Biological Invasions

, Volume 16, Issue 10, pp 2221–2245 | Cite as

Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: multiple introductions revealed by mitochondrial sequence data

  • M. Pilar Cabezas
  • Raquel Xavier
  • Madalena Branco
  • António M. Santos
  • José Manuel Guerra-García
Original Paper


The caprellid Caprella scaura, native to the western Indian Ocean, is one striking example of a successful invader. It was first recorded in the Iberian Peninsula in Gerona (north-eastern coast of Spain), in 2005, and has recently been reported throughout the Mediterranean and Atlantic coasts of this region. The most likely vector of introduction and distribution is within the hull-fouling community on recreational craft. However, beyond the dates of detection, the introduction history of C. scaura remains unclear. Direct sequencing of mitochondrial DNA (cytochrome c oxidase subunit I) was used to compare genetic composition in native and introduced populations in order to infer the invasion history of this species. In addition, 18S rDNA sequences were used to resolve phylogenetic relationships within this species and with the morphologically closest species Caprella californica and Caprella scauroides. The high genetic divergence and population subdivision found between non-native Iberian populations together with a high level of genetic diversity in some populations indicate multiple geographical sources and introduction points for this caprellid. Our data suggest that Iberian populations may derive from at least two sources: (1) Pacific Australian, and (2) Indian Ocean, either directly, or, more likely, through stepping-stone events from central Mediterranean population(s). Atlantic Iberian populations seem to be the most recently established populations. On the other hand, this is the first study providing molecular evidence confirming C. scaura, C. californica and C. scauroides as distinct species. It also provides strong molecular evidence that C. scaura typica and C. scaura scaura correspond to the same subspecies, and the Japanese C. scaura diceros and the Chilean C. scaura spinirostris could merit specific rank.


Caprellid amphipod COI gene Invasion pathways Non-native species Population genetics Taxonomy 



The authors would like to thanks to Macarena Ros, Carlos Navarro-Barranco and Elena Baeza-Rojano for their kind help and assistance during field work. Special thanks to N. L. Demchenko (CSJAP, Japan), L. Hughes (CSAUS, Australia), C. d’Udekem d’Acoz (CSGRE, Greece), J. Nuñez (CSTEN, Tenerife), C. S. Serejo and M. B. Lacerda (CSBRA, Brazil), R. A. King and D. N. Knott (CSCHA, Charleston), L. Montelli (CCWAU, Australia), and the California Academy of Sciences Invertebrate Zoology (San Francisco, CA) (CCSFB, CCSFE) for providing some of the samples used in the present study. Financial support of this work was provided by the Ministerio de Economía y Competitividad (Project CGL2011-22474, internal reference 2011-707) co-financed by FEDER funds of the European Union, by the Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía (Project P11-RNM-7041) and FCT: PTDC/MAR/104169/2008. R. Xavier and M. Branco have FCT Grants with references SFRH/BPD/75851/2011 and SFRH/BPD/40073/2007, respectively. M. P. Cabezas was supported by a PhD Grant ‘III Plan Propio de Investigación’, from the University of Seville.


  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Contr 19:716–723Google Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  3. Aoki M, Kikuchi T (1990) Caprella bidentata Utinomi, 1947 (Amphipoda: Caprellidea), a synonym of Caprella monoceros Mayer, 1890, supported by experimental evidence. J Crustacean Biol 10:537–543Google Scholar
  4. Arimoto I (1976) Taxonomic studies of caprellids (Crustacea, Amphipoda, Caprellidae) found in the Japanese adjacent waters. Special publications from the Seto Marine Biological Laboratory Series III, 1–299. Nippon Printing & Publishing Co, Ltd, OsakaGoogle Scholar
  5. Ashton GV (2006) Distribution and dispersal of the non-native caprellid amphipod, Caprella mutica Schurin 1935. Dissertation, University of AberdeenGoogle Scholar
  6. Ashton GV, Boos K, Shucksmith R, Cook E (2006) Rapid assessment of the distribution of marine non-native species in marinas in Scotland. Aquat Invasions 1:209–213Google Scholar
  7. Ashton GV, Stevens MI, Hart MC, Green DH, Burrows MT, Cook EJ, Willis KJ (2008) Mitochondrial DNA reveals multiple Northern Hemisphere introductions of Caprella mutica (Crustacea, Amphipoda). Mol Ecol 17:1293–1303PubMedGoogle Scholar
