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| NAS - Nonindigenous Aquatic Species |
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Common Name: green alga, grass kelp
Synonyms and Other Names: Hollow green weed
Taxonomy: available through 
Identification:
This species of green alga exhibits yellow to light green and smooth, lubricous, hollow thalli that may be branched or unbranched and filiform to strap- or horn-shaped, with disciform holdfasts. Cells are polygonal, quadrangular, angular, or sub-rectangular in shape and arranged in rows or somewhat irregularly (Kapraun 1970; Koeman and van den Hoek 1984; Hadi et al. 1989; Sahoo et al. 2003).
In the Great Lakes, subsp. paradoxa and subsp. flexuosa both occur. Typically, the former is branched while the latter is unbranched (Lougheed and Stevenson 2004). In the Great Lakes, subsp. paradoxa is <0.16 µm across, while subsp. flexuosa is up to 3.6 mm across (Lougheed and Stevenson 2004). See Koeman and van den Hoek (1984) for some gamete and zoospore dimensions.
Size: up to 4mm across
Native Range:
Unknown. This species is widespread. It occurs around the world in inland and/or coastal waters of Latin America and the Caribbean, Asia, Europe, Australia, the U.S.A., Mexico, and various islands in the Pacific Ocean (Kowalski 1975; Trono 1975; Webber 1975; Riouall 1976; Sivalingam 1977; Morton 1978; Vaughan 1978; Bird and McIntosh 1979; Lobel and Ogden 1981; Kies and Dworsky 1982; Rodriguez de Rios and Lobo 1984; Grant and Prasad 1985; Guner et al. 1985; Ho 1987; Hadi et al. 1989; Khotimchenko 1993; Beach et al. 1995; Martinez-Murillo and Aladro-Lubel 1996; Magnusson 1997; Schories et al. 1997; Fernandez et al. 1998; Woolcott and King 1999; Hodgson and McDermid 2000; Tabudravu et al. 2002; Matik-Skoko et al. 2004; Lourenco et al. 2006; Sahoo et al. 2006).
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Interactive maps: Continental US, Alaska, Hawaii, Caribbean
Nonindigenous Occurrences: E. flexuosa was recorded for the first time in 2003 in Muskegon Lake, which occurs at the junction of the Muskegon River with Lake Michigan. It has also been recorded from White Lake and Mona Lake, which are part of the same drainage (Lougheed and Stevenson 2004; Lougheed 2005).
Ecology: E. flexuosa is primarily a marine species but can tolerate freshwater conditions and is considered euryhaline. It is fast growing and prefers littoral zones with some wave action. In the Lake Michigan watershed it occurs in mesotrophic to eutrophic aquatic habitats. Its establishment could have been spurred by increased salt concentrations since the 1850s from industrial sources and de-icing salts, as well as a lack of native grazing pressure.
In Muskegon Lake, the two subspecies co-occur in littoral zone macrophyte beds, although E. flexuosa subsp. paradoxa has been recorded to comprise 61% of the macroalgae present by biovolume and E. flexuosa subsp. flexuosa only 31%. In White Lake, Enteromorpha has been known to comprise 5% of the macroalgae present, and in Mona Lake, 20% (Lougheed and Stevenson 2004).
E. flexuosa is known from diverse habitats around the world and has been recorded in salinities ranging from 0.5–34‰. It has been recorded in tidal pools, on mudflats, in sea dikes, in polyhaline man-made waters, in oligohaline ponds, in drainage ditches, on rocks, and in warm calm waters below low tide (Kapraun 1970; Koeman and van den Hoek 1984; Hadi et al. 1989; Sahoo et al. 2003).
To reproduce, dioecious gametophytes produce male and female gametes with 2 flagellae, while sporophytes produce zoospores with 4 flagellae (Koeman and van den Hoek 1984). Zoospores can be stored in the dark for over 50 days and still germinate with a 35% survival rate, indicating that transport in ballast water is possible (Beach et al. 1995; Kolwalkar et al. 2007). Swarmers may be released with increasing exposure at night and greater desiccation, whereas vegetative growth may typically occur with shorter exposure times (Mairh et al. 1985).
Means of Introduction: E. flexuosa was very likely transported in ballast water or on ship hulls to the Great Lakes basin (Lougheed and Stevenson 2004).
Status: Established where recorded.
Impact of Introduction:
A) Realized: Unknown.
