Ascidian introductions through the Suez Canal: The case study of an Indo-Pacific species

Marine Pollution Bulletin

Volumn 64, Issue 10, 2012, Pages 2060-2068

  Rius, Marc ^a,b   Shenkar, Noa ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Erythrean invasion; Genetic diversity; Lessepsian migration; Population connectivity; Species range; Tunicates

Indexed keywords

ERYTHREAN INVASION; GENETIC DIVERSITY; LESSEPSIAN MIGRATION; POPULATION CONNECTIVITY; SPECIES RANGES; TUNICATES;

GENES; TAXONOMIES;

HYDRAULIC STRUCTURES;

COLONIZATION; FILTER FEEDER; GENETIC VARIATION; GEOGRAPHICAL DISTRIBUTION; INVASIVE SPECIES; TAXONOMY;

AMINO ACID SEQUENCE; ARTICLE; ASCIDIACEA; BIOGEOGRAPHY; GENETIC DISTANCE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; GEOGRAPHICAL VARIATION (SPECIES); HAPLOTYPE; HERDMANIA MOMUS; HERDMANIA PALLIDA; MEDITERRANEAN SEA; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; SPECIES DIFFERENCE; SPECIES DISTRIBUTION;

ANIMALS; BIODIVERSITY; CONSERVATION OF NATURAL RESOURCES; GENETIC VARIATION; INDIAN OCEAN; INTRODUCED SPECIES; MEDITERRANEAN SEA; PHYLOGENY; UROCHORDATA;

EGYPT; SUEZ CANAL;

ASCIDIA; ASCIDIACEA; CHORDATA; HERDMANIA MOMUS; UROCHORDATA;

EID: 84866771137     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2012.06.029     Document Type: Article

References (111)

