Biological Invasions

, Volume 18, Issue 3, pp 619–630 | Cite as

Role of ships’ hull fouling and tropicalization process on European carcinofauna: new records in Galician waters (NW Spain)

  • José A. Cuesta
  • Bruno Almón
  • Jacinto Pérez-Dieste
  • Juan E. Trigo
  • Rafael Bañón
Original Paper


Ten unusual decapod crustacean species are reported for the coasts of Galicia (NW Spain), eight of them recorded for the first time in this area. Three species: Pilumnopeus africanus, Charybdis hellerii and Pachygrapsus gracilis, are non-indigenous species. The reports of Panopeus africanus and Inachus aguiarii represent the northernmost localities of these African species, whose previous North limits were in the Southwestern European coasts. Remaining five species: Xaiva biguttata, Bathynectes longipes, Parthenopoides massena, Monodaeus couchii and Homola barbata are scarcely known species found within their distribution range. Updated data about these species are given, both from the point of view of their distribution and identification (morphological and molecular methods), as well as the potential pathways for introduction of the non-indigenous ones. According to evidence presented in the present study, biofouling still remains an important vector of species transmission and surely has been undervalued with respect to ballast water.


Biofouling Tropicalization Northeast Atlantic Ocean Non-indigenous species Crabs First records 



We wish to thank the fisherman Alejandro Argibay (vessel “Xa me Vedes”) for providing the specimens and data of various crab species caught in Galician waters. We gratefully acknowledge the assistance of the members of Grupo do Estudo do Medio Mariño (GEMM) in conducting sampling dives. Thanks are due to Carlos Sánchez Nieto for his help on molecular laboratory work. Special thanks to Alberto Serrano and Marian Blanco (Instituto Español de Oceanografía of Santander) for providing additional data of M. couchii. Four anonymous reviewers provided useful comments and corrections that clearly improved the manuscript. Funds for DNA analysis were provide by MEGALOPADN project (CGL2009-11225) funded by the “Ministerio de Economía y Competividad” Spanish Plan R + D + I and FEDER.


