- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Biology and Ecology
- Latitude/Altitude Ranges
- Water Tolerances
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Impact Summary
- Environmental Impact
- Threatened Species
- Risk and Impact Factors
- Similarities to Other Species/Conditions
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Grateloupia turuturu Yamada
Local Common Names
- Japan: tsurutsuru
- USA: gracie; red menace; red tide
Summary of InvasivenessTop of page
G. turuturu is a nuisance organism that can out-compete many native seaweeds within the low intertidal and shallow subtidal zones due to its large size and ability to reproduce quickly via sporic and vegetative reproduction (Barillé-Boyer et al., 2004; MIT Sea Grant Coastal Resources, 2009). Thus, it can alter typical trophic patterns and cause a loss of habitat (Vitousek et al., 1997; Walker and Kendrick, 1998; Marston and Villalard-Bohnsack, 1999; Simon et al., 2001; Torbett et al., 2004; Wallentinus and Nyberg, 2007). The plant also has the repertoire of an effective invader (Farnham, 1980; Harlin and Villalard-Bohnsack, 2001; Balcom, 2009), as it grows fast and has a high reproductive output; it grows well in nutrient enriched waters, in 22 to 37 ppt salinity, and can survive 12-52 ppt and 4-29°C (Simon et al., 1999; 2001). According to Gladych et al. (2009) juvenile sporelings of G. turuturu in Long Island Sound, USA, have a thermal optimum of 25°C, and they can develop satisfactorily at 15 and 20°C. Many of these tolerances exceed those associated with other seaweeds within the lower shorelines, including Chondrus crispus, Mastocarpus stellatus and Palmaria palmata. See Burns and Mathieson (1972a, b), Mathieson (1982), Mathieson and Burns (1975), and Liu and Pang (2009) for specific details of physiological tolerances of these three taxa. As G. turuturu has broad patterns of growth, reproduction and physiological tolerances, it is considered to be one of the five most-threatening introduced species with respect to its potential to become invasive (Nyberg and Wallentinus, 2005; Inderjit et al., 2006).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Plantae
- Phylum: Rhodophyta
- Class: Florideophyceae
- Subclass: Rhodymeniophycidae
- Order: Halymeniales
- Family: Halymeniaceae
- Genus: Grateloupia
- Species: Grateloupia turuturu
Notes on Taxonomy and NomenclatureTop of page
Foliose species of Grateloupia are notoriously difficult to identify because of morphological variability and a lack of clear-cut morphological characters (Marston and Villalard-Bohnsack, 2002; Barreiro et al., 2006; Figueroa et al., 2007; García-Jiménez et al., 2008). In contrast to external morphological variability, the internal reproductive structures of Grateloupia are remarkably homogenous, with conical auxiliary cells and carpogonial branches occurring in separate ampullae (Womersley, 1994). The genus has undergone several taxonomic revisions (Howe, 1914; Dawson, 1954; Ardré and Gayral, 1961; Dawson et al., 1964; Kraft, 1977; Wang et al., 2000; Kawaguchi et al., 2001) and accurate determinations of species identifications, geographic ranges, and invasive patterns require a synthesis of molecular, morphological-anatomical, and reproductive data (Knowlton, 2000; Wattier and Maggs, 2001; Zuccarello and West, 2002; Zuccarello et al., 2002; Ciniglia et al., 2004; Clerck et al., 2005; Saunders and Withall, 2006). At present approximately 60 species of Grateloupia are recognized (D’Archino et al., 2007; Guiry and Guiry, 2010), and it is the most diverse genus within the red algal family Halymeniaceae (Kraft, 1977; Gavio and Fredericq, 2002; Clerck et al., 2005; Guiry and Guiry, 2010). Some species have been synonymized because of substantial intraspecific and within-individual variation of gross morphology, while several cryptic taxa have been differentiated and found to be either previous synonyms or new taxa (Clerck et al., 2005). For example, Gavio and Fredericq (2002) used rbcL sequence analysis to confirm that the correct name for the invasive Japanese species of Grateloupia found within the North Atlantic (Farnham and Irvine, 1973; Farnham, 1978; Irvine, 1983; Irvine and Farnham, 1983; Verlaque et al., 2005) was G. turuturu Yamada (1941: p. 205) rather than G. doryphora (Montagne) Howe (1914: p. 169).
