Low genetic variability of sargassum muticum (phaeophyceae) revealed by a global analysis of native and introduced populations

Journal of Phycology

Volumn 46, Issue 6, 2010, Pages 1063-1074

  Cheang, Chi Chiu ^a   Chu, Ka Hou ^a   Fujita, Daisuke ^b   Yoshida, Goro ^c   Hiraoka, Masanori ^d   Critchley, Alan ^e   Choi, Han Gil ^f   Duan, Delin ^g   Serisawa, Yukihiko ^h   Ang, Put O ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^c FISHERIES RESEARCH AGENCY   (Japan)

^d KOCHI UNIVERSITY   (Japan)

^e Acadian Seaplants Limited   (Canada)

^f Wonkwang University   (South Korea)

^g INSTITUTE OF OCEANOLOGY   (China)

^h UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Genetic diversity; Internal transcribed spacer 2 (ITS2); Invasion; Pacific oyster; RUBISCO spacer; Sargassum muticum; TrnW_TrnI spacer

Indexed keywords

CRASSOSTREA GIGAS; OSTREIDAE; PHAEOPHYCEAE; SARGASSUM; SARGASSUM MUTICUM;

EID: 78649836202     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2010.00901.x     Document Type: Article

References (97)

1. Andreakis, N., Procaccini, G., Maggs, C. & Kooistra, W. H. C. F. 2007. Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol. Ecol. 16:2285-99.
2. Andrew, N. L. & Viejo, R. M. 1998. Ecological limits to the invasion of Sargassum muticum in northern Spain. Aquat. Bot. 60:251-63.
3. Banks, M. A., McGoldrick, D. J., Borgeson, W. & Hedgecock, D. 1994. Gametic incompatibility and genetic divergence of Pacific and Kumamoto oysters, Crassostrea gigas and C. sikamea. Mar. Biol. 121:127-35.
4. Barrett, E. M. 1963. The California oyster industry. Res. Agency Calif. Department Fish Game Fish Bull. 123:1-103.
5. Boudouresque, C. F. & Verlaque, M. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 44:32-8.
6. Britton-Simmons, K. H. 2004. Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar. Ecol. Prog. Ser. 277:61-78.
7. Cheang, C. C. 2003. Genetic and morphological variation among populations of Sargassum hemiphyllum (Phaeophyta). M. phil. thesis, the Chinese University of Hong Kong, Hong Kong, 136 pp.
8. Cheang, C. C., Chu, K. H. & Ang, P. O. 2008. Morphological and genetic variation in the populations of Sargassum hemiphyllum (Phaeophyceae) in northwestern Pacific. J. Phycol. 44:855-65.
9. Cheang, C. C., Chu, K. H. & Ang, P. O. 2010. Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae, Heterokontophyta) in northwestern Pacific. Mol. Ecol. 19:2933-48.
10. Cho, G. Y., Boo, S. M., Nelson, W. & Clayton, M. N. 2005. Genealogical partitioning and phylogeography of Colpomenia peregrine (Scytosiphonaceae, Phaeophyceae), based on plastid rbcL and nuclear ribosomal DNA internal transcribed spacer sequences. Phycologia 44:103-11.
11. Cho, G. Y., Kogame, K., Kawai, H. & Boo, S. M. 2007. Genetic diversity of Scytosiphon lomentaria (Scytosiphonaceae, Phaeophyceae) from the Pacific and Europe based on RUBISCO large subunit and spacer, and ITS nrDNA sequences. Phycologia 46:657-65.
12. Clement, M., Posada, D. & Crandall, K. A. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-9.
13. Coyer, J. A., Hoarau, G., Stam, W. T. & Olsen, J. L. 2004. Geographically specific heteroplasmy of mitochondrial DNA in the seaweed, Fucus serratus (Heterokontophyta: Phaeophyceae, Fucales). Mol. Ecol. 13:1323-6.
14. Critchley, A. T. 1983a. Sargassum muticum: a taxonomic history including world-wide and western Pacific distributions. J. Mar. Biol. Assoc. U. K. 63:617-25.
