Zoogeographical patterns of flatfish (Pleuronectiformes) parasites in the Northeast Atlantic and the importance of the Portuguese coast as a transitional area

Joana Ferreira Marques; Maria João Santos; Henrique Nogueira Cabral

doi:10.3989/scimar.2009.73n3461

Authors

Joana Ferreira Marques Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia
Maria João Santos Universidade do Porto, Faculdade de Ciências, Departamento de Zoologia e Antropologia
Henrique Nogueira Cabral Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia

DOI:

https://doi.org/10.3989/scimar.2009.73n3461

Keywords:

biogeography, macroparasites, Pleuronectiformes, Northeast Atlantic, Mediterranean Sea, multivariate analyses

Abstract

Parasites are recognised as an excellent source of information on the distribution of their hosts. Here, the macroparasite fauna of 20 species of Pleuronectiformes belonging to five different families and inhabiting the Portuguese coast was investigated and compared with that known in four other areas (the North Sea, north Northeast Atlantic, Mediterranean Sea and Northwest African coast) in order to determine (1) their zoogeographical pattern and (2) the role of the Portuguese coast as an intermediate biogeographic province. Macroparasites infecting Pleuronectiformes sampled along the Portuguese coast were collected using standard parasitological techniques, whereas data on those in the other four areas were obtained from the literature, rendering a total of 73 macroparasite species. Both sets of data were then compiled in a presence/absence matrix. Hosts and macroparasites were placed into zoogeographical categories according to their known distribution, and patterns were evaluated using multidimensional scaling and cluster analysis. The zoogeography of hosts and parasites was not entirely concordant, although that of endoparasites was generally consistent with the patterns for marine free-living species. On the other hand, only specific ectoparasites truly mirrored the distribution of their hosts. These differences reflect the importance of host ecology and dispersal and environmental factors on the patterns revealed. The Portuguese coast seems to play a significant role in the distribution of Pleuronectiformes’ parasites along the Northeast Atlantic and Mediterranean Sea, due to its transitional character and to the sympatric occurrence of related hosts, both promoting the acquisition of new parasite species or the maintenance of historical host-parasite relationships.

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Author Biographies

Maria João Santos, Universidade do Porto, Faculdade de Ciências, Departamento de Zoologia e Antropologia

CIMAR Laboratório Associado / CIIMAR, Porturgal

Henrique Nogueira Cabral, Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia

Universidade de Lisboa, Faculdade de Ciências, Departamento de Biologia Animal, Portugal

References

Almada, V.C., R.F. Oliveira, E.J. Gonçalves, A.J. Almeida, R.S. Santos and P. Wirtz. – 2001. Patterns of diversity of the northeastern Atlantic blennid fish fauna (Pisces: Blenniidae). Global Ecol. Biogeogr., 10: 411-422. doi:10.1046/j.1466-822X.2001.00244.x

Álvarez, F., R. Iglesias, A.I. Paramá, J. Leiro and M. Sanmartín. – 2002. Abdominal macroparasites of commercially important flatfishes (Teleostei: Scophtalmidae, Pleuronectidae, Soleidae) in the northwest Spain (ICES IXa). Aquaculture, 213: 31-53. doi:10.1016/S0044-8486(02)00025-X

Bartoli, P., D.I. Gibson and R.A. Bray. – 2005. Digenean species diversity in teleost fish from a nature reserve off Corsica, France (Western Mediterranean), and a comparison with other Mediterranean regions. J. Nat. Hist., 39: 47-70. doi:10.1080/00222930310001613557

Belghyti, D., P. Aguesse and C. Gabrion. – 1993. Éthologie Alimentaire de Citharus linguatula et Dicologoglossa cuneata sur les côtes atlantiques du Maroc. Vie Milieu, 43: 95-108.

Berendzen, P.B. and W.W. Dimmick. – 2002. Phylogenetic relationships of Pleuronectiformes based on molecular evidence. Copeia, 3: 642-652. doi:10.1643/0045-8511(2002)002[0642:PROPBO]2.0.CO;2

Blaylock, R.B., L. Margolis, J.C. Holmes. – 1998. Zoogeography of the parasites of Pacific halibut (Hippoglossus stenolepis) in the northeast Pacific. Can. J. Zool., 76: 2262-2273. doi:10.1139/cjz-76-12-2262

Briggs, J.C. – 1974. Marine Zoogeography. McGraw-Hill, New York.

Briggs, J.C. – 2006. Proximate sources of marine biodiversity. J. Biogeogr., 33: 1-10. doi:10.1111/j.1365-2699.2005.01374.x

Bush, A.O., J.C. Fernadez, G.W. Esch and J.R. Seed. – 2001. Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge.

