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

Aitken-Ander, P. & Levin, N.L. (1985) Occurrence of adult and developmental stages of Proctoeces maculatus (Trematoda: Digenea) in the gastropod Crepidula convexa . Transactions of the American Microscopical Society 104, 250260.Google Scholar
Aldana, M., Gonzalez, K., Loot, G., Pulgar, J. & Marquet, P.A. (2009) First intermediate host of the digenean trematode Proctoeces lintoni (Fellodistomidae) in Chile. Journal of Parasitology 95, 14081414.CrossRefGoogle ScholarPubMed
Bartoli, P. & Gibson, D.I. (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.Google Scholar
Bartoli, P. & Jousson, O. (2003) The life-cycle of Podocotyle scorpaenae (Opecoelidae: Digenea) demonstrated by comparative analysis of ribosomal DNA sequences. pp. 1727 in Combes, C. & Jourdane, J. (Eds) Livre hommage à Louis Euzet. Perpignan, Presses Universitaires de Perpignan.Google Scholar
Bartoli, P., Jousson, O. & 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
Born-Torrijos, A., Kostadinova, A., Raga, J.A. & Holzer, A.S. (2012) Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitising prosobranch snails in a Western Mediterranean lagoon. Parasitology International 61, 450460.Google Scholar
Bray, R.A. (1983) On the fellodistomid genus Proctoeces Odhner, 1911 (Digenea), with brief comments on two other fellodistomid genera. Journal of Natural History 17, 321339.Google Scholar
Bray, R.A. & Gibson, D.I. (1980) The Fellodistomidae (Digenea) of fishes of the northeast Atlantic. Bulletin of the British Museum (Natural History) (Zoology Series) 37, 199293.Google Scholar
Bray, R.A., Waeschenbach, A., Cribb, T.H., Weedall, G.D., Dyal, P. & Littlewood, D.T.J. (2009) The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitologica 54, 310329.Google Scholar
Criscione, C.D., Poulin, R. & Blouin, M.S. (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dolgikh, A.V. (1965a) Larval trematodes–parasites of molluscs from the Crimean shore of the Black Sea. Autoreferat dissertachii na soiskanie uchenoj stepeni kandidata biologicheskikh nauk. Lovoskii Ordena Lenina gosudarstvennikh, Universitet im Ivan Franko, Lvov (in Russian).Google Scholar
Dolgikh, A.V. (1965b) Progenetic metacercaria of the genus Proctoeces in Black Sea mollusks. Materialy Nauchnoî Konferentsii Vsesoyuznogo Obshchestva Gel'mintologov 2, 8488 (in Russian).Google Scholar
Dolgikh, A.V. (1967) On progenesis in trematodes of the genus Proctoeces Odhner, 1911. Parazitologiya 1, 219221 (in Russian).Google Scholar
Dolgikh, A.V. (1968) Helminthofauna of molluscs of northern part of the Black Sea. Biologiya Morya, Kiev 14, 114126 (in Russian).Google Scholar
Dolgikh, A.V. (1969) Some results of the study of the helminth fauna of molluscs in the Black Sea. Problemy Parazitologiî Trudy VI Nauchnoi Konferentsii Parazitologov USSR 1, 9697 (in Russian).Google Scholar
Dolgikh, A.V. (1970) Material on the helminth fauna of molluscs on the Caucasian coasts of the Black Sea. Biologiya Morya, Kiev 20, 328 (in Russian).Google Scholar
Dollfus, R.P. (1965) Metacercaria: Proctoeces progeneticus (Trematoda: Digenea) chez une Gibbula (Gastropoda Prosobranchiata) de la côte Atlantique du Maroc. Observations sur la famille Fellodistomatidae. Annales de Parasitologie Humaine et Comparée 39, 755774.Google Scholar
Dollfus, R.P. (1966) Metacercaire progénétique de Proctoeces chez un gastropode prosobranche de la côte Atlantique du Maroc. Proceedings of the First International Congress of Parasitology, Rome, 21–26 September 1964, Vol. C4. pp. 536537. Oxford, Pergamon Press.Google Scholar
Donald, K.M., Kennedy, M., Poulin, R. & Spencer, H.G. (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34, 557568.Google Scholar
Durieux, E. (2007) Ecologie du système hôte – parasite, juvéniles G0 de sole (Solea solea) – métacercaires de Digènes: dynamique et effets de l'infestation Thesis, Université de la Rochelle, France.Google Scholar
Freeman, R.F.H. (1963) Experimental infection of two species of wrasse with the digenean Proctoeces subtenuis . Journal of the Marine Biological Association of the United Kingdom 43, 113123.Google Scholar
Freeman, R.F.H. & Llewellyn, J. (1958) An adult digenetic trematode from an invertebrate host: Proctoeces subtenuis (Linton) from the lamellibranch Serobicularia plana (Da Costa). Journal of the Marine Biological Association of the United Kingdom 37, 435457.Google Scholar
Froese, R. & Pauly, D. (2015) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org (version July 2015).Google Scholar
Georgiev, B., Biserkov, V. & Genov, T. (1986) In toto staining method for cestodes with acetocarmine. Helminthologia 23, 279281.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696704.Google Scholar
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.Google Scholar