15. Critchley, A. T. & Dijkema, R. 1984. On the presence of the introduced brown alga Sargassum muticum, attached to commercially imported Ostrea edulis in the S.W. Netherlands. Bot. Mar. 27:211-6.
16. Critchley, A. T., Farnham, W. F. & Morrell, S. L. 1983. A chronology of the new European sites of attachment for the invasive brown alga, Sargassum muticum, 1973-1981. J. Mar. Biol. Assoc. U. K. 63:799-811.
17. Critchley, A. T., Farnham, W. F., Yoshida, T. & Norton, T. A. 1990. A bibliography of the invasive alga Sargassum muticum (Yendo) Fensholt (Fucales; Sargassaceae). Bot. Mar. 33:551-62.
18. Curiel, D., Bellemo, G., Marzocchi, M., Scattolin, M. & Parisi, G. 1998. Distribution of introduced Japanese macroalgae Undaria pinnatifida, Sargassum muticum (Phaeophyta) and Antithamnion pectinatum (Rhodophyta) in the Lagoon of Venice. Hydrobiologia 385:17-22.
19. Deysher, L. & Norton, T. A. 1982. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J. Exp. Mar. Biol. Ecol. 56:179-95.
20. Durand, C., Manuel, M., Boudouresque, C. F., Meinesz, A., Verlaque, M. & Le Parco, Y. 2002. Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea. J. Evol. Biol. 15:122-33.
21. Engel, C. R., Billard, E., Voisin, M. & Viard, F. 2008. Conservation and polymorphism of mitochondrial intergenic sequences in brown algae (Phaeophyceae). Eur. J. Phycol. 43:195-205.
22. Engelen, A. & Santos, R. 2009. Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? J. Ecol. 97:675-84.
23. Espinoza, J. 1990. The southern limit of Sargassum muticum (Yendo) Fensholt (Phaeophyta, Fucales) in the Mexican Pacific. Bot. Mar. 33:193-6.
24. Farnham, W. F., Fletcher, R. L. & Irvine, L. M. 1973. Attached Sargassum found in Britain. Nature 243:231-2.
25. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-91.
26. Fensholt, D. E. 1955. An emendation of the genus Cystophyllum (Fucales). Am. J. Bot. 42:305-22.
27. Fernández, C. 1999. Ecology of Sargassum muticum (Phaeophyta) on the north coast of Spain: IV. Sequence of colonization on a shore. Bot. Mar. 42:553-62.
28. Fraser, C. I., Spencer, H. G. & Waters, J. M. 2009. Glacial oceanographic contrasts explain phylogeography of Australian bull kelp. Mol. Ecol. 18:2287-96.
29. Geller, J. B. 1996. Molecular approaches to the study of marine biological invasions. In Ferraris, J. D. & Palumbi, S. R. [Eds.] Molecular Zoology. Wiley, New York, pp. 119-32.
30. Geller, J. B., Darling, J. A. & Carlton, J. T. 2010. Genetic perspectives on marine biological invasions. Annu. Rev. Mar. Sci. 2:367-93.
31. Geller, J. B., Walton, E. D., Grosholz, E. D. & Ruiz, G. M. 1997. Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Mol. Ecol. 6:901-6.
32. Goulletquer, P., Bachelet, G., Sauriau, P. G. & Noel, P. 2002. Open Atlantic coast of Europe - a century of introduced species into French waters. In Leppäkoski, E., Gollasch, S. & Olenin, S. [Eds.] Invasive Aquatic Species of Europe Distribution, Impacts and Management. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp. 276-90.
33. Grizel, H. & Héral, M. 1991. Introduction into France of the Japanese oyster (Crassostrea gigas). ICES J. Mar. Sci. 47:399-403.
34. Gurgel, C. F. D., Fredericq, S. & Norris, J. N. 2004. Phylogeography of Gracilaria tikvahiae (Gracilariaceae, Rhodophyta): a study of genetic discontinuity in a continuously distributed species based on molecular evidence. J. Phycol. 40:748-58.
35. Hales, J. M. & Fletcher, R. L. 1989. Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt. IV. The effect of temperature, irradiance and salinity on germling growth. Bot. Mar. 32:167-76.