DescriptionTop of page
Verlaque et al. (2005) give a detailed description of G. turuturu from the Thau Lagoon of Hérault, France. They note that its upright blades are 10-70 cm long, pinkish to dark red in colour, soft and gelatinous in texture, and attached to the substratum by means of small discoidal holdfasts. Specimens grow singly or more often in clumps; blades are linear-lanceolate foliose, 2-15 cm broad, 225-250 µm thick (400-575 µm in the basal portion), and are either simple or irregularly divided in one plane. The plant’s margins are either entire or with proliferations and are almost always undulate. Its thallus (i.e. the plant body of an alga) is multiaxial and has a central or primary axis composed of parallel aggregated filaments. Fronds consist of a compact outer cellular cortex (i.e. external tissue) and a loose internal filamentous medulla, which consists of a central core of tissue that is colourless. Medullary filaments are 3-6 µm in diameter; they are loosely interlaced, with some of them tending to be periclinal in young thalli but becoming randomly arranged in older individuals. The cortex is 5-6 cells thick; outer cortical cells are 4-9 µm in diameter by 6-14 µm in length and they are ovoid to cylindrical. Gametophytes are monoecious, having separate male and female reproductive structures over the entire thallus, except for basal portions. Auxiliary cells (i.e. specialized cells that receive a zygotic nucleus or a division product) are produced in ampullae or specialized clusters, which are initiated in the inner cortex. Auxiliary cells are small, conical and composed of 2-3 ampullary filaments, which are 10-11 cells long. Mature auxiliary cells are oval in shape and significantly larger than other ampullary cells. The carpogonium, or female sex organ that contains the egg, is the terminal cell in a two celled carpogonial branch (filament); 2-3 simple carpogonial ampullae (filaments) occur near a carpogonial branch. A cystocarp, or female reproductive structure that include the carposporophyte, represents a multicellular phase in the plant’s life history that results from the development of the zygote and is terminated by carpospore production. Cystocarps are spherical; they do not protrude, and are 220-290 µm broad, including the outer wall or pericarp; an ostiole or opening of the cystocarp is either non-protruding or slightly depressed. Spermatangia (i.e. mother cells that produce a single spermatium or male gamete) are cut off from outer cortical cells; they are 4-5 µm in diameter and 2-3 are produced from each mother cell. Tetrasporangia (sporangia that produce four tetraspores, usually by meiosis) are oblong, cruciately divided (divided in two planes at right angles to each other), 29-40 µm long and 19-29 µm wide, and scattered over the entire thallus, except for the basal portion; they arise laterally from cortical cells in the third to fifth cortical cell layers from the surface without any modification of the cortex.
Other descriptions of the species are provided by Irvine (1983; a detailed description from Great Britain, using the name G. doryphora), Bárbara and Cremades (2004; from the Iberian peninsula), D'Archino et al. (2007; from New Zealand), Saunders and Withall (2006; from Tasmania), Patten (2006b; from Long Island Sound, USA), Salem Sound Coastwatch (2009; from the Gulf of Maine, USA) and Harlin and Villalard-Bohnsack (2001; from Rhode Island, USA).
DistributionTop of page
G. turuturu is a Pacific species that grows natively in China (Xia, 2004), Japan (Yoshida, 1998; Yoshida et al., 1990), Korea (Lee and Kang, 2001; Lee, 2008), and the far-eastern seas of Russia [Perestenko, 1996 (‘1994’)]. It has been introduced to the Pacific coast of Mexico, Australasia, the east coast of North Americe and Europe. Molecular studies by Marston and Villalard-Bohnsack (2002) for Rhode Island populations have indicated a uniformity of genetic composition (i.e. ITS and COX sequences) between Rhode Island, Portsmouth (England), Tholen Island (The Netherlands), and Brittany and Hérault (France). See 'History of Introduction and Spread' section for further details.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Japan||Present||Native||Yoshida et al., 1990; Yoshida, 1998; Kawaguchi et al., 2001; Verlaque et al., 2005|
|-Hokkaido||Present||Native||Wang et al., 2000; Kawaguchi et al., 2001; Gavio and Fredericq, 2002; Verlaque et al., 2005; Figueroa et al., 2007|
|Korea, Republic of||Present||Native||Lee and Kang, 2001; Gavio and Fredericq, 2002; Lee, 2008|
|Mexico||Localised||2008||Introduced||Invasive||Aguilar-Rosas et al., 2010|
|USA||Present||Present based on regional distribution.|
|-Connecticut||Localised||Introduced||Invasive||Dominion Resources Services Inc, 2004; Gladych et al., 2006; Saunders and Withall, 2006|
|-Massachusetts||Localised||Introduced||Invasive||Mathieson et al., 2008a; Mathieson et al., 2008b; Go Metal Detecting, 2010|
|-New York||Localised||2000||Introduced||Invasive||Mathieson et al., 2008b; Gavio and Fredericq, 2002||Reported from the easternmost tip of Long Island (Montauk)|
|-Rhode Island||Widespread||Introduced||Invasive||Mathieson et al., 2008b; Villalard-Bohnsack and Harlin, 1997; Marston and Villalard-Bohnsack, 1999; Gavio and Fredericq, 2002; Marston and Villalard-Bohnsack, 2002; Bowden, 2005|
|France||Localised||Introduced||Invasive||Riouall et al., 1985; Cabioch et al., 1997; Cabioch et al., 1997; Simon et al., 2001; Gavio and Fredericq, 2002; Clerck et al., 2005; Verlaque et al., 2005|
|Italy||Localised||Introduced||Invasive||Tolomio, 1993; Sfriso and Curiel, 2007|
|Netherlands||Localised||Introduced||Invasive||Stegenga and Otten, 1997; Maggs and Stegenga, 1999; Marston and Villalard-Bohnsack, 2002|
|Portugal||Localised||Introduced||Invasive||Bárbara and Cremades, 2004; Araújo et al., 2009|
|Russian Federation||Present||Present based on regional distribution.|
|-Russian Far East||Present||1994||Native||Perestenko, 1996||Far-eastern seas of Russia|
|Spain||Localised||Introduced||Invasive||Bárbara and Cremades, 2004; Bárbara et al., 2005; Clerck et al., 2005; Barreiro et al., 2006; Barreiro et al., 2006; Figueroa et al., 2007|
|UK||Localised||Introduced||Invasive||Farnham and Irvine, 1973; Farnham, 1997; Maggs and Stegenga, 1999; Maggs and Stegenga, 1999; Gavio and Fredericq, 2002; Marston and Villalard-Bohnsack, 2002|
|-Channel Islands||Localised||1995||Introduced||Invasive||Farnham, 1997||First found in the Channel Islands & northern Spain (as Grateloupia doryphora)|
|Australia||Present||Present based on regional distribution.|
|-Tasmania||Localised||Introduced||Invasive||ABC News, Australian Broadcasting Corporation; Saunders and Withall, 2006|
|New Zealand||Localised||2005||Introduced||Invasive||D'Archino et al., 2007||Muritai, Wellington Harbour, New Zealand : molecular confirmation|
History of Introduction and SpreadTop of page
Prior to critical molecular studies (Gavio and Fredericq, 2002), knowledge of the introduction and spread of G. turuturu was confounded because of its misidentification as G. doryphora as well as confusion with other morphologically similar species such as the native taxon G. lanceola (see Pictures). G.turuturu (as G. doryphora) was initially discovered in the eastern North Atlantic by Farnham in the Solent area of southern England in 1969 (Farnham and Irvine, 1973). After a decade (1979) it had only expanded about 20 km from its original wave-exposed site at Southsea (Maggs and Stegenga, 1999); at this time it was not present at nearby Portsmouth Harbour (Farnham, 1980). Subsequently it was found in the Thau Lagoon of Hérault, France by Riouall et al. (1985) during 1982 and referred to as G. doryphora (Verlaque, 2001; Cormaci et al., 2004; Verlaque et al., 2005). It is still present in this same lagoon (Verlaque et al., 2005), although it is not invasive, perhaps because four other Asiatic Grateloupia species are present, including G. asiatica, G. lanceolata, G. luxurians and G. patens.
