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Sargassum muticum
(wire weed)

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Datasheet

Sargassum muticum (wire weed)

Summary

  • Last modified
  • 19 November 2019
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Sargassum muticum
  • Preferred Common Name
  • wire weed
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Plantae
  •     Phylum: Phaeophyta
  •       Class: Phaeophyceae
  •         Order: Fucales
  • Summary of Invasiveness
  • S. muticum has successfully invaded temperate coastlines on the Pacific coast of North America and western coasts of Europe. Initial introductions to both regions are attributed to transport with oyster stock for...

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Identity

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Preferred Scientific Name

  • Sargassum muticum (Yendo) Fensholt, 1955

Preferred Common Name

  • wire weed

Other Scientific Names

  • Sargassum kjellmanianum sensu Okamura (in part)
  • Sargassum kjellmanianum f. muticum Yendo

International Common Names

  • English: japweed; strangle weed
  • French: sargasse Japonaise

Local Common Names

  • Germany: Japanischer Beerentang
  • Japan: tama-hahaki-moku
  • Netherlands: Japans bessenwier

Summary of Invasiveness

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S. muticum has successfully invaded temperate coastlines on the Pacific coast of North America and western coasts of Europe. Initial introductions to both regions are attributed to transport with oyster stock for aquaculture, but the species has since dispersed widely due to intrinsic characters including high growth rates, long life span, high fecundity, capacity for self-fertilization, and multiple dispersal mechanisms including germling settlement, peripatetic (“stone-walking”) plants and rafting or floating of entire plants or detached fragments (Eno et al., 1997; Strong et al., 2009). The latter can enable marginal dispersal of up to 50 km (Farnham et al., 1981) and possibly even 1000 km (Deysher and Norton, 1981). S. muticum is also known to foul or become entangled on vessels, which provides an additional mechanism for long distance dispersal. Once established, the annual shedding of branches facilitates persistence, as the perennial holdfast is more resilient to adverse environmental conditions.

Within its native range in Japan and China, S. muticum is one of thirty or more Sargassum species and is rather unobtrusive, growing only in the infralittoral fringe and to no more than about 1.5 m in length (Rueness, 1989; Ribera and Boudouresque, 1995). However, it can occupy a broader niche in its invaded range. For example, in Europe, it can be found from intertidal pools down to depths of 20 m, and can grow to more than 10 m in length (Ribera and Boudouresque, 1995).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Plantae
  •         Phylum: Phaeophyta
  •             Class: Phaeophyceae
  •                 Order: Fucales
  •                     Family: Sargassaceae
  •                         Genus: Sargassum
  •                             Species: Sargassum muticum

Notes on Taxonomy and Nomenclature

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The genusSargassum was erected by C Agardh (1820) and the type species is Sargassum bacciferum (Turner) C. Agardh (=Sargassum natans (Linnaeus) Gaillon). The genus is very large, with close to 850 species names currently listed in Algaebase (http://www.algaebase.org), of which around 350 are flagged as current (Guiry and Guiry, 2009). The genus is widely distributed in warm and temperate waters, especially in the Indo-west Pacific and Australia, and is most prolific in tropical-subtropical regions (Tseng et al., 1985; Womersley, 1987). J Agardh (1889) recognized five subgenera: Arthrophycus, Bactrophycus, Phyllotrichia, Sargassum and Schizophycus. The sub-genus Sargassum (“Eusargassum”) is most common in the tropical-subtropical regions, whereas the subgenera Phyllotrichia and Arthrophycus have their centres of distribution in southern Australian and Bactrophycus isnative only to the eastern Asiatic region (Tseng et al., 1985; Womersley, 1987).

Sargassum muticum was first described by Yendo (1907) as a form of Sargassum kjellmanianum, then raised to the rank of species by Fensholt (1955). S. kjellmanianum is now considered to be a synonym of Sargassum miyabei Yendo (Yoshida, 1978).

Description

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Thallus to 2 (-10) m tall, arising from a felty, fibrous discoid holdfast up to 1.5 cm in diameter; main axis usually solitary on the holdfast, upright, terete, 2-3 mm in diameter and up to 5 cm high, usually unbranched, sometimes once or twice branched toward the apex; lateral branches spirally arranged, repeatedly and alternately branched to form an intricate, bushy thallus; leaves linear-lanceolate on the basal portion of stipe, to 10 cm long, the margins toothed; leaves of the upper stipe narrow, often only 4 mm long, with the margins entire or toothed and no midribs; vesicles (pneumatocysts) spherical to obovoid, in clusters or single in leaf axils, with round or mucronate apices; receptacles terete, shortly stipitate, arising from the leaf axils, occasionally forked, 10-12 mm long and 1-2 mm in diameter, plants monoecious, male and female reproductive organs in separate conceptacles, but androgenous, with both sexes present in the same receptacles.