36. Harries, D. B., Cook, E., Donnan, D. W., Mair, J. M., Harrow, S. & Wilson, J. R. 2007a. The establishment of the invasive alga Sargassum muticum on the west coast of Scotland: rapid northwards spread and identification of potential new areas for colonization. Aquat. Invasions 2:367-77.
37. Harries, D. B., Harrow, S., Wilson, J. R., Mair, J. M. & Donnan, D. W. 2007b. The establishment of the invasive alga Sargassum muticum on the west coast of Scotland: a preliminary assessment of community effects. J. Mar. Biol. Assoc. U. K. 87:1057-67.
38. Hoarau, G., Coyer, J. A., Veldsink, J. H., Stam, W. T. & Olsen, J. L. 2007. Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol. Ecol. 16:3606-16.
39. Hwang, E. K. & Dring, M. J. 2002. Quantitative photoperiodic control of erect thallus production in Sargassum muticum. Bot. Mar. 45:471-5.
40. International Union for the Conservation of Nature. 2000. IUCN guidelines for the prevention of biodiversity loss caused by alien invasive species. Available at: (last accessed 20 August 2010).
41. Kang, J. W. 1966. On the geographical distribution of marine algae in Korea. Bull. Pusan Fish. Coll. 7:1-125.
42. Karlsson, J. & Loo, L. O. 1999. On the distribution and the continuous expansion of the Japanese seaweed -Sargassum muticum- in Sweden. Bot. Mar. 42:285-94.
43. Kashenko, N. V. 1999. Benthic communities of macrophytic algae in Vostok Bay, the Sea of Japan. Russ. J. Mar. Biol. 25:360-4.
44. Kendrick, G. A. & Walker, D. I. 1995. Dispersal of propagules of Sargassum spp. (Sargassaceae: Phaeophyta): observations of local patterns of dispersal and consequences for recruitment and population structure. J. Exp. Mar. Biol. Ecol. 192:273-88.
45. Kojima, S., Segawa, R. & Hayashi, I. 1997. Genetic differentiation among populations of the Japanese turban shell Turbo (Batillus) cornutus corresponding to warm currents. Mar. Ecol. Prog. Ser. 150:149-55.
46. Kraan, S. 2008. Sargassum muticum (Yendo) Fensholt in Ireland: an invasive species on the move. J. Appl. Phycol. 20:825-32.
47. Lindstrom, S. C. 1977. An Annotated Bibliography of the Benthic Marine Algae of Alaska. Alaska Department of Fish & Game, Juneau, Alaska, 172 pp.
48. Loughnane, C. & Stengel, D. B. 2002. Attached Sargassum muticum (Yendo) Fensholt found on the west coast of Ireland. Ir. Nat. J. 27:70-2.
49. McIvor, L., Maggs, C. A., Provan, J. & Stanhope, M. J. 2001. rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol. Ecol. 10:911-9.
50. Meusnier, I., Valero, M., Olsen, J. & Stam, W. 2004. Analysis of rDNA ITS1 indels in Caulerpa taxifolia (Chlorophyta) supports a derived, incipient species status for the invasive strain. Eur. J. Phycol. 39:83-92.
51. Mineur, F., Belsher, T., Johnson, M. P., Maggs, C. A. & Verlaque, M. 2007b. Experimental assessment of oyster transfers as a vector for macroalgal introductions. Biol. Conserv. 137:237-47.
52. Mineur, F., Johnson, M., Maggs, C. & Stegenga, H. 2007a. Hull fouling on commercial ships as a vector of macroalgal introduction. Mar. Biol. 151:1299-307.
53. Miura, O., Torchin, M. E., Kuris, A. M., Hechinger, R. F. & Chiba, S. 2006. Introduced cryptic species of parasites exhibit different invasion pathways. Proc. Natl. Acad. Sci. U. S. A. 103:19818-23.
54. Moore, C. G. & Harries, D. B. 2009. Appearance of Heterosiphonia japonica (Ceramiales: Rhodophyceae) on the west coast of Scotland, with notes on Sargassum muticum (Fucales: Heterokontophyta). Mar. Biodivers. Rec. 2:e131. DOI:
55. Muirhead, J. R., Gray, D. K., Kelly, D. W., Ellis, S. M., Heath, D. D. & Macisaac, H. J. 2008. Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol. Ecol. 17:1020-35.
56. Norton, T. A. 1976. Why is Sargassum muticum so invasive? Br. Phycol. J. 11:197-8.
57. Norton, T. A. 1977. Ecological experiments with Sargassum muticum. J. Mar. Biol. Assoc. U. K. 57:33-43.
58. Oak, J. H., Suh, Y. & Lee, I. K. 2002. Phylogenetic relationships of Sargassum subgenus Bactrophycus (Sargassaceae, Phaeophyceae) inferred from rDNA ITS Sequences. Algae 17:235-48.
59. Okamura, K. 1924. Icones of Japanese Algae. Kazamashobo, Tokyo, Japan, 258 pp.
60. Oudot-Le Secq, M. P., Loiseaux-de Goër, S., Stam, W.T. and Olsen, J. L. 2006. Complete mitochondrial genomes of the three brown algae (Heterokonta: Phaeophyceae) Dictyota dichotoma, Fucus vesiculosus and Desmarestia viridis. Curr. Genet. 49:47-58.
61. Phillips, N. 1995. Biogeography of Sargassum (Phaeophyta) in the Pacific basin. In Abbott, I. A. [Ed.] Taxonomy of Economic Seaweeds Volume 5. California Sea Grant College System, La Jolla, California, pp. 107-45.
62. Phillips, N. E., Smith, C. M. & Morden, C. W. 2005. Testing systematic concepts of Sargassum (Fucales, Phaeophyceae) using portions of the rbcLS operon. Phycol. Res. 53:1-10.
63. Pijanka, R. 2006. History on the half-shell: the Kumamoto oyster flourishes on North American menus. Pac. Rim Mag. Available at: (last accessed 20 August 2010).
64. Posada, D. & Crandall, K. A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-8.
65. Provan, J., Booth, D., Todd, N. P., Beatty, G. E. & Maggs, C. A. 2008. Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Divers. Distrib. 14:343-54.
66. Provan, J. I. M., Murphy, S. & Maggs, C. A. 2005. Tracking the invasive history of the green alga Codium fragile ssp. tomentosoides. Mol. Ecol. 14:189-94.
67. Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-4.
68. Rueness, J. 1989. Sargassum muticum and other introduced Japanese macroalgae: biological pollution of European coasts. Mar. Pollut. Bull. 20:173-6.
69. Ruiz, G. M., Carlton, J. T., Grosholz, E. D. & Hines, A. H. 1997. Global invasions of marine and estuarine habitats by non-indigenous species: Mechanisms, extent, and consequences. Am. Zool. 37:621-32.
70. Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S. et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32:305.
71. Scagel, R. F. 1956. Introduction of a Japanese alga, Sargassum muticum into the northeast Pacific. Fish. Res. Pap. Dep. Fish. State Wash. 1:49-58.
72. Stæhr, P. A., Pedersen, M. F., Thomsen, M. S., Wernberg, T. & Krause-Jensen, D. 2000. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar. Ecol. Prog. Ser. 207:79-88.
73. Steele, E. N. 1964. The Immigrant Oyster (Ostrea gigas) Now Known as the Pacific Oyster. Pacific Coast Oyster Growers Association Inc., Olympia, Washington, USA, 179 pp.
74. Steen, H. & Rueness, J. 2004. Comparison of survival and growth in germlings of six fucoid species (Fucales, Phaeophyceae) at two different temperature and nutrient levels. Sarsia 89:175-83.
75. Stiger, V., Horiguchi, T., Yoshida, T., Coleman, A. W. & Masuda, M. 2003. Phylogenetic relationships within the genus Sargassum (Fucales, Phaeophyceae), inferred from ITS-2 nrDNA, with an emphasis on the taxonomic subdivision of the genus. Phycol. Res. 51:1-10.
76. Sunnucks, P. 2000. Efficient genetic markers for population biology. Trends Ecol. Evol. 15:199-203.
77. Swofford, D. L. 2000. PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Ver. 4.0b10. 4.0b10. Sinauer Associates, Sunderland, Massachusetts.
78. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-9.
79. Tellier, F., Meynard, A. P., Correa, J. A., Faugeron, S. & Valero, M. 2009. Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: vicariance or parapatry? Mol. Phylogenet. Evol. 53:679-93.
80. Thomson, J. M. 1952. The acclimatization and growth of the Pacific oyster (Gryphaea gigas) in Australia. Aust. J. Mar. Freshw. Res. 3:64-73.
81. Tsang, L. M., Chan, B. K. K., Ma, K. Y. & Chu, K. H. 2008. Genetic differentiation, hybridization and adaptive divergence in two subspecies of the acorn barnacle Tetraclita japonica in the northwestern Pacific. Mol. Ecol. 17:4151-63.
82. Tseng, C. K. & Chang, C. F. 1954. Studies on Chinese Sargassums, II. Sargassums kjellmanianum Yendo. Acta Bot. Sin. 3:353-66.
83. Tseng, C. K. & Lu, B. R. 2000. Flora algarum Marinarum sinicarum, Tomus III Phaeophyta, No. II Fucales. Science Press, Beijing, China, 238 pp.
84. Uwai, S., Kogame, K., Yoshida, G., Kawai, H. & Ajisaka, T. 2009. Geographical genetic structure and phylogeography of the Sargassum horneri/filicinum complex in Japan, based on the mitochondrial cox3 haplotype. Mar. Biol. 156:901-11.
85. Uwai, S., Nelson, W., Neill, K., Wang, W. D., Aguilar-Rosas, L. E., Boo, S. M., Kitayama, T. & Kawai, H. 2006b. Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes - origins and succession of introduced populations. Phycologia 45:687.
86. Uwai, S., Yotsukura, N., Serisawa, Y., Muraoka, D., Hiraoka, M. & Kogame, K. 2006a. Intraspecific genetic diversity of Undaria pinnatifida in Japan, based on the mitochondrial cox3 gene and the ITS1 of nrDNA. Hydrobiologia 553:345-56.
87. Verlaque, M., Durand, C., Huisman, J., Boudouresque, C. F. & Le Parco, Y. 2003. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur. J. Phycol. 38:325-39.
88. Voisin, M., Engel, C. R. & Viard, F. 2005. Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc. Natl. Acad. Sci. U. S. A. 102:5432-7.
89. Wallentinus, I. 1999. Introduction and transfer of plants. In Munro, A. L. S., Utting, S. D. & Wallentinus, I. [Eds.] Status of Introductions of Non-indigenous Marine Species to North Atlantic Waters 1981-1991. ICES Cooperative Research Report Vol. 231. International Council for the Exploration of the Sea, Copenhagen, Denmark, pp. 1-43.
90. Yendo, K. 1907. The Fucacaeae of Japan. J. Coll. Sci. Imperial Univ. Tokyo 21:1-174.
91. Yoshida, T. 1978. Lectotypification of Sargassum kjellmanianum and S. miyabei (Phaeophyta, Sargassaceae). Jpn. J. Phycol. 26:121-4.
92. Yoshida, T. 1983. Japanese species of Sargassum subgenus Bactrophycus (Phaeophyta, Fucales). J. Fac. Sci. Hokkaido Imperial Univ. Ser. V (Bot.) 13:99-246.
93. Yoshida, T. 1998. Marine Algae of Japan. Uchida Rokakuho Publishing Co. Ltd., Tokyo, Japan, 1222 pp.
94. Yoshida, T., Stiger, V. & Horiguchi, T. 2000. Sargassum boreale sp. nov. (Fucales, Phaeophyceae) from Hokkaido, Japan. Phycol. Res. 48:125-31.
95. Zhao, F., Liu, F., Liu, J., Ang, P. & Duan, D. 2008. Genetic structure analysis of natural Sargassum muticum (Fucales, Phaeophyta) populations using RAPD and ISSR markers. J. Appl. Phycol. 20:191-8.
96. Zink, R. M. 2002. Methods in comparative phylogeography, and their application to studying evolution in the North American aridlands. Integr. Comp. Biol. 42:953-9.
97. Zuccarello, G. C., West, J. & Rueness, J. 2002. Phylogeography of the cosmopolitan red alga Caulacanthus ustulatus (Caulacanthaceae, Gigartinales). Phycol. Res. 50:163-72.