Undaria pinnatifida

Invasion History

First Non-native North American Tidal Record: 2000
First Non-native West Coast Tidal Record: 2000
First Non-native East/Gulf Coast Tidal Record:

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General Invasion History:

Undaria pinnatifida is native to the Northwest Pacific, from Vladivostok, Russia (Golikov et al. 1976), southward on the coasts of Japan, Korea, China, and Hong Kong (Huang 2001; Guiry and Guiry 2016). In its native range, it is widely cultivated as a food plant (Floc'h et al. 1996; Silva et al. 2002). It has been widely introduced around the globe, including Atlantic France where it is cultured as food (1st record 1983, Floc'h et al. 1996); the Mediterranean coast of France where it was introduced accidentally with Pacific Oysters from Japan (1st record 1971, Verlaque 2001); and several other regions, including New Zealand (1st record 1987, Hay and Luckens 1987); Australia (1st record 1988, Valentine 2003); Argentina (1st record 1992, Casas et al. 2004); and California (1st record 2000, Silva et al. 2002). Its occurrence in small yacht harbors, marinas, and fishing ports as well as commercial shipping harbors suggests that hull fouling is the most frequent vector (Hay 1990; Fletcher and Farrell 1999). Ballast water transport of spores is also possible – Undaria pinnatifida's spores survive up to 14 days in light, however their survival in darkness is not known.

North American Invasion History:

Invasion History on the West Coast:

Undaria pinnatifida was first found on the West coast of North America at Cabrillo Beach, Los Angeles, California in 2000 (Silva et al. 2002). In the same year, it was found in Santa Barbara Harbor and in Channel Islands Harbor and Port Hueneme, Oxnard (Silva et al. 2002). In 2001, it was found on floating docks in Monterey Bay (Silva et al. 2002). Attempts were made to control the alga, by divers physically removing fronds (Monterey Bay National Marine Sanctuary 2009). However, in June 2009, U. pinnatifida was detected at Pillar Point in Half Moon Bay and the San Francisco Marina and South Beach Harbor in San Francisco Bay (Zabin et al. 2009). By 2012, it was seen at additional locations in the Bay, including Fort Mason, Pier 39, Fisherman’s Wharf, and along the Hyde Street pier in San Francisco (Fimrite 2012). The Smithsonian Environmental Research Center's Tiburon group has been sponsoring monitoring and removal efforts. Undaria pinnatifida has continued to spread to new harbors and bays in California, including San Diego Bay in 2004 (Miller 2009, cited by Kaplanis et al. 2016); Morro Bay in 2009; Oceanside Harbor in 2013; Mission Bay in 2014; and Santa Cruz Harbor in 2014 (Kaplanis et al. 2016).

Invasion History Elsewhere in the World:

The first documented introduction of Undaria pinnatifida was discovered in the Thau Lagoon, Sete, France, on the Mediterranean Sea, an estuary extensively used for oyster culture (Grizel 1991; Verlaque 2001). In the Mediterranean Sea, U. pinnatifida has become established in the Lagoon of Venice (Adriatic Sea) (Occhipinti Ambrogi 2000), and the Gulf of Taranto, Italy (Cecere et al. 2000). On the Atlantic Cost, U. pinnatifida was deliberately planted for attempted cultivation near the Isle de Groix, the Isle of Ushant, and St. Malo (Brittany) in 1983, by IFREMER (French Institute for Exploration of the Seas), and persisted around cultivation sites after cultivation was abandoned (Castric-Fey et al. 1993; Floc'h et al. 1996). From the Brittany peninsula, U. pinnatifida spread north and south in a spotty fashion. It became established in Galicia, Spain, on the Atlantic Coast by 1988 (Fletcher and Farrell 1999; Peteiro 2008), but was not reported from the Bay of Biscay (Gijón, Asturias, Spain) until 1995 (Peteiro 2008). In 2007, it was discovered in Northern Portugal (Araujo et al. 2009). To the north, it was first found in Port Hamble on the Isle of Wight, England, on the English Channel in 1994 (Fletcher and Farrell 1999), and spread east to the Zeebrugge, Belgium, on the North Sea, and Yeserke, Netherlands, on the Oosterschelde Estuary in 1999 (Wolff 2005; Kerckhof et al. 2007). In harbor surveys in the English Channel in 2004, it occurred from Brighton in the East to Torquay (Cornwall) in the west (Arenas et al. 2006). In 2012, it was found in Belfast Lough, Northern Ireland, where it is now established, and was considered likely to spread northward (Minchin and Nunn 2014).