  8. Audet D, Davis DS, Miron G, Moriyasu M, Benhalima K, Campbell R (2003) Geographical expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova Scotian shore into the southeastern Gulf of St Lawrence, Canada. J Shellfish Res 22:255–262Google Scholar
  9. Baeza-Rojano E, Calero-Cano S, Hachero-Cruzado I, Guerra-García JM (2013) A preliminary study of the Caprella scaura amphipod culture for potential use in aquaculture. J Sea Res 83:146–151Google Scholar
  10. Baird HP, Miller KJ, Stark J (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antartic amphipods. Mol Ecol 20:3439–3454PubMedGoogle Scholar
  11. Bakir K, Katagan T (2011) On the occurrence of Caprella scaura Templeton, 1836 (Crustacea: Amphipoda) in Turkish waters. Zool Middle East 52:125–126Google Scholar
  12. Barrowclough GF, Zink RM (2009) Funds enough, and time: mtDNA, nuDNA and the discovery of divergence. Mol Ecol 18:2934–2936Google Scholar
  13. Cabezas MP, Guerra-García JM, Baeza-Rojano E, Redondo-Gómez S, Figueroa ME, Luque T, García-Gómez JC (2010) Exploring molecular variation in the cosmopolitan Caprella penantis (Crustacea: Amphipoda): results from RAPD analysis. J Mar Biol Assoc UK 90:617–622Google Scholar
  14. Cabezas MP, Cabezas P, Machordom A, Guerra-García JM (2013a) Hidden diversity and cryptic speciation refute cosmopolitan distribution in Caprella penantis (Crustacea: Amphipoda: Caprellidae). J Zool Syst Evol Res 51:85–99Google Scholar
  15. Cabezas MP, Navarro-Barranco C, Ros M, Guerra-García JM (2013b) Long-distance dispersal, low connectivity and molecular evidence of a new cryptic species in the obligate rafter Caprella andreae Mayer, 1890 (Crustacea: Amphipoda: Caprellidae). Helgol Mar Res 67:483–497Google Scholar
  16. Carlton JT (1996) Marine bioinvasions: the alternation of marine ecosystems by nonindigenous species. Oceanography 9:36–43Google Scholar
  17. Carlton JT, Eldredge LG (2009) Marine bioinvasions of Hawai‘i: the introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian archipelago. Bishop Museum Press, Honolulu, HawaiiGoogle Scholar
  18. Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130Google Scholar
  19. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedGoogle Scholar
  20. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedGoogle Scholar
  21. Cockman B, Albone P (1987) Caprellidae of the Swan River estuary. In: John J (ed) Swan River estuary, ecology and management, Curtin University, Environmental Studies Group report no. 1. Curtin University of Technology, Perth, Australia, pp 163–177Google Scholar
  22. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558PubMedGoogle Scholar
  23. Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J, Ballesteros E, Bianchi CN et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One 5(8):e11842. doi: 10.1371/journal.pone.0011842 PubMedCentralPubMedGoogle Scholar
  24. Concepcion GT, Kahng SE, Crepeau MW, Franklin EC, Coles SL, Toonen RJ (2010) Resolving natural ranges and marine invasions in a globally distributed octocoral (genus Carijoa). Mar Ecol Prog Ser 401:113–127Google Scholar
  25. Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer & Associates, SunderlandGoogle Scholar
  26. Cook EJ, Jahnke M, Kerckhof F, Minchin D, Faasse M, Boos K, Ashton G (2007) European expansion of the introduced amphipod Caprella mutica Schurin 1935. Aquat Invasions 2:411–421Google Scholar
  27. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystems engineers. Oikos 97:153–166Google Scholar
  28. Davies N, Villablanca FX, Roderick GK (1999) Determining the source of the individuals: multilocus genotyping in nonequilibrium population genetics. Trends Ecol Evol 14:17–21PubMedGoogle Scholar
  29. Dougherty C, Steinberg JE (1953) Notes on the skeleton shrimps (Crustacea, Caprellidea) of California. Proc Biol Soc Wash 66:39–50Google Scholar
  30. Duda TF (1994) Genetic population structure of the recently introduced Asian clam, Potamocorbula amurensis, in San Francisco Bay. Mar Biol 119:235–241Google Scholar
  31. EU (2008) Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off J EU L 164:19–40Google Scholar
  32. EU (2011) Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of the Regions: our life insurance, our natural capital: an EU biodiversity strategy to 2020. COM/2011/244. Brussels, European CommissionGoogle Scholar
  33. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedGoogle Scholar