  1. Abelló P, Hispano C (2006) The capture of the Indo-Pacific crab Charybdis feriata (Linnaeus, 1758) (Brachyura: Portunidae) in the Mediterranean Sea. Aquat Invasions 1(1):13–16CrossRefGoogle Scholar
  2. Almón B, Pérez J, Bañón R, Trigo J (2014) First record of Caprella mutica from the Iberian Peninsula: expansion southwards in European waters. Mar Biodivers Rec 7(e30):1–4Google Scholar
  3. Alvarez-Salgado XA, Labarta U, Fernández-Reiriz MJ, Figueiras FG, Rosón G, Piedracoba S, Filgueira R, Cabanas JM (2008) Renewal time and the impact of harmful algal blooms on the extensive mussel raft culture of the Iberian coastal upwelling system (SW Europe). Harmful Algae 7:849–855CrossRefGoogle Scholar
  4. Bañón R (2012) Introducción al estudio de las especies exóticas marinas en Galicia. Rev Galega Rec Mariños (Monog.) 3:1–67Google Scholar
  5. Bañón R, Rolán E, García-Tasende M (2008) First record of the purple dye murex Bolinus brandaris (Gastropoda: Muricidae) and a revised list of non native molluscs from Galician waters (Spain, NE Atlantic). Aquat Invasions 3:331–334CrossRefGoogle Scholar
  6. Bañón R, Fernández J, Trigo JE, Pérez-Dieste J, Barros-García D, De Carlos A (2015) Range expansion, biometric features and molecular identification of the exotic ark shell Anadara kagoshimensis from Galician waters, NW Spain. J Mar Biol Assoc UK 95:545–550CrossRefGoogle Scholar
  7. Barnard KH (1955) Additions to the fauna-list of South African Crustacea and Pycnogonida. Ann S Afr Mus 43:1–107Google Scholar
  8. Castejón D, Guerao G (2013) A new record of the American blue crab, Callinectes sapidus Rathbun, 1896 (Decapoda: Brachyura: Portunidae), from the Mediterranean coast of the Iberian Peninsula. Bioinvasions Rec 2:141–143CrossRefGoogle Scholar
  9. Crandall KA, Fitzpatrick JFJ (1996) Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Syst Biol 45:1–26CrossRefGoogle Scholar
  10. Cuesta Mariscal JA, García Raso JE, González Gordillo JI (1991) Primera cita de Rhithropanopeus harrisii (Crustacea Decapoda, Brachyura, Xanthidae) en la Península Ibérica. Bol IEO 7:149–153Google Scholar
  11. Cuesta JA, Drake P, Arias AM (2015) First record of the blue crab Callinectes exasperatus (Decapoda, Brachyura, Portunidae) for European waters. Mar Biodivers Rec 8(e36):1–4Google Scholar
  12. d’Udekem d’Acoz C (1999) Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes aunord de 25°N. Collect Patrim Nat 40, Mus natl Hist nat: Paris. ISBN: 2-86515-114-10. XGoogle Scholar
  13. Dauvin JC, Tous Rius A, Ruellet T (2009) Recent expansion of two invasive crabs species Hemigrapsus sanguineus (de Haan, 1835) and H. takanoi Asakura and Watanabe 2005 along the Opal Coast, France. Aquat Invasions 4:451–465CrossRefGoogle Scholar
  14. de Man JG (1913) Sur une nouvelle observation de crabes habitant les coquilles vides des balanes. Bull Mus natl Hist nat Paris 19:9–11Google Scholar
  15. de Man JG (1914) Description de deux espèces nouvelles du genre Pilumnus Leach et d’une jeune femelle du Pil. longicornis Hilgd., découvertes dans des coquilles vides de balanes. Bull Soc Zool France Paris 39:330–343Google Scholar
  16. Dineen JF, Clark PF, Hines AH, Reed SA, Walton HP (2001) Life history, larval description, and natural history of Charybdis hellerii (Decapoda, Brachyura, Portunidae), an invasive crab in the Western Atlantic. J Crustac Biol 21:774–805CrossRefGoogle Scholar
  17. Drake P, Marco-Herrero E, Subida MD, Arias AM, Cuesta JA (2014) Host use pattern of the pea crab Afropinnotheres monodi: potential effects on its reproductive success and geographical expansion. Mar Ecol Prog Ser 498:203–215CrossRefGoogle Scholar
  18. Estoup A, Largiadèr CR, Perrot E, Chourrout D (1996) Rapid one tube DNA extraction for reliable PCR detection of fish polymorphic marker and transgenes. Mol Mar Biol Biotech 5:295–298Google Scholar
  19. Félix-Hackradt F, Hackradt C, Treviño-Otón J, García-Chartón JA (2010) Continued expansion of Percnon gibbesi (Crustacea: Decapoda: Plagusiidae) into western Mediterranean waters. Mar Biodivers Rec 3(e22):1–3Google Scholar