In 1984 G. turuturu was recorded from Milford Haven, Wales near an oyster farm (Maggs and Stegenga, 1999). By 1989 it had reached the Isle of Wight, only 8 km offshore from the Solent coast where it was originally found (Farnham 1997). By 1995 it was recorded from northern Spain, and the Channel Islands between southern Great Britain and northern France (Farnham, 1997). In the meantime it had also spread northwards to Yerseke in the Dutch Oosterscheld (Stegenga and Otten, 1997), as well as southward to Brittany and Roscoff in France (Cabioch et al., 1997; Simon et al., 1999; Marston and Villalard-Bohnsack, 2002; Clerck et al., 2005), Portugal (ICES, 1992; Araújo et al., 2003; 2009; Bárbara and Cremades, 2004), and Spain (Pérez-Cirera et al., 1989; Bárbara et al., 2004; 2005; Barreiro et al., 2006; Clerck et al., 2005). Thus, G. turuturu has exhibited an expansive colonization of several northeastern Atlantic areas.
Within the Mediterranean, records for G. doryphora and/or G. turuturu from the Strait of Messina, the Adriatic Sea, and the Venice Lagoon (Masi and Gargiulo, 1982; Giaccone et al., 1985; Gargiulo et al., 1992; Tolomio, 1993; Sfriso and Curiel, 2007) need to be critically evaluated. In discussing some of these populations Verlaque et al. (2005) notes that the Venice Lagoon is heavily impacted by species introductions from Asia (Tolomio 1993) and G. doryphora specimens reported there are probably G. turuturu or (and?) G. lanceolata (see Pictures). Further Grateloupia doryphora thalli recorded in the southern Mediterranean, in Sicily (Masi and Gargiulo, 1982) and in the south of Spain (Rull Lluch et al., 1991) may be G. lanceola, a species described from Spain and the Atlantic coast of North Africa (Agardh, 1851) and previously regarded as conspecific with G. doryphora (Ardé and Gayral 1961; Dawson et al., 1964) based upon a likeness in foliose habit (see Benhissoune et al., 2002). The identity of these populations awaits molecular determination. Similar comments can be made regarding other records of Grateloupia from the Canary Island, Angola, Côte d’Ivoire, Gambia, Ghana, Liberia, Mauritania, Namibia, and Senegal (John et al., 2003; 2004). For example, García-Jiménez et al. (2008) recently showed the occurrence of G. lanceolata near fish aquaculture areas in the Canary Islands, plus ?G. imbricata Holmes that was previously identified as G. doryphora (Haroun et al., 2002).
Maggs and Stegenga (1999) suggest that many European populations of G. turuturu occur in the vicinity of shellfish farms, which suggests they were transported via commercial molluscs. Several investigators (Ribera and Boudouresque, 1995; Cabioch et al., 1997; Reise et al., 1999; Verlaque, 2001; Ribera Siguan, 2002; Wallentinus, 2002; Schaffelke et al., 2006) have also suggested that the transport of oysters for aquaculture was a probable vector for G. turuturu’s introduction into the eastern Atlantic and Mediterranean. For example, multiple transports of oysters have occurred within the Thau Lagoon of Hérault, France, a major site of shellfish aquaculture in the Mediterranean Sea (Trousselier et al., 1991). Initially the native oyster (Ostrea edulis) was transported to the Lagoon from England and Ireland between 1920 and 1929 (Grizel, 1994; Verlaque, 2001). Faced with successive oyster diseases, the professionals in this field have since 1961 been forced to resort to imported species (Hamon and Tournier, 1990; Pichot, 1991; Verlaque et al., 2005). Thus, adults and spat of the Portuguese oysters [Crassostrea angulata] were introduced between 1961-1971, while a massive importation of 280 million Japanese oysters [C. gigas] occurred directly from Japan during 1971 to 1976 (Grizel and Heral, 1991; Verlaque, 2001). Since 1976, the only spat officially authorized to enter the Thau Lagoon is that produced in the Atlantic.
