Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-28T18:46:31.708Z Has data issue: false hasContentIssue false
  • English
  • Français

Host-parasite relationships in flatfish (Pleuronectiformes) – the relative importance of host biology, ecology and phylogeny

Published online by Cambridge University Press:  07 September 2010

J. F. MARQUES ,
M. J. SANTOS ,
C. M. TEIXEIRA ,
M. I. BATISTA  and
H. N. CABRAL
J. F. MARQUES*
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
M. J. SANTOS
Affiliation:
Universidade do Porto, Faculdade de Ciências, Departamento de Biologia, Rua do Campo Alegre, s/n, FC4, 4169-007 Porto, Portugal CIMAR - Laboratório Associado/CIIMAR - Centro Interdisciplinar de Investigação Marinha e Ambiental, Rua dos Bragas, 177, 4050-123 Porto, Portugal
C. M. TEIXEIRA
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
M. I. BATISTA
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
H. N. CABRAL
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal Universidade de Lisboa, Faculdade de Ciências, Departamento de Biologia Animal, Campo Grande, 1749-016 Lisboa, Portugal
*
*Corresponding author: Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, Lisboa, Portugal. Tel.: +351 217 500 000 (ext. 22575). Fax: +351 217 500 207. E-mail: jimarques@fc.ul.pt
Get access Rights & Permissions [Opens in a new window]

Summary

The extent to which host biology, ecology and phylogeny determine the diversity of macroparasite assemblages has been investigated in recent years in several taxa, including fish. However, consensus has not been reached probably as a result of data being collected from different sources, different temporal scales or host and parasite biogeography and phylogeny having greater influence than expected. The present study evaluates the relative importance of 27 biological, ecological and phylogenetic characteristics of 14 flatfish species on the diversity of their ecto- and endoparasite assemblages, comprising a total of 53 taxa. Redundancy analyses were applied to the mean abundance of each parasite taxa infecting each host and to the richness, taxonomic distinctness and variance in taxonomic distinctness calculated for each assemblage within each host. Only a few host characteristics contributed significantly to the observed patterns: host distribution was more important in determining the type and mean abundance of ectoparasites present in an assemblage, whereas diversity of these assemblages were mainly related to the host's maximum size. Endoparasite mean abundance and diversity were mostly influenced by the number of food items ingested and by the presence of Crustacea and Polychaeta in the diet. However, the sympatric occurrence of related hosts also played an important role in the diversity values found in macroparasite assemblages. Results showed that a host characteristic has different importance according to the host-parasite relationship being examined, suggesting an important role for host-parasite co-evolution on the diversity of extant macroparasite assemblages.

Keywords

diversityflatfishhost-characteristicsmacroparasitesredundancy analysesrichness
Type
Research Article
Information
Parasitology , Volume 138 , Issue 1 , January 2011 , pp. 107 - 121
Copyright
Copyright © Cambridge University Press 2010