Descriptions and figures:
Yoshida (1983): 138, figs. 20-23
Lee and Yoo (1992): 141, fig. 5
Braun (2008): 254, fig. 101.11
 
Publications on S. muticum prior to 1990 are collated in Critchley et al. (1990).

Plant Type

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Perennial

Distribution

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Type locality: Itsumo, Wakayama Prefecture, Honshu, Japan (Yoshida, 1983).

Native to Japan, China and Korea; introduced to the Pacific coast of North America and western Europe. Now distributed on the western coast of North America, from southern southeast Alaska to Mexico, and in Europe on Atlantic coasts from Norway to Portugal, along the southern coast of England between Plymouth and Eastbourne, around the coast of Ireland, and at several locations within the Mediterranean Sea.
 
The subgenus Bactrophycus is considered to be a Pacific basin subgenus with an apparent centre of diversity in eastern Asia, but with species widely distributed through the western Pacific north of the tropics (Phillips, 1995). Phillips (1995) considers that the distribution of Bactrophycus suggests it to be a temperate subgenus, unable to populate subtropical to tropical areas, or possibly cross thermal boundaries to other temperate areas. The evidence quoted is the inability of S. muticum to have naturally invaded northern Pacific or Atlantic temperate regions, despite its establishment and spread as a nuisance weed in these regions when anthropogenically translocated.

Distribution Table

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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.

Last updated: 10 Jan 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Asia

ChinaPresent, WidespreadNativeYoshida (1983); Phillips (1995); Zhao FengJuan et al. (2008)
-ShandongPresent, WidespreadNativeZhao FengJuan et al. (2008)
JapanPresent, WidespreadNativePhillips (1995)
-HonshuPresent, WidespreadNativeYoshida (1983)
-KyushuPresent, WidespreadNativeYoshida (1983)
-ShikokuPresent, WidespreadNativeYoshida (1983)
South KoreaPresent, WidespreadNativeYoshida (1983); Lee and Yoo (1992); Phillips (1995)

Europe

BelgiumPresent, LocalizedIntroduced1999Wallentinus (2004)Zeebrugge, Oostende
DenmarkPresent, WidespreadIntroduced1984Christensen (1984); Thomsen et al. (2007)
FrancePresent, WidespreadIntroduced1976InvasiveGruet (1976); Verlaque (2001); Plouguerné et al. (2006)Found in Normandy, prompted by discovery in England
IrelandPresent, WidespreadIntroducedKraan (2008); Simkanin (2004)First reported: 1990s
ItalyPresent, LocalizedIntroducedInvasiveCuriel et al. (1998)Lagoon of Venice
NetherlandsPresent, WidespreadIntroduced1977InvasivePrud'homme van Reine (1977); Nienhuis (1982)
NorwayPresent, LocalizedIntroduced1989InvasiveRueness (1989)
PortugalPresent, WidespreadIntroduced1989InvasiveEngelen and Santos (2009); Monteiro et al. (2009)Northwest coast
SpainPresent, WidespreadIntroducedInvasiveFernández et al. (1990)First observed on Galician coast in 1986; First reported: 1980s
SwedenPresent, WidespreadIntroduced1987InvasiveKarlsson and Loo (1999)
United KingdomPresent, WidespreadIntroduced1971InvasiveFarnham et al. (1973); Harries et al. (2007)Hampshire; first record of attached Sargassum plants in Britain
-Channel IslandsPresent, LocalizedIntroduced1982InvasiveCritchley and Morrell (1982)Jersey (3 sites)

North America

CanadaPresentCABI (Undated)Present based on regional distribution.
-British ColumbiaPresent, WidespreadIntroduced1944InvasivePhillips (1995)
MexicoPresent, WidespreadIntroduced1973InvasiveEspinoza (1990)
United StatesPresentCABI (Undated)Present based on regional distribution.
-AlaskaPresentIntroducedScagel et al. (1993)
-CaliforniaPresent, WidespreadIntroduced1965InvasiveAbbott and Hollenberg (1976); Phillips (1995)
-HawaiiAbsent, Intercepted only1999Abbott and Huisman (2004)Oahu, single collection on barge towed from San Diego
-WashingtonPresent, WidespreadIntroducedInvasivePhillips (1995)

Sea Areas

Atlantic - NortheastPresent, WidespreadIntroduced1971Guiry and Guiry (2009)
Pacific - NortheastPresent, WidespreadIntroduced1944Guiry and Guiry (2009)
Pacific - NorthwestPresent, WidespreadNativeGuiry and Guiry (2009)

History of Introduction and Spread

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S. muticum was introduced to Puget Sound on the west coast of North America around the mid-twentieth century, apparently with consignments of the Japanese oyster Crassostrea gigas supplied to restock of oyster beds (Scagel, 1956; Abbott and Hollenberg, 1976). Herbarium specimens confirm its presence in British Columbia in 1944 (Jones, 1974). The species subsequently spread steadily southward and was reported from Humboldt County, California in 1945, then first observed on Santa Catalina Island in 1970, spreading rapidly during the following year to Orange and San Diego Countys (Abbott and Hollenberg, 1976). The first report of S. muticum in Mexico was in 1973 (Devinny, 1978), and it has since spread down the coast of Baja California (Espinoza, 1990). To the north, S. muticum is known from Prince of Wales Island in southern southeast Alaska (Elder, 2009).