Farnham (1978; 1980) suggested that secondary transport of established populations occurred in the Solent area of southern England via boat traffic. Similarly Simon et al. (2001) noted the occurrence of attached G. turuturu on ship hulls, yachts and pontoons on the Brittany coast (France); they compared the adaptation of this species to floating structures with that of the invasive kelp Undaria pinnatifida, which grows well on these various substrata (D’Archino et al., 2007). Simon et al. (2001) also record “stone-rafting” where drifting fertile blades attached to small cobbles/rocks are dispersed by currents and/or wave action. Marston and Villalard-Bohnsack (2002) noted that specimens of G. turuturu (as G. doryphora) from Portsmouth, England, Tholen Island, The Netherlands, and Brittany and Hérault, France were genetically similar to those from Rhode Island, USA; hence, they were probably transported long distances via boat traffic, including microscopic spores in ballast water and macroscopic fronds on ship hulls.
In the Northwest Atlantic G. turuturu extends from Boston Harbour, Massachusetts to Rhode Island, Connecticut, and Long Island, New York (Pederson et al., 2005; Mathieson et al., 2008a,b). It was initially recorded in 1994 from the Beavertail Point area near Bristol, Rhode Island in Narragansett Bay, apparently introduced either directly from Japan (or possibly Korea) via ballast water or ship hulls or secondarily on vessels from Europe (Villalard-Bohnsack and Harlin, 1997; Harlin and Villalard-Bohnsack, 2001; 2002). By 1997 it was identified at nine other sites in Narragansett Bay (Harlin and Villalard-Bohnsack, 1999; Bowden, 2005). In 2000 it was reported from two additional Narragansett Bay sites (Newport and Warwick, Rhode Island), plus the easternmost tip of Long Island at Montauk Point, New York (Mathieson et al., 2008a,b). Between 2003 and 2004 it expanded its range along the shore of Narragansett Bay, as well as migrating westward to Waterford, Connecticut, in Long Island Sound (Dominion Resources Services Inc, 2004; Bowden, 2005; Saunders and Withall, 2006). During 2006 G. turuturu was collected near Fall River, Massachusetts within Mount Hope Bay, which is in the northeastern corner of the greater Narragansett Bay region straddling the Massachusetts-Rhode Island state line (Salem Sound Coastwatch, 2009; Go Metal Detecting, 2010). Molecular and morphological analyses have suggested that the populations in Long Island Sound are identical to those in Narragansett Bay (Balcom, 2009).
By 2007 G. turuturu was discovered in Massachusetts, occurring at two small marinas at both ends of the Cape Cod Canal in Massachusetts (i.e. Sandwich Marina and Massachusetts Maritime Academy in Buzzard, Massachusetts) and within Boston’s Inner Harbour (Mathieson et al., 2008a,b). The most parsimonious hypothesis for this expansion is that G. turuturu spread into the Gulf of Maine via the Cape Cod Canal. The presence of G. turuturu in Boston Harbour represents a major leap northward (>132 km) in just 12 years. In addition, it breached Cape Cod, which is a natural boundary between warm and cold temperate floras (Humm, 1969; Hoek, 1975; Hooper et al., 2002). This northward movement was probably associated with transport on boat hulls through the Cape Cod Canal, like the vessel-mediated transport of G. turuturu within the Solent region of southern England (Farnham, 1980) and the Brittany coast of France (Simon et al., 2001). Most recently (2008) G. turuturu was recorded at another northern Massachusetts site (Wareham) just north of the Cape Cod Canal. Its broad physiological tolerances (Simon et al., 1999) suggests that it may expand as far north as the Bay of Fundy. Furthermore, its arrival in a major international port (i.e. Boston) may launch it onto new global shipping corridors in North America as well as around the world (Ruiz and Hewitt, 2002). In discussing the introduction of another Asiatic species, Grateloupia imbricata, into the Canary Islands, García-Jiménez et al. (2008) note that the advantageous geographic position of the islands makes them a trade and communication hub between Europe, America and Asia, and most specifically with Korea, Japan and China, due to the presence of large important harbours on the islands that have supported conspicuous trade and fishery activities over the past 50 years. Such facts point to international shipping as the plausible vector for many introductions via ballast waters and hull fouling (Schaffelke et al., 2006; Mineur et al., 2007).
G. turuturu has recently been recorded from the Pacific coast of Mexico (Ensenada Harbour in Todos Santos Bay, Baja California), growing attached to docks, buoys and boat hulls, in association with G. lanceolata, which had been previously reported from southern California. Maritime traffic between Japan and Mexico is suggested as the vector of introduction.