B) Potential: In nutrient rich marine coastal areas, blooms of E. flexuosa are known to foul benthic communities, beaches, and man-made materials, and have the potential to smother aquatic plants, replace native algae, change redox conditions, and alter native food webs. It is unknown if impacts in freshwater regions could be similar; however, it is hypothesized that shading of macrophytes could become problematic in the Great Lakes if blooms were sustained for long periods of time. Moreover, E. flexuosa is a poor host to diatoms in Muskegon Lake. If it were to replace Oedogonium and Cladophora, which support many diatoms, food webs depending on such epiphytes could be negatively affected (Lougheed and Stevenson 2004). In the Wadden Sea intertidal flats, the presence of dense mats of E. flexuosa and other Enteromorpha spp. have been associated with decreases in brown and red algae (Schories et al. 1997).
Remarks:
References
Beach, K. S., C. M. Smith, T. Michael, and H.-W. Shin. 1995. Photosynthesis in reproductive unicells of Ulva fasciata and Enteromorpha flexuosa: implications for ecological success. Marine Ecology Progress Series 125(1-3):229-237.
Bird, K. T. and R. P. McIntosh. 1979. Notes on the marine algae of Guatemala. Revista de Biologia Tropical 27(2):163-170.
Fernandez, O. A., K. J. Murphy, A. L. Cazorla, M. R. Sabbatini, M. . Lazzari, J. C. J. Domaniewski, and J. H. Irigoyen. 1998. Interrelationships of fish and channel environmental conditions with aquatic macrophytes in an Argentine irrigation system. Hydrobiologia 380:15-25.
Grant, J. M. and D. Prasad. 1985. Chemical composition of some useful seaweeds of Jamaica, West Indies. Journal of Phycology 21(suppl.):15.
Guner, H., V. Aysel, A. Sukatar, and M. Ozturk. 1985. The flora of the Aegean Sea, Turkey. I. Cyanophyta, Chlorophyta, Phaeophyta, and Angiospermae. DOGA Bilim Dergisi Seri A Temel Bilimler 9(2):272-282.
Hadi, R., A. M. Hadi, K. M. Bahram, and A. A. S. Hassan. 1989. The new recorded species of Enteromorpha in Baghdad area, Iraq. Bulletin of the Iraq Natural History Museum 8(2):163-172.
Ho, Y. B. 1987. Metals in 19 intertidal macroalgae in Hong Kong waters. Marine Pollution Bulletin 18(10):564-566.
Hodgson, L. M. and J. K. McDermid. 2000. Marine plants of Pohnpei and Ant Atoll: Chlorophyta, Phaeophyta, and Magnoliophyta. Micronesica 32(2):289-307.
Kapraun, D. F. 1970. Field and cultural studies of Ulva and Enteromorpha in the vicinity of Port Aransas, Texas. Contributions in Marine Science 15:205-285.
Khotimchenko, S. V. 1993. Fatty acids of green macrophytic algae from the Sea of Japan. Phytochemistry (Oxford) 32(5):1203-1207.
Kies, L. and N. Dworsky. 1982. Species composition and biomass of floating and dried algal mats in shallow ponds from the vicinity of Pevestorf District of Luechow, Dannenberg, Lower Saxony, West Germany. Mitteilungen aus dem Institut fuer Allgemeine Botanik Hamburg 18:71-84.
Koeman, R. P. T. and C. Van Den Hoek. 1984. The taxonomy of Enteromorpha Chlorophyceae in the Netherlands. 3. The sections Flexuosae and Clathratae and an addition to the section Proliferae. Cryptogamie Algologie 5(1):21-61.
Kolwalkar, J. P., S. S. Sawant, and V. K. Dhargalkar. 2007. Fate of Enteromorpha flexuosa (Wolfen) J. Agardh and its spores in darkness: implications for ballast water management. Aquatic Botany 86(1):86-88.
Kowalski, W. 1975. Occurrence of the species of a marine green alga Enteromorpha in the Szczecin, Pomerania inland waters. Fragmenta Floristica et Geobotanica 21(4):527-536.
Lobel, P. S. and J. C. Ogden. 1981. Foraging by the herbivorous parrotfish Sparisoma radians. Marine Biology (Berlin) 64(2):173-184.
Lougheed, V. L. 2005. An invasive macroalga (Enteromorpha flexuosa) in Muskegon Lake. IAGLR Conference & Program Abstracts 48:115.
