Scientia Marina, Vol 70, No 4 (2006)

Genetic and morphologic differentiation of the Lusitanian toadfish (Halobatrachus didactylus) between estuarine and coastal areas in Portugal

Joana F. Marques
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Lisboa , Portugal

Ana Luísa Rego
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Lisboa , Portugal

José Lino Costa
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Lisboa , Portugal

Maria José Costa
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Lisboa , Portugal

Henrique N. Cabral
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Lisboa , Portugal


The Lusitanian toadfish, Halobatrachus didactylus (Bloch and Schneider, 1801), is distributed from the Ghana coast to the Iberian Peninsula, being particularly abundant on the south coast of Portugal. The differentiation of this species along the Portuguese coast was assessed through the analysis of 10 samples, considering morphological characters (20 morphometric and 16 meristic) and genetic markers (10 allozymes, 11 loci). Southern samples included estuaries and their adjacent coastal areas, given that this species inhabits both environments, whereas western samples only comprised estuaries. Morphometric and meristic data discriminant analysis evidenced some differentiation between estuarine and coastal populations. This was not entirely corroborated by the genetic analysis, which showed an overall pattern of low FST (0.042) and Nei’s genetic distance, even between geographically distant areas. However, higher values of these parameters were found between estuaries of the south coast and their adjacent coastal areas, suggesting that estuarine systems play a major role in such differentiation. Results are discussed regarding toadfish life-history pattern and Portuguese coast geomorphology, giving an insight into the biological and environmental factors influencing population sub-structuring.


Halobatrachus didactylus differentiation; allozymes; morphology; population structure; coastal areas

Full Text:



Alayse, J.P. – 1987. Le complexe Solea lascaris: mise en evidence par l’étude du polymorphisme enzymatique de deux espèces sympatriques en Mer d’Iroise. Biochem. Syst. Ecol., 15: 204–273. doi:10.1016/0305-1978(87)90031-7

Alexandrino, P. – 1996. Genetic and morphological differentiation among some Portuguese populations of allis shad Alosa alosa (L., 1758) and twaite shad Alosa fallax (Lacépède, 1803). Pub. Espec. Inst. Esp. Oceanog., 21: 15-24.

Avise, J.C., C.A. Reeb and N.C. Saunders. – 1987. Geographic population structure and species differences in mitochondrial DNA of mouthbrooding marine catfishes (Ariidae) and demersal spawning toadfishes (Batrachoididae). Evolution, 41: 991-1002. doi:10.2307/2409187

Ayvazian, S.G., M.S. Johnson and D.J. McGlashan. – 1994. High levels of genetic subdivision of marine and estuarine populations of the estuarine catfish Cnidoglanis macrocephalus (Plotosidae) in southwest Australia. Mar. Biol., 118: 25-31. doi:10.1007/BF00699216

Beheregaray, L.B. and P. Sunnucks. – 2001. Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Mol. Ecol., 10: 2849-2866. doi:10.1046/j.1365-294X.2001.t01-1-01406.x

Belkhir, K., P. Borsa, L. Chikhi, N. Rafauste and F. Bonhomme. – 1996-2001. GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations. Université de Montpellier II, Montpellier.

Bilton, D.T., J. Paula and J.D.D. Bishop. – 2002. Dispersal, genetic differentiation and speciation in estuarine organisms. Est. Coast. Shelf Sci., 55: 937-952. doi:10.1006/ecss.2002.1037

Cabral, H.N., F. Castro, D. Linhares and P. Alexandrino. – 2003a. Genetic differentiation of Solea solea (Linnaeus, 1758) and Solea senegalensis Kaup, 1858, (Pisces: Pleuronectiformes) from several estuarine systems of the Portuguese coast. Sci. Mar., 67: 43-52.

Cabral, H.N., J.F. Marques, A.L. Rego, A.I. Catarino, J. Figueiredo and J. Garcia. – 2003b. Population differentiation of Synaptura lusitanica Capello, 1868, along the Portuguese coast. J. Sea Res., 50: 167-175. doi:10.1016/S1385-1101(03)00060-1

Castilho, R. and B.J. McAndrew. – 1998. Population structure of seabass in Portugal: evidence from allozymes. J. Fish Biol., 53: 1038-1049. doi:10.1111/j.1095-8649.1998.tb00461.x

Chaplin, J.A., G.A. Baudains, H.S. Gill, R. McCulloch and I.C. Potter. – 1998. Are assemblages of black bream (Acanthopagrus butcheri) in different estuaries genetically distinct? Int. J. Salt Lake Res., 6: 303-321. doi:10.1007/BF02447913

Chikhi, L., F. Bonhomme and J.-F. Agnese. – 1998. Low genetic variability in a widely distributed and abundant clupeid species, Sardinella aurita. New empirical results and interpretations. J. Fish Biol., 52: 861-878.