  34. Excoffier L, Smouse P, Quattro J (1992) Analyses of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  35. Facon B, Pointier JP, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367PubMedGoogle Scholar
  36. Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782PubMedGoogle Scholar
  37. Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606Google Scholar
  38. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  39. Foster JM, Heard RW, Knott DM (2004) Northern range extensions from Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) on the Florida Gulf Coast and in South Carolina. Gulf Caribb Res 16:65–69Google Scholar
  40. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  41. Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55:314–322PubMedGoogle Scholar
  42. Galil BS, Occhipinti-Ambrogi A, Gollasch S (2008) Biodiversity impacts of species introductions via marine vessels. In: Abdulla A, Linden O (eds) Maritime traffic effects on biodiversity in the Mediterranean Sea: review of impacts, priority areas and mitigation measures. IUCN Centre for Mediterranean Cooperation, Malaga, pp 117–157Google Scholar
  43. Gollasch S (2002) The importance of ship hull fouling as a vector for species introduction into the North Sea. Biofouling 18:105–121Google Scholar
  44. Grabowski M, Rewicz T, Bacela-Spychalska K, Konopacka A, Mamos T, Jazdzewski K (2012) Cryptic invasion of Baltic lowlands by freshwater amphipod of Pontic origin. Aquat Invasions 7:337–346Google Scholar
  45. Guerra-García JM (2003) The Caprellidea (Crustacea: Amphipoda) from Mauritius Island, Western Indian Ocean. Zootaxa 232:1–24Google Scholar
  46. Guerra-García JM, Thiel M (2001) La fauna de caprélidos (Crustacea: Amphipoda: Caprellidea) de la costa de Coquimbo, centro-norte de Chile, con una clave taxonómica para la identificación de especies. Rev Chil Hist Nat 74:873–883Google Scholar
  47. Guerra-García JM, Ros M, Dugo-Cota A, Burgos V, Flores-León AM, Baeza-Rojano E, Cabezas MP, Núñez J (2011) Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar Biol 158:2617–2622Google Scholar
  48. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3-0. Syst Biol 59:307–321PubMedGoogle Scholar
  49. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  50. Hampton JO, Spencer PBS, Alpers DL, Twigg LE, Woolnough AP, Doust J (2004) Molecular techniques, wildlife management and the important of genetic population structure and dispersal: a case study with feral pigs. J Appl Ecol 41:735–743Google Scholar
  51. Hänfling B, Carvalho GR, Brandl R (2002) mt-DNA sequences and possible invasion pathways of the Chinese mitten crab. Mar Ecol Prog Ser 238:307–310Google Scholar
  52. Harrison RJ (1940) On the biology of the Caprellidae. Growth and moulting of Pseudoprotella phasma Montagu. J Mar Biol Assoc UK 24:483–493Google Scholar
  53. Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512PubMedCentralPubMedGoogle Scholar
  54. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, SunderlandGoogle Scholar
  55. Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Divers Distrib 18:101–110Google Scholar
  56. Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71Google Scholar
  57. Hou Z, Li S (2010) Intraspecific or interspecific variation: delimitation of species boundaries within the genus Gammarus (Crustacea, Amphipoda, Gammaridae), with description of four new species. Zool J Linn Soc Lon 160:215–253Google Scholar
  58. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedGoogle Scholar
  59. Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecol Appl 11:1789–1799Google Scholar
  60. Kaluza P, Kölzsch A, Gastner MT, Blasius B (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103PubMedCentralPubMedGoogle Scholar
  61. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518PubMedCentralPubMedGoogle Scholar
  62. Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591PubMedGoogle Scholar
  63. Krapp T, Lang C, Libertini A, Melzer RR (2006) Caprella scaura Templeton, 1836 sensu lato (Amphipoda: Caprellidae) in the Mediterranean. 6. Org Divers Evol 6(Electr Suppl 3):1–18Google Scholar
  64. Laubitz DR (1970) Studies on the Caprellidae (Crustacea, Amphipoda) of the American North Pacific. Publ Océanogr Biol Natl Mus Nat Sci (Can) 1:1–89Google Scholar
  65. Laubitz DR (1995) Caprellidea (Crustacea: Amphipoda) from the southern and western Indian Ocean. Mésogée 54:81–100Google Scholar
