Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Grateloupia turuturu

Toolbox

Datasheet

Grateloupia turuturu

Summary

  • Last modified
  • 06 November 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Grateloupia turuturu
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Plantae
  •     Phylum: Rhodophyta
  •       Class: Florideophyceae
  •         Subclass: Rhodymeniophycidae
  • Summary of Invasiveness
  • 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 r...

Don't need the entire report?

Generate a print friendly version containing only the sections you need.

Generate report

Pictures

Top of page
PictureTitleCaptionCopyright
Morphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia species. (A) Habit of Palmaria palmata specimen from the Northwest Atlantic, showing mature frond with forking tips and proliferating base; scale bar 2.5 cm (after Taylor, 1962). (B) Habit of a tetrasporangial specimen of P. palmata from Great Britain, showing tetrasporangial sori in middle portion of blade and multiple blades arising from a basal discoid holdfast; scale bar 2.0 cm (after Irvine 1983). (C) A tetrasporophytic specimen of G. doryphora from Bahia de Ancon, Peru; scale bar 5 cm (after Gavio and Fredericq, 2002).
TitleMorphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia sp.
CaptionMorphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia species. (A) Habit of Palmaria palmata specimen from the Northwest Atlantic, showing mature frond with forking tips and proliferating base; scale bar 2.5 cm (after Taylor, 1962). (B) Habit of a tetrasporangial specimen of P. palmata from Great Britain, showing tetrasporangial sori in middle portion of blade and multiple blades arising from a basal discoid holdfast; scale bar 2.0 cm (after Irvine 1983). (C) A tetrasporophytic specimen of G. doryphora from Bahia de Ancon, Peru; scale bar 5 cm (after Gavio and Fredericq, 2002).
CopyrightArthur C. Mathieson
Morphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia species. (A) Habit of Palmaria palmata specimen from the Northwest Atlantic, showing mature frond with forking tips and proliferating base; scale bar 2.5 cm (after Taylor, 1962). (B) Habit of a tetrasporangial specimen of P. palmata from Great Britain, showing tetrasporangial sori in middle portion of blade and multiple blades arising from a basal discoid holdfast; scale bar 2.0 cm (after Irvine 1983). (C) A tetrasporophytic specimen of G. doryphora from Bahia de Ancon, Peru; scale bar 5 cm (after Gavio and Fredericq, 2002).
Morphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia sp.Morphology, anatomy and reproduction of Palmaria palmata (dulse) and three different Grateloupia species. (A) Habit of Palmaria palmata specimen from the Northwest Atlantic, showing mature frond with forking tips and proliferating base; scale bar 2.5 cm (after Taylor, 1962). (B) Habit of a tetrasporangial specimen of P. palmata from Great Britain, showing tetrasporangial sori in middle portion of blade and multiple blades arising from a basal discoid holdfast; scale bar 2.0 cm (after Irvine 1983). (C) A tetrasporophytic specimen of G. doryphora from Bahia de Ancon, Peru; scale bar 5 cm (after Gavio and Fredericq, 2002).Arthur C. Mathieson

Identity

Top of page

Preferred Scientific Name

  • Grateloupia turuturu Yamada

Local Common Names

  • Japan: tsurutsuru
  • USA: gracie; red menace; red tide

Summary of Invasiveness

Top 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 Tree

Top 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 Nomenclature

Top of page
Irvine (1983) notes a chequered history for the identification of Grateloupia turuturu, which she designated as Grateloupia dorphyphora in Great Britain. British plants were initially identified as either Kallymenia J. Agardh (1842) or Schizmenia J. Agardh (1851). However, the cystocarp (part of the female reproductive structure) of Schizmenia is different from that of Grateloupia as it contains fewer large carposporangia (i.e. sporangia-producing carpospores) that are not surrounded by enveloping filaments. G. turuturu also differs from other foliose algae in Great Britain such as Kallymenia and Halymenia C. Agardh (1817) as it lacks well-developed highly refractive stellate cells within its internal tissue (i.e. medullar).

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).
 
Various taxonomic treatments of G. turuturu have also been made (Guiry and Guiry, 2010). For example, John et al. (2003) listed G. doryphora as a synonym of G. turuturu, whereas John et al. (2004) cited both G. doryphora and G. lanceolata (Okamura) Kawaguchi (1997: p. 20) as synonyms of G. turuturu. By contrast, Dawson (1954) and Dawson et al. (1964) cited G. doryphora as a distinct species and G. lanceola (J. Agardh) J. Agardh (1851: p. 182) as one of its synonyms, while Ardré and Gayral (1961) listed G. lanceola as a distinct species with multiple synonyms, including G. doryphora (Howe, 1914). Recent molecular and morphological evaluations (Pérez-Cirera et al., 1989; Bárbara and Cremades, 2004; Barreiro et al., 2006; Figueroa et al., 2007) have confirmed that G. turuturu, G. doryphora and G. lanceola are distinct species (Guiry and Guiry, 2010) and that several cryptic and/or synonymous taxa should be delineated within this complex. For example, Gavio and Fredericq (2002) confirmed that G. doryphora has a Southern Hemisphere distribution and is only known to occur in Peru and Chile. In a later synopsis of distributional patterns of G. doryphoraGuiry and Guiry (2010) noted the plant’s occurrence in Mexico [Dawson (1954) as G. abbreviata Kylin 1941: p. 10 and G. multiphylla Dawson 1954: p. 251], Venezuela (Ganesan, 1990) and a few other locations, but these have not been confirmed molecularly. Recent work by Wilkes et al. (2006) from the Strait of Messina (between Sicily and Italy) has shown that further study of foliose Grateloupia from the Mediterranean is needed, including a re-evaluation of names previously applied to entities in this complex that are neither G. doryphora nor G. turuturu. Barreiro et al. (2006) and Figueroa et al. (2007) confirmed the presence of the native species G. lanceola in Galicia (northwest Spain) and the northwestern coasts of Africa where it was initially described by J. Agardh (1851); older records report it from the African coast between Angola and Morocco (Bornet, 1892; Dangeard, 1949; 1952; Gayral, 1958; Ardré and Gayral, 1961; Bodard, 1965), Pérez-Cirera et al. (1989) report it from southeast Spain. Apparently Galicia is the only area in Europe where both G. turuturu and G. lanceola are sympatric (Bárbara and Cremades, 2004).
 
The type location for G. turuturu is either cited as Muroran, Hokkaido, Japan (Verlaque et al., 2005) or as a series of syntype Japanese locations (Yamada, 1941; Guiry and Guiry, 2010), including Muroran, Otaru, and Hakodate, Hokkaido; Enoshima and Hayama, Sagami Province; and Amatura, Bosyu Province. According to Yoshida (1998), the type specimen is located within the herbarium of Hokkaido University in Sapporo; it is labelled as “Halymenia turuturu Okamura in herb” and is designated as specimen #022063.
 