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

REFERENCES

Aguirre-Macedo, M. L., Vidal-Martínez, V. M., González-Solís, D. and Caballero, P. I. (2007). Helminth communities of four commercially important fish species from Chetumal Bay, Mexico. Journal of Helminthology 81, 19–31. doi: 10.1017/S0022149X0721209X.Google Scholar
Azevedo, M. F. C., Oliveira, C., Pardo, B. G., Martinez, P. and Foresti, F. (2008). Phylogenetic analysis of the order Pleuronectiformes (Teleostei) based on sequences of 12S and 16S mitochondrial genes. Genetics and Molecular Biology 31 (Suppl.), 284–292. doi: 10.1590/S1415-47572008000200023.CrossRefGoogle Scholar
Bordes, F., Morand, S. and Ricardo, G. (2008). Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158, 109–116. doi: 10.1007/s00442-008-1115-x.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Cabral, H. N., Catarino, A. I., Figueiredo, J., Garcia, J. and Henriques, M. (2003). Feeding ecology, age, growth and sexual cycle of the Portuguese sole Synaptura lusitanica. Journal of the Marine Biological Association of the United Kingdom 83, 613–618. doi:10.1017/S0025315403007549 h.CrossRefGoogle Scholar
Clarke, K. R. and Gorley, R. N. (2001). PRIMER v5: user manual/tutorial. PRIMER-E, Plymouth, UK.Google Scholar
Clarke, K. R. and Warwick, R. M. (1998). A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35, 523–531. doi: 10.1046/j.1365-2664.1998.3540523.x.Google Scholar
Clarke, K. R. and Warwick, R. M. (1999). The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Marine Ecology Progress Series 184, 21–29.CrossRefGoogle Scholar
Deniel, C. (1981). Les poissons plats (Téléostéens – Pleuronectiformes) en Baie de Douarnenez. Reproduction, croissance et migration des Bothidae, Scophthalmidae, Pleuronectidae et Soleidae. Ph.D. dissertation, Université de Bretagne Occidentale, Brest, France.Google Scholar
Froese, , Pauly, R., , D. (eds.) (2009). FishBase. World Wide Web electronic publication. www.fishbase.org, version (07/2009).Google Scholar
Gibson, D. I., Bray, R. A. and Harris, E. A. (Compilers) (2008). Host-Parasite Database of the Natural History Museum, London, UK. http://www.nhm.ac.uk/research-curation/projects/host-parasites/.Google Scholar
González, M. T. and Poulin, R. (2005) Nested patterns in parasite component communities of a marine fish along its latitudinal range on the Pacific coast of South America. Parasitology 131, 569–577. doi: 10.1016/j.ijpara.2005.07.016.CrossRefGoogle ScholarPubMed
Koie, M. (2001). The life cycle of Dycheline (Cucullanellus) minutus (Nematoda: Cucullanidae). Folia Parasitologica 48, 304–310.CrossRefGoogle ScholarPubMed
Korallo, N. P., Vinarski, M. V., Krasnov, B. R., Shenbrot, G. I., Mouillot, D. and Poulin, R. (2007). Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages. Diversity and Distributions 13, 353–360. doi: 10.1111/j.1472-4642.2007.00332.x.CrossRefGoogle Scholar
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Degen, A. A. (2004). Flea species richness and parameters of host body, host geography and host ‘milieu’. Journal of Animal Ecology 73, 1121–1128. doi: 10.1111/j.0021-8790.2004.00883.x.Google Scholar
Lile, N. K. (1998). Alimentary tract helminths of four pleuronectid flatfish in relation to host phylogeny and ecology. Journal of Fish Biology 53, 945–953.CrossRefGoogle Scholar
Link, J. S., Fogarty, M. J. and Langton, R. W. (2005). The trophic ecology of flatfishes. In Flatfishes Biology and Exploitation (ed. Gibson, , , R. N.), pp. 185–212. Fish and Aquatic Resources Series, Blackwell Publishing, Oxford, UK.CrossRefGoogle Scholar
Luque, J. L. and Poulin, R. (2008). Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72, 189–204. doi: 10.1111/j.1095-8649.2007.01695.x.CrossRefGoogle Scholar
Luque, J. L., Mouillot, D. and Poulin, R. (2004). Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128, 671–682. doi: 10.1017/S0031182004005050.CrossRefGoogle ScholarPubMed
MacKenzie, K. (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124 (Suppl.), S153–S163. doi: 10.1017/S0031182002001518.CrossRefGoogle ScholarPubMed