Recently G. turuturu has also been recorded from Tasmania (Saunders and Withall, 2006; Tasmanian Planning Commission, 2009) and New Zealand (D’Archino et al., 2007). Its introduction to both Tasmania (~2003) and New Zealand (?2005) may have been due to shipping as in Rhode Island (Villalard-Bohnsack and Harlin, 1997; 2001).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|England and Wales||Asia||1969||Aquaculture (pathway cause)
Hitchhiker (pathway cause)
|Yes||No||Farnham (1975); Farnham (1978); Farnham and Irvine (1973)|
|England and Wales||1984||Aquaculture (pathway cause)
Hitchhiker (pathway cause)
|Yes||No||Maggs and Stegenga (1999)||Milford Haven, near an oyster farm|
|France||Asia||1982||Aquaculture (pathway cause)||Yes||No||Verlaque (2001); Verlaque et al. (2005)||To Thau Lagoon.|
|France||1997||Aquaculture (pathway cause)||Yes||No||Cabioch et al. (1997); Simon et al. (1999)||Brittany|
|Mexico||Asia||2008||Hitchhiker (pathway cause)||Yes||No||Aguilar-Rosas et al. (2010)|
|Netherlands||by 1997||Aquaculture (pathway cause)||Yes||No||Stegenga and Otten (1997)||Near an oyster farm (Maggs and Stegenga, 1999)|
|New Zealand||Asia||?2005||Hitchhiker (pathway cause)||Yes||No||D'Archino et al. (2007)|
|Portugal||1997||Hitchhiker (pathway cause)||Yes||No||Araújo et al. (2003); Araújo et al. (2009); Bárbara and Cremades (2004); ICES (1992)|
|Spain||1991||Yes||No||Bárbara and Cremades (2004); Bárbara et al. (2003); Bárbara et al. (2005); Barreiro et al. (2006); Clerck et al. (2005); Pérez-Cirera et al. (1989)|
|Tasmania||Asia||~2003||Hitchhiker (pathway cause)||Yes||No||Saunders and Withall (2006)|
|USA||1996||Hitchhiker (pathway cause)||Yes||No||Villalard-Bohnsack and Harlin (1997)||Rhode Island specimens from Narragansett Bay are gentically similar to those from Europe.|
Risk of IntroductionTop of page
The major vectors for G. turuturu introductions appear to be molluscan aquaculture, deliberate transportation of shellfish, and accidental transfer on boats. Hewitt et al. (2007) suggest that a reduction of accidental transport, including enhanced legal responsibilities, is critical to minimize future introductions of macroalgae. Enhanced sanitary procedures within aquaculture facilities are also important, as many of the microscopic stages of G. turuturu can be carried on the surfaces of shells and they exhibit extensive vegetative reproduction. Further development of international monitoring instruments and regional agreements may assist with hull fouling, which is probably the most significant and poorly managed transport mechanism for macroalgae (Hewitt et al., 2007). Based upon genetic uniformity of G. turuturu plants in Rhode Island and Long Island Sound (USA), Portsmouth (England), Tholen Island (The Netherlands), and Brittany and Herault (France) (Marston and Villalard-Bohnsack, 2002; Bowden, 2005) it would appear that many macroscopic reproductive populations have been transported long distances on boat hulls or as spores within ballast waters. Large scale transport between Europe, Tasmania and New Zealand may also have been mediated by boat traffic.Again the potential for transport throughout the world from an international port such as Boston Harbour or Las Palmas de Gran Canaria should be emphasized.
HabitatTop of page
G. turuturu populations within the North Atlantic usually occur at semi-exposed and protected open coastal sites, as well as within coastal embayments and harbours that have little wave action but fast tidal currents (Farnham, 1980; Irvine, 1983). Typically the plant grows on rocky substrata, including small (to 60 mm) loosely embedded stones (Irvine, 1983), within the low intertidal and shallow subtidal zones (to ~ 3-8 feet below Mean Low Water), as well as within low tide pools (Villalard-Bohnsack and Harlin, 2001). It is able to grow in eutrophic embayments with highly variable temperature and salinity regimes. Based upon detailed seasonal studies in Rhode Island, Harlin and Villalard-Bohnsack (2001) found that G. turuturu typically grows to its maximal length and peak biomass during late summer and early autumn, while the opposite patterns are evident in late spring and early summer. They observed that the plant’s lowest percent coverage followed the lowest water temperature (3°C) and a reduction in size or loss of older individuals (Connecticut Sea Grant, 2009). All intertidal plants that were not in tide pools were killed by both high (>20°C) and low (freezing) air temperatures beginning in early summer and early winter, respectively. Seasonal studies near Brittany in the English Channel by Cabioch et al. (1997) showed a similar seasonal sequence as that observed in Rhode Island, except that the periods of maximum and minimum size and percent cover were earlier. In Brittany, young algal specimens were found in early autumn (September); in spring, adults reached maximum size and cover when they began to discolour, and in summer their blades turned yellow and disintegrated. Average winter water temperatures in Brittany range from ~9-11°C versus ~4°C in Rhode Island, with these differences and other temperature extremes (both lower and higher in Rhode Island) being possible causes of different seasonal growth patterns. In describing seasonal growth of G. turuturu (as G. doryphora) in Great Britain Irvine (1983) noted that peak growth also occurred in the summer with over 90% of the individuals being fertile at this time.
Habitat ListTop of page
|Coastal areas||Principal habitat|
|Intertidal zone||Secondary/tolerated habitat|
|Estuaries||Principal habitat||Harmful (pest or invasive)|
|Inshore marine||Principal habitat||Harmful (pest or invasive)|
|Inshore marine||Principal habitat||Natural|
|Inshore marine||Principal habitat||Productive/non-natural|
Biology and EcologyTop of page
Molecular studies by Marston and Villalard-Bohnsack (2002) have documented a uniformity of genetic composition (i.e. ITS and COX sequences) for G. turuturu populations from Rhode Island and Long Island Sound, USA (Balcom, 2009). In addition, specimens of G. turuturu from Portsmouth (England), Tholen Island (The Netherlands), and Brittany and Hérault (France) are also genetically similar to those from Rhode Island. Hence it would appear that many populations have been transported long distances via boat hulls or ballast, including those found in Tasmania and New Zealand.