The three common names for G. turuturu within the Northwest Atlantic are “gracie”, “red menace”, and “red tide” (Patten, 2006a; Go Metal Detecting, 2010; SGNIS, 2010). The first name is a children’s nickname, while the other two names refer to the plant’s rapid growth, large reddish appearance, and potential dominance within the low intertidal-shallow subtidal zones.

Description

Top 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).

Distribution

Top 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 Table

Top 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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaPresent2004NativeXia, 2004
JapanPresentNativeYoshida et al., 1990; Yoshida, 1998; Kawaguchi et al., 2001; Verlaque et al., 2005
-HokkaidoPresentNativeWang et al., 2000; Kawaguchi et al., 2001; Gavio and Fredericq, 2002; Verlaque et al., 2005; Figueroa et al., 2007
Korea, Republic ofPresentNativeLee and Kang, 2001; Gavio and Fredericq, 2002; Lee, 2008

North America

MexicoLocalised2008Introduced Invasive Aguilar-Rosas et al., 2010
USAPresentPresent based on regional distribution.
-ConnecticutLocalisedIntroduced Invasive Dominion Resources Services Inc, 2004; Gladych et al., 2006; Saunders and Withall, 2006
-MassachusettsLocalisedIntroduced Invasive Mathieson et al., 2008a; Mathieson et al., 2008b; Go Metal Detecting, 2010
-New YorkLocalised2000Introduced Invasive Mathieson et al., 2008b; Gavio and Fredericq, 2002Reported from the easternmost tip of Long Island (Montauk)
-Rhode IslandWidespreadIntroduced 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

Europe

FranceLocalisedIntroduced 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
ItalyLocalisedIntroduced Invasive Tolomio, 1993; Sfriso and Curiel, 2007
NetherlandsLocalisedIntroduced Invasive Stegenga and Otten, 1997; Maggs and Stegenga, 1999; Marston and Villalard-Bohnsack, 2002
PortugalLocalisedIntroduced Invasive Bárbara and Cremades, 2004; Araújo et al., 2009
Russian FederationPresentPresent based on regional distribution.
-Russian Far EastPresent1994NativePerestenko, 1996Far-eastern seas of Russia
SpainLocalisedIntroduced 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
UKLocalisedIntroduced 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 IslandsLocalised1995Introduced Invasive Farnham, 1997First found in the Channel Islands & northern Spain (as Grateloupia doryphora)

Oceania

AustraliaPresentPresent based on regional distribution.
-TasmaniaLocalisedIntroduced Invasive ABC News, Australian Broadcasting Corporation; Saunders and Withall, 2006
New ZealandLocalised2005Introduced Invasive D'Archino et al., 2007Muritai, Wellington Harbour, New Zealand : molecular confirmation

History of Introduction and Spread

Top 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, 2002Clerck 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., 2006Clerck 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).

Introductions

Top of page
Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous 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 Introduction

Top 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.

G. turuturu’s broad physiological tolerances, perennial growth pattern, and diverse means of reproduction (i.e. vegetative and sporic reproduction) all contribute to successful recruitment in a new (alien) environment. Species richness and physical disturbance in a receiving environment may also contribute to the plant’s potential success as an invader (Dunstan and Johnson, 2007). The dramatic increase in abundance of G. turuturu and Ulva lactuca within the Bay of Biscay, France three weeks after the “Erika” oil spill and the mortality of sea urchins document the “opportunistic” growth patterns of both species (Barillé-Boyer et al., 2004).

Habitat

Top 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 List

Top of page
CategorySub-CategoryHabitatPresenceStatus
Littoral
Coastal areas Principal habitat
Intertidal zone Secondary/tolerated habitat
Brackish
Estuaries Principal habitat Harmful (pest or invasive)
Estuaries Principal habitat Natural
Estuaries Principal habitat Productive/non-natural
Marine
 
Inshore marine Principal habitat Harmful (pest or invasive)
Inshore marine Principal habitat Natural
Inshore marine Principal habitat Productive/non-natural

Biology and Ecology

Top of page

Genetics

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.

Reproductive Biology

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.           

Associations

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.

Environmental Requirements

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.

Climate

Top of page
ClimateStatusDescriptionRemark
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 Ranges

Top of page
Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
41-52 41-42

Water Tolerances

Top of page
ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
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 enemies

Top of page
Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Lacuna vincta Herbivore not specific
Tectura testudinalis Herbivore not specific

Notes on Natural Enemies

Top 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 Dispersal

Top 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 Summary

Top of page
CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Environmental Impact

Top 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 Species

Top of page
Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
Chondrus crispus (carrageen)No details No detailsCompetition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growthBalcom, 2009; Harlin and Villalard-Bohnsack, 1999; Harlin and Villalard-Bohnsack, 2001; Salem Sound Coastwatch, 2009
Mastocarpus stellatusNo details No detailsCompetition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growthFarnham, 1980; Harlin and Villalard-Bohnsack, 2001
Palmaria palmata (dulse)No details No detailsCompetition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growthFarnham, 1980; Harlin and Villalard-Bohnsack, 2001
Saccharina latissimaNo details No detailsCompetition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growthFarnham, 1980; Harlin and Villalard-Bohnsack, 2001
Saccharina longicrurisNo details No detailsCompetition - monopolizing resources; Competition - shading; Competition - smothering; Rapid growthFarnham, 1980; Harlin and Villalard-Bohnsack, 2001

Risk and Impact Factors

Top 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
  • Gregarious
  • Reproduces asexually
Impact outcomes
  • Altered trophic level
  • Conflict
  • 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
Impact mechanisms
  • Antagonistic (micro-organisms)
  • Competition - monopolizing resources
  • Competition - shading
  • Competition - smothering
  • Fouling
  • Rapid growth
  • Rooting
Likelihood of entry/control
  • 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

Uses

Top 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/Conditions

Top 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 Control

Top 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.

Presently there are very few success stories regarding the eradication of destructive, invasive, non-native seaweeds. One example is associated with the infestation of the green alga Caulerpa taxifolia in southern California (http://www.sccat.net/eradication/Final-Eradication-Declaration-Recommendation-FULL-Package.pdf) (see Appendix A, page 7, figure 3). This invasive seaweed was found at two southern California sites during mid-2000: Agua Hedionda Lagoon in San Diego County and Huntington Harbour, Orange County. The occurrence of C. taxifolia in California represented its first infestations in the United States. Apparently it was introduced by improper disposal of the contents of home aquaria. Eradication of existing infestations and prevention of new ones were of critical importance, because of the plant’s invasive history, particularly in the Mediterranean. In southern California large tarpaulins were put over areas where it was growing, chlorine was put under them and sandbags were placed on top to keep them in place. It was concluded that short-term losses of native marine life associated with this treatment would be considerably less than the long-term losses if C. taxifolia were to spread in and/or beyond the infested waters. Communication and coordination with stakeholders (lagoon users and others) were important components of the eradication efforts. After nearly six years eradication in both sites was complete.