Byrnes, T. and K. Rohde. – 1992. Geographical distribution and host specificity of ectoparasites of Australian bream, Acanthopagrus spp. (Sparidae). Folia Parasitol., 39: 249-264.

Carney, J.P. and T.A. Dick. – 2000. Parasite biogeography: a review of the origins and ideas with specific examples from holarctic fishes. Vie Milieu, 50: 221-243.

Carvalho-Varela, M. and V. Cunha-Ferreira. – 1987. Helminth parasites of the common sole, Solea solea, and the Senegalese sole, Solea senegalensis, on the Portuguese continental coast. Aquaculture, 67: 135-138. doi:10.1016/0044-8486(87)90018-4

Cordero del Campillo, M., L.C. Ordóñez and A.R. Feo. – 1994. Indice- Catálogo de Zooparásitos Ibéricos. Universidad de Léon, Léon.

Cowie, R.H. and B. S. Holland. – 2006. Dispersal is fundamental to biogeography and the evolution of biodiversity on oceanic islands. J. Biogeogr., 33: 193-198. doi:10.1111/j.1365-2699.2005.01383.x

Dana, J.D. – 1853. On an isothermal oceanic chart illustrating the geographical distribution of marine animals. Am. J. Sci., 66: 153-157.

de Meeus, T., R. Marin and F. Renaud. – 1992. Genetic heterogeneity within populations of Lepeophtheirus europaensis (Copepoda: Caligidae) parasitic on two host species. Int. J. Parasitol., 22: 1179-1181. doi:10.1016/0020-7519(92)90039-N

Domingues, V.S., M. Alexandrou, V.C. Almada, D.R. Robertson, A. Brito, R.S. Santos and G. Bernardi. – 2008. Tropical fishes in a temperate sea: evolution of the wrasse Thalassoma pavo and the parrotfish Sparisoma cretense in the Mediterranean and the adjacent Macaronesian and Cape Verde Archipelagos. Mar. Biol., 154: 465-474. doi:10.1007/s00227-008-0941-z

El-Darsh, H.E.M. and P.J. Whitfield. – 1999. The parasite community infecting flounders, Platichthys flesus, in the tidal Thames. J. Helminthol., 73: 203-214.

Froese, R. and D. Pauly. – 2006. FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2006). Gibson, D.I. – 1972. Flounder parasites as biological tags. J. Fish Biol., 4: 1-9.

González, M.T. and C.A. Moreno. – 2005. The distribution of the ectoparasite fauna of Sebastes capensis from the southern hemisphere does not correspond with zoogeographical provinces of free-living marine animals. J. Biogeogr., 32: 1539-1547. doi:10.1111/j.1365-2699.2005.01323.x

González, M.T., C. Barrientos and C.A. Moreno. – 2006. Biogeographical patterns in endoparasite communities of a marine fish (Sebastes capensis Gmelin) with extended range in the Southern Hemisphere. J. Biogeogr., 33: 1086-1095. doi:10.1111/j.1365-2699.2006.01488.x

Gubbay, S. – 1995. Marine region 5: Northeast Atlantic. In: The World Bank, The World Conservation Union (IUCN), Great Barrier Reef Marine Park Authority (eds.), A Global Representative System of Marine Protected Areas, Volume 1. Australian Government, Australia.

Hayward, C.J. – 1997. Distribution of external parasites indicates boundaries to dispersal of sillaginid fishes in the Indo-West Pacific. Mar. Freshw. Res., 48: 391-400. doi:10.1071/MF96125

Kartavtsev, Y.P., T.-J. Park, K.A. Vinnikov, V.N. Ivankov, S.N. Sharina and J.-S. Lee. – 2007. Cytochrome b (Cyt-b) gene sequence analysis in six flatfish species (Teleostei, Pleuronectidae), with phylogenetic and taxonomic insights. Mar. Biol., 152: 757-773. doi:10.1007/s00227-007-0726-9

Krasnov, B.R., G.I. Shenbrot, D. Mouillot, I.S. Khokhlova and R. Poulin. – 2005. Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? J. Biogeogr., 32: 633-644. doi:10.1111/j.1365-2699.2004.01206.x

Lebedev, B.I. – 1969. Basic regularities in the distribution of monogeneans and trematodes of marine fishes in the world ocean. Zool. Zh., 48: 41-50.