Costa, J.L. – 1993. Abundance and distribution of the toadfish Halobatrachus didactylus on the Mira estuary (Portugal): seasonal variations and ruling factors. J. Fish Biol., 43 (Suppl. A): 330.

Goudet, J., S. Raymond, T. de Meeüs and F. Rousset. – 1996. Testing differentiation in diploid populations. Genetics, 144: 1933-1940.

Gyllensten, U. – 1985. The genetic structure of fish: differences in the intraspecific distribution of biochemical genetic variation between marine, anadromous and freshwater species. J. Fish Biol., 26: 691-699. doi:10.1111/j.1095-8649.1985.tb04309.x

Hair Jr., J.F., R. Anderson, R. Tatham and W. Black. – 1996. Multivariate data analysis with readings. Prentice Hall Incorporated, New Jersey.

Harris, H. and D.A. Hopkinson. – 1976. Handbook of enzyme electrophoresis in human genetics. North-Holland publishers, Amesterdam.

Humphries, J.M., F.L. Bookstein, B. Chernoff, G.R. Smith, R.L. Elder and S.G. Poss. – 1981. Multivariate discrimination by shape in relation to size. Syst. Zool., 30: 291-308. doi:10.2307/2413251

Hurlbut, T. and D. Clay. – 1998. Morphometric and meristic differences between shallow- and deep-water populations of White hake (Urophycis tenuis) in the southern Gulf of St Lawrence. Can. J. Fish. Aquat. Sci., 55: 2274-2282. doi:10.1139/cjfas-55-10-2274

Ihssen, P.E., D.O. Evans, W.J. Christie, J.A. Reckahn and R.L. DesJardine. – 1981. Life history, morphology, and electrophoretic characteristics of five allopatric stocks of Late whitefish (Coregonus clupeaformis) in the Great Lakes region. Can. J. Fish. Aquat. Sci., 38: 1790-1807. doi:10.1139/f81-226

Kinsey, S.T., T. Orsoy, T.M. Bert and B. Mahmoudi. – 1994. Population structure of the Spanish sardine Sardinella aurita: natural morphological variation in a genetically homogeneous population. Mar. Biol., 118: 309-317. doi:10.1007/BF00349798

Lindsey, C.C. – 1988. Factors controlling meristic variation. Fish Physiol., 11: 197-274. doi:10.1016/S1546-5098(08)60215-0

Mantel, N. – 1967. The detection of disease clustering and a generalized regression approach. Cancer Res., 27: 209-220.

Misra, R.K. and J.E. Carscadden. – 1987. A multivariate analysis of morphometrics to detect differences in populations of Capelin (Mallotus villosus). J. Cons. Int. Explor. Mer, 43: 99-106.

Murphy, R.W., J.W. Sites, D.G. Burth Jr. and C.H. Haufler. – 1996. Proteins: Isozyme electrophoresis. In: D.M. Hills, C. Moritz and B.K. Mable (eds.), Molecular systematics, pp. 51-120. Sinauer Associates, Massachussets.

Murta, A.G. – 2000. Morphological variation of Horse mackerel (Trachurus trachurus) in the Iberian and North African Atlantic: implications for stock identification. ICES J. Mar. Sci., 57: 1240-1248. doi:10.1006/jmsc.2000.0810

Nei, M. – 1978. Estimation of the average heterozygosity and genetic distance from a small number of individuals. Genetics, 89: 583-590.

