Swim bladder nematodes (anguillicoloides crassus) disturb silvering in European eels (anguilla anguilla)

Journal of Parasitology

Volumn 98, Issue 4, 2012, Pages 695-705

  Fazio, Graldine ^a   Sasal, Pierre ^b   Mouahid, Gabriel ^c,d   Lecomte Finiger, Raymonde ^c   Mon, Hlne ^c,d  

^a Independent Researcher   (France)

^b Centre de Biologie et d Ecologie Tropicale et Méditerranéenne   (France)

^c UNIVERSITÉ DE PERPIGNAN   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANDROGEN RECEPTOR ALPHA; HEMOGLOBIN ALPHA CHAIN; SCOTOPSIN; UNCLASSIFIED DRUG; 11 OXOTESTOSTERONE; 11-KETOTESTOSTERONE; DRUG DERIVATIVE; HEMOGLOBIN CHAIN; OPSIN; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; TESTOSTERONE;

BIOLOGICAL INVASION; BODY SIZE; ECOLOGICAL IMPACT; EEL; FITNESS; GENE EXPRESSION; HEMOGLOBIN; INTRODUCED SPECIES; LIFE HISTORY TRAIT; NEMATODE; PARASITE INFESTATION; PHENOTYPIC PLASTICITY; POPULATION DECLINE; REPRODUCTIVE SUCCESS;

ANGUILLA (FISH); ANGUILLICOLOIDES CRASSUS; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL INFECTION; GENE EXPRESSION; INTESTINE; LIFE HISTORY; LIVER SIZE; METAMORPHOSIS; MIGRATION; NEMATODE; NEMATODIASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC PLASTICITY; REPRODUCTION; ADAPTATION; AIR SAC; ANIMAL; ANIMAL DISEASE; DRACUNCULOIDEA; DRUG EFFECT; ELECTROLYTE BALANCE; EYE; FIN (ORGAN); FISH DISEASE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LIVER; MALE; METABOLISM; PARASITOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; POPULATION MIGRATION; SKIN PIGMENTATION; SPIRURID INFECTION; VISUAL SYSTEM FUNCTION;

ANGUILLA ANGUILLA; ANGUILLIDAE; NEMATODA;

ADAPTATION, PHYSIOLOGICAL; AIR SACS; ANGUILLA; ANIMAL FINS; ANIMAL MIGRATION; ANIMALS; DRACUNCULOIDEA; EYE; FISH DISEASES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMOGLOBIN SUBUNITS; LIVER; MALE; OCULAR PHYSIOLOGICAL PHENOMENA; OPSINS; RECEPTORS, ANDROGEN; REPRODUCTION; SKIN PIGMENTATION; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SPIRURIDA INFECTIONS; TESTOSTERONE; WATER-ELECTROLYTE BALANCE;

EID: 84867477852     PISSN: 00223395     EISSN: 19372345     Source Type: Journal    
DOI: 10.1645/GE-2700.1     Document Type: Article

References (69)