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.

References

Top of page

ABC News (Australian Broadcasting Corporation), 2008. Japanese marine pest spreading around Tasmania. Japanese marine pest spreading around Tasmania. unpaginated. http://www.abc.net.au/news/stories/2008/05/08/2238550.htm

Agardh JG, 1851. [English title not available]. (Species genera et ordines algarum, seu descriptiones succinctae specierum, generum et ordinum, quibus algarum regnum constituitur. Volumen secundum: algas florideas complectens. Part 1.) Lundae [Lund]: C. W. K. Gleerup, i-xii, 1-351.

Aguilar-Rosas R, Aguilar-Rosas LE, Hiroshi K, NiNi W, 2010. First report on the Japanese species Grateloupia lanceolata (Okamura) Kawaguchi and Grateloupia turuturu Yamada (Halymeniaceae, Rhodophyta) in Baja California, Mexico. In: XX International Seaweed Symposium, Ensenada, Baja California, México [ed. by Cabello-Pasini, A.]., México: International Seaweed Association and Universidad Autónoma de Baja California, 112-113.

Araújo R, Bárbara I, Santos G, Rangel M, Sousa Pinto I, 2003. [English title not available]. (Fragmenta Chorologica Occidentalia, Algae, 8572-8640.) Fragmenta Chorologica Occidentalia, Algae, 8572-8640, 60. 405-409.

Araújo R, Bárbara I, Tibaldo M, Berecibar E, Tapia PD, Pereira R, Santos R, Pinto IS, 2009. Checklist of benthic marine algae and cyanobacteria of northern Portugal. Botanica Marina, 52:24-46.

Ardré F, Gayral P, 1961. [English title not available]. (Quelques Grateloupia de l'Atlantique et du Pacifique.) Revue Algologique (n. s.), 6:405-409.

Balcom NC, 2009. G. turuturu: a red seaweed invading Long Island Sound. G. turuturu: a red seaweed invading Long Island Sound. Groton, Connecticut: Connecticut Sea Grant, 2 pp. http://web2.uconn.edu/seagrant/publications/ais/gratelou.pdf

Bárbara I, Calvo S, Cremades J, Diaz P, Dosil J, Peña V, López Varela C, Novo T, 2003. [English title not available]. (Fragmenta chorological occidentalia, algae, 8641-8747.) Anales del Jardin Botánico de Madrid, 60:409-416.

Bárbara I, Cremades J, 2004. [Grateloupia lanceola verses G. turuturu (Gigartinales, Rhodophyta) in the Iberian Peninsula]. (Grateloupia lanceola versus G. turuturu (Gigartinales, Rhodophyta) en la Peninsula Iberica.) Anales del Jardin Botánico de Madrid, 61:103-118.

Bárbara I, Cremades J, Calvo S, López-Rodríguez MC, Dosil J, 2005. Checklist of the benthic marine and brackish Galician algae (NW Spain). Anales del Jardin Botánico de Madrid, 62:69-100.

Barreiro R, Quintela M, Bárbara I, Cremades J, 2006. RAPD differentiation between an invasive and a native species of Grateloupia (Rhodophyta) in Galicia (NW Spain). Phycologia, 46:213-217.

Barrillé-Boyer AL, Gruet Y, Barillé L, Harin N, 2004. Temporal changes in community structure of tide pools following the "Erika" oil spill. Aquatic Living Resources, 17:323-328.

Benhissoune S, Boudouresque CF, Perret-Boudouresque M, Verlaque M, 2002. A checklist of the seaweeds of the Mediterranean and Atlantic coasts of Morocco. III. Rhodophyceae (excluding Ceramiales). Botanica Marina, 45:391-412.

Bird K, Habig C, Debusk T, 1982. Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). Journal of Phycology, 18:344-348.

Blaschik N, Whitlach R, Kraemer GP, Yarish C, Lin S, 2007. Spread & impacts of the non-indigenous Rhodophycean alga, G. turuturu, on eastern Long Island Sound. In: Spread & impacts of the non-indigenous Rhodophycean alga, G. turuturu, on eastern Long Island Sound. 74.

Bodard M, 1965. [English title not available]. (Grateloupia senegalensis, nouvelle espèce de l'Ouest africain (Rhodophytes, Cryptonémiales).) Bulletin de L' Institut Fondamental d'Afrique Noire Sér (Sciences Naturelle), 27:1211-1220.

Bold HC, Wynne MJ, 1985. Introduction to the algae: structure and reproduction. Englewood Cliffs, New Jersey: Prentice-Hall, Inc., 720 pp.

Bonnemaison T, 1822. [English title not available]. (Essai d'une classification des hydrophites loculées, ou plantes marines articulées qui croissent en France.) Journal de Physique, de Chimie, d'Histoire Naturelle et des Arts, 94:138-148.

Bornet E, 1892. [English title not available]. (Les algues de P.-K.-A. Schousboe.) Mémoires societe imperiale des sciences naturelles, Cherbourg, 28:165-376.

Bowden MM, 2005. Code red: Roger Williams biologists track new species of seaweed in Narragansett Bay. The Bridge. Code red: Roger Williams biologists track new species of seaweed in Narragansett Bay. The Bridge, Spring 2005. Roger Williams University, 16-17.

Burns RL, Mathieson AC, 1972. Ecological studies of economic red algae. II. Culture studies of Chondrus crispus Stackhouse and Gigartina stellata (Stackhouse) Batters. Journal of Experimental Marine Biology and Ecology, 8:1-6.

Burns RL, Mathieson AC, 1972. Ecological studies of economic red algae. III. Growth and reproduction of natural and harvested populations of Gigartina stellata (Stackhouse) Batters in New Hampshire. Journal of Experimental Marine Biology and Ecology, 9:77-95.

Cabioch J, Castric-Fey A, L'Hardy-Halos MT, Rio A, 1997. [English title not available]. (Grateloupia doryphora et Grateloupia filicina var. luxurians (Rhodophyta, Halymeniaceae) sur les côtes de la Bretagne.) Cryptogamie Algologie, 18:117-137.

Cabioch J, Giraud G, 1982. [English title not available]. (La structure hildenbrandioïde stratégie adaptive chez les Floridées.) Phycologia, 21:307-315.

Chiang YM, 1993. The developmental sequence of the marine red alga Grateloupia filicina in culture. Korean Journal of Phycology, 8:231-237.

Ciniglia C, Yoon HS, Pollio A, Pinto G, Bhattacharya D, 2004. Hidden biodiversity of the extremophilic Cyanidiales red algae. Molecular Ecology, 13:1827-1838.