  20. Galil BS (2008) Alien species in the Mediterranean Sea—which, when, where, why? Hydrobiologia 606:105–116CrossRefGoogle Scholar
  21. Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean Sea. Biol Invasions 11:359–372CrossRefGoogle Scholar
  22. Galil BS, Kevrekidis K (2002) Exotic decapods and stomatopods off Rhodes Island (Greece) and the eastern Mediterranean Transient. Crustaceana 75:925–930CrossRefGoogle Scholar
  23. Galil B, Froglia C, Noël P (2002) Crustaceans: decapods and stomatopods. In: Briand F (ed) CIESM atlas of exotic species in the mediterranean, vol 2. CIESM Publishers, MonacoGoogle Scholar
  24. García-de-Lomas J, Dana ED, López-Santiago J, González R, Ceballos G, Ortega F (2010) Management of the Chinese mitten crab, Eriocheir sinensis (H. Milne Edwards, 1853) in the Guadalquivir Estuary (Southern Spain). Aquat Invasions 5:323–330CrossRefGoogle Scholar
  25. García-Raso JE, González-Gurriarán E, Sarda F (1987) Estudio comparativo de la fauna de Crustáceos Decápodos Braquiuros de tres áreas de la Península Ibérica (Galicia, Málaga y Cataluña). Investig Pesq 51:43–55Google Scholar
  26. Godwin LS (2003) Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling 19:123–131CrossRefPubMedGoogle Scholar
  27. Gollasch S (1996) Untersuchungen des Arteintrages durch den internationalen Schiffsverkehr unter besonderer Berücksichtigung nichtheimischer Arten. Dissertation, Universität HamburgGoogle Scholar
  28. Gollasch S (1999) The Asian decapod Hemigrapsus penicillatus (de Haan, 1835) (Grapsidae, Decapoda) introduced in European waters: status quo and future perspective. Helgol Meeresunters 52:359–366CrossRefGoogle Scholar
  29. Gollasch S (2002) The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling 18:105–121CrossRefGoogle Scholar
  30. Gómez-Gesteira M, Gimeno L, De Castro M et al (2011) The state of climate in NW Iberia. Climate Res 48:109–144CrossRefGoogle Scholar
  31. González-Gurriarán E, Méndez M (1986) Crustáceos Decápodos das Costas de Galicia. I. Brachyura. Cuadernos da Área de Ciencias Biolóxicas, Seminario de Estudos Galegos, vol 2, 2ª edn. O Castro-Sada, A Coruña, Ed. Do CastroGoogle Scholar
  32. Johnson DS (2014) Fiddler on the roof: a northern range extension for the marsh fiddler crab Uca pugnax. J Crustac Biol 34:671–673CrossRefGoogle Scholar
  33. Kocatas K (1981) Liste preliminaire et repartition des Crustacés Décapodes des eaux turques. Rapp Comm Int Mer Médit 27:161–162Google Scholar
  34. Macho G, Vázquez E, Giráldez R, Molares J (2010) Spatial and temporal distribution of barnacle larvae in the partially mixed estuary of the Ría de Arousa (Spain). J Exp Mar Biol Ecol 392:129–139CrossRefGoogle Scholar
  35. Maldonado M, Uriz MJ (1992) Relationships between sponges and crabs: patterns of epibiosis on Inachus aguiarii (Decapoda, Majidae). Mar Biol 113:282–286Google Scholar
  36. Manning RB (1993) West African pinnotherid crabs, subfamily Pinnotherinae (Crustacea, Decapoda, Brachyura). Bull Mus natl Hist nat Paris, sér. 4. Sect A 15:125–177Google Scholar
  37. Manning RB, Holthuis LB (1981) West African brachyuran crabs (Crustacea: Decapoda). Smithson Contrib Zool 306:1–379CrossRefGoogle Scholar
  38. Marco-Herrero M, Abelló P, Drake P, García Raso JE, González-Gordillo JI, Guerao G, Palero F, Cuesta JA (2015) Annotated checklist of brachyuran crabs (Crustacea, Decapoda) of the Iberian Peninsula (SW Europe). Sci Mar 79:243–256CrossRefGoogle Scholar
  39. Monod TH (1956) Hippidea et Brachyura ouest africains. Mem Inst Franç Afrique Noire 45:1–674Google Scholar
  40. Neves AM (1975) Sobre uma colecção de Crustáceos Decápodes da Baía de Setúbal (Portugal). Est Fauna Port 5:1–48Google Scholar
  41. Özcan T, Katağan T, Irmak E (2010) An exotic crab, Charybdis hellerii (A. Milne-Edwards, 1867) along the Turkish coasts. Bihar Biol 4:1–5Google Scholar
  42. Perez FF, Padin XA, Pazos Y, Gilcoto M, Cabanas M, Pardo PC, Doval MD, Farina-Bustos L (2010) Plankton response to weakening of the Iberian coastal upwelling. Glob Change Biol 16:1258–1267CrossRefGoogle Scholar