1. ACOU, A., P. BOURY, P. LAFFAILLE, A. J. CRIVELLI, AND E. FEUNTEUN. 2005. Towards a standardized characterization of the potentially migrating silver European eel (Anguilla anguilla, L.). Archiv für Hydrobiologie 164: 237-255.
2. ARCHER, S., A. HOPE, AND J. C. PARTRIDGE. 1995. The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proceedings of the Royal Society of London - Series B 262: 289-295.
3. BAERWALD, M. R., A. B. WELSH, R. P. HEDRICK, AND B. MAY. 2008. Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling. BMC Genomics 9: 37.
4. BIRON, D. G., H. MOURA, L. MARCHÉ, A. L. HUGHES, AND F. THOMAS. 2005. Towards a new conceptual approach to ''parasitoproteomics.'' Trends in Parasitology 21: 162-168.
5. BLANC, G., S. BONNEAU, S. BAGIANTI, AND A. J. PETTER. 1992. Description of the larval stages of Anguillicola crassus (Nematoda, Dracunculoidea) using light and scanning electron microscopy. Aquatic Living Resources 5: 307-318.
6. BOLGER, T., AND P. L. CONNOLLY. 1989. The selection of suitable indices for measurement and analysis of fish condition. Journal of Fish Biology 34: 171-182.
7. BUCHMANN, K. 1993. Epidemiology and control of Pseudodactylogyrus infections in intensive eel culture systems: Recent trends. Bulletin Français de la Pêche et de la Pisciculture 328: 66-73.
8. BURNHAM, K. P., AND D. R. ANDERSON. 2002. Model selection and multimodel inference: A practical information-theoretic approach, 2nd edition. Springer, New York, New York, 496 p.
9. CARDINAL, R. N., AND M. R. F. AITKEN. 2006. ANOVA for the behavioural sciences researcher. Lawrence Erlbaum Associates, Mahwah, New Jersey, 440 p.
10. COLLINS, C. M., K. OLSTAD, E. STERUD, C. S. JONES, L. R. NOBLE, T. A. MO, AND C. O. CUNNINGHAM. 2007. Isolation of a FIP2-like gene from Atlantic salmon (Salmo salar L.), found upregulated following infection with the monogenean parasite Gyrodactylus salaris Malmberg, 1957. Fish and Shellfish Immunology 22: 282-288.
11. COMBES, C. 1995. Interactions durables. Ecologie et évolution du parasitisme. Masson, Paris, France, 512 p.
12. CUTLER, C. P., I. L. SANDERS, G. LUKE, N. HAZON, AND G. CRAMB. 1996. Ion transport in teleosts: Identification and expression of ion transporting proteins in branchial and intestinal epithelia of the European eel. In Society for Experimental Biology Seminar Series, S. J. Ennion and G. Goldspink (eds.). Cambridge University Press, Cambridge, U.K., p. 43-74.
13. DE CHARLEROY, D., V. M. H. CANNAERTS, H. AUGUSTIJHN, L.GRISEZ, J.H. BOON, AND F. OLLEVIER. 1990. An improved method for artificial infection of the European eel, Anguilla anguilla, with Anguillicola crassus (Nematoda, Dracunculoidea). Journal of Applied Ichthyology 6: 182-188.
14. DUFOUR, S., M. SCHMITZ, P. ELIE, P. VERNIER, Y. ZOHAR, E. BURZAWAGE ́RARD, N. LE BELLE, AND B. VIDAL. 2003. Reproductive endocrinology of the European eel, Anguilla anguilla. In Eel biology, K. Aida, K. Tsukamoto, and K. Yamauchi (eds.). Springer Verlag, Tokyo, Japan, p. 373-383.
15. DURIF, C., S. DUFOUR, AND P. ELIE. 2005. The silvering process of Anguilla anguilla: A new classification from the yellow resident to the silver migrating stage. Journal of Fish Biology 66: 1025-1043.
16. 2006. Impact of silvering stage, age, body size and condition on reproductive potential of the European eel. Marine Ecology-Progress Series 327: 171-181.
17. V. VAN GINNEKEN, S. DUFOUR, T. MÜ LLER, AND P. ELIE. 2009. Seasonal evolution and individual differences in silvering eels from different locations. In Spawning migration of the European eel, G. van den Thillart, S. Dufour, and J. C. Rankin (eds.). Springer Netherlands, Dordrecht, The Netherlands, p. 13-38.