1. Abbott D.P., Newberry A.T., Morris K.M. Section 6B: ascidians (Urochordata). Reef and Shore Fauna of Hawaii 1997, Bishop Museum Press, Honolulu. G. Lambert (Ed.).
2. Becerro M.A., Turon X. Reproductive cycles of the ascidians Microcosmus sabatieri and Halocynthia papillosa in the northwestern Mediterranean. Marine Ecology 1992, 13:363-373.
3. Benjamini Y., Yekutieli D. The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics 2001, 29:1165-1188.
4. Berrill N.J. The Tunicata with an Account of the British Species 1950, Ray Society, London.
5. Bitar G., Ocaña O., Ramos-Esplá A.A. Contribution of the Red Sea alien species to structuring some benthic biocenosis in the Lebanon Coast (Eastern Mediterranean). Rapports de la Commission Internationale Exploration de la Mer Méditerranée 2007, 38:437-438.
6. Bonhomme F., Baranes A., Golani D., Harmelin-Vivien M. Lack of mitochondrial differentiation between Red Sea and Mediterranean populations of the Lessepsian rabbitfish, Siganus rivulatus (Perciformes: Siganidae). Scientia Marina 2003, 67:215-217.
7. Bucciarelli G., Golani D., Bernardi G. Genetic cryptic species as biological invaders: the case of a Lessepsian fish migrant, the hardyhead silverside Atherinomorus lacunosus. Journal of Experimental Marine Biology and Ecology 2002, 273:143-149.
8. Bullard S.G., Carman M.R. Current trends in invasive ascidian research. Invasive Species: Detection, Impact and Control 2009, 57-79. Nova Science Pub Inc. C.P. Wilcox, R.B. Turpin (Eds.).
9. Bullard S.G., Lambert G., Carman M.R., Byrnes J., Whitlatch R.B., Ruiz G., Miller R.J., Harris L., Valentine P.C., Collie J.S., Pederson J., McNaught D.C., Cohen A.N., Asch R.G., Dijkstra J., Heinonen K. The colonial ascidian Didemnum sp. A: Current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. Journal of Experimental Marine Biology and Ecology 2007, 342:99-108.
10. Carlton J.T., Geller J.B. Ecological roulette: the global transport of nonindigenous marine organisms. Science 1993, 261:78-82.
11. Castilla J.C., Guiñez R., Caro A.U., Ortiz V. Invasion of a rocky intertidal shore by the tunicate Pyura praeputialis in the Bay of Antofagasta, Chile. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:8517-8524.
12. Çinar M.E., Bilecenoglu M., öztürk B., Can A. New records of alien species on the Levantine coast of Turkey. Aquatic Invasions 2006, 1:84-90.
13. Clarke, K.R., Gorley, R.N., 2006. PRIMER v.6: User Manual/Tutorial. PRIMER-E, Plymouth.
14. Clement M., Posada D., Crandall K.A. TCS: a computer program to estimate gene genealogies. Molecular Ecology 2000, 9:1657-1659.
15. Cohen A.N., Harris L.H., Bingham B.L., Carlton J.T., Chapman J.W., Lambert C.C., Lambert G., Ljubenkov J.C., Murray S.N., Rao L.C., Reardon K., Schwindt E. Rapid assessment survey for exotic organisms in southern California bays and harbors, and abundance in port and non-port areas. Biological Invasions 2005, 7:995-1002.
16. Coll M., Piroddi C., Steenbeck J., Kaschner K., Ben Rais Lasram F., Aguzzi J., Ballesteros E., Niké Bianchi C., Corbera J., Dailianis T., Danovaro R., Estrada M., Froglia C., Galil B.S., Gasol J.M., Gertwagen R., Gil J., Guilhaumon F., Kesner-Reyes K., Kitsos M.S., Koukouras A., Lampadariou N., Laxamana E., López-Fé de la Cuadra C.M., Lotze H.K., Martin D., Mouillot D., Oro D., Raicevich S., Rius-Barile J., Saiz-Salinas J.I., San Vicente C., Somos S., Templado J., Turon X., Vafidis D., Villanueva R., Voultsiadou E. The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS One 2010, 5:e11842.
17. Coutts A.D.M., Dodgshun T.J. The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Marine Pollution Bulletin 2007, 54:875-886.
18. Chao, A., Shen, T.-J., 2009. SPADE (Species Prediction and Diversity Estimation). http://www.chao.stat.nthu.edu.tw/softwareCE.html.
19. de Rivera C.E., Steves B.P., Fofonoff P.W., Hines A.H., Ruiz G.M. Potential for high-latitude marine invasions along western North America. Diversity and Distributions 2011, 17:1198-1209.
20. Epelbaum A., Pearce C.M., Barker D.J., Paulson A., Therriault T.W. Susceptibility of non-indigenous ascidian species in British Columbia (Canada) to invertebrate predation. Marine Biology 2009, 156:1311-1320.
21. Estoup A., Baird S.J.E., Ray N., Currat M., Cornuet J.M., Santos F., Beaumont M.A., Excoffier L. Combining genetic, historical and geographical data to reconstruct the dynamics of bioinvasions: application to the cane toad Bufo marinus. Molecular Ecology Resources 2010, 10:886-901.