G. turuturu can reproduce both by spores (see Pictures) and by vegetative propagation. The plant has a typical triphasic life history, involving gametophytic, carposporophytic, and tetrasporic phases (Bold and Wynne, 1985). Gametophytic and sporophytic phases are isomorphic, with the former producing diploid carpospores and ultimately tetrasporophytes and the latter haploid tetraspores and gametophytes. Both types of spores are non-motile and are discharged in dense masses. The spores ultimately settle after being in the plankton and then produce small rounded discs via a germ tube; following divisions of its tube tip a circular attached crust can send up many upright “shoots” that ultimately produce tens of thousands of additional spores (Harlin and Villalard-Bohnsack, 2001; Balcom, 2009). The germination patterns described above are similar to those described for G. turuturu (as G. doryphora) in France and G. filicina in both France (Cabioch et al., 1997) and northern Taiwan (Chiang, 1993). Thus, there no obvious developmental differences between these two species or in the development of G. turuturu on different coasts. Aside from the patterns of sporeling development described above, filaments produced from crusts can also develop into other discs by division of an apical cell. Additionally, regenerative plantlets can grow from fragments of discoid crusts (Kuishuang et al., 2004) as well as the production of plants from portions of blades (Heinonen, 2007).
Harlin and Villalard-Bohnsack (2001) record four major recruitment strategies for G. turuturu populations in Rhode Island: (1) spores develop into small crusts that give rise to filaments and blades; (2) filaments and/or crusts produce new crusts; (3) new blades develop from old crust; and (4) blades regenerate from old damaged blades (see Pictures). The possession of several different recruitment strategies obviously enhances the plant’s ability to survive unfavourable conditions as well as spread widely. For example, a basal crust formed by tightly arranged small cells with dense contents may be more resistant to environmental extremes and grazing, giving the species an adaptive advantage over macroalgae that do not produce a crust (Lubchenco and Cubit, 1980; Cabioch and Giraud, 1982; Littler and Arnold, 1982). Harlin and Villalard-Bohnsack (2001) note that the appearance of 300 new blades on an experimental plate within one month was evidence that G. turuturu could recruit rapidly to new spaces. See comments in the 'Risk of Introduction' section regarding the rapid recruitment and “opportunistic growth patterns” of G. turuturu three weeks after the “Erika” oil spill in the Bay of Biscay, France (Barillé-Boyer et al., 2004).
In New England and Great Britain new blades can appear year-round from basal crusts (see Pictures), but they sometimes become reduced during winter or other adverse periods (Irvine, 1983; Harlin and Villalard-Bohnsack, 2001). Hence, the plant can either act as a pseudoperennial (sensu Knight and Parke, 1931), which regenerates upright fronds from residual basal material similar to herbaceous perennials growing in gardens, or its intact fronds can survive multiple years like a true perennial. Cystocarps and tetrasporangia may occur year-round in Great Britain, with a peak in summer and over 90% of the individuals being fertile at this time (Irving, 1983). Sporelings can also be found year-round in Great Britain but they are most abundant in the summer; overwintering sporelings produce mature plants the following year. Harlin and Villalard-Bohnsack (2001) describe analogous reproductive patterns in New England.
Physiology and Phenology
“Seed production” of G. turuturu on nori-nets has been perfected in Japan utilizing the plant’s extensive vegetative reproductive capacities (Huang et al., 1999). That is, callus masses can be excised from explants maintained in an undifferentiated state for over five years (i.e. by subculturing every 2-3 months) on solid culture media (i.e ASP12NTA, 1.2% agar) supplemented with 0.1 mg/L of indole-3-acetic acid (IAA) and 6-benzylaminopurine (BAP). Ultimately these callus cells can be dispersed upon twines of nori-net or oyster shell, and they will attach and develop into crusts in a liquid PES medium. Upright fronds can be produced after 6-8 weeks (i.e. at room temperature) and upon transfer of the nets or shells to the sea they exhibit accelerated growth during January to April, reaching peak size after five months. Hence, the regenerative capacities of G. turuturu are very important economically in Japan.
As noted previously Chondrus crispus (Irish moss) and Palmaria palmata (dulse), plus various Polysiphonia and kelp species (Laminaria/Saccharina), are commonly associated with G. turuturu within the low intertidal and shallow subtidal zones, at least in the Northwest Atlantic. Preliminary field studies in Long Island Sound (New York, USA) suggest that more animals live on Chondrus (Irish moss) than G. turuturu (Patten, 2006a; Blaschik et al., 2007). Chondrus serves as habitat for blue mussels and other invertebrates, as well as algal epiphytes that provide food for crustaceans (Jones, 2007; Balcom, 2009). Several small invertebrates also live on/in populations of G. turuturu, including shrimps, snails, and juvenile fish and crabs (N. Blaschik, University of Connecticut, USA, personal communication, 2009). Currently there is little evidence of herbivory on Grateloupia (R. Whitlatch, University of Connecticut, USA, personal communication, 2009), perhaps because of the plant’s inhibitory chemical constituents (Miyazawa and Ito, 1974; Simon-Collin et al., 2002; 2004; Hellio et al., 2004; Denis et al., 2009; 2010). For example, Hellio et al. (2004) found that isethionic acid and floridoside isolated from G. turuturu inhibited settlement of Balanus amphitrite cyprid larvae. Similarly microbiological studies by Pang et al. (2006) showed that the settlement of bacteria in seawater was impaired by the presence of G. turuturu versus Saccharina japonica and Palmaria palmata, Thus, enhanced growth of Grateloupia could cause a shift or reduced diversity of associated seaweeds, animals, and bacteria.
G. turuturu grows well in nutrient enriched waters, in 22 to 37 ppt salinity, and can survive 12-52 ppt and 4-29°C (Simon et al., 1999; 2001). According to Gladych et al. (2009) juvenile sporelings of G. turuturu in Long Island Sound, USA, have a thermal optimum of 25°C, and they can develop satisfactorily at 15 and 20°C. Harlin and Villalard-Bohnsack (2001) found in Rhode Island, USA, that all intertidal G. turuturuthat were not in tide pools were killed by both high (>20°C) and low (freezing) air temperatures beginning in early summer and early winter, respectively.
