Head morphology and piscivory of European eels, Anguilla anguilla, predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus

Freshwater Biology

Volumn 60, Issue 10, 2015, Pages 1977-1987

  Pegg, Josephine ^a   Andreou, Demetra ^a   Williams, Chris F ^b   Britton, J Robert ^a  

^a BOURNEMOUTH UNIVERSITY   (United Kingdom)

^b ENVIRONMENT AGENCY   (United Kingdom)

Author keywords

Complex life cycle; Individual specialisation; Non native parasite; Paratenic host; Stable isotope analysis

Indexed keywords

EID: 84941189265     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/fwb.12624     Document Type: Article

References (67)

1. Aprahamian M.W. (2000) The growth rate of eel in tributaries of the lower River Severn, England, and its relationship with stock size. Journal of Fish Biology, 56, 223-227.
2. Barber I., Hoare D. & Krause J. (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries, 10, 131-165.
3. Barry J., Mcleish J., Dodd J.A., Turnbull J.F., Boylan P. & Adams C.E. (2014) Introduced parasite Anguillicola crassus infection significantly impedes swim bladder function in the European eel Anguilla anguilla (L.). Journal of Fish Diseases, 37, 921-924.
4. Barus V. & Prokes M. (1996) Length-weight relations of uninfected and infected eels (Anguilla anguilla) by Anguillicola crassus (nematoda). Folia Zoologica, 45, 183-189.
5. Benesh D.P., Chubb J.C. & Parker G.A. (2014) The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths. Proceedings of the Royal Society B-Biological Sciences, 281, 20141462.
6. Blanchet S., Mejean L., Bourque J.-F., Lek S., Thomas F., Marcogliese D.J. et al. (2009) Why do parasitized hosts look different? Resolving the 'chicken-egg' dilemma. Oecologia, 160, 37-47.
7. Bolnick D.I., Svanback R., Fordyce J.A., Yang L.H., Davis J.M., Hulsey C.D. et al. (2003) The ecology of individuals: incidence and implications of individual specialization. American Naturalist, 161, 1-28.
8. Bond A.L. & Diamond A.W. (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications, 21, 1017-1023.
9. Britton J.R., Jackson M.C. & Harper D.M. (2009) Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology, 136, 1367-1373.
10. Britton J.R., Pegg J. & Williams C.F. (2011) Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS ONE, 6, e26365.
11. Bulte G., Irschick D.J. & Blouin-Demers G. (2008) The reproductive role hypothesis explains trophic morphology dimorphism in the northern map turtle. Functional Ecology, 22, 824-830.
12. Cucherousset J., Acou A., Blanchet S., Britton J.R., Beaumont W.R.C. & Gozlan R.E. (2011) Fitness consequences of individual specialisation in resource use and trophic morphology in European eels. Oecologia, 167, 75-84.
13. Decharleroy D., Grisez L., Thomas K., Belpaire C. & Ollevier F. (1990) The life cycle of Anguillicola crassus. Diseases of Aquatic Organisms, 8, 77-84.
14. Ewald P.W. (1995) The evolution of virulence - a unifying link between parasitology and ecology. Journal of Parasitology, 81, 659-669.
15. Folstad I. & Karter A.J. (1992) Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603-622.
16. Galaktionov K.V. (1996) Life cycles and distribution of seabird helminths in arctic and sub-arctic regions. Bulletin of the Scandinavian Society of Parasitology, 6, 31-49.
17. Garcia-Berthou E. (2001) On the misuse of residuals in ecology: testing regression residuals versus the analysis of covariance. Journal of Animal Ecology, 70, 708-711.
18. Grey J. (2006) The use of stable isotope analyses in freshwater ecology: current awareness. Polish Journal of Ecology, 54, 563-584.
19. Hoole D., Bucke D., Burgess P. & Wellby I. (2001) Diseases of Carp and other Cyprinid Fishes. Fishing News Books, Oxford.