The first attached plants of Sargassum found in Britain, identified as S. muticum, were found in early 1973 on a sheltered shore in the Bembridge lagoons, Hampshire (Farnham et al., 1973). Some thirty scattered plants were initially reported, but larger numbers of plants were subsequently found with some estimated to be at least 2 years old, putting introduction back to at least 1971 (Farnham, 1980). A drift plant found at Southsea in mid-1971 was also later identified to be S. muticum. By 1980 the distribution of this seaweed extended from Plymouth, in Devon, to Eastbourne, in Sussex, a distance of over 300 km (Farnham, 1980). Plants were found on the Channel Islands in 1982 (Critchley and Morrell, 1982), and in north Cornwall in 1991 and 1992 (Eno et al., 1997).
 
S. muticum is considered to have first colonized Ireland in the early to mid 1990s, was recorded in Strangford Lough, Northern Ireland in 1995 (Boaden, 1995), and has since spread all around the coastline colonizing County Donegal for the first time in 2006 (Kraan, 2008). The species was recorded in southwest Wales in 1997 (Eno et al., 1997) and in Scotland firstly in Loch Ryan in 2004, and since from the Isle of Cumbrae and Loch Fyne in the Firth of Clyde (Harries et al., 2007).
 
The discovery of S. muticum in England in the early 1970s prompted searches on the other side of the English Channel, and attached plants were found in Normandy (Greuet, 1976; Kopp, 1976; Cosson et al., 1977) and drift material near Boulogne and in the Netherlands (Compère, 1977; Prud’homme van Reine, 1977). The source of the S. muticum is suspected to have been with oysters imported for aquaculture to France from Japan, Korea and British Columbia from 1966 onward (Farnham, 1980). S. muticum now occurs all along the western coasts of France, from the region Vendee to the north of Normandy (Plouguerné et al., 2006) and was found in the Thau Lagoon on the Mediterranean coast of France in 1980 (Pérez et al., 1984; Verlaque, 2001) from where it has since spread along the Languedoc open coast (Knoeffler-Peguy et al., 1985). S. muticum was first observed in the Lagoon of Venice in 1992 and, by 1998, was found in densities of up to 70-80 plants/m2 (Curiel et al., 1998).
 
S. muticum was first recorded in the southwest Netherlands in 1980 (Nienhuis, 1982), and in northwestern Denmark in 1984 (Christensen, 1984) and now dominates the algal assemblage in waters shallower than 6 m in this area (Thomsen et al., 2007). It was recorded drifting in 1985 on the Swedish west coast, but first found attached in 1987 (Karlsson and Loo, 1999). S. muticum was found in Norway in 1988 (Rueness, 1989), subsequently spreading northward to Bergen by 1993 (Wallentinus, 1999), and in Belgium in 1999 (Wallentinus, 2004).
 
In Hawaii, S. muticum was found attached to the hull of a barge at the Campbell Industrial Park Harbour, near Pearl Harbour, Oahu, in December 1999, soon after the barge arrived after being towed from San Diego, California (Abbott and Huisman, 2004). Up until 2004, yearly checks had not found further specimens.
 
The rate of spread of S. muticum along the northwest American coast has been estimated at about 60 km/year (Farnham et al., 1981), along the English south coast about 30 km/year (Farnham et al., 1981) and in the northeast Atlantic at around 70 km per year (F Mineur, unpublished data cited in Engelen and Santos, 2009). In Ireland, the rate of spread within one bay was estimated to be 2-3 km/year, and along the coastline about 54 km/year (Kraan, 2008). In Denmark, after first colonizing Limfjorden, S. muticum spread from west to east at a rate of 15 to 17 km/year (Stæhr et al., 2000).

Risk of Introduction

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Temperate coastlines on the Atlantic coast of North America and across all oceans in the southern hemisphere would seem to provide receptive environments for S. muticum colonization. Although primary introductions to both North America and Europe are attributed to translocation with oyster stock, the species has been known to foul vessels, which presents a potential alternative vector for long distance transfer to these new regions. Temperatures across the tropics may be a barrier to transfer between hemispheres, but this cannot be guaranteed, and is not a barrier to trans-Atlantic translocation.