18. ESTIMATION OF THE REPRODUCTION CAPACITY OF EUROPEAN EEL (EELREP). 2005. Final report of the EU project Q5RS-2001-01836, 272 p.
19. EUROPEAN INLAND FISHERIES ADVISORY COMMISSION (EIFAC), AND INTERNATIONAL COUNCIL FOR THE EXPLORATION OF THE SEA (ICES). 2007. Report of the 2007 session of the Joint EIFAC/ICES Working Group on Eels. Bordeaux, France, 3-7 September 2007. EIFAC Occasional Paper. No. 38, ICES CM 2007/ACFM:23. ICES, Bordeaux, France, 526 p.
20. FALIEX, E., C. DA SILVA, G. SIMON, AND P. SASAL. 2008. Dynamic expression of immune response genes in the sea bass, Dicentrarchus labrax, experimentally infected with the monogenean Diplectanum aequans. Fish and Shellfish Immunology 24: 759-767.
21. FAST, M. D., N. W. ROSS, D. M. MUISE, AND S. C. JOHNSON. 2006. Differential gene expression in Atlantic salmon infected with Lepeophtheirus salmonis. Journal of Aquatic Animal Health 18: 116-127.
22. FAZIO, G., H. MONÉ, R. LECOMTE-FINIGER, AND P. SASAL. 2008. Differential gene expression analysis in European eels (Anguilla anguilla, L. 1758) naturally infected by macroparasites. Journal of Parasitology 94: 571-577.
23. G. MOUAHID, AND P. SASAL. 2008. Biased sex ratio in the European eel (Anguilla anguilla) swimbladder parasite Anguillicola crassus, experimentally induced by 11-ketotestosterone. Journal of Parasitology 94: 956-958.
24. P. SASAL, R. LECOMTE-FINIGER, C. DA SILVA, B. FUMET, AND H. MONÉ. 2008. Macroparasite communities in European eels Anguilla anguilla from French Mediterranean lagoons, with special reference to invasive species Anguillicola crassus and Pseudodactylogyrus spp. Knowledge and Management of Aquatic Ecosystems 390-391: 06.
25. FOSTIER, A., B. JALABERT, R. BILLARD, B. BRETON, AND Y. ZOHAR. 1983. The gonadal steroids. Fish Physiology 9: 277-373.
26. FRECKLETON, R. 2002. On the misuse of residuals in ecology: Regression of residuals vs. multiple regression. Journal of Animal Ecology 71: 722.
27. GARCÍA-BERTHOU, E. 2001. On the misuse of residuals in ecology: Testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology 70: 708-711.
28. HAENEN, O. L. M., T. A. M. VAN WIJNGAARDEN, AND F. H. M. BORGSTEEDE. 1994. An improved method for the production of infective third-stage juveniles of Anguillicola crassus. Aquaculture 123: 163-165.
29. M. H. T. VAN DER HEIJDEN, J. HÖ GLUND, J. B. J. W. CORNELLISSEN, L. A. M. G. VAN LEENGOED, F. H. M. BORGSTEEDE, AND W. B. VAN MUISWINKEL. 1996. Effects of experimental infections with different doses of Anguillicola crassus (Nematoda, Dracunculoidea) on European eel (Anguilla anguilla). Aquaculture 141: 41-57.
30. HIROSE, S., T. KANEKO, N. NAITO, AND Y. TAKEI. 2003. Molecular biology of major components of chloride cells. Comparative Biochemistry and Physiology B 136: 593-620.
31. HOCHBERG, M. E., Y. MICHALAKIS, AND T. DEMEEû S. 1992. Parasitism as a constraint on the rate of life-history evolution. Journal of Evolutionary Biology 5: 491-504.
32. JOHANSSON, M.-L., G. DAVE, A. LARSSON, K. LEWANDER, AND U. LIDMAN. 1974. Metabolic and hematological studies on the yellow and silver phases of the European eel, Anguilla anguilla L. III. Hematology. Comparative Biochemistry and Physiology B 47: 593-594.
33. JOHNSON, C. R., AND C. A. FIELD. 1993. Using fixed-effects model multivariate analysis of variance in marine biology and ecology. In Oceanography and marine biology. An annual review, Vol. 31, A. D. Ansell, R. N. Gibson, and M. Barnes (eds.). UCL Press Ltd., London, U.K., p. 177-221.