MarBEF Data System (2008). European register of marine species http://www.marbef.org.Google Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151–164. doi: 10.1007/s10393-004-0028-3.CrossRefGoogle Scholar
Marques, J. F. and Cabral, H. N. (2007). Effects of sampling size on fish parasite prevalence, mean abundance and mean intensity estimates. Journal of Applied Ichthyology 23, 158–162. doi: 10.1111/j.1439-0426.2006.00823.x.CrossRefGoogle Scholar
Marques, J. F., Santos, M. J. and Cabral, H. N. (2006). Soleidae macroparasites along the Portuguese coast: latitudinal variation and host-parasite associations. Marine Biology 150, 285–298. doi: 10.1007/s00227-006-0339-8.CrossRefGoogle Scholar
Marques, J. F., Santos, M. J. and Cabral, H. N. (2009). Zoogeographical patterns of flatfish (Pleuronectiformes) parasites in the north-east Atlantic and the importance of the Portuguese coast as a transitional area. Scientia Marina 73, 461–471. doi: 10.3989/scimar.2009.73n3461.CrossRefGoogle Scholar
Muñoz, G., Grutter, A. S. and Cribb, T. H. (2006). Endoparasite communities of five fish species (Labridae: Cheilininae) from Lizard Island: how important is the ecology and phylogeny of the hosts? Parasitology 132, 363–374. doi: 10.1017/S0031182005009133.CrossRefGoogle ScholarPubMed
Munroe, T. A. (2005). Systematic diversity of the Pleuronectiformes. In Flatfishes Biology and Exploitation (ed. Gibson, , , R. N.), pp. 10–41. Fish and Aquatic Resources Series, Blackwell Publishing, Oxford, UK.CrossRefGoogle Scholar
Patterson, B. D., Dick, C. W. and Dittmar, K. (2008). Parasitism by bat flies (Diptera: Streblidae) on neotropical bats: effects of host body size, distribution, and abundance. Parasitology Research 103, 1091–1100. doi: 10.1007/s00436-008-1097-y.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776. doi: 10.1017/S0031182006002150.CrossRefGoogle ScholarPubMed
Poulin, R. and Rohde, K. (1997). Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny. Oecologia 110, 278–283. doi: 10.1007/s004420050160.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology 75, 277–293.CrossRefGoogle ScholarPubMed
Raibaut, A., Combes, C. and Benoit, F. (1998). Analysis of the parasitic copepod species richness among Mediterranean fish. Journal of Marine Systems 15, 185–206.CrossRefGoogle Scholar
Teixeira, C. M. and Cabral, H. N. (2010). Comparative analysis of the diet, growth and reproduction of the soles, Solea solea and Solea senegalensis, occurring in sympatry along the Portuguese coast. Journal of the Marine Biological Association of the United Kingdom (in the Press) doi: 10.1017/S0025315410000238.CrossRefGoogle Scholar
Teixeira, C. M., Batista, M. I. and Cabral, H. N. (2010). Diet, growth and reproduction of four flatfishes on the Portuguese coast. Scientia Marina 74, 223–233. doi: 10.3989/scimar.2010.74n2223.CrossRefGoogle Scholar
Teixeira, C. M., Pinheiro, A. and Cabral, H. N. (2009). Feeding ecology, growth and sexual cycle of the sand sole, Solea lascaris, along the Portuguese coast. Journal of the Marine Biological Association of the United Kingdom 89, 621–627. doi: 10.1017/S0025315409002562.CrossRefGoogle Scholar
ter Braak, C. J. F. and Smilauer, P. (2002). Canoco for Windows Version 4.5. Biometris – Plant Research International, Wageningen, The Netherlands.Google Scholar
Timi, J. T. and Poulin, R. (2003). Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it? International Journal for Parasitology 33, 1353–1362. doi: 10.1016/S0020-7519(03)00203-0.CrossRefGoogle Scholar
Verneau, O., Du Preez, L. and Badets, M. (2009). Lessons from parasitic flatworms about evolution and historical biogeography of their vertebrate hosts. Comptes Rendus Biologies 332, 149–158. doi: 10.1016/j.crvi.2008.08.019.Google Scholar
Warwick, R. M. and Clarke, K. R. (1995). New biodiversity measures reveal a decrease in taxonomic distinctness with increasing stress. Marine Ecology Progress Series 129, 301–305.CrossRefGoogle Scholar
Warwick, R. M. and Clarke, K. R. (2001). Practical measures of marine biodiversity based on relatedness of species. Oceanography and Marine Biology, An Annual Review 39, 207–231.Google Scholar