Nielsen, E.E., P.H. Nielsen, D. Meldrup and M.M. Hansen. – 2004. Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and North Sea. Mol. Ecol., 13: 585-595. doi:10.1046/j.1365-294X.2004.02097.x

Pampoulie, C., E.S. Gysels, G.E. Maes, B. Hellemans, V. Leentjes, A.G. Jones and F.A.M. Volchaert. – 2004. Evidence for finescale genetic structure and estuarine colonisation in a potential high gene flow marine goby (Pomatischistus minutos). Heredity, 92: 434-445. doi:10.1038/sj.hdy.6800438

Pasteur, N., M. Autem, P. Pichot and M. Goucha. – 1985. Structure génétique de la sole (Solea vulgaris Quensel, 1806; Téléostéens, Soléidés): premier catalogue de polymorphismes biochemiques acessibles par l’electrophorèse en gel d’amidon. Rev. Trav. Inst. Pêches Mar., 47: 37-54.

Pinheiro, A., C.M. Teixeira, A.L. Rego, J.F. Marques and H.N. Cabral. – 2005. Genetic and morphological variation of Solea lascaris (Risso, 1810) along the Portuguese coast. Fish. Res., 73: 67-78. doi:10.1016/j.fishres.2005.01.004

Raymond, M. and F. Rousset. – 1995. GENEPOP: population genetics software for exact tests and ecumenism. J. Heredity, 86: 248-249.

Ricker, W.E. – 1973. Linear regressions in fishery research. J. Fish. Res. Board Can., 30: 409-434.

Roldán, M.I., R.G. Perrotta, M. Cortey and C. Pla. – 2000. Molecular and morphologic approaches to discrimination of variability patterns in Chub mackerel, Scomber japonicus. J. Exp. Mar. Biol. Ecol., 253: 63-74. doi:10.1016/S0022-0981(00)00244-6

Roux, C. – 1986. Batrachoididae. In: P.J.P. Whitehead, M.L. Bauchot, J.C. Hureau, J. Nielsen and E. Tortonese. (eds.) Fishes of the North-eastern Atlantic and Mediterranean, vol. III, 1360-1361. UNESCO, Paris.

Santos, M.E., T. Modesto, R.J. Matos, M.S. Grober, R.F. Oliveira and A. Canário. – 2000. Sound production by the Lusitanian toadfish, Halobatrachus didactylus. Bioacoustics, 10: 309-321.

Shaklee, J.B., F.W. Allendorf, D.C. Moritz and G.S. Whitt. – 1990. Gene nomenclature for protein-coding loci in fish. Trans. Amer. Fish. Soc., 119: 2-15. doi:10.1577/1548-8659(1990)119<0002:GNFPLI>2.3.CO;2

Smith, P.J. and Y. Fujio. – 1982. Genetic variation in marine teleosts: high variability in habitat specialists and low variability in habitat generalists. Mar. Biol., 69: 7-20. doi:10.1007/BF00396955

Sobral, D. and J. Gomes. – 1997. Peixes litorais. Estuário do Sado. ICN, Lisboa.

Spanakis, E., N. Tsimenides and E. Zouros. – 1989. Genetic differences between populations of sardine, Sardina pilchardus, and anchovy, Engraulis encrasicolus, in the Aegean and Ionian seas. J. Fish Biol., 35: 417-437. doi:10.1111/j.1095-8649.1989.tb02993.x

Stefanni, S., P.J. Miller and P. Torricelli. – 1996. Studio comparativo di due popolazioni di Pomatoschistus minutus (Teleostei: Gobiidae) della laguna veneta e di Plymouth (UK). Atti Conveg. Assoc. Ital. Ittiol. Acque Dolci (AIIAD), 4: 385-390.

Stefanni, S., E.S. Gysells, F.A.M. Volckaert and P.J. Miller. – 2003. Allozyme variation and genentic divergence in the sand goby, Pomatoschistus minutus (Teleostei: Gobiidae). J. Mar. Biol. Assoc. U.K., 83: 1143-1149. doi:10.1017/S0025315403008403h

Tudela, S. – 1999. Morphological variability in a Mediterranean, genetically homogeneous population of the European anchovy, Engraulis encrasicolus. Fish. Res., 42: 229-243. doi:10.1016/S0165-7836(99)00052-1

Ward, R.D., M. Woodwark and O.F. Skibinski. – 1994. A comparison of genetic diversity levels in marine, freshwater and anadromous fishes. J. Fish Biol., 44: 213-232. doi:10.1111/j.1095-8649.1994.tb01200.x

Weir, B.S. and C.C. Cockerham. – 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. doi:10.2307/2408641

Wright, S. – 1965. The interpretation of population structure by Fstatistics with special regard to systems of mating. Evolution, 19: 395-420. doi:10.2307/2406450

Copyright (c) 2006 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support