22. Estoup A., Guillemaud T. Reconstructing routes of invasion using genetic data: why, how and so what?. Molecular Ecology 2010, 19:4113-4130.
23. Excoffier L., Lischer H.E.L. Arlequin suite v.3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 2010, 10:564-567.
24. Fitzpatrick B.M., Fordyce J.A., Niemiller M.L., Reynolds R.G. What can DNA tell us about biological invasions?. Biological Invasions 2012, 14:245-253.
25. Frankham R. Resolving the genetic paradox in invasive species. Heredity 2005, 94:385.
26. Frydenberg J., Pertoldi C., Dahlgaard J., Loeschcke V. Genetic variation in original and colonizing Drosophila buzzatii populations analysed by microsatellite loci isolated with a new PCR screening method. Molecular Ecology 2002, 11:181-190.
27. Galil B.S. A sea under siege - alien species in the Mediterranean. Biological Invasions 2000, 2:177-186.
28. Galil B.S. Taking stock: inventory of alien species in the Mediterranean Sea. Biological Invasions 2009, 11:359-372.
29. Geller J.B., Darling J.A., Carlton J.T. Genetic perspectives on marine biological invasions. Annual Review of Marine Science 2010, 2:367-393.
30. Golani D. Environmentally-induced meristic changes in Lessepsian fish migrants, a comparison of source and colonizing populations. Bulletin de l'Institut Oceanographique, Monaco 1990, 7:143-152.
31. Golani D., Azzuro E., Corsini-Foka M., Falautano M., Andaloro F., Bernardi G. Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biology Letters 2007, 3:541-545.
32. Goodbody I. Continuous breeding in three species of tropical ascidian. Proceedings of the Zoological Society, London 1961, 136:403-409.
33. Goodbody I. The ascidian fauna of a Jamaican lagoon: 30years of change. Revista de Biología Tropical Suplemento 1993, 41:35-38.
34. Goren M., Galil B.S. A review of changes in the fish assemblages of Levantine inland and marine ecosystems following the introduction of non-native fishes. Journal of Applied Ichtyology 2005, 21:364-370.
35. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41:95-98.
36. Harant H. Rapport sur les Tuniciers. Transactions of the Zoological Society of London 1927, 22:365-373.
37. Hartmeyer R. über einige Ascidien aus dem Golf von Suez 1915, Sitzber Ges.
38. Hassan M., Bonhomme F. No reduction in neutral variability of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. Journal of Fish Biology 2005, 66:865-870.
39. Hassan M., Harmelin-Vivien M., Bonhomme F. Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus). Journal of Experimental Marine Biology and Ecology 2003, 291:219-232.
40. Herdman W.A. Report on the Tunicata collected during the voyage of HMS Challenger during the years 1873-1876. Part I, Ascidiae simplices. Report on the scientific results of the exploring voyage of HMS 'Challenger' during the years 1875-1876. Zoology 1882, 6:1-296.
41. Herdman W.A. Report on the Tunicata collected during the voyage of HMS Challenger during the years 1873-1876. Part II, Ascidiae compositae. Report on the scientific results of the exploring voyage of HMS 'Challenger' during the years 1875-1876. Zoology 1886, 14:1-425.
42. Holland B.S. Genetics of marine bioinvasions. Hydrobiologia 2000, 420:63-71.
43. Izquierdo-Muñoz A., Díaz-Valdés M., Ramos-Esplá A.A. Recent non-indigenous ascidians in the Mediterranean Sea. Aquatic Invasions 2009, 4:59-64.
44. ST and its relatives do not measure differentiation. Molecular Ecology 2008, 17:4015-4026.
45. ST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Molecular Ecology 2009, 18:2088-2091.
46. Kott P. The ascidians of Australia I. Stolidobranchiata Lahille and Phlebobranchiata Lahille. Australian Journal of Marine and Freshwater Research 1952, 3:205-334.
47. Kott P. The ascidians of the reef flats of Fiji. Proceedings of the Linnean Society of New South Wales 1982, 105:147-212.
48. Kott P. The Australian Ascidiacea, Part 1. Phlebobranchia and Stolidobranchia. Memoirs of the Queensland Museum 1985, 23:1-438.
49. Kott P. The genus Herdmania Lahille, 1888 (Tunicata, Ascidiacea) in Australian waters. Zoological Journal of the Linnean Society 2002, 134:359-374.
50. Kott P., Goodbody I. The ascidians of Hong Kong. Proceedings of the First International Marine Biological Workshop: The Flora and Fauna of Hong Kong and Southern China 1982, 503-554. University Press, Hong Kong. B.S. Morton, C.K. Tseng (Eds.).
51. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 2008, 9:299-306.
52. Lambert C.C., Lambert G. Non-indigenous ascidians in southern California harbors and marinas. Marine Biology 1998, 130:675-688.
53. Lambert G. A global overview of ascidian introductions and their possible impact on the endemic fauna. The Biology of Ascidians 2001, 249-257. Springer-Verlag, Tokyo. H. Sawada, H. Yokosawa, C.C. Lambert (Eds.).
54. Lambert G. Nonindigenous ascidians in tropical waters. Pacific Science 2002, 56:291-298.
55. Lambert G. Ecology and natural history of the protochordates. Canadian Journal of Zoology 2005, 83:34-50.
56. Lambert G. Invasive sea squirts: a growing global problem. Journal of Experimental Marine Biology and Ecology 2007, 342:3-4.
57. Lejeusne C., Chevaldoné P., Pergent-Martini C., Boudouresque C.F., Pérez T. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in Ecology and Evolution 2010, 25:250-260.
58. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
59. Locke A. A screening procedure for potential tunicate invaders of Atlantic Canada. Aquatic Invasions 2009, 4:71-79.
60. Locke A., Carman M. An overview of the 2nd International Invasive Sea Squirt Conference. What we learned. Aquatic Invasions 2009, 4:1-4.
61. López-Legentil S., Turon X., Planes S. Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Molecular Ecology 2006, 15:3957-3967.
62. Lotan A., Fine M., Ben-Hillel R. Synchronization of the life cycle and dispersal pattern of the tropical invader scyphomedusan Rhopilema nomadica is temperature dependent. Marine Ecology Progress Series 1994, 109:59-65.
63. Loya Y. The coral reefs of Eilat - past, present and future: three decades of coral community structure studies. Coral Health and Disease 2004, 1-34. Springer-Verlag, Heidelberg. E. Rosenberg, Y. Loya (Eds.).
64. Loya Y. How to influence environmental decision makers? The case of Eilat (Red Sea) coral reefs. Journal of Experimental Marine Biology and Ecology 2007, 344:35-53.
65. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Research 1967, 27:209-220.
66. Mayr E. Systematics and the Origin of Species: from a Viewpoint of a Zoologist 1942, Columbia University Press, New York.
67. Meyer C.P. Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society 2003, 79:401-459.
68. Michaelsen W. Expedition S. M. Schiff Pola in das Roten Meer nördliche und südliche halfte 1895/96-1897/98 zoologische Ergebnisse. XXXII Ascidia Ptychobranchia und Dictyobranchia des Roten Meeres. Denkschriften der Akademie der wissenschaften Wien 1919, 95:1-120.
69. Millar R.H. Ascidians from Mozambique, East Africa. Journal of Natural History 1956, 9:913-932.
70. Millar R.H. The biology of ascidians. Advances in Marine Biology 1971, 9:1-100.
71. Millar R.H. Ascidians from the Indo-West Pacific region in the Zoological Museum, Copenhagen (Tunicata, Ascidiacea). Steenstrupia 1975, 3:205-336.
72. Millar R.H. Ascidians collected during the International Indian Ocean Expedition. Journal of Natural History 1988, 22:823-848.
73. Monniot C. Ascidies de Nouvelle-Calédonia XI. Phlébobranches et Stolidobranches Du Plateau Chesterfield. Bulletin du Muséum National d'Histoire Naturelle. Paris Série 1992, 4(14a):1-22.
74. Monniot C. Stolidobranch ascidians from the tropical western Indian Ocean. Zoological Journal of the Linnean Society 2002, 135:65-120.
75. Monniot C., Monniot F. Records of ascidians from Bahrain, Arabian Gulf with three new species. Journal of Natural History 1997, 31:1623-1643.
76. Monniot F., Monniot C. Ascidians from the tropical western Pacific. Zoosystema 2001, 23:201-383.
77. Mooney E.H., McGraw J.B. Alteration of selection regime resulting from harvest of American ginseng, Panax quinquefolius. Conservation Genetics 2007, 8:57-67.
78. Moum T., árnason E. Genetic diversity and population history of two related seabird species based on mitochondrial DNA control region sequences. Molecular Ecology 2001, 10:2463-2478.
79. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
80. Nishikawa T. Revision of the ascidian genus Herdmania (Urochordata: Ascidiacea) inhabiting Japanese waters. Species Diversity 2002, 7:217-250.
81. Pérès J.M. Ascidies recoltees sur les cotes mediterraneannes d'Israel. Bulletin of the Research Council of Israel 1958, 7B:143-150.
82. Pérez-Portela R., Turon X., Bishop J.D.D. Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Marine Ecology Progress Series 2012, 451:93-105.