  66. Lefébure T, Douady CJ, Gouy M, Gibert J (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Mol Ecol 40:435–447Google Scholar
  67. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedGoogle Scholar
  68. Lim STA, Alexander CG (1986) Reproductive behaviour of the caprellid amphipod Caprella scaura typica Mayer, 1890. Mar Behav Physiol 12:217–230Google Scholar
  69. Martínez J, Adarraga I (2008) First record of invasive caprellid Caprella scaura Templeton, 1836 sensu lato (Crustacea: Amphipoda: Caprellidae) from the Iberian Peninsula. Aquat Invasions 3:165–171Google Scholar
  70. Mayer P (1890) Die Caprelliden des Golfes von Neapel und der angrenzenden Meeres Abschnitte. Fauna und Flora des Golfes von Neapel 17:1–55Google Scholar
  71. Mayer P (1903) Die Caprelliden der Siboga-Expedition. Siboga Exped 34:1–160Google Scholar
  72. McCain JC (1968) The Caprellidae (Crustacea: Amphipoda) of the Western North Atlantic. Bull US Natl Mus 278:1–147Google Scholar
  73. McCain JC, Steinberg JE (1970) Amphipoda-I, Caprellidea-I. In: Gruner HE, Holthuis LB (eds) Crustaceorum catalogus 2. Dr. W. Junk Publishers, The Hague, The Netherlands, pp 1–78 Google Scholar
  74. Minchin D, Floerl O, Savini D, Occhipinti-Ambrogi A (2006) Small craft and the spread of exotic species. In: Davenport J, Davenport JD (eds) The ecology of transportation: managing mobility for the environment. Springer, Dortdrecht, NL, pp 99–118Google Scholar
  75. Minchin D, Lodola A, Occhipinti-Ambrogi A (2012) The occurrence of Caprella scaura (Amphipoda: Caprellidae) in marinas in Lanzarote Island (Canary Archipelago, Macaronesia). Mar Biodivers Rec 5:1–5Google Scholar
  76. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492Google Scholar
  77. Montelli L (2010) The recent geographical expansion of Caprella californica (Caprellidea: Caprellidae) around the coastline of Australia. Biol Invasions 12:725–728Google Scholar
  78. Mori A, Yamato S (1993) Caprella simia Mayer, 1903 (Crustacea: Amphipoda: Caprellidae) collected from the body surface of a frogfish Antennarius striatus (Shaw & Nodder, 1794). Nnmki-Seiburu 35:41–46Google Scholar
  79. Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320PubMedGoogle Scholar
  80. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  81. Occhipinti-Ambrogi A (2000) Biotic invasions in a Mediterranean lagoon. Biol Invasions 2:165–176Google Scholar
  82. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedGoogle Scholar
  83. Rambaut A, Drummond AJ (2007) Tracer v1.4.
  84. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedGoogle Scholar
  85. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225Google Scholar
  86. Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828Google Scholar
  87. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedGoogle Scholar
  88. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedGoogle Scholar
  89. Ros M, Guerra-García JM (2012) On the occurrence of the tropical caprellid Paracaprella pusilla Mayer, 1890 (Crustacea: Amphipoda) in Europe. Mediterr Mar Sci 13:134–139Google Scholar
  90. Ros M, Vázquez-Luis M, Guerra-García JM (2013a) The tropical caprellid amphipod Paracaprella pusilla: a new alien crustacean in the Mediterranean Sea. Helgol Mar Res. doi: 10.1007/s10152-013-0353-4 Google Scholar
  91. Ros M, Guerra-García JM, González-Macías M, Saavedra A, López-Fe CM (2013b) Influence of fouling communities on the establishment success of alien caprellids (Crustacea: Amphipoda) in Southern Spain. Mar Biol Res 9:261–273Google Scholar
  92. Ros M, Guerra-García JM, Navarro-Barranco C, Cabezas MP, Vázquez-Luis M (2014) The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomy history. Mediterr Mar Sci 15:145–155Google Scholar
  93. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632Google Scholar
  94. Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332Google Scholar
  95. Schulz MK, Alexander CG (2001) Aggressive behaviour of Caprella scaura typica Mayer, 1890. (Crustacea: Amphipoda). Mar Freshw Behav Physiol 34:181–187Google Scholar
  96. Sconfietti R, Danesi P (1996) Variazioni strutturali in comunità di peracaridi agli estremi opposti del bacino di Malamocco (Laguna di Venezia). Soc Ital Ecol, Atti 17:407–410Google Scholar
  97. Sconfietti R, Mangili F, Savini D, Occhipinti-Ambrogi A (2005) Diffusion of the alien species Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Northern Adriatic Sea. Biol Mar Mediterr 12:335–337Google Scholar