Lougheed, V. L. and R. J. Stevenson. 2004. Exotic marine macroalgae (Enteromorpha flexuosa) reaches bloom proportions in a coastal lake of Lake Michigan. Journal of Great Lakes Research 30(4):538-544.
Lourenco, S. O, E. Barbarino, A. Nascimento, J. N. P. Freitas, and G. S. Diniz. 2006. Tissue nitrogen and phosphorus in seaweeds in a tropical eutrophic environment: what a long-term study tells us. Journal of Applied Phycology 18(3-5):389-398.
Magnusson, G. 1997. Diurnal measurements of Fv/Fm used to improve productivity estimates in macroalgae. Marine Biology (Berlin) 130(2):203-208.
Mairh, O. P., R. S. Pandey, A. Tewari, R. M. Oza, and H. V. Joshi. 1985. Seasonal phenomena, growth, and swarmer liberation rhythm in Enteromorpha flexuosa (Chlorophyceae occurring on the coast of Okha, India). Proceedings of the Indian National Science Academy Part B Biological Sciences 51(3):381-385.
Martinez-Murillo, M. E. and m. A. Aladro-Lubel. 1996. Sessile ciliates epibiontic of algae in the Tamiahua Lagoon, Veracruz, Mexico. Tropical Ecology 37(2):265-272.
Matik-Skoko, S., B. Antolic, and M. Kraljevic. 2004. Ontogenetic and seasonal feeding habits of the annular seabream (Diplodus annularis L.) in Zostera sp. beds, eastern Adriatic Sea. Journal of Applied Ichthyology 20(5):376-381.
Morton, O. 1978. Some interesting records of algae from Ireland. Irish Naturalists’ Journal 19(7):240-242.
Riouall, R. 1976. Quantitative study of macrophytic algae of loose substratum from Prevost Pond, Herault, France. Naturalia Monspeliensia 26:73-94.
Rodriguez De Rios, N. and M. Lobo. 1984. 2 additions to the marine alga flora of Venezuela. Ernstia 25:1-7. Sahoo, D., N. Sahu, and D. Sahoo. 2003. A critical survey of seaweed diversity of Chilika Lake, India. Algae - Inchon 18(1):1-12.
Sahoo, D., P. Baweja, and N. Kushwah. 2006. Developmental studies in Porphyra vietnamensis: a high-temperature resistant species from the Indian coast. Journal of Applied Phycology 18(3-5):279-286.
Schories, D., A. Albrech, and H. Lotze. 1997. Historical changes and inventory of macroalgae from Koenigshafen Bay in the northern Wadden Sea. Helgolaender Meeresuntersuchungen 51(3):321-341.
Sivalingam, P. M. 1977. Marine algal distribution in Penang Island, Malaysia. Bulletin of the Japanese Society of Phycology 25(4):202-209.
Tabudravu, J. N., P. Gangaiya, S. Sotheeswaran, and G. R. South. 2002. Enteromorpha flexuosa (Wulfen) J. Agardh (Chlorophyta: Ulvales): evaluation as an indicator of heavy metal contamination in a tropical estuary. Environmental Monitoring and Assessment 75(2):201-213.
Trono, G. C. Jr. 1975. The marine benthic algae of Bulusan and vicinity province of Sorsogon, Philippines. Part 1. Introduction and Chlorophyta. Kalikasan 4(1):23-41.
Vaughan, F. A. 1978. Food habits of the sea bream Archosargus rhomboidalis and comparative growth on plant and animal food. Bulletin of Marine Science 28(3):527-536.
Webber, E. E. 1975. Recent additions to the marine algal flora of Nahant, Massachusetts, USA. Rhodora 77(811):430-433.
Woolcott, G. W. and R. J. King. 1999. Ulva and Enteromorpha (Ulvales, Ulvophyceae, Chlorophyta) in eastern Australia: comparison of morphological features and analyses of nuclear rDNA sequence data. Australian Systematic Botany 12(5):709-725.
Author: Rochelle Sturtevant
Contributing Agencies: 
NOAA - GLERL
Revision Date: 11/7/2007 Citation for this information:
Rochelle Sturtevant. 2009. Enteromorpha flexuosa subsp. flexuosa and flexuosa subsp. paradoxa. USGS Nonindigenous Aquatic Species Database, Gainesville, FL.
<http://nas.er.usgs.gov/queries/FactSheet.asp?speciesID=2726> Revision Date: 11/7/2007
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