Clerck O de, Gavio B, Fredericq S, Bárbara I, Coppejans E, 2005. Systematics of Grateloupia filicina (Halymeniaceae, Rhodophyta), based on rbcL sequence analyses and morphological evidence, including the reinstatement of G. minima and the description of G. capensis sp. nov. Journal of Phycology, 41:391-410.

Connecticut Sea Grant, 2009. Invasive species of Long Island Sound. Invasive species of Long Island Sound. Groton, Connecticut: University of Connecticut Sea Grant Program, unpaginated. http://web2.uconn.edu/seagrant/whatwedo/ais/listour.php

Cormaci M, Furnari G, Giaccone G, Serio D, 2004. Alien macrophytes in the Mediterranean sea: a review. Recent Research Developments in Environmental Biology, 1:153-202.

Crouan PL, Crouan HM, 1858. [English title not available]. (Note sur quelques algues marines nouvelles de la rade de Brest.) Annales des Sciences Naturelles, Botanique Sér, 4:69-75.

Dangeard P, 1949. [Marine algae of the west coast of Morocco]. (Les algues marines de la côte occidentale du Maroc.) Le Botaniste, 34:89-189.

Dangeard P, 1952. [English title not available]. (Algues de la presqu'ile du Cap Vert (Dakar) et de ses environs.) Le Botaniste, 36:195-329.

D'Archino R, Nelson WA, Zuccarello GC, 2007. Invasive marine red alga introduced to New Zealand waters: first record of G. turuturu (Halymeniaceae, Rhodophyta). New Zealand Journal of Marine and Freshwater Research, 41:35-42.

Darwin CR, 1854. A monograph on the sub-class Cirripedia, with figures of all the species. The Balanidae (or Sessile Cirripedes); the Verrucidae, etc. London, UK: The Ray Society, 684 pp.

Dawes CJ, 1981. Marine botany. New York, USA: John Wiley & Sons, 628 pp.

Dawson EY, 1954. Marine red algae of Pacific Mexico. Part 2: Cryptonemiales (cont.). Allan Hancock Pacific Expedition, 17:241-397.

Dawson EY, Acleto C, Foldvik N, 1964. The seaweeds of Peru. Nova Hedwigia, 13:1-111.

Denis C, Morançais M, Li M, Deniaud E, Gaudin P, Wielgosz-Collin G, Barnathan G, Jaouen P, Fleurence J, 2010. Study of the chemical composition of the edible red macroalgae G. turuturu from Brittany (France). Food Chemistry, 119:913-917.

Denis C, Morançais M, Li M, Gaudin P, Fleurence J, 2009. Effect of enzymatic digestion on thallus degradation and extracton of hydrosoluble compounds from G. turuturu. Botanica Marina, 52:262-267.

Dominion Resources Services Inc, 2004. Monitoring the marine environment of Long Island Sound at Millstone Power Station, Waterford, Connecticut. Annual report. Waterford, CT: Millstone Environmental Laboratory, Dominion Resources Services Incorporated, unpaginated.

Dunstan PK, Johnson CR, 2007. Mechanisms of invasion: can the recipient community influence invasion rates? Botanica Marina, 50:361-372.

Eno NC, Clarck RA, Sanderson WG, 1997. Non-native marine species in British waters: a review and directory. Peterborough, UK: Joint Nature Conservation Committee, unpaginated.

Farnham WF, 1975. Seaweeds and their allies (algae). In: The Natural History of Pagham Harbour Part II [ed. by Rayner, R. W.]. Bognor Regis, UK: Bognor Regis Natural Science Society, 37-46.

Farnham WF, 1978. Introduction of marine algae into the Solent, with special reference to the genus Grateloupia. Portsmouth, UK: Portsmouth Polytechnic, unpaginated.

Farnham WF, 1980. Studies on aliens in the marine flora of southern England. In: The Shore Environment. Volume 2: Ecosystems [ed. by Price, J. H.\Irvine, D. E. G.\Farnham, W. F.]. London, UK: Academic Press, 875-914.

Farnham WF, 1997. [Invasive species of the English Channel and Atlantic coasts]. (Espèces invasives sur les côtes de la Manche et de l'Atlantique.) In: Dynamique d'espèces marines, application à l'expansion de Caulerpa taxifolia en Mèditerranée. Paris, France: Lavoizsier Tec & Doc, 15-35.

Farnham WF, Irvine LM, 1973. The addition of a foliose species of Grateloupia in the British marine flora. British Phycological Journal, 8:208-209.

Figueroa L, Korbee N, Clerck O de, Bárbara I, Gall ERA, 2007. Characterization of Grateloupia lanceolata (Halymeniales, Rhodophyta), an obscure foliose Grateloupia from the Iberian Peninsula, based on morphology, comparative sequence analysis and mycosporine-like amino acid composition. European Journal of Phycology, 42(3):231-242.

Ganesan EK, 1990. A catalog of benthic marine algae and seagrasses of Venezuela. Caracas: Fondo Editorial Conicit, 237 pp.

García-Jiménez P, Geraldino PJL, Boo SM, Robaina RF, 2008. Red alga Grateloupia imbricata (Halymeniaceae), a new species introduced into the Canary islands. Phycological Research, 56:166-171.

Gargiulo MG, Masi FDe, Tripodi G, 1992. Sargassum muticum (Yendo) Fensholt (Phaeophyta, Fucales) is spreading in the Lagoon of Venice. Giorm. Bot. Ital, 126:359.

Gavio B, Fredericq S, 2002. G. turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. European Journal of Phycology, 37:349-360.

Gayral P, 1958. [Algae of the Atlantic coast of Morocco]. (Algues de la Côte Atlantique Marocaine.) Rabat, Morocco: Collection la Nature au Maroc, 523 pp.

Giaccone G, Colonna P, Graziano C, Mannino AM, Tornatore E, Cormaci M, Furnari G, Scammaca B, 1985. [English title not available]. (Revisione della flora marina di Sicilia e isole minori.) Gioenia di Scienze Naturali Catania, 18:537-781.

Gladych R, Blaschik NB, Kraemer GP, Whitlach R, Yarish C, 2007. Potential ecosystem changes caused by an introduced red alga, Grateloupia turuturu Yamada in Long Island Sound. In: Marine Bioinvasions: Fifth International Conference on Marine Bioinvasions [ed. by Pederson, J.]. Cambridge, Massachusetts, USA: MIT Sea Grant College Program, 58.

Gladych R, Keser M, Yarish C, 2006. Initial observations and monitoring of G. turuturu Yamada along the Connecticut coast in Long Island Sound. In: Phycological Society of America, 60th Annual Meeting, Univ. Alaska Southeast, Juneau, Alaska. unpaginated.

Gladych R, Yarish C, Kraemer G, 2009. Tracking and predicting a path of invasion along the southern New England coast: G. turuturu Yamada. In: 48th Northeast Algal Symposium, University of Massachusetts, Amherst, Massachusetts. 32.