  98. Serejo CS (1998) Gammaridean and caprellidean fauna (Crustacea) associated with the sponge Dysidea fragilis Johnston at Arraial de Cabo, Rio de Janeiro, Brazil. Bull Mar Sci 63:363–385Google Scholar
  99. Simon-Bouhet B, Garcia-Meunier P, Viard F (2006) Multiple introductions promote range expansion of the mollusk Cyclope neritea (Nasariidae) in France: evidence from mitochondrial sequence data. Mol Ecol 15:1699–1711PubMedGoogle Scholar
  100. Souissi JB, Kahri C, Salem MB, Zaouali J (2010) Les espèces non indigènes du macrobenthos des lagunes du sud-est Tunisien: point sur la situation. Rapports de la Commission Intérnationale pour l’Exploration Scientifique de la Mer Méditerranée 39:449Google Scholar
  101. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lomaba AL, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57(7):573–583Google Scholar
  102. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedGoogle Scholar
  103. Stimpson W (1857) The Crustacea and Echinodermata of the Pacific shores of North America. Boston J Nat Hist 6:503–513Google Scholar
  104. Takeuchi I, Hirano R (1995) Clinging behavior of the epifaunal caprellids (Amphipoda) inhabiting the Sargassum zone on the Pacific coast of Japan, with its evolutionary implications. J Crustacean Biol 15:481–492Google Scholar
  105. Takeuchi I, Oyamada A (2013) Description of two species of Caprella (Crustacea: Amphipoda: Caprellidae) from the North Pacific; C. californica Stimpson, 1857 and C. scauroides Mayer, 1903, with a new appraisal of species ranking for C. scauroides. Helgol Mar Res 67:371–381Google Scholar
  106. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumer S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedGoogle Scholar
  107. Templeton R (1836) Descriptions of some undescribed exotic Crustacea. Trans Entomol Soc Lond 1:185–198Google Scholar
  108. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensivity of progressive multiple sequence alignment through sequence weighting, position-specific gal penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralPubMedGoogle Scholar
  109. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953PubMedCentralPubMedGoogle Scholar
  110. Utinomi H (1947) Caprellidea of Japan and adjacent waters. Seibutu Suppl 1:68–82Google Scholar
  111. Whiting MF (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool Scr 1:93–104Google Scholar
  112. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359Google Scholar
  113. Witt JDS, Threloff DL, Hebert PDN (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Mol Ecol 15:3073–3082PubMedGoogle Scholar
  114. Xavier R, Santos AM, Lima FP, Branco M (2009) Invasion or invisibility: using genetic and distributional data to investigate the alien or indigenous status of the Atlantic populations of the peracarid isopod, Stenosoma nadejda (Rezig 1989). Mol Ecol 18:3283–3290PubMedGoogle Scholar
  115. Xavier R, Zenboudji S, Lima FP, Harris DJ, Santos AM, Branco M (2011) Phylogeography of the marine isopod Stenosoma nadejda (Rezig, 1989) in North African Atlantic and western Mediterranean coasts reveals complex differentiation patterns and a new species. Biol J Linn Soc 104:419–431Google Scholar
  116. Zardus JD, Hadfield MG (2005) Multiple origins and incursions of the Atlantic barnacle Chthamalus proteus in the Pacific. Mol Ecol 14:3719–3733PubMedGoogle Scholar
  117. Zenetos A, Vassilopoulou V, Salomidi M, Poursanidis D (2008) Additions to the marine alien fauna of Greek waters (2007 update). Mar Biodivers Rec 1:1–8Google Scholar
  118. Zenetos A, Gofas S, Verlaque M, Cinar ME, García-Raso JE, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Sioku I, Violanti D, Sfriso A, San-Martin G, Giangrande A, Katagan T, Ballesteros E, Ramos-Espla A, Mastrototaro F, Ocaña O, Zingone A, Gambi MC, Streftaris N (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
  119. Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • M. Pilar Cabezas
    • 1
    • 2
  • Raquel Xavier
    • 2
    • 3
  • Madalena Branco
    • 2
  • António M. Santos
    • 2
    • 4
  • José Manuel Guerra-García
    • 1
  1. 1.Laboratorio de Biología Marina, Departamento de Zoología, Facultad de BiologíaUniversidad de SevillaSevilleSpain
  2. 2.CIBIO, Centro de Investigaçaõ em Biodiversidade e Recursos GenéticosVairãoPortugal
  3. 3.School of Biological SciencesCardiff UniversityCardiffUK
  4. 4.Departamento de BiologiaFaculdade de Ciências da Universidade do PortoPortoPortugal

Personalised recommendations