  43. Poupin J, Davie PJF, Cexus JC (2005) A revision of the genus Pachygrapsus Randall, 1840 (Crustacea: Decapoda: Brachyura, Grapsidae), with special reference to the Southwest Pacific species. Zootaxa 1015:1–66Google Scholar
  44. Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721CrossRefGoogle Scholar
  45. Rodríguez A, Paula J (1993) Larval and postlarval development of the mud crab Panopeus africanus Milne Edwards (Decapoda, Xanthidae) reared in the laboratory. J Crustac Biol 13:296–308CrossRefGoogle Scholar
  46. Rodríguez G, Suárez H (2001) Anthropogenic dispersal of decapod crustaceans in aquatic environments. Interciencia 26:282–288Google Scholar
  47. Schubart CD (2011) Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian and anphi-atlantic differentiation based on mtDNA. Zool Anz 250:472–478CrossRefGoogle Scholar
  48. Schubart CD, Huber MGJ (2006) Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bull Fr Pêche Piscic 380–381:1019–1028CrossRefGoogle Scholar
  49. Schubart CD, Cuesta JA, Felder DL (2002) Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea. J Crustac Biol 22:28–44CrossRefGoogle Scholar
  50. Schubart CD, Guerao G, Abelló P (2012) First record and evidence of an established population of the North American mud crab Dyspanopeus sayi (Brachyura: Heterotremata: Panopeidae) in the western Mediterranean. Sci Mar 76:79–85CrossRefGoogle Scholar
  51. Serrano A, Sánchez F, Punzón A, Velasco F, Olaso I (2011) Deep sea megafaunal assemblages off the northern Iberian slope related to environmental factors. Sci Mar 75:425–437CrossRefGoogle Scholar
  52. Subida MD, Arias AM, Drake P, García-Raso JE, Rodríguez A, Cuesta JA (2011) On the occurrence of Afropinnotheres monodi Manning, 1993 (Decapoda: Pinnotheridae) in European waters. J Crustac Biol 31:367–369CrossRefGoogle Scholar
  53. Tavares M, Amouroux JM (2003) First record of the non-indigenous crab, Charybdis hellerii (A. Milne-Edwards, 1867) from French Guyana (Decapoda, Brachyura, Portunidae). Crustaceana 76:625–630CrossRefGoogle Scholar
  54. Thoma BP, Guinot D, Felder DL (2014) Evolutionary relationships among American mud crabs (Crustacea: Decapoda: Brachyura: Xanthoidea) inferred from nuclear and mitochondrial markers, with comments on adult morphology. Zool J Linn Soc 170:86–109CrossRefGoogle Scholar
  55. Türkay M (2001) Decapoda. 284–292. In: Costello MJ, Emblow C, White R (eds) European register of marine species. A check-list of the marine species in Europe and a bibliography of guides to their identification. Collect Patrim Nat 50. Mus natl Hist nat, Paris. ISBN: 2-85653-538-0Google Scholar
  56. Urgorri V, Solorzano MR, Besteiro C, Ramil F (1990) Crustáceos Decápodos Braquiuros de Galicia existentes en las colecciones del Museo de Historia natural `Luis Iglesias’ (Galicia). Bol R Soc Esp Hist Nat (Secc Biol) 85:5–15Google Scholar
  57. Wolff T (1954) Occurrence of two East American species of crabs in European waters. Nature 174:188–189CrossRefGoogle Scholar
  58. Yeo DCJ, Ahyong ST, Lodge DM, Ng PKL, Naruse T, Lane DJW (2010) Semisubmersible oil platforms: understudied and potentially major vectors of biofouling-mediated invasions. Biofouling 26:179–186CrossRefPubMedGoogle Scholar
  59. Zariquiey Álvarez R (1968) Crustáceos decápodos ibéricos. Invest Pesq 32:1–510Google Scholar
  60. Zenetos A, Gofas S, Verlaque V et al (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterr Mar Sci 11:381–493Google Scholar
  61. Zenetos A, Gofas S, Morri C et al (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Mediterr Mar Sci 13:328–352Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • José A. Cuesta
    • 1
  • Bruno Almón
    • 2
  • Jacinto Pérez-Dieste
    • 2
  • Juan E. Trigo
    • 2
  • Rafael Bañón
    • 2
  1. 1.Instituto de Ciencias Marinas de Andalucía, CSICPuerto RealSpain
  2. 2.Grupo de Estudos do Medio Mariño (GEMM)RibeiraSpain

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