In the Southern Hemisphere, U. pinnatifida was first discovered in 1987 in Wellington Harbor, New Zealand (Hay and Luckens 1987), on the North Island. By 2004, it occurred in Waitemata Harbor (Russell et al. 2008), near the north end of the North Island, and at Stewart Island, at the south end of the South Island (Nelson 1999). In 2006, U. pinnatifida was discovered on the mooring ropes of a fishing boat off the Sub-Antarctic Snares Islands (48.03°S). Eradication was considered, but found to be not feasible (Invasive Species Specialist Group 2009; Global Invasive Species Program 2009). In another group of New Zealand Sub-Antarctic Islands, the Chatham Islands, the kelp was successfully eradicated from a sunken ship hull 2 km offshore, using heat treatment (Wotton et al. 2004). In 1988, this seaweed was found in Triabunna, Tasmania (Valentine 2003), and has become widespread on the east coast of the island (Valentine and Johnson 2005). In 1996, it was first discovered on continental Australia, at Point Wilson in Port Phillip Bay, Victoria (Currie et al. 1999; Lewis 1999). We are not aware of continental Australian records outside of Port Phillip Bay. Undaria pinnatifida has also invaded the Southwest Atlantic. In 1992, it was found in Gulfo Nuevo, Patagonia, Argentina (Casas et al. 2004). By 2000, it had colonized most of the Gulf (Casas et al. 2008), and in 2005 it was found in Ria Deseado in southern Patagonia (47.75°S) (Martin and Cuevas 2006). Currently, in Patagonia, it ranges from 38 to 48°S (Casas et al. 2004; Pereyra et al. 2014; Raffo et al. 2014; Schwindt et al. 2014).

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Description

The macroscopic form of Undaria pinnatifida is a diploid sporophyte consisting of a holdfast, stipe (stem), and blade. The fronds are usually 1000 - 2000 mm long (sometimes 3000 mm), with the blade drawn into many lobes about 500-800 mm long. The blade has a 1-2 cm midrib running along its length, and is golden-brown in color, while the rib is paler. The blade is dotted with small white structures called cryptostomidia. The lower parts of the frond are extended into wings (pinnae). The holdfast spreads at its base, with dichotomous branches. As the frond matures, spirals of ruffled structure develop along the stipe above the holdfast. These are sporophylls and along the edges of the ruffles are fertile areas called sori, which are groups of sporangia, where diploid nuclei divide into haploid spores. The haploid gametophytes are microscopic and filamentous. The macroscopic stage (the sporophyte) is usually present through the late winter to early summer months and a microscopic stage (the gametophyte) is present during the colder months. This description is based on: Perez et al. 1981, Lewis 1999, Silva et al. 2002, Pereyra et al. 2014, Guiry 2016, and Guiry and Guiry 2016.

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Taxonomy

Ecology

General:

The fronds of Undaria pinnatifida are diploid sporophytes. Haploid spores are produced in sori, clusters of sporangia, located on frilled structures called sporophylls, which are wing-like extensions of the stipe. The male gametophytes release spores, which typically swim for 5-6 hours (Silva et al. 2002), but remain viable in suspension with light for up to 14 days (Forrest et al. 2000). Each spore has two flagella, which fertilize eggs retained in the female gametophytes. The fertilized eggs then develop into embryonic sporophytes (Perez et al. 1981; Hay and Luckens 1987; Silva et al. 2002). In Japan, the sporophytes germinate in late-summer and autumn, grow through winter and spring, and mature, shedding spores in mid-summer (Hay and Luckens 1987). Seasonal cycles vary among regions. In New Zealand, sporelings occurred throughout the year, but most adult sporophytes shed spores and degenerated in late summer and early autumn (Hay and Villouta 1993).

Undaria pinnatifida grows well in cold-temperate to subtropical waters. In Japan, it occurs in waters where surface temperatures drop to 0°C, and also where summer temperatures reach 27°C (Funahashi, 1973, cited by Hay 1990). Recruitment of sporophytes was best at 13°C and lower at 17 and 21°C (Thornber et al. 2014). It grows at salinities of 20-37 PSU, but is rare at the lower end to this range (Silva et al. 2002). It grows from lower subtidal to depths of 5-15 m in Russia and Japan (Golikov et al. 1976; Saito 1975, cited by Silva et al. 2002), but has been found growing as deep as 25 m off Catalina Island, California (Silva et al. 2002). The compensation point of light intensity for photosynthesis (the minimum for growth) was 17.4 µE m-3s-1. Photosynthesis increased with light intensity up to 119.5 µE m-3s-1, and was saturated past that point. The optimum temperature for photosynthesis was 20°C and decreased sharply at higher temperatures (Choi et al. 2005). Undaria pinnatifida grows on rocky seabed habitats, but also on breakwater, piers, floats, oyster reefs, wood, bottles, ropes, and ship/boat hulls (Hay and Lukens 1987; Floc'h et al. 1996; Silva et al. 2002). It is grazed by herbivores, including sea-urchins, gastropods, and amphipods in New Zealand (Jiménez et al. 2015), and by the Kelp Crab Pugettia producta in California (Thornber et al. 2004).

