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Determinants of life-history traits in a fish ectoparasite: a hierarchical analysis

Published online by Cambridge University Press:  27 April 2011

G. LOOT ,
N. POULET ,
S. BROSSE ,
L. TUDESQUE ,
F. THOMAS  and
S. BLANCHET
G. LOOT*
Affiliation:
Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse cedex 4, France
N. POULET
Affiliation:
ONEMA, Le Nadar Hall C 5 sq Félix Nadar 94300 Vincennes, France
S. BROSSE
Affiliation:
Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse cedex 4, France
L. TUDESQUE
Affiliation:
Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse cedex 4, France
F. THOMAS
Affiliation:
IRD, MIVEGEC (UMR CNRS/IRD/UM1), 911 Av. Agropolis, BP 64501, FR-34394 Montpellier cedex 5, France
S. BLANCHET
Affiliation:
Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse cedex 4, France Station Expérimentale du CNRS à Moulis, U.S.R 2936, 09100 Moulis, France
*
*Corresponding author: Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse cedex 4, France. Tel: +33 5 61 55 85 81. Fax: +33 5 61 55 67 28. E-mail: loot@cict.fr
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Summary

Objective. Unravelling the determinants of parasite life-history traits in natural settings is complex. Here, we deciphered the relationships between biotic, abiotic factors and the variation in 4 life-history traits (body size, egg presence, egg number and egg size) in the fish ectoparasite Tracheliastes polycolpus. We then determined the factors affecting the strength of the trade-off between egg number and egg size. Methods. To do so, we used 4-level (parasite, microhabitat, host and environment) hierarchical models coupled to a field database. Results. Variation in life-history traits was mostly due to individual characteristics measured at the parasite level. At the microhabitat level (fins of fish hosts), parasite number was positively related to body size, egg presence and egg number. Higher parasite number on fins was positively associated with individual parasite fitness. At the host level, host body size was positively related to the individual fitness of the parasite; parasites were bigger and more fecund on bigger hosts. In contrast, factors measured at the environmental level had a weak influence on life-history traits. Finally, a site-dependent trade-off between egg number and egg size existed in this population. Conclusion. Our study illustrates the importance of considering parasite life-history traits in a hierarchical framework to decipher complex links between biotic, abiotic factors and parasite life-history traits.

Keywords

freshwater ecosystemhierarchical modeltrade-offfecunditymultilevel modelseggCopepodsCyprinidaeparasite