Habitat

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In Japan, the species grows in the lower intertidal to upper subtidal on rocks in sheltered locations protected from wave action (Yoshida, 1983). The habitat is similar along the Pacific coast of North America and in Europe, but the distribution can extend up to the mid-intertidal and down to depths of 20 m (Ribera and Boudouresque, 1995); locally abundant, often forming dense stands on rocks in quiet water in the lower intertidal to subtidal (3–5 m) (Abbott and Hollenberg, 1976). On exposed coasts S. muticum can be restricted to wave-protected tide pools and seems unable to develop in high hydrodynamic conditions (Engelen and Santos, 2009). In Denmark, S. muticum was among the most abundant algae at 0 to 4 m depths, and recorded to 8 m deep (Thomsen et al., 2007); in Sweden most populations occur at depths less than 6 m, but it has been recorded down to 14 m (Karlsson and Loo, 1999). Stable boulder substratum (>10 cm in diameter) can facilitate Sargassum abundance (Thomsen et al., 2006). In the Lagoon of Venice, the species is found on various substrata, including stones, wood, mooring lines and wharves (Curiel et al., 1998).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Littoral
Intertidal zone Secondary/tolerated habitat Harmful (pest or invasive)
Intertidal zone Secondary/tolerated habitat Natural
Brackish
Estuaries Secondary/tolerated habitat Harmful (pest or invasive)
Lagoons Secondary/tolerated habitat Harmful (pest or invasive)
Marine
Inshore marine Principal habitat Harmful (pest or invasive)
Inshore marine Principal habitat Natural

Biology and Ecology

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Genetics

In four native populations of S. muticum on the Shandong Peninsula in China, RAPD and ISSR markers indicated a low level of intrapopulation genetic diversity and high level of interpopulation genetic differentiation (Zhao et al., 2008).
 
The cytochrome oxidase I sequence of S. muticum was published in McDevit and Saunders (2009).
             
Reproductive Biology
 
S. muticum has a monophasic pseudo-perennial life history with annual lateral branches growing from a perennial holdfast and short main axis. Plants are monoecious, with male and female reproductive structures developing in separate conceptacles, but with both conceptacle types co-occurring in the same receptacles. Fertilized eggs germinate while within the mucilaginous substance surrounding the receptacle and develop tiny rhizoids, then are released as germlings after 1 to 3 days (Fletcher 1980, Norton 1981) which possibly increases the probability of survival (Yoshida, 1983; Engelen and Santos, 2009). Germling dispersal distance is low and germlings generally settle within 2-3 (-30) m of parent plants (Deysher and Norton, 1981; Kendrick and Walker, 1995; Andrew and Viejo, 1998).
 
Along with high growth rates of 2-4 cm per day (Lewey and Farnham, 1981; Nicholson et al., 1981), the high fecundity of S. muticum, together with monoecious receptacles, a perennial life history (Fensholt, 1955; Norton, 1976; Norton and Deysher, 1989), germling settlement, and the plants buoyancy and propensity to drift (Norton, 1976) when detached are intrinsic traits facilitating the invasive success of the species (Strong et al., 2009). Fertile branches cast off during summer months can float and survive for up to 3 months (Farnham et al., 1981).
 
Physiology and Phenology
 
The maturation period of S. muticum in its native range is winter to early summer (Yoshida, 1983). In European waters, the species also shows strong seasonality. In northern waters, there is rapid growth from May to July, after which it senesces at the time of maximum fertility (Wernberg et al., 2000). In the Mediterranean, branch growth starts in September-October with significant vegetative growth over winter leading to a canopy more than 3 m tall (Curiel et al., 1998). Branches are shed in June-July after receptacle maturity. A shorter period of growth and reproduction and longer period of dormancy has been observed at higher tidal levels (Fernández, 1999).
 
The pseudo-perennial life history of S. muticum, with annual growth then shedding of fertile branches, leads to annual variation in the apparent abundance, density and cover of the species. In Denmark, for example, mean cover varied from around 5%, in autumn and winter, to 25% in mid-summer (Thomsen et al., 2006).
 
In Baja California reproductive plants were found throughout the year but with marked seasonality in extent; maximum reproductive development occurs in late spring and early summer (May to July) and minimum in winter (December to March) (Aguilar-Rosas and Galindo, 1990). In Europe, receptacles generally develop on lateral branches in spring, and deteriorate at the end of summer or early autumn (Engelen and Santos, 2009). Brittany populations were mature only between May and September, corresponding to the period of highest measured seawater temperatures (Plouguerné et al., 2006). In England, Portugal, Japan and southern California, S. muticum has been found to expel eggs in synchronized pulses around spring tides, coinciding with new and full moons (Fletcher, 1980; Norton, 1981; Engelen et al., 2008).
 
Phenolic content of S. muticum in Brittany was maximal during the reproductive period which was hypothesized as providing maximum protection of the fertile receptacles from both grazing and solar radiation (Plouguerné et al., 2006).
 