Go Metal Detecting, 2010. Go metal detecting. Go metal detecting. unpaginated. http://gometaldetecting.com/beach-rakes.htm

Grizel H, 1994. [English title not available]. (Réflexions sur les problèmes d'introduction de mollusques.) In: Introduced species in European Coastal Waters. European Commission EUR 15309 EN, Ecosystem Research Report 8 [ed. by Boudouresque, C. F.\Briand, F.\Nolan, C.]. 50-55.

Grizel H, Héral M, 1991. Introduction into France of the Japanese oyster (Crassostrea gigas). Journal du Conseil International pour l'Exploration de la Mer, 47:399-403.

Guiry M, Guiry W, 2010. AlgaeBase version 4.3 world-wide electronic publication. AlgaeBase version 4.3 world-wide electronic publication. Galway, Ireland: National University of Ireland, unpaginated. http://www.algaebase.org

Guiry MD, West JA, Kim DH, Masuda M, 1984. Reinstatement of the genus Mastocarpus kutzing (Rhodophyta). Taxon, 33:53-63.

Hamon PY, Pichot Y, 1994. [English title not available]. (La Conchyliculture en Méditerranée,1 ère partie.) Equinoxe, 52:25-35.

Hamon PY, Tournier H, 1990. [Study of the mollusc stocks reared in Thau Lagoon from 1981 to 1987]. (Étude des stocks de mollusques élevés dans l'étang de Thau de 1981 á 1987.) Étude des stocks de mollusques élevés dans l'étang de Thau de 1981 á 1987. Sète: Ifremer, unpaginated. [R.I.D.R.V.-90.43-RA/Sète.]

Harlin MM, Villalard-Bohnsack M, 1999. A large red seaweed invades Narragansett bay. Maritimes, 41:6-9.

Harlin MM, Villalard-Bohnsack M, 2001. Seasonal dynamics and recruitment strategies of the invasive seaweed Grateloupia doryphora (Halymeniaceae, Rhodophyta) in Narragansett Bay and Rhode Island Sound, Rhode Island, USA. Phycologia, 40:468-474.

Harlin MM, Villalard-Bohnsack M, 2002. An invasive red seaweed: Morphology and recruitment in Rhode Island Waters. RINHewS The Newsletter of the Rhode Island Natural History Survey, 9(1):May 2002.

Haroun RJ, Gil-Rodríguez MC, Díaz de Castro J, Prud'homme van Reine WF, 2002. A checklist of the marine plants from the Canary Islands (Central Eastern Atlantic Ocean). Botanica Marina, 45:139-169.

Heinonen K, 2007. Risk assessment review of invasive species in Long Island Sound. Avery Point, Connecticut, USA: University of Connecticut, Marine Sciences Department, 58 pp.

Hellio C, Simon-Colin C, Clare AS, Deslandes E, 2004. Isethionic acid and floridoside isolated from the red alga, G. turuturu inhibit settlement of Balanus amphitrite cyprid larvae. Biofouling, 20:139-145.

Hewitt CL, Campbell ML, Schaffelke B, 2007. Introductions of seaweeds: accidental transfer pathways and mechanisms. Botanica Marina, 50:326-337.

Hoek van den C, 1975. Phytogeographic provinces along the coasts of the northern Atlantic Ocean. Phycologia, 14:317-330.

Holmes EM, 1896. New marine algae from Japan. Journal of the Linnean Society of London, Botany, 31:248-260.

Hooper RG, Mathieson AC, Wilce RT, 2002. Geographic distributions of marine algae along the Northeastern Coast of North America. In: NEAS Keys to Benthic Marine Algae of the Northeastern Coast of North America from Long Island Sound to the Strait of Belle Isle. Contribution No. 2 [ed. by Sears, J.]. Dartmouth, Massachusetts, USA: Northeast Algal Society, 133-136.

Howe MA, 1914. The marine algae of Peru. Memoirs of the Torrey Botanical Club, 15:1-185.

Huang W, Fujita Y, Ninomiya M, Ohno M, 1999. Seed production and cultivation of G. turuturu (Cryptonemiales, Rhodophyta) by callus culture. Bulletin Marine Science Fisheries Kochi University, 19:1-7.

Humm HJ, 1969. Distribution of marine algae along the Atlantic coast of North America. Phycologia, 7:43-53.

ICES, 1992. Report of the working group on introductions and transfers of marine organisms. Lisbon, Portugal: International Council for the Exploration of the Sea, 92 pp.

Inderjit, Chapman D, Ranelletti M, Kaushik S, 2006. Invasive marine algae: an ecological perspective. Botanical Review, 72:153-178.

Irvine LM, 1983. Seaweeds of the British Isles, volume 1, Rhodophyta; Part 2A: Cryptonemiales (sensu stricto) Palmariales, Rhodymeniales. London, UK: British Museum (Natural History), 113 pp.

Irvine LM, Farnham WF, 1983. Halymeniaceae. In: Seaweeds of the British Isles, volume 1, Rhodophyta; Part 2A: Cryptonemiales (sensu stricto) Palmariales, Rhodymeniales [ed. by Irvine, L. M.]. London: British Museum (Natural History), 17-51.

John DM, Lawson GW, Ameka GK, 2003. The marine macroalgae of the tropical West Africa subregion. Berlin & Stuttgart, Germany: J. Cramer, 217 pp. [Beihefte zur Nova Hedwigia 125.]

John DM, Prud'homme van Reine WF, Lawson GW, Kostermans TB, Price JH, 2004. A taxonomic and geographical catalogue of the seaweeds of the western coast of Africa and adjacent islands. Berlin & Stuttgart, Germany: J. Cramer, 339 pp. [Beihefte zur Nova Hedwigia 127.]

Jones E, 2007. Community interactions in an epiphytic algal community. In: Benthic Ecology Meeting, Georgia Tech University, Atlanta. 134.

Kawabata SJ, 1954. On the structure of the frond, and the reproductive organ of Pachymeniopsis lanceolata Yamada (Aeodes lanceolata. Okam.). Japanese Journal of Phycology (Sôrui), 2:67-71.

Kawaguchi S, 1997. Taxonomic notes on the Halymeniaceae (Gigartinales, Rhodophyta) from Japan, III. Synonymization of Pachymeniopsis Yamada in Kawabata with Grateloupia C. Agardh. Phycological Research, 45:9-21.

Kawaguchi S, Wang HW, Horiguchi T, Sartoni G, Masuda M, 2001. A comparative study of the red alga Grateloupia filicina (Halymeniaceae) from the northwestern Pacific and Mediterranean with the description of Grateloupia asiatica, sp. nov. Journal of Phycology, 37:433-442.

Knight M, Parke M, 1931. Manx algae. Memoir Liverpool Marine Biological Commission, 30:1-147.

Knowlton N, 2000. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia, 420:73-90.