Information

Type
Research Article
Information
Parasitology , Volume 138 , Issue 7 , June 2011 , pp. 848 - 857
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Anderson, R. M. (1993). Epidemiology. In Modern Parasitology (ed. Cox, F. E. G.), pp. 75–116. Blackwell, Oxford, UK.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, B 265, 1283–1289.CrossRefGoogle Scholar
Barber, I. (2005). Parasites grow larger in faster growing fish hosts. International Journal for Parasitology 35, 137–143.CrossRefGoogle ScholarPubMed
Blanchet, S., Méjean, L., Bourque, J. F., Lek, S., Thomas, F., Marcogliese, D. J., Dodson, J. J. and Loot, G. (2009). Why parasitized hosts look different? Resolving the “chicken-egg” dilemma. Oecologia 160, 37–47.CrossRefGoogle ScholarPubMed
Blanckenhorn, W. U. and Heyland, A. (2004). The quantitative genetics of two life history trade-offs in the yellow dung fly in abundant and limited food environments. Evolutionary Ecology 18, 385–402.CrossRefGoogle Scholar
Bohlin, T., Hamrin, S., Heggberget, T. G., Rasmussen, G. and Saltveit, S. J. (1989). Electrofishing – theory and practice with special emphasis on salmonids. Hydrobiologia 173, 9–43.CrossRefGoogle Scholar
Boxshall, G. (2005). Crustacean parasites In Marine Parasitology, (ed. Rohde, K.), pp. 147–149. Collingwood, Vic., Australia.Google Scholar
Byers, J. E., Blakeslee, A. M. H., Linder, E., Cooper, A. B. and Maguire, T. J. (2008). Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89, 439–451.CrossRefGoogle ScholarPubMed
Carle, F. L. and Strub, M. R. (1978). A new method for estimating population size from removal data. Biometrics 34, 621–830.CrossRefGoogle Scholar
Combes, C. (2001). The Ecology and Evolution of Intimate Interactions. Chicago University Press, Chicago, IL, USA.Google Scholar
Cox, E. (1991). What is the Basis for Using Diatoms as Monitors of River Quality? (ed. Whitton, B. A., Rott, E. and Friedrich, G.), pp. 33–40. Institut für Botanik, Universität Innsbruck, Austria.Google Scholar
Crompton, D. W. T. (1991). Nutritional interactions between hosts and parasites. In Parasite-host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. A. and Bolis, L.), pp. 228–257. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Diez, J. M. and Pulliam, H. R. (2007). Hierarchical analysis of species distributions and abundance across environmental gradients. Ecology 88, 3144–3152.CrossRefGoogle ScholarPubMed
de Meeûs, T., Raibaut, A. and Renaud, F. (1993). Comparative life history of two species of sea lice. In Pathogens of Wild and Farmed Fish (ed. Boxsiiat, L. and Defaye, D.), pp. 61–67. Ellis Horwood, New York, USA.Google Scholar
Dobson, F. S. and Murie, J. O. (1987). Interpretation of intraspecific life history patterns: evidence from Columbian ground squirrels. The American Naturalist 129, 382–397.CrossRefGoogle Scholar
Drucker, E. G. and Lauder, G. V. (2002). Experimental hydrodynamics of fish locomotion: functional insights from wake visualization. Integrative and Comparative Biology 42, 243–257.CrossRefGoogle ScholarPubMed
Eisen, R. J. and Schall, J. J. (2000). Life history of a malaria parasite (Plasmodium mexicanum): independent traits and basis for variation. Proceedings of the Royal Society of London, B 267, 793–799.CrossRefGoogle ScholarPubMed
Fryer, G. (1982). The Parasitic Copepoda and Branchiura of British Freshwater Fishes. A Handbook and Key. Freshwater Biological Association Scientific Publication. The Ferry House, Ambleside, Cumbria.Google Scholar
Grace, J. B. (2006). Structural Equation Modelling and Natural Systems. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Grenfell, B. and Harwood, J. (1997). (Meta)population dynamics of infectious diseases. Trends in Ecology & Evolution 12, 395–399.CrossRefGoogle ScholarPubMed
Grenouillet, G., Brosse, S., Tudesque, L., Lek, S., Baraille, Y. and Loot, G. (2008). Concordance among stream assemblages and spatial autocorrelation along a fragmented gradient. Diversity and Distributions 14, 592–603.CrossRefGoogle Scholar
Hakalahti, T., Hakkinen, H. and Valtonen, E. T. (2004). Ectoparasitic Argulus coregoni (Crustacea : Branchiura) hedge their bets – studies on egg hatching dynamics. Oikos 107, 295–302.CrossRefGoogle Scholar
Hawlena, H., Abramsky, Z., Krasnov, B. R. and Saltz, D. (2007). Host defence versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on its rodent host Meriones crassus. International Journal for Parasitology 37, 919–925.CrossRefGoogle ScholarPubMed
Herreras, M. V., Montero, F. E., Marcogliese, D. J., Raga, J. A. and Balbuena, J. A. (2007). Phenotypic tradeoffs between egg number and egg size in three parasitic anisakid nematodes. Oikos 116, 1737–1747.CrossRefGoogle Scholar
Hughes, W. O. H., Petersen, K. S., Ugelvig, L. V., Pedersen, D., Thomsen, L., Poulsen, M. and Boomsma, J. J. (2004). Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. Bmc Evolutionary Biology 4, 45.CrossRefGoogle Scholar
Jennings, J. B. and Calow, P. (1975). The relationship between high fecundity and the evolution of endoparasitism. Oecologia 31, 109–115.CrossRefGoogle Scholar
Jessup, C. M. and Bohannan, B. J. M. (2008). The shape of an ecological trade-off varies with environment. Ecology Letters 11, 947–959.CrossRefGoogle ScholarPubMed
Jones, J. T., Breeze, P. and Kusel, J. R. (1989). Schistosome fecundity – influence of host genotype and intensity of infection. International Journal for Parasitology 19, 769–777.CrossRefGoogle ScholarPubMed
Kabata, Z. (1986). Redescriptions of and comments on four little-known Lernaeopodidae (Crustacea: Copepoda). Canadian Journal Zoology 64, 1852–1859.CrossRefGoogle Scholar
Kabata, Z. and Cousens, B. (1973). Life cycle of Salmincola californiensis (Dana, 1852) (Copepoda: Lernaeopodidae). Journal of the Fisheries Research Board of Canada 30, 881–903.CrossRefGoogle Scholar