20. Jackson A.L., Inger R., Parnell A.C. & Bearhop S. (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology, 80, 595-602.
21. Jackson M.C., Donohue I., Jackson A.L., Britton J.R., Harper D.M. & Grey J. (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE, 7, e31757.
22. Jacoby D. & Gollock M. (2014) Anguilla anguilla. The IUCN Red List of Threatened Species. Version 2014.3. Vol. 26/1/14. IUCN, Available at: www.iucnredlist.org.
23. Kennedy C.R. (2007) The pathogenic helminth parasites of eels. Journal of Fish Diseases, 30, 319-334.
24. Kirk R.S. (2003) The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology, 10, 385-394.
25. Knopf K. & Lucius R. (2008) Vaccination of eels (Anguilla japonica and Anguilla anguilla) against Anguillicola crassus with irradiated L(3). Parasitology, 135, 633-640.
26. Knopf K. & Mahnke M. (2004) Differences in susceptibility of the European eel (Anguilla anguilla) and the Japanese eel (Anguilla japonica) to the swim-bladder nematode Anguillicola crassus. Parasitology, 129, 491-496.
27. Knudsen R., Curtis M.A. & Kristoffersen R. (2004) Aggregation of helminths: the role of feeding behavior of fish hosts. Journal of Parasitology, 90, 1-7.
28. Koops H. & Hartmann F. (1989) Anguillicola infestations in Germany and in German eel imports. Journal of Applied Ichthyology-Zeitschrift Fur Angewandte Ichthyologie, 5, 41-45.
29. Krist A.C. (2000) Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens. Journal of Parasitology, 86, 262-267.
30. Lafferty K.D. (1999) The evolution of trophic transmission. Parasitology Today, 15, 111-115.
31. Lammens E. & Visser J.T. (1989) Variability of mouth width in European eel, Anguilla anguilla, in relation to varying feeding conditions in 3 Dutch lakes. Environmental Biology of Fishes, 26, 63-75.
32. Lefebvre F., Contournet P. & Crivelli A.J. (2002) The health state of the eel swimbladder as a measure of parasite pressure by Anguillicola crassus. Parasitology, 124, 457-463.
33. Lefebvre F., Fazio G., Mounaix B. & Crivelli A.J. (2013) Is the continental life of the European eel Anguilla anguilla affected by the parasitic invader Anguillicoloides crassus? Proceedings of the Royal Society B-Biological Sciences, 280, 20122916.
34. Lindenfors P., Nunn C.L., Jones K.E., Cunningham A.A., Sechrest W. & Gittleman J.L. (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecology and Biogeography, 16, 496-509.
35. Marcogliese D.J. (2007) Evolution of parasitic life in the ocean: paratenic hosts enhance lateral incorporation. Trends in Parasitology, 23, 519-521.
36. Medoc V., Rigaud T., Motreuil S., Perrot-Minnot M.-J. & Bollache L. (2011) Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften, 98, 825-835.
37. Melia P., Bevacqua D., Crivelli A.J., De Leo G.A., Panfili J. & Gatto M. (2006) Age and growth of Anguilla anguilla in the Camargue lagoons. Journal of Fish Biology, 68, 876-890.
38. Miura O., Kuris A.M., Torchin M.E., Hechinger R.F. & Chiba S. (2006) Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proceedings of the Royal Society B-Biological Sciences, 273, 1323-1328.
39. Moehl K., Grosse K., Hamedy A., Wueste T., Kabelitz P. & Luecker E. (2009) Biology of Alaria spp. and human exposition risk to Alaria mesocercariae-a review. Parasitology Research, 105, 1-15.
40. Moore J.W. & Semmens B.X. (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters, 11, 470-480.
41. Moore S.L. & Wilson K. (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297, 2015-2018.
42. Morand S., Robert F. & Connors V.A. (1995) Complexity in parasite life-cycles - population biology of cestodes in fish. Journal of Animal Ecology, 64, 256-264.