Nutrition
 
The overall intensity and temporal variability of nutrient supply have been found to interact in their effects on growth of S. muticum (Incera et al., 2009), but the effect was not consistent between shores. In one location more plants grew in low intensity, high temporal variability conditions, while in another there were more plants in high intensity and low variability conditions. These differences were considered to possibly reflect intrinsic abiotic or biotic differences between the habitats that may affect settlement, dispersal and survivorship (Incera et al., 2009). Germling growth in culture is stimulated by nutrient enrichment (Steen, 2003).
 
Environmental Requirements
 
Where S. muticum occurs on the Pacific coast of North America water temperatures can range between a winter minimum of 1-3ºC in British Columbia to a summer maximum of 18oC in southern California (Farnham, 1980). Estuarine populations in Oregon tolerate salinities of 20ppt (Kjeldsen and Phinney, 1972). S. muticum germling growth increases over the range 5 to 25ºC (Norton, 1977a; Hales and Fletcher, 1989) and, although capable of growing at 7ºC, growth is much slower than at 17ºC (Steen, 2003).
 
Eno et al. (1997) state ideal conditions for growth to be 25ºC and 34 ppt salinity, but with ability to grow at temperatures of 10 to 30ºC and salinities of 6.4 to 34 ppt.Populations cannot be sustained for prolonged periods below 15 ppt due to the suppression of reproduction (Stæhr et al., 2000).
 
Development of erect thalli has been demonstrated in culture to be a genuine photoperiodic response with stipe differentiation suppressed under night break regimes (Hwang and Dring, 2002). Photoperiodic response has also been observed in the promotion of elongation of main branches under a short day, and suppression under long day regimes (Uchida et al., 1991).

Climate

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ClimateStatusDescriptionRemark
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
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 Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Depth (m b.s.l.) 0 6 Optimum 20 tolerated, can extend into low intertidal and mid-intertidal pools
Salinity (part per thousand) 34 Optimum 6.8 to 34 tolerated (Eno et al., 1997)
Water temperature (ºC temperature) 25 Optimum -1 to 30 tolerated. Sporelings survive 5-25 in culture (Farnham, 1980)

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Ampithoe mea Herbivore Whole plant not specific Norton and Benson, 1983
Dexamine spinosa Herbivore Whole plant not specific Strong et al., 2009
Lacuna variegata Herbivore Seedlings/Whole plant not specific Norton and Benson, 1983
Psammechinus miliaris Herbivore Whole plant not specific Pedersen et al., 2005

Notes on Natural Enemies

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Native herbivores, including sea urchins, gastropods and a sea hare (Critchley et al., 1986; Britton-Simmons, 2004; Monteiro et al., 2009), have been found to have a low food preference for invasive S. muticum compared to native macroalgae. A herbivore has only shown a preference for S. muticum in one study, the sea urchin Psammechinus miliaris in Denmark, and then the preference was only weak for the invasive species over the native Halidrys siliquosa (Pedersen et al., 2005). Field studies, also in Denmark, found that although grazing gastropods and urchins were common in S. muticum beds all year, there was no correlation between grazer and Sargassum abundance, suggesting that grazers do not control adult Sargassum (Thomsen et al., 2006). Low grazing is possibly a consequence of the relatively high levels of phenolic compounds in Sargassum (Monteiro et al., 2009).

Investigations on faunas inhabiting S. muticum in Washington, USA, identified an amphipod, Ampithoë mea, and a gastropod, Lacuna variegata, which grazed on the alga (Norton and Benson, 1983). Estimates based on the abundance of grazers on plants and their feeding rates suggested that in late summer, a period of slow growth, grazers could remove more tissue than was being formed. However, earlier in the year when growth was higher more tissue would be produced than removed by the grazers. Epilithic L. variegata can retard the colonization of S. muticum by consuming newly settled germlings (Norton and Benson, 1983).
 
Apart from herbivores, a second biotic pressure on macroalgae in temperate marine habitats is epiphyte overgrowth, which can reduce photosynthesis below the compensation point and decrease gas exchange (Strong et al., 2009). Studies on shallow subtidal populations of S. muticum in Northern Ireland found that herbivorous amphipod abundance was greater on the invasive than on native macroalgae, and ectocarpoid fouling was comparable on all plants (Strong et al., 2009). The combination of amphipod grazing and ectocarpoid fouling led to a rapid decline of both S. muticum and ectocarpoid biomass, and heavy ectocarpoid fouling also resulted in thalli loss from S. muticum stands. The overall effect was a thinning of the invasive population.

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

The effective dispersal range of germlings from fertile S. muticum plants is generally less than 5 m (Andrew and Viejo, 1998). However, detached thalli, with flotation assisted by the gas filled vesicles on the side branches, can be dispersed by currents and travel many kilometers along coastlines (Deysher and Norton, 1981; Engelen and Santos, 2009). Colonization at the destination can be facilitated by the release of germlings. A 2-year time lag has been observed between the first occurrence of drifting plants in a previously uncolonized area and the established of attached populations, with a further 2-year time lag before populations expand extensively (Karlsson and Loo, 1999).
 