Kraft GT, 1977. The morphology of Grateloupia intestinalis from New Zealand, with some thoughts on generic criteria within the family Cryptonemiacaeae (Rhodophyta). Phycologia, 16:43-51.

Kuishuang S, Jinxia W, Baicheng Z, 2004. Production and application of filaments of G. turuturu (Halymeniaceae, Rhodophyta). Journal of Applied Phycology, 16:431-437.

Kuntze O, 1891. [Revision of the plant genera, Part 2]. (Revisio generum plantarum, Pars 2.) Leipzig, London: Arthur Felix, Dulalu & Co., 375-1011.

Kylin H, 1941. [Californian Rhodophyta]. (Californische Rhodophyceen.) Acta Universitatis Lundensis, 37:1-71.

Lane CE, Mayes C, Druehl LD, Saunders GW, 2006. A multi-gene molecular investigation of the kelps (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. Journal of Phycology, 42:493-512.

Lee Y, 2008. Marine algae of Jeju. Seoul, Korea: Academy Publication, 177 pp.

Lee Y, Kang S, 2001. A catalogue of the seaweeds in Korea. Jeju, Korea: Cheju National University Press, 662 pp.

Levring T, Hoppe HA, Scmid OJ, 1969. Marine algae. A survey of research and utilization. Hamburg: Cram de Gruyter & Company, 421 pp.

Li WW, Ding ZF, 1998. A new genus of Cryptonemiaceae-Sinotubimorpha. Journal of Guangdon Ocean University, 24:140-184.

Littler MM, Arnold KE, 1982. Primary productivity of marine macroalgal functional-form groups from southwestern North America. Journal of Phycology, 18:307-311.

Liu F, Pang SJ, 2009. Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae G. turuturu and Palmaria palmata. Journal of Experimental Marine Biology and Ecology, 383:82-87.

Loiseaux-de Goër S, Noailles MC, 2008. [Algae of Roscoff]. (Algues de Roscoff.) Roscoff, France: Station Biologique de Roscoff, 215 pp.

Lubchenco J, Cubit J, 1980. Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology, 61:676-687.

Maggs CA, Stegenga H, 1999. Red algal exotics on north sea coasts. Helgoländer Meeresuntersuchungen, 52:243-258.

Maiz NB, Boudouresque CF, Gerbal M, 1986. [Algal flora of Thau Lagoon: Grateloupia doryphora (Montagne) Howe and G. filicina (Wulfen) C. Agardh]. (Flore algal de l'Etang de Thau: Grateloupia doryphora (Montagne) Howe et G. filicina (Wulfen) C. Agardh.) Thallographica, 9:39-49.

Marston M, Villalard-Bohnsack M, 1999. The use of molecular genetics to investigate the geographic origin and vector of an invasive red alga. In: Marine Bioinvasion: First International Conference [ed. by Pederson, J.]. Cambridge, Massachusetts, USA: MIT Sea Grant College Program, 244-250.

Marston M, Villalard-Bohnsack M, 2002. Molecular variability and potential sources of Gratelopia doryphora (Halymeniacae), an invasive species in Rhode Island waters (USA). Journal of Phycology, 38:649-658.

Masi F de, Gargiulo GM, 1982. ['Grateloupia doryphora' (Mont.) Howe (Rhodophyta, Cryptonemiales) in the Mediterranean]. ('Grateloupia doryphora' (Mont.) Howe (Rhodophyta, Cryptonemiales) en Méditerranée.) Alliona, 25:105-108.

Mathieson AC, 1982. Reproductive phenology and sporeling ecology of Chondrus crispus Stackhouse. In: Proceedings of the Republic of China-U.S. Cooperative Science Seminar on Cultivation of Economic algae [ed. by Tsuda, R.\Chiang, Y. M.]. Mangilao, Guam: University of Guam Laboratory Publication, 33-40.

Mathieson AC, Burns RL, 1975. Ecological studies of economic red algae. V. Growth and reproduction of natural and harvested populations of Chondrus crispus Stackhouse in New Hampshire. Journal of Experimental Marine Biology and Ecology, 17:137-156.

Mathieson AC, Dawes CJ, Pederson J, Gladych RA, Carlton JT, 2008. The Asian red seaweed G. turuturu (Rhodophyta) invades the Gulf of Maine. Biological Invasions, 10:985-988.

Mathieson AC, Pederson J, Dawes CJ, 2008. Rapid assessment surveys of fouling and introduced seaweeds in the Northwest Atlantic. Rhodora, 110:406-478.

Mineur F, Jonson MP, Maggs C, Stegenga H, 2007. Hull fouling on commercial ships as a vector of macroalgal introduction. Marine Biology, 151:1299-1307.

MIT Sea Grant Coastal Resources, 2009. Introduced species- descriptions. MIT Sea Grant Coastal Resources. Introduced species- descriptions. MIT Sea Grant Coastal Resources. unpaginated. http://massbay.mit.edu/exoticspecies/exoticmaps/descriptions_intro.html

Miyazawa K, Ito K, 1974. Isolation of a new peptide, L-Citrullinyl-L-arginine, from a red alga G. turuturu. Bulletin of the Japanese Society of Scientific Fisheries, 40:815-818.

Müller OF, 1776. [English title not available]. (Zoologiee danicee prodromus seu animalium Danire et Norvegiee indigenarum characteres, nomina et synonyma imprimis popularium Havniee.) Zoologiee danicee prodromus seu animalium Danire et Norvegiee indigenarum characteres, nomina et synonyma imprimis popularium Havniee. unpaginated.

Neish AC, Shacklock PF, Fox CH, Simpson FJ, 1977. The cultivation of Chondrus crispus. Factors affecting growth under greenhouse conditions. Canadian Journal of Botany, 55:2263-2271.

Nyberg CD, Wallentinus I, 2005. Can species traits be used to predict marine macroalgal introduction? Biological Invasions, 7:265-279.

Pang SJ, Xiao T, Shan TF, Wang ZF, Gao SQ, 2006. Evidence of the intertidal red alga G. turuturu in turning Virbio parahaemolyticus into non-culturable state in the presence of light. Aquaculture, 260:1-4.

Patten MP van, 2006. Beware of the red menace. Wrack Lines Magazine, 6:8-10.

Patten MP van, 2006. Seaweeds of Long Island Sound. Avery Point, Groton, CT, USA: Connecticut Sea Grant College Program, University of Connecticut,, 104 pp.

Pederson J, Bullock RR, Carlton J, Dijkstra J, Dobroski N, Dyrynda P, Fisher R, Harris L, Hobbs N, Lambert G, Lazo-Wasem E, Mathieson A, Miglietta MP, Smith J, Smith J, Tyrrell M, 2005. Marine invaders in the northeast; rapid assessment survey of non-native and native marine species of floating dock communities. August 2003. Marine invaders in the northeast; rapid assessment survey of non-native and native marine species of floating dock communities. August 2003. Cambridge, Massachusetts, USA: MIT Sea Grant College Program, 40 pp. [MIT Sea Grant College Program Publication No. 05-3.]