Lile, N.K., O. Halvorsen and W. Hemmingsen. – 1994. Zoogeographical classification of the macroparasite faunas of four flatfish species from the northeastern Atlantic. Polar Biol., 14: 137-141. doi:10.1007/BF00234976

Link, J.S., M.J. Fogarty and R. Langton. – 2005. The trophic ecology of flatfishes. In: R.N. Gibson (ed.), Flatfishes Biology and Exploitation, pp. 185-212. Blackwell Publishing, Oxford.

MacKenzie, K. and P. Abaunza. – 1998. Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish. Res., 38: 45-56. doi:10.1016/S0165-7836(98)00116-7

MacKenzie, K. and D.I. Gibson. – 1970. Ecological studies of some parasites plaice and flounder. In: A. Taylor and R. Muller R (eds.), Aspects of fish parasitology. Symp. Br. Soc. Parasitol., 8: 1-42.

Manter, H.W. – 1966. The zoogeography of trematodes of marine fishes. Exp. Parasitol., 4: 62-86. doi:10.1016/0014-4894(55)90024-2

Marques, J.F. and H.N. Cabral. – 2007. Effects of sample size on fish parasites prevalence, mean abundance and mean intensity estimates. J. Appl. Ichthyol., 23: 158-162. doi:10.1111/j.1439-0426.2006.00823.x

Marques, J.F., M.J. Santos and H.N. Cabral. – 2005. Biogeography of parasites of Pleuronectiformes (Pisces) in the North Atlantic. Proc. IX Eur. Multicolloq. Parasitol., 2: 493-498.

Mas-Coma, S. – 1992. Parasitologia ecologica y evolutiva: aspectos aplicados. Avances en Parasitología, Protozoologia, pp: 43-65. Universidade de Santiago de Compostela, Santiago de Compostela.

McDowall, R.M. – 2000. Biogeography of the southern cool-temperate galaxioid fishes: evidence from metazoan macroparasite faunas. J. Biogeogr., 27: 1221-1229. doi:10.1046/j.1365-2699.2000.00490.x

Mejía-Madrid, H.H., E. Vázquez-Domínguez and G. Pérez-Ponce de León. – 2007. Phylogeography and freshwater basins in central Mexico: recent history as revealed by the fish parasite Rhabdochona lichtenfelsi (Nematoda). J. Biogeogr., 34: 787-801. doi:10.1111/j.1365-2699.2006.01651.x

Mosquera, J., M. Gómez-Gesteira and V. Pérez-Villar. – 2000. Using parasites as biological tags of fish populations: a dynamical model. Bull. Math. Biol., 62: 87-99. doi:10.1006/bulm.1999.0142

Moyle, P.B. and J.J. Cech. – 1996. Fishes: An introduction to ichthyology. Prentice Hall, New Jersey.

Nekola, J.C. and P.S. White. – 1999. The distance decay of similarity in biogeography and ecology. J. Biogeogr., 26: 867-878. doi:10.1046/j.1365-2699.1999.00305.x

Nicoll, W. – 1915. A list of trematode parasites of British marine fishes. Parasitology, 7: 339-378.

Nolf, D. and C. Marques da Silva. – 1997. Otolithes de poissons pliocènes (Plaisancien) de Vale de Freixo, Portugal. Rev. Micropaléonthol., 40: 273-282.

Oliva, M.E. and M.T. González. – 2005. The decay of similarity over geographical distance in parasite communities of marine fishes. J. Biogeogr., 32: 1327-1332.

Page, R.D.M. – 2003. Tangled trees: phylogeny, cospeciation, and coevolution. University of Chicago Press, Chicago.

Pais, A., P. Merella, M.C. Follesa, G. Garippa and D. Golani. – 2008. New data on Gaidropsarus granti (Regan, 1903) (Gadiformes: Lotidae) from the Mediterranean Sea, with emphasis on its parasites. Sci. Mar., 72: 461-468. doi:10.3989/scimar.2008.72n3461

Palm, H.W., S. Klimpel and C. Bucher. – 1999. Checklist of metazoan fish parasites of German coastal waters. Institut für Meereskunde an der Christian-Albrechts-Universität Kiel, Kiel.

Papoutsoglou, S.E. and E.G. Papaparaskeva-Papoutsoglou. – 1977. Metazoan parasites of Solea solea (L.) from Porto-Largo, north Aegean Sea, Greece. Mem. Biol. Mar. Oceanogr., 7: 21-33.