Adult S. muticum plants are also reported to be able to disperse across sediments by peripatetic “stone-walking” when the buoyancy of the plant exceeds the weight of the anchoring stone (Critchley, 1981; Wallentinus, 1999; Strong et al., 2006). The plant and anchor then lift and are moved by wave, tide or other water currents.
 
Accidental Introduction
 
The initial introduction of S. muticum to both Pacific North America and Europe is attributed to accidental movement with oyster stock (Scagel, 1956; Eno et al., 1997), and importations of oysters from southern England to the Netherlands were found to have attached individuals of the plant (Critchley and Dijkema, 1984). The species has been known to be transported after entanglement of plants around the steering gear of vessels (Critchley et al., 1983), and as hull fouling (Abbott and Huisman, 2004). In Ireland S. muticum was often found in or near harbours, mooring areas, anchorage sites and pontoons, suggesting boats as a likely vector for both arrival in Ireland from the United Kingdom or France and further distribution in Irish waters (Kraan, 2008).
 

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Aquaculture Yes
Hitchhiker Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stock Yes
Floating vegetation and debris Yes
Ship hull fouling Yes Yes

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Positive and negative

Economic Impact

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S. muticum is considered a pest and fouling species which interferes with recreational and commercial use of waterways, particularly when it becomes detached and forms large floating masses (Farnham et al., 1981; Critchley et al., 1986; Engelen and Santos, 2009). The alga has been responsible for fouling fishing gear and boat propellers (causing boating accidents), and blocking intake pipes of aquaculture facilities (Ribera and Boudouresque, 1995; Kraan, 2008). It can also be a fouling organism on oyster beds, can ‘steal’ colonized oysters by rafting, and be a potential nuisance to commercial fisherman through fouling of nets and oyster ropes (Critchley, 1981; Critchley et al., 1986; Ribera and Boudouresque, 1995).

Environmental Impact

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Impact on Habitats

In the southern Wadden Sea, S. muticum has become a significant habitat forming species in shallow subtidal areas that had become unvegetated following the decline of the seagrass Zostera marina during the 1930s (Polte and Buschbaum, 2008). Similar habitat modification has been noted in Northern Ireland, where extensive colonization of unvegetated soft sediments has generated a new epibenthic habitat that, in turn, has modified resident infaunal assemblages (Strong et al., 2006). Stands of S. muticum also caused strong temperature stratification by cooling of the water just above the sediment, and heating a thin water layer associated with the canopy. High densities of S. muticum canrestrict water exchange with adjacent non-canopy areas, resulting in the stagnant water within the stands becoming extremely warm on sunny days (Strong et al., 2006).
 
Impact on Biodiversity

The potential effects of invasive S. muticum on seagrass beds has long been a concern, initially because of the observation that in British Columbia the invader occupied sheltered shallow habitats usually occupied by the seagrass Zostera marina (Dreuhl, 1973). The concern was subsequently discounted by studies that suggested that S. muticum required a solid substrate for attachment (North, 1973; Fletcher and Fletcher, 1975; Norton, 1977b) and small stones, gravel and sand were unsuitable (Thomsen et al., 2006). Den Hartog (1997) found that S. muticum could replace Z. marina in littoral pools with unconsolidated substratum, but was unable to invade closed Z. marina beds on soft substrata. However, on more sandy or gravelly substrata, and where beds were in decline as a consequence of normal bed dynamics, S. muticum could rapidly occupy available space (den Hartog, 1997). Investigations into the growth of S. muticum within Zostera beds in southern England found that the alga could colonize soft sediments, most likely by drifting fragments becoming trapped within the seagrass allowing settlement on the seagrass matrix in an otherwise unfavourable environment (Tweedley et al., 2008). Once settled, S. muticum may interfere with seagrass bed regeneration. Zostera germlings have not been found in S. muticum stands (den Hartog, 1997). S. muticum has also established in seagrass beds in Ireland (Kraan, 2008).

Studies in the subtidal have indicated significant effects of S. muticum on subtidal native assemblages through overgrowing and shading underlying species (Ambrose and Nelson, 1982; Critchley et al., 1986; Givernaud et al., 1991; Curiel et al., 1998; Stæhr et al., 2000; Britton-Simmons, 2004). S. muticum has been reported to prevent re-establishment of the giant kelp Macrocystis pyrifera (Ambrose and Nelson, 1982), to displace Halidrys siliquosa, and to reduce cover of Laminaria, Fucus and Codium species through competition for hard substrate and light (Stæhr et al., 2000). In British Columbia, high native diversity was found to facilitate invader recruitment of S. muticum but to decrease growth and/or survivorship (White and Shurin, 2007). In Washington State, S. muticum had a strongly negative indirect effect on a native sea urchin by reducing the abundance of its preferred food, a native kelp species (Britton-Simmons, 2004).
 