Hall, K.A., Cribb, T.H. & Barker, S.C. (1999) V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Systematic Parasitology 43, 8192.Google Scholar
Jousson, O. & Bartoli, P. (1999) The life-cycle of three species of the Mesometridae (Digenea) with comments on the taxonomic status of this family. Systematic Parasitology 44, 217228.Google Scholar
Jousson, O. & Bartoli, P. (2000) The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n. comb. (Digenea, Opecoelidae): evidence from molecules and morphology. International Journal for Parasitology 30, 747760.Google Scholar
Jousson, O., Bartoli, P., Zaninettia, L. & Pawlowskia, J. (1998) Use of the ITS rDNA for elucidation of some life-cycles of Mesometridae (Trematoda, Digenea). International Journal for Parasitology 28, 14031411.Google Scholar
Jousson, O., Bartoli, P. & Pawlowski, J. (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal of Parasitology 29, 18531858.Google Scholar
Lang, W.H. & Dennis, E.A. (1976) Morphology and seasonal incidence of infection of Proetoeces maculatus (Looss, 1901) Odhner, 1911 (Trematoda) in Mytilus edulis L. Ophelia 15, 6575.Google Scholar
Loot, G., Aldana, M. & Navarrete, S.A. (2005) Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 203212.Google Scholar
Loot, G., Blanchet, S., Aldana, M. & Navarrete, S.A. (2008) Evidence of plasticity in the reproduction of a trematode parasite: the effect of host removal. Journal of Parasitology 94, 2327.Google Scholar
Machkevsky, V.K. (1985) Some aspects of the biology of the trematode, Proctoeces maculatus, in connection with the development of mussel farms in the Black Sea. pp. 109110 in Hargis, J.W. (Ed.) Parasitology and pathology of marine organisms of the world ocean. Washington, DC, US Department of Commerce.Google Scholar
Martinez, J.C. (1972) Recherches sur quelques stades larvaires de digènes parasites de Mytilus galloprovincialis Lmk. Thesis, Université des Sciences et Techniques du Languedoc, France.Google Scholar
Martinez, J.C. (1974) La progenèse dans le cycle evolutif de Proctoeces maculatus (Looss, 1901) Odhner, 1911 (Trematoda, Fellodistomatidae). Bulletin de la Société d'Histoire Naturelle de l'Afrique du Nord 64, 3946.Google Scholar
Oliva, M.E., Valdivia, I.M., Cárdenas, L., George-Nascimento, M., Gonzalez, K., Guiñez, R.E. & Cuell, D. (2010) Molecular and experimental evidence refuse the life cycle of Proctoeces lintoni (Fellodistomidae) in Chile. Parasitology Research 106, 737740.Google Scholar
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T.J. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.Google Scholar
Pina, S.M.R., Russell-Pinto, F. & Rodrigues, P. (2007) Clarification of Cercaria sevillana (Digenea: Microphallidae) life cycle using morphological and molecular data. Journal of Parasitology 93, 318322.Google Scholar
Pina, S., Tajdari, J., Russell-Pinto, F. & Rodrigues, P. (2009a) Morphological and molecular studies on life cycle stages of Diphtherostomum brusinae (Digenea: Zoogonidae) from northern Portugal. Journal of Helminthology 83, 321331.Google Scholar
Pina, S., Barandela, T., João Santos, M., Russell-Pinto, F. & Rodrigues, P. (2009b) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological, and molecular data. Journal of Parasitology 95, 353359.Google Scholar
Prévot, G. (1965) Complément à la connaissance de Proctoeces maculatus (Looss, 1901) Odhner, 1911 [syn. P. erythraeus Odhner, 1911 et P. subtenuis (Linton, 1907) Hanson, 1950]. (Trematoda, Digenea, Fellodistomatidae). Bulletin de la Société Zoologique de France 90, 175179.Google Scholar
Shimura, S. & Egusa, S. (1979) A new digenetic trematode, Proctoeces ichiharai n. sp. (Fellodistomidae) from topshell, Batillus cornutus (Gastropoda). Bulletin of the Japanese Society of Scientific Fisheries 45, 12491253.Google Scholar
Stunkard, H.W. & Uzmann, J.R. (1959) The life-cycle of the digenetic trematode, Proctoeces macutatus (Looss, 1901) Odhner, 1911 [syn: P. subteuuis (Linton, 1907) Hanson, 1950], and a description of Cercaria adranocerca n. sp. Biological Bulletin, Marine Biological Laboratory, Woods Hole 116, 184193.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.Google Scholar
Tkach, V.T., Littlewood, D.T.J., Olson, P.D., Kinsella, M.J. & Swiderski, Z. (2003) Molecular phylogenetic analysis of the Microphalloidea Morozov, 1955 (Trematoda: Digenea): a bigger data set resolves fewer genera. Systematic Parasitology 56, 115.Google Scholar
Valdivia, I.M., Cardenas, L., Gonzalez, K., Jofré, D., George-Nascimento, M., Guiñez, R. & Oliva, M.E. (2010) Molecular evidence confirms that Proctoeces humboldti and Proctoeces chilensis (Digenea: Fellodistomidae) are the same species. Journal of Helminthology 84, 341347.Google Scholar
Wardle, W.J. (1980) On the life-cycle stages of Proctoeces macutatus (Digenea: Fellodistomidae) in mussels and fishes from Galveston Bay, Texas. Bulletin of Marine Science 30, 737743.Google Scholar