Pardo, B.G., A. Machordom, F. Foresti, M.F.C. Azevedo, R. Bañón, L. Sánchez and P. Martínez. – 2005. Phylogenetic analysis of flatfish (Order Pleuronectiformes) based on mitochondrial 16S rDNA sequences. Sci. Mar., 69: 531-543. doi:10.3989/scimar.2005.69n4531

Petter, A.J. and J. Cabaret. – 1995. Ascaridoid nematodes of teleostean fishes from the eastern North Atlantic and Seas of the north of Europe. Parasite, 2: 217-223.

Petter, A.J. and B.M. Radujkovic. – 1989. Parasites des poisons marins du Montenegro: Nematodes. Acta Adriat., 30: 195-236.

Poulin, R. and S. Morand. – 2000. The diversity of parasites. Q. Rev. Biol., 75: 277-293. doi:10.1086/393500

Poulin, R. – 1998. Evolutionary ecology of parasites: from individuals to communities. Chapman and Hall, London.

Poulin, R. – 2003. The decay of similarity with geographical distance in parasite communities of vertebrate hosts. J. Biogeogr., 30: 1609-1615. doi:10.1046/j.1365-2699.2003.00949.x

Renaud, F. and C. Gabrion. – 1988. Speciation of cestoda: Evidence of two sibling species in the complex Bothrimonus nylandicus (Schneider 1902) (Cestoda: Cyathocephalidea). J. Parasitol., 97: 139-147.

Rodrigues, H.O., M. Carvalho-Varela, S.S. Rodrigues and R. Cristofaro. – 1975a. Nova contribuição para o estudo dos nematódeos de peixes do oceano Atlântico - costa continental Portuguesa e costa do Norte da África. Mem. Inst. Oswaldo Cruz, 73: 127-134.

Rodrigues, H.O., D. Noronha and M. Carvalho-Varela. – 1975b. Alguns acantocéfalos de peixes do oceano Atlântico, costa continental Portuguesa e costa do Norte da África. Mem. Inst. Oswaldo Cruz, 73: 209-214.

Rohde, K. – 2002. Ecology and biogeography of marine parasites. Adv. Mar. Biol., 43: 1-86. doi:10.1016/S0065-2881(02)43002-7

Rohde, K. and C.J. Hayward. – 2000. Oceanic barriers as indicated by scombrid fishes and their parasites. Int. J. Parasitol., 30: 579-583. doi:10.1016/S0020-7519(00)00023-0

Sasal, P., Desdevises, Y. and S. Morand. – 1998. Host-specialization and species diversity in fish parasites: phylogenetic conservatism? Ecography, 21: 639-643. doi:10.1111/j.1600-0587.1998.tb00557.x

Stireman, J.O. – 2005. The evolution of generalization? Parasitoid flies and the perils of inferring host range evolution from phylogenies. J. Evol. Biol., 18: 325-336. doi:10.1111/j.1420-9101.2004.00850.x

Van Damme, P.A. and F. Ollevier. – 1996. The population dynamics of Lernaeocera lusci and L. branchialis on intermediate hosts. Helgol. Meeresunters., 50: 177-190. doi:10.1007/BF02367150

van den Broek, W.L.F. – 1979a. Copepod ectoparasites of Merlangius merlangus and Platichthys flesus. J. Fish Biol., 14: 371-380. doi:10.1111/j.1095-8649.1979.tb03531.x

van den Broek, W.L.F. – 1979b. Infection of estuarine populations of Cryptocotyle lingua (Creplin). J. Fish Biol., 14: 395-402. doi:10.1111/j.1095-8649.1979.tb03534.x

Vinarski, M.V., N.P. Korallo, B.R. Krasnov, G.I. Shenbrot and R. Poulin. – 2007. Decay of similarity of gamasid mite assemblages parasitic on Palaearctic small mammals: geographic distance, host-species composition or environment. J. Biogeogr., 34: 1691-1700. doi:10.1111/j.1365-2699.2007.01735.x

Waltari, E., E.P. Hoberg, E.P. Lessa and J.A. Cook. – 2007. Eastward Ho: phylogeographical perspectives on colonization of hosts and parasites across the Beringian nexus. J. Biogeogr., 34: 561-574. doi:10.1111/j.1365-2699.2007.01705.x

Williams, H.H. – 1959. A list of parasitic worms, including 22 new records, from marine fishes caught off the British Isles. Ann. Mag. Nat. Hist., ser. 13: 705-715.

Zeddam, J.L., P. Berrebi, F. Renaud, A. Raibaut and C. Gabrion. – 1998. Characterization of two species of Lepeophtheirus (Copepoda, Caligidae) from flatfishes. Description of Lepeophtheirus europaensis sp. nov. Parasitology, 96: 129-144.