In Portugal, on the highly exposed southwestern coast, S. muticum develops in sheltered tide pools originally inhabited by Cystoseira humilis (Engelen et al., 2008). However, studies have generally found little, no, or variable impact of S. muticum on intertidal shore assemblages (De Wreede, 1983; 1996; Viejo, 1997; Sánchez and Fernández, 2005; Buschbaum et al., 2006; Harries et al., 2007; Olabarria et al., 2009). In Scotland, significant differences were found in the intertidal algal and faunal communities associated with S. muticum and native algae (Harries et al., 2007). Reduced abundance of the dominant native alga Dictyota dichotoma in areas dominated by Sargassum was attributed to competition for space or shading, and elevated, but less diverse, faunal abundance was suggested to be a result of increased detrital input. In Northern Ireland the influence of the species varied between sites, ranging from a strong perturbation to moderate enhancement of infaunal density (Strong et al., 2006). Overall, Harries et al. (2007) concluded that, although establishment of dense areas of S. muticum would cause ecological change, the changes were unlikely to constitute serious ecological degradation or result in significant loss of biodiversity.
 
Possible positive effects of S. muticum on biodiversity through habitat-forming are also indicated by Buschbaum et al. (2006), who found more than 60 species of epibiont associated with the species on islands in the North Sea (German Bight). Total and average species richness were similar on rocky and sandy shoes but, whereas on rocky shores the epibiota was similar on a native fucoid, on sandy shores the only native habitat-providing species supported a different and less diverse assemblage than the invader. In the southeastern North Sea, despite its successful dispersal and increasing densities, S. muticum had not replaced other indigenous macroalgae, nor is there evidence of negative impacts on native species (Buschbaum et al., 2006). On the contrary, S. muticum may provide a suitable habitat for native species, such as epiphytic red algae, which became rare following the disappearance of its previous habitat, the European oyster beds that were lost in the 1950s due to over-exploitation.
 
The mobile epifauna colonizing S. muticum in Spain was also found to be similar to that on native species (Viejo, 1999). Where Sargassum colonizes areas with previously low macroalgal abundance, the associated epiphytic and epifaunal communities can potentially boost secondary production through increased temporal and spatial availability of food for omnivorous fishes and decapods (Viejo, 1999). However, where S. muticum reduces the abundance of indigenous perennial algae, the annual loss of branches could have a negative effect on invertebrate abundance through seasonal reduction in plant biomass.
 
S. muticum functions as a significant habitat forming species in the Wadden Sea where seagrass habitat was lost in the 1930s, and presence is correlated with increased number of native snake pipefish, Entelurus aequoreus (Polte and Buschbaum, 2008). Snake pipefish have been considered a red list species in the Wadden Sea (Berg et al., 1996). This association of pipefish with S. muticum is attributed to higher zooplankton densities with the Sargassum beds, which serve as prey to the pipefish (Polte and Buschbaum, 2008). The complex structure of S. muticum may also provide shelter for the pipefish from predation (Polte and Busschbaum, 2008).
 
Algal drift (wrack) promotes an increase in the abundance of sandy beach macrofauna by providing a food source or shelter for small invertebrates (Rodil et al., 2008). Comparisons of macrofaunal assemblages in S. muticum and native algal wrack have demonstrated differences in composition and abundance, indicating that replacement of native wrack deposits by invasive wrack may have important effects on macrofaunal assemblages and ecosystem function on sandy beaches (Rodil et al., 2008).

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Abundant in its native range
  • Pioneering in disturbed areas
  • Long lived
  • Fast growing
  • Has high reproductive potential
  • Has high genetic variability
Impact outcomes
  • Ecosystem change/ habitat alteration
  • Infrastructure damage
  • Modification of hydrology
  • Modification of natural benthic communities
  • Modification of successional patterns
  • Negatively impacts aquaculture/fisheries
  • Reduced amenity values
  • Reduced native biodiversity
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
  • Transportation disruption
Impact mechanisms
  • Competition - monopolizing resources
  • Competition - shading
  • Fouling
  • Rapid growth
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Uses

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Economic Value

Sargassum spp. are a potential source of alginates and for the biosorption of heavy metals (Eno et al., 1997; Davis et al., 2004). In China S. muticum is used as a feed source for holothurian and abalone aquaculture (Zhao et al., 2008). However, after mechanical clearing trials in England, no use was found for the harvested Sargassum (Critchley et al., 1986; De Wreede, 1996).
 
Extracts of S. muticum have been shown to inhibit bacteria, diatoms, macroalgae, and fungi, and also barnacle settlement (Hellio et al., 2002; 2004; Plouguerné et al., 2008). A chloroform extract inhibited two bacteria, a microalgae and several fungal strains, leading to a conclusion that S. muticum could provide suitable compounds or templates for industrial anti-microfouling applications (Plouguerné et al., 2008).
 