34. KALUJNAIA, S., I. S. MCWILLIAM, V. A. ZAGUINAIKO, A. L. FEILEN, J. NICHOLSON, N. HAZON, C. P. CUTLER, R. J. BALMENT, A. R. COSSINS, M. HUGHES, AND G. CRAMB. 2007. Salinity adaptation and gene profiling analysis in the European eel (Anguilla anguilla) using microarray technology. General and Comparative Endocrinology 152: 274-280.
35. KIRK, R. S. 2003. The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology 10: 385-394.
36. LAI, J. C. C., I. KAKUTA, H. O. L. MOK, J. L. RUMMER, AND D. RANDALL. 2006. Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. The Journal of Experimental Biology 209: 2734-2738.
37. LARSEN, L. O., AND S. DUFOUR. 1993. Growth, reproduction and death in lampreys and eels. In Fish ecophysiology, J. C. Rankin, and F. B. Jensen (eds.). Chapman and Hall, London, U.K., p. 72-104.
38. LARSSON, P., S. HAMRIN, AND L. OKLA. 1990. Fat content as a factor inducing migratory behavior in the eel (Anguilla anguilla L.) to the Sargasso Sea. Naturwissenschaften 77: 488-490.
39. MICHALAKIS, Y., AND M. E. HOCHBERG. 1994. Parasitic effects on host lifehistory traits: A review of recent studies. Parasite 1: 291-294.
40. MIURA, C., T. MIURA, M. YAMASHITA, K. YAMAUCHI, AND Y. NAGAHAMA. 1996. Hormonal induction of all stages of spermatogenesis in germsomatic cell coculture from immature Japanese eel testis. Development Growth and Differentiation 38: 257-262.
41. MIURA, T., AND C. I. MIURA. 2003. Molecular control mechanisms of fish spermatogenesis. Fish Physiology and Biochemistry 28: 181-186.
42. K. YAMAUCHI, H. TAKAHASHI, AND Y. NAGAHAMA. 1991. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proceedings of the National Academy of Sciences USA 88: 5774-5778.
43. MOLNÁR, K., F. BASKA, G. CSABA, R. GLÁVITS, AND C. SZÉKELY. 1993. Pathological and histological studies of the swimbladder of eels Anguilla anguilla infected by Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15: 41-50.
44. MÜ NDERLE, M., B. SURES, AND H. TARASCHEWSKI. 2004. Influence of Anguillicola crassus (Nematoda) and Ichthyophthirius multifiliis (Ciliophora) on swimming activity of European eel Anguilla anguilla. Diseases of Aquatic Organisms 60: 133-139.
45. NEGOVETICH, N. J., AND G. W. ESCH. 2008. Quantitative estimation of the cost of parasitic castration in Helisoma anceps using a matrix population model. Journal of Parasitology 94: 1022-1030.
46. NIELSEN, M. E. 1999. An enhanced humoral immune response against the swimbladder nematode, Anguillicola crassus, in the Japanese eel, Anguilla japonica, compared with the European eel, A. anguilla. Journal of Helminthology 73: 227-232.
47. AND M. D. ESTEVE-GASSENT. 2006. The eel immune system: Present knowledge and the need for research. Journal of Fish Diseases 29: 65-78.
48. OLIVEREAU, M., AND J. OLIVEREAU. 1985. Effect of 17alpha- methyltestosterone on the skin and gonads of freshwater male silver eels. General and Comparative Endocrinology 57: 64-71.
49. OLSVIK, P. A., K. K. LIE, A. E. O. JORDAL, T. O. NILSEN, AND I. HORDVIK. 2005. Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Molecular Biology 6: 21-30.
50. PALSTRA, A. P., D. F. M. HEPPENER, V. J. T. VAN GINNEKEN, C. SZÉKELY, AND G. E. E. J. M. VAN DEN THILLART. 2007. Swimming performance of silver eels is severely impaired by the swim bladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology 352: 244-256.
51. PANKHURST, N. W. 1982. Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). Journal of Fish Biology 21: 127-140.
52. AND P. W. SORENSEN. 1983. Degeneration of the alimentary tract in sexually maturing European eels Anguilla anguilla (L.) and American eels Anguilla rostrata (LeSueur). Canadian Journal of Zoology 62: 1143-1149.