ClimateTop of page
|Cf - Warm temperate climate, wet all year||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Water TolerancesTop of page
|Parameter||Minimum Value||Maximum Value||Typical Value||Status||Life Stage||Notes|
|Depth (m b.s.l.)||0||2.4||Optimum||Grows in the low intertidal and shallow subtidal zones, plus low tide pools (Villalard-Bohnsack and Harlin, 2001) (values below mean low water)|
|Salinity (part per thousand)||22||37||Optimum||12-52 tolerated (Simon et al., 1999, 2001)|
|Turbidity (JTU turbidity)||Optimum||Prefers limited turbidity|
|Water temperature (ºC temperature)||25||Optimum||4-29 tolerated. Although its optimum is 25 it can develop satisfactorily at 15-20 (Gladych et al., 2009)|
Natural enemiesTop of page
Notes on Natural EnemiesTop of page
Several small invertebrates live on/amongst populations of G. turuturu, including shrimps, snails, and juvenile fish and crabs. Even so, there is little evidence of herbivory on G. turuturu, except for a few ancillary comments by Harlin and Villalard-Bohnsack (2001) and others (Heinonen, 2007) concerning the herbivorous snail Lacuna vincta and the limpet Tectura testudinalis that may be found on older blades. Villalard-Bohnsack and Harlin (1997) reported extensive grazing tracks from Lacuna on Grateloupia’s blades, while they were not observed on its crustose base; analogous patterns were also noted for T. testudinalis (Heinonen 2007). Thus, the crustose base of G. turuturu appears to be more resistant to herbivory and other environmental extremes than its foliose blades, a pattern that is reported to occur in many other seaweeds (Lubchenco and Cubit, 1980; Cabioch and Giraud, 1982; Littler and Arnold, 1982).
Means of Movement and DispersalTop of page
One of the major vectors for G. turuturu’s introductions appears to be molluscan aquaculture, including deliberate transportation of shellfish that has allowed direct transfer of juvenile microscopic stages (Ribera and Boudouresque, 1995; Cabioch et al., 1997; Maggs and Stegenga, 1999; Reise et al., 1999; Ribera Siguan, 2002; Wallentinus, 2002; Schaffelke et al., 2006). Localized transport of macroscopic plants via “stone-rafting”or drifting of fertile blades on small cobbles/rocks may also occur (Simon et al., 2001), as well as accidental transfer on boats. For example, the plant’s recent northward movement from Long Island Sound into the Gulf of Maine (USA) was probably associated with transport on boat hulls through the Cape Cod Canal, like that noted in the Solent region of southern England (Farnham, 1978; 1980) and the Brittany coast of France (Simon et al., 2001). Transport of spores in ballast water may also be associated with long distance transport (Marston and Villalard-Bohnsack, 2002). The genetic similarity of specimens of G. turuturu (as G. doryphora) from Portsmouth (England), Tholen Island (The Netherlands), and Brittany and Hérault (France) suggests that long-range transport may occur via boats. Large-scale transport between Europe, Tasmania and New Zealand may also be mediated by boat traffic, particularly associated with international ports.
Impact SummaryTop of page
Environmental ImpactTop of page
There is a potential for substantial environmental impacts on native biota due to the invasive properties of G. turuturu. These impacts range from altered productivity, nutrient cycling and trophic patterns, to altered biodiversity within nearshore commuities. Unfortunately few experimental data are available to predict specific impacts, and only general suggestions can be made. For example, in the North Atlantic 4-5 major plant species [Chondrus crispus, Mastocarpus stellatus, Palmaria palmata, Saccharina latissima and S. longicruris] occur within the low intertidal-shallow subtidal zones that can be directly impacted by G. turuturu, in part because of its large stature, reduction in sunlight to understorey vegetation, etc. (Simon et al., 2001). The diminished functional roles of these plants, including altered productivity, nutrient cycling and generalized trophic dynamics should be noted, as well as the diminished economic value of native plants as sources of phycocolloids (carrageenan and alginic acid) and direct food consumption. For example, Chondrus serves as a habitat for a much greater diversity of associated animals than G. turuturu (N. Blashick, University of Connecticut, USA, personal communication, 2009), while the latter also seems to have some differential impacts on barnacle and bacterial associations (Hellio et al., 2004; Pang et al., 2006). Thus, enhanced growth of Grateloupia could cause a shift or reduced diversity of associated seaweeds, animals, and bacteria.