43. Moravec F., Dicave D., Orecchia P. & Paggi L. (1994) Experimental observations on the development of Anguillicola crassus (Nematoda, Dracunculoidea) in its definitive host, Anguilla anguilla (Pisces). Folia Parasitologica, 41, 138-148.
44. Moriarty C. (1974) Studies of the eel Anguilla anguilla in Ireland. 3. In the Shannon catchment. Irish Fisheries Investigations Series, 14, 25.
45. Nagasawa K., Kim Y.G. & Hirose H. (1994) Anguillicola crassus and A. globiceps (Nematoda, Dracunculoidea) Parasitic in the swimbladder of eels (Anguilla japonica and Anguilla anguilla) in east Asia - A review. Folia Parasitologica, 41, 127-137.
46. Palstra A.P., Heppener D.F.M., Van Ginneken V.J.T., Szekely C. & Van Den Thillart G.E.E.J.M. (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.
47. Parnell A.C., Inger R., Bearhop S. & Jackson A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE, 5, e9672.
48. Pelster B. (2015) Swimbladder function and the spawning migration of the European eel Anguilla anguilla. Frontiers in Physiology, 5, 486.
49. Phillips D.L., Inger R., Bearhop S., Jackson A.L., Moore J.W., Parnell A.C. et al. (2014) Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology, 92, 823-835.
50. Phillips D.L., Newsome S.D. & Gregg J.W. (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia, 144, 520-527.
51. Poole W.R. & Reynolds J.D. (1996) Growth rate and age at migration of Anguilla anguilla. Journal of Fish Biology, 48, 633-642.
52. Post D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83, 703-718.
53. Proman J.M. & Reynolds J.D. (2000) Differences in head shape of the European eel, Anguilla anguilla (L.). Fisheries Management and Ecology, 7, 349-354.
54. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, Available at: http://www.R-project.org/
55. Robert F., Renaud F., Mathieu E. & Gabrion C. (1988) Importance of the paratenic host in the biology of Bothriocephalus gregarius (Cestoda, Pseudophyllidea), a parasite of the turbot. International Journal for Parasitology, 18, 611-621.
56. Schabuss M., Kennedy C.R., Konecny R., Grillitsch B., Reckendorfer W., Schiemer F. et al. (2005) Dynamics and predicted decline of Anguillicola crassus infection in European eels, Anguilla anguilla, in Neusiedler See, Austria. Journal of Helminthology, 79, 159-167.
57. Schalk G. & Forbes M.R. (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos, 78, 67-74.
58. Smith T.B. & Skulason S. (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annual Review of Ecology and Systematics, 27, 111-133.
59. Stock B.C. & Semmens B.X. (2013) MixSIAR GUI User Manual, version 1.0. Available at: http://conserver.iugo-cafe.org/user/brice.semmens/MixSIAR.
60. Sures B. & Streit B. (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology, 123, 185-191.
61. Szekely C. (1994) Paratenic hosts for the parasitic nematode Anguillicola crassus in Lake Balaton, Hungary. Diseases of Aquatic Organisms, 18, 11-20.
62. R Core Development Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, Available at: http://www.R-project.org.
63. Tesch F.W. (1977) The Eel: Biology and Management of Anguillid Eels. Chapman and Hall, London.
64. Tesch F.W. (2003) The Eel. Blackwell, Oxford.
65. Thomas K. & Ollevier F. (1992) Paratenic hosts of the swimbladder nematode Anguillicola crassus. Diseases of Aquatic Organisms, 13, 165-174.
66. Viljoen H., Bennett N.C., Ueckermann E.A. & Lutermann H. (2011) The role of host traits, season and group size on parasite burdens in a cooperative mammal. PLoS ONE, 6, e27003.
67. Wuertz J., Knopf K. & Taraschewski H. (1998) Distribution and prevalence of Anguillicola crassus (Nematoda) in eels Anguilla anguilla of the rivers Rhine and Naab, Germany. Diseases of Aquatic Organisms, 32, 137-143.