Perestenko LP, 1996. Red algae of the far-eastern seas of Russia. St. Petersburg: Rossiiskaia Akademiia Nauk, Botanichesk Insitut im. V. L. Komarova [Komarov Botanical Institute, Russian Academy of Science], 330 (331) pp.

Pérez-Cirera JL, Cremades J, Bárbara I, 1989. [English title not available]. (Grateloupia lanceola (Cryptonemiales, Rhodophyta) en las coastas de la Peninsula Ibérica: studio morfológico y anatómico.) Lazaroa, 11:123-134.

Pichot P, 1991. [English title not available]. (Thau: l'élevage des mollusques- historique.) In: ECOTHAU, synthèse des résultats [ed. by Jouffre, D.\Amanieu, M.]. Montpellier, France: Université Montpellier II, 32-34.

Quintela M, Barreiro R, Bárbara I, Cremades J, 1999. [English title not available]. (Aplicación de la técnica de RAPD como ayuda en la differciación de especies foliosa del género Grateloupia (Gigartinales, Rhodophyta).) In: XIII Symposio de Botánica Criptogámica Madrid [ed. by Crespo, A.]. Madrid, Spain: Universidad Complutense de Madrid, unpaginated.

Reise K, Gollasch S, Wolff WJ, 1999. Introduced marine species of the North Sea Coasts. Helgoländer wissenschaftliche Meeresuntersuchungen, 52:219-234.

Ribera A, Boudouresque CF, 1995. Introduced marine plants, with special reference to macroalgae: mechanisms and impact. In: Progress in Phycological Research, Vol. 11 [ed. by Round, F. E.\Chapman, D. J.]. Amsterdam: Biopress Ltd., 187-268.

Ribera Siguan MA, 2002. Pathways of biological invasions of marine plants. In: Invasive Species: Vectors and Management Stategies [ed. by Ruiz, G. M.\Carlton, J. T.]. Washington, USA: Island Press, 183-226.

Riouall R, Guiry MD, Codomier L, 1985. [English title not available]. (Introduction d'une espèce foliacées de Grateloupia dans la flore marine de l'Etang de Thau (Hérault, France).) Cryptogamie Algologie, 6:91-98.

Ruiz G, Hewitt CL, 2002. Towards understanding patterns of coastal marine invasions: a prospectus. In: Invasive Aquatic Species of Europe, Distribution, Impacts and Management [ed. by Leppäkoski, E.\Gollasch, S.\Olenin, S.]. Dordrecht: Kluwer Academic Publishers, 529-547.

Rull Lluch J, Ribera MA, Gomez Garreta A, 1991. [English title not available]. (Quelques Rhodophyta intéressantes de la Méditerrantée.) Nova Hedwigia, 52:149-155.

Salem Sound Coastwatch, 2009. Guide to marine invaders in the Gulf of Maine: G. turuturu, red algae. Guide to marine invaders in the Gulf of Maine: G. turuturu, red algae. unpaginated. http://www.mass.gov/czm/invasives/docs/invaders/g_turuturu.pdf

Saunders GW, Withall RD, 2006. Collections of the invasive species G. turuturu (Halymeniales, Rhodophyta) from Tasmania, Australia. Phycologia, 45:711-714.

Schaffelke B, Smith JE, Hewitt CL, 2006. Introduced macroalgae- a growing concern. Journal of Applied Phycology, 18:529-541.

Sfriso A, Curiel D, 2007. Check-list of seaweeds recorded in the last 20 years in Venice lagoon, and a comparison with the previous records. Botanica Marina, 50:22-58.

SGNIS, 2010. Try to arrest Gracie "the blade" red algae. Sea Grant Nonindigenous Species Site (SGNIS). unpaginated. http://www.sgnis.org/kids/Atlantic/bookem/bookem_Gracie.html

Silva P, 2009. [English title not available]. (Index Nominum Algarum Bibliographia Phycologica Universalis.) Index Nominum Algarum Bibliographia Phycologica Universalis. Berkeley, California, USA: Center for Phycological Documentation, University Herbarium, University of California, unpaginated. http://ucjeps.berkeley.edu/INA.html

Simon C, Gall EA, Deslandes E, 2001. Expansion of the red alga Grateloupia doryphora along the coast of Brittany, France. Hydrobiologia, 443:23-29.

Simon C, Gall EA, Levavasseur G, Deslandes E, 1999. Effects of short-term variations of salinity and temperature on the photosynthetic response to the red alga Grateloupia doryphora from Brittany (France). Botanica Marina, 42:437-440.

Simon-Colin C, Kervarec N, Pichon R, Bessieres MA, Deslandes E, 2002. Charaterization of N-methyl-L-methionine sulfoxide and isethionic acid from the marine red alga Grateloupia doryphora. Phycological Research, 50:125-128.

Simon-Colin C, Kervarec N, Pichon R, Bessieres MA, Deslandes E, 2004. Purification and characterization of 4-methane sulfinyl-2-methylamino butyric acid from the red alga Grateloupia doryphora Howe. Phytochemistry Reviews, 3:367-370.

Stegenga H, Karremans M, Simons J, 2007. [English title not available]. (Zeewieren van de voormalige oesterputten bij Yerseke.) Gorteria, 32:125-143.

Stegenga H, Otten BG, 1997. [English title not available]. (Recente veranderingen in de Nederlandse Zeewierflora III. Nieuwe vestigingen van soorten in de roodwiergenera Choreocolax (Choreocolaceae), Grateloupia (Cryptonemiales), Ceramium en Seirospora (Ceramiaceae).) Gorteria, 23:69-76.

Suringar WFR, 1873. [English title not available]. (Illustrationes des algues du Japon.) Musée Botanique de Leide, 1:77-90.

Tasmanian Planning Commission, 2009. State of the environment, Tasmania 2009. State of the environment, Tasmania 2009. unpaginated. http://soer.justice.tas.gov.au/2009/

Taylor WR, 1962. Marine algae of the Northeastern Coast of North America. Revised edition. Ann Arbor, USA: Univ. Michigan Press, 509 pp.

Tolomio C, 1993. First record of Grateloupia doryphora (Mont.) Howe (Rhodophyceae) from the Lagoon of Venice. Lavoir, Società Veneto di Scienze Naturali, 18:215-220.

Torbett J, Fuda T, Piercey FP, Villalard-Bohnsack M, Marston M, 2004. Impact of the invasive alga G. turuturu (Halymeniaceae, Rhodophyta) on the native alga Chondrus crispus (Gigartinaceae, Rhodophyta). In: 43th Northeast Algal Symposium, University of Connecticut, Avery Point, Connecticut. 49.