Threatened SpeciesTop of page
|Threatened Species||Conservation Status||Where Threatened||Mechanism||References||Notes|
|Chondrus crispus (carrageen)||No details No details||Competition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growth||Balcom, 2009; Harlin and Villalard-Bohnsack, 1999; Harlin and Villalard-Bohnsack, 2001; Salem Sound Coastwatch, 2009|
|Mastocarpus stellatus||No details No details||Competition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growth||Farnham, 1980; Harlin and Villalard-Bohnsack, 2001|
|Palmaria palmata (dulse)||No details No details||Competition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growth||Farnham, 1980; Harlin and Villalard-Bohnsack, 2001|
|Saccharina latissima||No details No details||Competition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growth||Farnham, 1980; Harlin and Villalard-Bohnsack, 2001|
|Saccharina longicruris||No details No details||Competition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growth||Farnham, 1980; Harlin and Villalard-Bohnsack, 2001|
Risk and Impact FactorsTop of page Invasiveness
- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Highly adaptable to different environments
- Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
- Pioneering in disturbed areas
- Long lived
- Fast growing
- Has high reproductive potential
- Reproduces asexually
- Altered trophic level
- Damaged ecosystem services
- Ecosystem change/ habitat alteration
- Infrastructure damage
- Modification of natural benthic communities
- Modification of successional patterns
- Monoculture formation
- Negatively impacts animal health
- Negatively impacts livelihoods
- Negatively impacts aquaculture/fisheries
- Reduced native biodiversity
- Threat to/ loss of native species
- Antagonistic (micro-organisms)
- Competition - monopolizing resources
- Competition - shading
- Competition - smothering
- Rapid growth
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
UsesTop of page
G. turuturu is used as a direct source of food in the Orient as well as a source of a carrageenan-agar hybrid polymers (Levring et al., 1969; Denis et al., 2009; 2010). Although no precise economic data are available, it is obviously significant enough in Japan to foster biotechnological studies of “seed production”, callus development, and outplanting (Huang et al., 1999). Again this is based upon its extensive regenerative capacities. Its chemical composition and potential medicinal values are currently being evaluated (Miyazawa and Ito, 1974; Simon-Collin et al., 2002; 2004; Hellio et al., 2004; Pang et al., 2006; Denis et al., 2009; 2010;), particularly as a means of utilizing an unexploited source of several chemicals (Denis et al., 2009; 2010).
Similarities to Other Species/ConditionsTop of page
G. turuturu superficially resembles dulse or Palmaria palmata. However, Palmaria has thicker, more leathery blades that typically branch dichotomously or palmately in contrast to G. turuturu’s more irregular and proliferous branching pattern, while the gelatinous and slippery texture of G. turuturu’s thallus (body) and its filamentous inner medulla contrast with the rounded internal cells of Palmaria (Balcom, 2009; Salem Sound Coastwatch, 2009). Further G. turuturu tends to grow in the low intertidal and shallow subtidal zones, while most other red algae inhabit deeper subtidal waters.
More probably, G. turuturu could be confused with other Asiatic Grateloupia species, with the native North Atlantic taxon G. lanceola, or the South American species G. doryphora. No conspicuous pale or green spots occur on G. turuturu, while they are present on G. lanceola (Bárbara and Cremades, 2004). Blades of G. turuturu are also thinner (i.e. 130-250 µm) than those of G. lanceola, which vary from 200-450 µm. G. turuturu can also be distinguished anatomically from G. doryphorasensu stricto (see Pictures) because of its anticlinal arrangement of medullary filaments, its thinner outer cortex of roundish cells, and an abrupt transition between the cortex and internal medull (Gavio and Fredericq, 2002). By contrast, G. doryphora has a dense medulla of small rhizine-like roundish cells in transverse section, a thicker cortex of elliptical cells, a periclinal medullary arrangement in longitudinal section, and a gradual transition between cortex and medulla.
See Verlaque et al. (2005) for a detailed comparison of five Grateloupia species found within the Thau Lagoon, including G. turuturu.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Regarding this one success story, several points can be made regarding the invasive pattern of G. turuturu. Foremost, there has been no real success in retarding its advances via shell fish or boat traffic. The fact that microscopic propagules can be transported via ballast water or as microscopic germlings on shellfish or vessels means that juvenile plants are difficult to discern compared with Caulerpa taxifolia. Further, G. turuturu has several means of vegetative reproduction like C. taxifolia, and macroscopic plants attached to ships' hulls can release thousands of spores in sheltered harbours. As suggested by Hewitt et al. (2007), reductions of accidental transport and enhanced legal responsibilities of ship owners are key factors, as well as enhanced sanitary procedures within aquaculture facilities. An outreach or educational component is a key factor in reducing the plant’s continued expansion (Balcom, 2009; Connecticut Sea Grant, 2009; MIT Sea Grant Coastal Resources, 2009; Salem Sound Coastwatch, 2009; SGNIS, 2010). Unfortunately the outlook is not very positive, unless a coordinated and well funded program is initiated like that enacted in California for C. taxifolia. However, these were localized and conspicuous populations, whereas G. turuturu can be confused with other seaweeds.
ReferencesTop of page
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ContributorsTop of page
The author is indebted to several individuals who helped with field and laboratory studies dealing with G. turuturu populations in the Northwest Atlantic, particularly James Carlton (Williams College-Mystic Seaport, Connecticut), Clinton J. Dawes (University of South Florida, Tampa, Florida), Rebecca Gladych (University of Connecticut @Avery Point, Connecticut), Anita Klein (University of New Hampshire, Durham, New Hampshire), and Judith Pederson (Massachusetts Institute of Technology Sea Grant Program, Cambridge, Massachusetts). The early studies of Marilyn Harlin (formerly University of Rhode Island, Kingston, Rhode Island) and Martine Villalard-Bohnsack (formerly Roger Williams University, Bristol, Rhode Island) laid the groundwork for these more recent studies. The molecular studies by Brigitte Gavio and Suzanne Fredericq (University of Louisiana at Lafayette, Lafayette, Louisiana) were also fundamental in clarifying the taxonomy of invasive G. turuturu and related taxa within the North Atlantic and other geographies. Heather Talbot of the Jackson Estuarine Laboratory, University of New Hampshire is also acknowledged for her help with several logistical items, including the scanning of figures.
05/02/10 Original text by:
Arthur Mathieson, University of New Hampshire Marine Program, Jackson Estuarine Laboratory, 85 Adams Point Road, Durham, NH 03824, USA
Clinton Dawes, Consultant, USA
Distribution MapsTop of page
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