Keitt, T. H. and Urban, D. L. (2005). Scale-specific inference using wavelets. Ecology 86, 2497–2504.CrossRefGoogle Scholar
Krasnov, B., Khokhlova, I. and Shenbrot, G. (2002). The effect of host density on ectoparasite distribution: An example of a rodent parasitized by fleas. Ecology 83, 164–175.CrossRefGoogle Scholar
Krist, A. C., Jokela, J., Wiehn, J. and Lively, C. M. (2004). Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction. Journal of Evolutionary Biology 17, 33–40.CrossRefGoogle Scholar
Lafferty, K. D. (2009 a). The ecology of climate change and infectious diseases. Ecology 90, 888–900.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2009 b). Calling for an ecological approach to studying climate change and infectious diseases. Ecology 90, 932–933.CrossRefGoogle ScholarPubMed
Lecointe, C., Coste, M. and Prygiel, J. (1993). Omnidia software for taxonomy, calculation of diatom indices and inventories management. Hydrobiologia 269/270, 509–513.CrossRefGoogle Scholar
Loot, G., Poulet, N., Reyjol, Y., Blanchet, S. and Lek, S. (2004). The effects of the ectoparasite Tracheliastes polycolpus (Copepoda: Lernaeopodidae) on the fins of rostrum dace (Leuciscus leuciscus burdigalensis). Parasitology Research 94, 16–23.CrossRefGoogle ScholarPubMed
McMahon, S. M. and Diez, J. M. (2007). Scales of association: hierarchical linear models and the measurement of ecological systems. Ecology Letters 10, 437–452.CrossRefGoogle ScholarPubMed
Morand, S. (1996). Life-history traits in parasitic nematodes: A comparative approach for the search of invariants. Functional Ecology 10, 210–218.CrossRefGoogle Scholar
Murray, K. and Conner, M. M. (2009). Methods to quantify variable importance: implications for the analysis of noisy ecological data. Ecology 90, 348–355.CrossRefGoogle ScholarPubMed
Nash, R. D. M., Valencia, A. H. and Geffen, A. J. (2006). The origin of Fulton's condition factor – Setting the record straight. Fisheries 31, 236–238.Google Scholar
Patrick, M. J. (1991). Distribution of enteric helminths in Glaucomys volans L (Sciuridae). A test for competition. Ecology 72, 755–758.CrossRefGoogle Scholar
Pinheiro, J. C. and Bates, D. M. (2002). Mixed-Effects Models in S and S-Plus. SPRINGER, New York.Google Scholar
Poulin, R. (1995 a). Evolution of parasite life history traits: myths and reality. Parasitology Today 11, 342–345.CrossRefGoogle Scholar
Poulin, R. (1995 b). Clutch size and egg size in free-living parasitic copepodes: a comparative analysis. Evolution 49, 325–336.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites. Chapman & Hall, London, UK.Google Scholar
Quinnell, R. J. (1988). Host age and the growth and fecundity of Hymenolepis diminuta in the rat. Journal of Helminthology 62, 158–162.CrossRefGoogle ScholarPubMed
R Development Core Team (2005). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Roff, D. A. (1992). The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York, USA.Google Scholar
Rossin, M. A., Poulin, R., Timi, J. T. and Malizia, A. I. (2005). Causes of inter-individual variation in reproductive strategies of the parasitic nematode Graphidioides subterraneus. Parasitology Research 96, 335–339.CrossRefGoogle ScholarPubMed
Schluter, D., Price, T. D. and Rowe, L. (1991). Conflicting Selection Pressures and Life-History Trade-Offs. Proceedings of the Royal Society of London, B 246, 11–17.Google Scholar
Seppala, O., Liljeroos, K., Karvonen, A. and Jokela, J. (2008). Host condition as a constraint for parasite reproduction. Oikos 117, 749–753.CrossRefGoogle Scholar
Smith, C. C. and Fretwell, S. D. (1974). The optimal balance between size and number of offspring. American Naturalist 108, 499–506.CrossRefGoogle Scholar
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford University Press, New York, USA.Google Scholar
Taylor, J. C., Prygiel, J., Vosloo, A., de la Rey, P. A. and van Rensburg, L. (2007). Can diatom-based pollution indices be used for biomonitoring in South Africa ? A case study of the Crocodile West and Marico water management area. Hydrobiologia 592, 455–464.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390.CrossRefGoogle ScholarPubMed
Timi, J. T., Lanfranchi, A. L. and Poulin, R. (2005). Is there a trade-off between fecundity and egg volume in the parasitic copepod Lernanthropus cynoscicola? Parasitology Research 95, 1–4.CrossRefGoogle Scholar
Timi, J. T., Lanfranchi, A. L. and Poulin, R. (2010). Consequences of microhabitat selection for reproductive success in the parasitic copepod Neobrachiella spinicephala (Lernaeopodidae). Parasitology 137, 1687–1694.CrossRefGoogle ScholarPubMed
Tsai, M. L., Li, J. J. and Dai, C. F. (2001). How host size may constrain the evolution of parasite body size and clutch size. The parasitic isopod Ichthyoxenus fushanensis and its host fish, Varicorhinus bacbatulus, as an example. Oikos 92, 13–19.CrossRefGoogle Scholar
Vignon, M. and Sasal, P. (2010). Multiscale determinants of parasite abundance: A quantitative hierarchical approach for coral reef fishes. International Journal for Parasitology 40, 443–451.CrossRefGoogle ScholarPubMed
Whiteman, N. K., Santiago-Alarcon, D., Johnson, K. P. and Parker, P. G. (2004). Differences in straggling rates between two genera of dove lice (Insecta: Phthiraptera) reinforce population genetic and cophylogenetic patterns. International Journal for Parasitology 34, 1113–1119.CrossRefGoogle ScholarPubMed
Wimberly, M. C., Yabsley, M. J., Baer, A. D., Dugan, V. G. and Davidson, W. R. (2008). Spatial heterogeneity of climate and land-cover constraints on distributions of tick-borne pathogens. Global Ecology and Biogeography 17, 189–202.CrossRefGoogle Scholar