The potential application of S. muticum extracts for antifouling has been further investigated (Bazes et al., 2009). After two months immersion fewer fouling organisms, and no barnacles or mussels, settled on a paint containing S. muticum extract than on one containing copper. The active compound was identified as most likely the fatty acid ester palmitic acid. However, palmitic acid is already commercially available and extracting the compound from Sargassum would be a more expensive process and therefore unlikely to be commercially viable (Bazes et al., 2009).
 
Environmental Services
 
Within its native range along the north coast of China, S. muticum is a dominant and ecologically important species that forms beds that act as nursery grounds for fish, shellfish and other marine organisms in the lower intertidal and upper subtidal (Tsukidate, 1984; Davis et al., 2004).
 
In Spain, S. muticum wrack has been demonstrated to be of trophic significance as an important food source to invertebrate consumers on sandy beaches (Rossi et al., 2009).

Uses List

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Animal feed, fodder, forage

  • Fodder/animal feed

Human food and beverage

  • Food additive

Materials

  • Pesticide

Similarities to Other Species/Conditions

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Identification of Sargassum species can be difficult due to both the large number of species and the plasticity of some morphological characters. The subgenera Bactrophycus and Arthrophycus differ to the other subgenera in having horizontally expanding, rather than vertical, leaves (Yoshida, 1983). Yoshida (1983) had difficulty in identifying clear differences between these two subgenera, so placed all species with horizontally expanding leaves distributed in the northern hemisphere in Bactrophycus and those in the southern hemisphere in Arthrophycus.

Keys to the species of the Sargassum subgenus Bactrophycus are provided by Yoshida (1983), Tseng et al. (1985) and Lee and Yoo (1992). Key characteristics of S. muticum are the spherical vesicles, discoid holdfast, short and erect main axis < 5 cm), spirally-arranged branches, and terete and simple receptacles.
 
In Japan and Korea it is suspected that early records of S. muticum may have been identified as S. kjellmannianum (=S. miyabei) (Yoshida, 1983; Lee and Yoo, 1992). The latter differs in having filamentous outgrowths from the holdfast, elliptical to fusiform apiculate vesicles, and being dioecious (Yoshida, 1983). The two species also differ in distribution with S. muticum inhabiting the southern, warmer coasts of Japan, and S. miyabei the cooler north (Yoshida, 1983).

Prevention and Control

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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.

Control

Cultural control and sanitary measures

Movement of oysters for aquaculture is a known vector for S. muticum and other macroalgal introductions and even visually clean shells can carry a high diversity of microscopic propagules (Mineur et al., 2007). Experiments have demonstrated that a short heat treatment, for example immersion for 3 s in 80-85oC seawater, has a lethal effect on macroalgal propagules and this could be included in oyster transfer protocols to reduce unintended species translocation (Mineur et al., 2007).
             
Physical/mechanical control
 
When first detected in the Solent in Britain, an attempt was made to eradicate S. muticum by hand picking (Farnham, 1980). This was subsequently deemed to be, at best, only an interim or palliative measure because of the high growth rates, immense reproductive output, and high regenerative ability of this species. Removal by trawling, cutting and suction has also been tried (Kraan, 2008). The costs of mechanical removal have been estimated to be approximately US $38 per wet weight tonne (Critchley et al., 1986; Schaffelke and Hewitt, 2007).
 
Biological control
 
Small germlings are consumed by herbivorous gastropods and amphipods, but this seems to have no restrictive effect on S. muticum (Kraan, 2008). The effect of herbivory on established plants also seems minimal (Norton and Benson, 1983; Monteiro et al., 2009; Strong et al., 2009).
 
Experimental studies on the effects of disturbance and propagule pressure on the invasion success of S. muticum found an interactive effect between these two factors (Britton-Simmons and Abbott, 2008). Grazing by urchins caused S. muticum to fail to establish when disturbances were very large and temporally abundant. However, at lower grazing intensities, the survivorship of Sargassum juveniles increased, in part because green urchins in the study do not consume adult S. muticum.
 
Chemical control
 
Chemical methods for eradicating S. muticum using herbicide have been tried but failed due to lack of selectivity and the large doses needed (Eno et al., 1997; Kraan, 2008).

References

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Links to Websites

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AlgaeBasehttp://www.algaebase.org
AquAlienshttp://aqualiens.tmbl.gu.se/english.html
Marine Life Information Network: Biology and Sensitivity Key Informationhttp://www.marlin.ac.uk
Massachusetts Office of Coastal Zone Management: Aquatic Invasive Species Programhttp://www.mass.gov/czm/invasives/
National Center for Biotechnology Informationhttp://www.ncbi.nlm.nih.gov/
OBIS: Ocean Biogeographic Information Systemhttp://www.iobis.org/Welcome.htm

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30/11/09 Original text by:

John Lewis, ES Link Services Pty Ltd Queensberry Place, North Melbourne, Vic. 3051, Australia

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