83. Pineda M.C., López-Legentil S., Turon X. The whereabouts of an ancient wanderer: global phylogeography of the solitary ascidian Styela plicata. PLoS ONE 2011, 6:e25495.
84. Por F.D. Lessepsian Migration. The Influx of Red Sea Biota into the Mediterranean by Way of the Suez Canal 1978, Springer-Verlag, Berlin.
85. Primo C., Vázquez E. Zoogeography of the southern African ascidian fauna. Journal of Biogeography 2004, 31:1987-2009.
86. Primo C., Vázquez E. Zoogeography of the southern New Zealand, Tasmanian and southern African ascidian fauna. New Zealand Journal of Marine and Freshwater Research 2008, 42:233-256.
87. Ramsay A., Davidson J., Landry T., Arsenault G. Process of invasiveness among exotic tunicates in Prince Edward Island, Canada. Biological Invasions 2008, 10:1311-1316.
88. Rho B.J. A study on the classification and the distribution of the Korean ascidians. Journal of the Korean Research Institute for Better Living 1971, 6:103-160.
89. Richardson D.M., PyŠek P. Fifty years of invasion ecology - the legacy of Charles Elton. Diversity and Distributions 2008, 14:161-168.
90. Richardson D.M., PyŠek P., Rejmánek M., Barbour M.G., Panetta F.D., West C.J. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 2000, 6:93-107.
91. Rius M., Heasman K.G., McQuaid C.D. Long-term coexistence of non-indigenous species in aquaculture facilities. Marine Pollution Bulletin 2011, 62:2395-2403.
92. Rius M., Pineda M.C., Turon X. Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biological Invasions 2009, 11:2181-2194.
93. Rius M., Turon X., Marshall D.J. Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages. Oecologia 2009, 159:873-882.
94. Rius M., Turon X., Ordóñez V., Pascual M. Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS ONE 2012, 7:e35815.
95. Rocha R.M., Bonnet N.Y.K., Baptista M.S., Beltramin F.S. Introduced and native Phlebobranch and Stolidobranch solitary ascidians (Tunicata: Ascidiacea) around Salvador, Bahia, Brazil. Zoologia 2012, 29:39-53.
96. Roman J., Darling J.A. Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution 2007, 22:454-464.
97. Savigny, J.C., 1816. Memoires sur les animaux sans vertebres, In: Dufour, G. (Ed.), Paris.
98. Shefer S., Abelson A., Mokady O., Geffen E. Red to Mediterranean Sea bioinvasion: natural drift through the Suez Canal, or anthropogenic transport?. Molecular Ecology 2004, 13:2333-2343.
99. Shenkar N., Bronstein O., Loya Y. Population dynamics of a coral reef ascidian in a deteriorating environment. Marine Ecology Progress Series 2008, 367:163-171.
100. Shenkar N., Loya Y. The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biological Invasions 2008, 10:1431-1439.
101. Shenkar N., Loya Y. Non-indigenous ascidians along the Mediterranean coast of Israel. Marine Biodiversity Records 2009, 2:e166.
102. Shenkar N., Swalla B.J. Global diversity of Ascidiacea. PLoS ONE 2011, 6:e20657.
103. Shenkar N., Zeldman Y., Loya Y. Ascidian recruitment patterns on an artificial reef in Eilat (Red Sea). Biofouling 2008, 24:119-128.
104. Spanier E., Galil B.S. Lessepsian migration - a continuous biogeographical process. Endeavour 1991, 15:102-106.
105. Spencer C.C., Neigel J.E., Leberg P.L. Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Molecular Ecology 2000, 9:1517-1528.
106. Templeton A.R., Crandall K.A., Sing C.F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data III. Cladogram estimation. Genetics 1992, 132:619-633.
107. Teske P.R., Rius M., McQuaid C.D., Styan C.A., Piggott M.P., Benhissoune S., Fuentes-Grünewald C., Walls K., Page M., Attard C.R.M., Cooke G.M., McClusky C.F., Banks S.C., Barker N.P., Beheregaray L.B. " Nested" cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions. BMC Evolutionary Biology 2011, 11:176.
108. Tsutsui N.D., Suarez A.V., Holway D.A., Case T.J. Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:5948-5953.
109. Turon X., López-Legentil S. Ascidian molecular phylogeny inferred from mtDNA data with emphasis on the Aplousobranchiata. Molecular Phylogenetics and Evolution 2004, 33:309-320.
110. Van Duyl F.C., Bak R.P.M., Sybesma J. The ecology of the tropical ascidian Trididemnum solidum I. Reproductive strategy and larval behavior. Marine Ecology Progress Series 1981, 6:35-42.
111. Van Name W.G. The North and South American ascidians. Bulletin of the American Museum of Natural History 1945, 84:1-476.