Trousselier M, Frisoni GF, Lasserre G, 1991. [English title not available]. (Presentation du cadre.) In: ECOTHAU, synthèse des résultats [ed. by Jouffre, D.\Amanier, M.]. Montpellier, France: Université Montpellier II, 11-17.

Verlaque M, 2001. Checklist of the macroalgae of Thau Lagoon (Herault, France): a hot spot of marine species introduction in Europe. Oceanologica Acta, 24:293-312.

Verlaque M, Brannock PM, Komatsu T, Villalard-Bohnsack M, Marston M, 2005. The genus Grateloupia C. Agardh (Halymeniaceae, Rhodophyta) in the Thau Lagoon (France, Mediterranean): a case study of marine plurispecific introductions. Phycologia, 44:477-496.

Villalard-Bohnsack M, Harlin M, 1997. The appearance of Grateloupia doryphora (Halymeniaceae, Rhodophyta) on the northeast coast of North America. Phycologia, 36:324-328.

Villalard-Bohnsack M, Harlin M, 2001. Grateloupia doryphora (Halymeniaceae, Rhodophyta) in Rhode Island waters (USA): geographical expansion, morphological variations and associated algae. Phycologia, 40:372-380.

Vitousek PM, D, Loope LL, Rejmanek M, Westbrooks R, 1997. Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology, 21:1-16.

Walker D, Kendrick GA, 1998. Threats to macroalgal diversity: marine habitat destruction and fragmentation, pollution and introduced species. Botanica Marina, 41:105-112.

Wallentinus I, 2002. Introduced marine algae and vacular plants in European aquatic environment. In: Invasive Aquatic Species of Europe, Distribution, Impacts and Management [ed. by Leppäkoski, E.\Gollasch, S.\Olenin, S.]. Dordrecht: Kluwer Academic Publishers, 27-52.

Wallentinus I, Nyberg CD, 2007. Introduced marine organisms as habitat modifers. Marine Pollution Bulletin, 55:323-332.

Wang HW, Kawaguchi S, Horiguchi T, Masuda M, 2000. Reinstatement of Grateloupia catenata (Rhodophyta, Halymeniaceae) on the basis of morphology and rbcL sequences. Phycologia, 39:288-237.

Wang HW, Kawaguchi S, Horiguchi T, Masuda M, 2001. A morphogical and molecular assessment of the genus Prionitis J. Agardh (Halymeniaceae, Rhodophyta). Phycological Research, 49:251-262.

Wattier RM, Maggs CA, 2001. Intraspecific variation in seaweeds: the application of new tools and approaches. Advances in Botanical Research, 35:171-212.

Wilkes RF, McIvor LM, Guiry MD, 2005. Using rbcL sequence data to reassess the taxonomic position of some Grateloupia and Dermocorynus species (Halymeniaceae, Rhodophyta) from the north-eastern Atlantic. European Journal of Phycology, 40:53-60.

Wilkes RJ, Morabito M, Gargiulo GM, 2006. Taxonomic considerations of a foliose Grateloupia species from the Straits of Messina. Journal of Applied Phycology, 18:663-669.

Womersley HBS, 1994. The marine benthic flora of southern Australia. Rhodophyta. Part IIIA, Bangiophyceae and Florideophyceae (Acrochaetiales, Nemaliales, Gelidiales, Hildenbrandiales and Gigartinales sensu lato). Canberra, Australia: Australian Biological Resources Study, 508 pp.

Xia BM, 2004. [Marine algal flora of China, Volume 2, Rhodophyta No. 3, Gelidiales, Cryptonemiales, Hildenbrandiales]. (Flora algarum marinarum sinicarum, Tomus II Rhodophyta No. III Gelidiales, Cryptonemiales, Hildenbrandiales.) Beijing: Science Press, 203 pp.

Yamada Y, 1941. Notes on some Japanese algae IX. Scientific Papers of the Institute of Algological Research, Faculty of Science, Hokkaido Imperial University, 2:195-215.

Yoshida T, 1998. Marine algae of Japan. Tokyo, Japan: Uchida Rokakuho Publishing Company, 25 + 1222 pp.

Yoshida T, Nakajima Y, Nakata Y, 1990. Check-list of marine algae of Japan (revised in 1990). Japanese Journal of Phycology, 38:269-320.

Zuccarello GC, Sandercock B, West JA, 2002. Diversity within red algal species: variation in world-wide samples of Spyridia filamentosa (Ceramiaceae) and Murayella periclados (Rhodomelaceae) using DNA markers and breeding studies. European Journal of Phycology, 37:403-417.

Zuccarello GC, West JA, 2002. Biogeography of the Bostrychia calliptera/B. pinnata complex (Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid DNA markers. Phycologia, 41:49-60.

Links to Websites

Top of page
WebsiteURLComment
ABC News (Australian Broadcasting Corporation), 2008. Japanese marine pest spreading around Tasmaniahttp://www.abc.net.au/news/stories/2008/05/08/2238550.htm
AlgaeBasehttp://www.algaebase.org
Canadian Inventory of Invasive Specieshttp://www.cwf-fcf.org/en/resources/encyclopedias/invasive-species/
CIESMhttp://www.ciesm.org/atlas/
Global Compendium of Weedshttp://www.hear.org/gcw/
Global Marine Species Assessment (IUCN/CI)http://www.sci.odu.edu/gmsa/
Gulf of Maine Census-Invasiveshttp://research.usm.maine.edu/gulfofmaine-census/education/tools-resources/overviews/invasives
IUCN, the International Union for Conservation of Naturehttp://www.iucnredlist.org
Marine Invasive Species in Penobscot Bay, Mainehttp://www.penbay.org/invasives.html
MIT Sea Grant: Center for Coastal Resourceshttp://massbay.mit.edu/exoticspecies
MIT Sea Grant: Introduced species descriptionshttp://mit.edu/exoticspecies/exoticmaps/despriptions_intro.html
NIMPIS 2011http://www.marinepests.gov.au/nimpisBalanus improvisus general information, National Introduced Marine Pest Information System,
Northeast Aquatic Nuisance Species Panelhttp://northeastans.org./pet/what.html
Northeast Marine Introduced Species (NEMIS)http://nemis.mit.edu/
Salem Sound Coastwatchhttp://www.salemsound.org
Smithsonian Environmental Research Center Marine Invasion Research Laboratoryhttp://www.serc.edu/labs/marine-invasions/databases/index.jsp
State of the environment, Tasmaniahttp://soer.justice.tas.gov.au/2009/table 432/index.php
University of Connecticut Sea Granthttp://www.seagrant.uconn.edu/LISINV.HTM:
USGS-Woods Hole Science Center-Marine Nuisance Species-Didemnumhttp://woodshole.er.usgs.gov/project-pages/stellwagen/didemnum/

Contributors

Top 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 Maps

Top of page
You can pan and zoom the map
Save map