53. PIERRON, F., M. BAUDRIMONT, S. DUFOUR, P. ELIE, A. BOSSY, S. BALOCHE, N. MESMER-DUDONS, P. GONZALEZ, J. P. BOURDINEAUD, AND J. C. MASSABUAU. 2008. How cadmium could compromise the completion of the European eel's reproductive migration. Environmental Science and Technology 42: 4607-4612.
54. ROHR, D. H., P. M. LOKMAN, P. S. DAVIE, AND G. YOUNG. 2001. 11- Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis. Comparative Biochemistry and Physiology A 130: 701-714.
55. SEVERIN, V. I. C., AND M. EL-MATBOULI. 2007. Relative quantification of immune-regulatory genes in two rainbow trout strains, Oncorhynchus mykiss, after exposure to Myxobolus cerebralis, the causative agent of whirling disease. Parasitology Research 101: 1019-1027.
56. SITJÀ -BOBADILLA, A., J. CALDUCH-GINER, A. SAERA-VILA, O. PALENZUELA, P. ÁLVAREZ-PELLITERO, AND J. PÉREZ-SÁNCHEZ. 2008. Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox, and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish and Shellfish Immunology 24: 610-619. SOLDATOV, A. A. 2005. Peculiarities of organization and functioning of the fish red blood system. Journal of Evolutionary Biochemistry and Physiology 41: 272-281.
57. SPRENGEL, G., AND H. LÜ CHTENBERG. 1991. Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Diseases of Aquatic Organisms 11: 31-35.
58. SURES, B., K. KNOPF, AND W. KLOAS. 2001. Induction of stress by the swim bladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123: 179-184.
59. SVEDÄ NG, H., AND H. WICKSTRÖM. 1997. Low fat contents in female silver eels: Indications of insufficient energetic stores for migration and gonadal development. Journal of Fish Biology 50: 475-486.
60. TESCH, F. W. 2003. The eel, 5th ed. Thorpe JE, Oxford, U.K., 408 p.
61. TSENG, M. C., W. N. TZENG, AND S. C. LEE. 2003. Historical decline in the Japanese eel Anguilla japonica in northern Taiwan inferred from temporal genetic variations. Zoological Studies 42: 556-563.
62. VAN GINNEKEN, V., B. BALLIEUX, R.WILLEMZE, K.COLDENHOFF, E.LENTJES, E. ANTONISSEN, O. HAENEN, AND G. VAN DEN THILLART. 2005. Hematology patterns of migrating European eels and the role of EVEX virus. Comparative Biochemistry and Physiology C 140: 97-102.
63. AND G. E. MAES. 2005. The European eel (Anguilla anguilla, Linnaeus), its life cycle, evolution and reproduction: A literature review. Reviews in Fish Biology and Fisheries 15: 367-398.
64. VETTIER, A., C. SZÉKELY, AND P. SÉBERT. 2003. Are yellow eels from Lake Balaton able to cope with high pressure encountered during migration to the Sargasso Sea? The case of energy metabolism. Animal Biology 53: 329-338.
65. WIRTH, T., AND L. BERNATCHEZ. 2003. Decline of North Atlantic eels: A fatal synergy? Proceedings of the Royal Society of London - Series B 270: 681-688.
66. WOOD, P., AND J. C. PARTRIDGE. 1993. Opsin substitution induced in retinal rods of the eel (Anguilla anguilla (L.)): A model for G-proteinlinked receptors. Proceedings of the Royal Society of London - Series B 254: 227-232.
67. WÜ RTZ, J., H. TARASCHEWSKI, AND B. PELSTER. 1996. Changes in gas composition in the swimbladder of the European eel (Anguilla anguilla) infected with Anguillicola crassus (Nematoda). Parasitology 112: 233-238.
68. ZAR, J. H. 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, New Jersey, 664 p.
69. ZHANG, H., K. FUTAMI, N. HORIE, A. OKAMURA, T. UTOH, N. MIKAWA, Y. YAMADA, S. TANAKA, AND N. OKAMOTO. 2000. Molecular cloning of freshwater and deep-sea rod opsin genes from Japanese eel Anguilla japonica and expressional analyses during sexual maturation. FEBSLetters 469: 39-43.