Consumers:

Crabs (Pugettia producta)

Trophic Status:

Primary Producer

PrimProd

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Habitats

General Habitat	Rocky	None
General Habitat	Oyster Reef	None
General Habitat	Marinas & Docks	None
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Vertical Habitat	Epibenthic	None

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Life History

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	0	Field temperatures- Funashi 1973, cited by Hay 1990
Maximum Temperature (ºC)	27	Field temperatures- Funashi 1973, cited by Hay 1990. Gametophytes had poor survival at temperatures over 28 C (Choi et al. 2014). In New Zealnd, photosynthesis (quantum yield) sharply decreased at 25 C at low salinites (12 and 6 PSU) (Bollen et al. 2016).
Minimum Salinity (‰)	20	But rare below 27 PSU (Silva et al. 2002). However, New Zealand populations maintained moderate rates of photosynthesis at salinities as low as 6 and 12 PSU (Bollen et al. 2016).
Maximum Salinity (‰)	37	Mediterranean Sea salinity
Minimum Reproductive pH	7.2	Lowest tested (Leal et al. 2017)
Minimum Duration	0	Zoospores can settle immediately to form gametophytes (Forrest et al. 2000).
Maximum Duration	14	Zoospores maintained in light and suspension can still settle and form gametophytes after 14 days (Forrest et al. 2000). Survival in darkness is not known.
Minimum Length (mm)	500	Wellington Harbor, New Zealand (Hay and Villouta 1993, at maturity, less favorable environment)
Maximum Length (mm)	3,000	Perez et al. 1981; Lewis 1999; Silva et al. 2002; Pereyra et al. 2015).
Broad Temperature Range	None	Cold temperate-Warm temperate
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

In its native range in the Northwest Pacific, Undaria pinnatifida is a widely harvested and cultivated sea vegetable. It has invaded coastal waters in Europe, North America, South America, and New Zealand. It has been listed by the Invasive Species Specialist Group of the World Conservation Union (IUCN) as one of the '100 worst invasive species.' (Invasive Species Specialist Group 2016). However, both negative and positive ecological impacts have been reported from invaded areas (Petrocelli and Cecere 2015). Epstein and Smale (2017) argue that U. pinnatifida may not be a driver of environmental change, and can be managed as a potentially valuable species, creating new habitat and fisheries. However, they acknowledge that these outcomes depend on environmental context and that effective policies will depend on local research (Epstein and Smale 2017). 

Economic Impacts

Undaria pinnatifida (Wakame) is a commercially valuable food species, intensively cultivated in Asian waters. It is not regarded as a pest or invasive species in its native range. Global harvests since 2000 are 1.5-2 million tons per year (Pickering et al. 2007; Food and Agriculture Organization 2016). At least one attempt was made to cultivate it in Atlantic France (Floc'h et al. 1993). Web searches indicate that fresh Wakame is imported to the U.S. and is available in Asian markets, but we do not know whether the plants are viable or potentially could be planted by individuals.

On the other hand, U. pinnatifida also fouls equipment used in aquaculture. Undaria pinnatifida has proliferated on mussel aquaculture farms in New Zealand, with subsequent spread to adjacent reefs (James and Shears 2016). It grows densely in marinas and docking areas (Fletcher and Farrell 1999; Farrell and Fletcher 2006; Sfriso and Facca 2013). In New Zealand, a risk assessment exercise concluded that U. pinnatifida posted moderate impacts to boating and aquaculture, but major risks to aesthetics and diving in high-value protected marine areas (Campbell and Hewitt 2013). Experimental and full-scale attempts to control this seaweed have been made in the Venice Lagoon, New Zealand, Tasmania, and California, intended to protect natural communities and fisheries. These involved divers in hand removal (Hewitt et al. 2005; Anderson 2006) or mechanical eradication (Curiel et al. 2001). In New Zealand, from 1997 to 2009, large-scale eradication efforts were conducted to protect areas of high natural value (e.g. Stewart Island) and donor port areas (e.g. Bluff Harbour), to prevent spread to Sub-Antarctic islands. This included removal of sporophytes from vessels, piers, and other artificial structures (Hewitt et al. 2005; Forrest and Hopkins 2013). A successful eradication in the Chatham Islands, on the hull of a sunken ship, involving using divers to place boxes with heat elements and flatme torches against the hull, was successful, at a cost of ~$ 3 million NZ dollars (Wotton et al. 2004). Since the gametophyte and early sporophyte stages are microscopic, control by hand monitoring will require continuous monitoring and removal efforts (Curiel et al. 2001; Hewitt et al. 2005). In New Zealand, the cost of the control efforts and the continued spread of U. pinnatifida led to the abandonment of the control program (Forrest and Hopkins 2013).

Ecological Impacts

Competition- The invasion of U. pinnatifida in the Venice Lagoon is believed to have decreased abundance of native understory seaweeds (Curiel et al. 1998; Curiel et al. 2001). However, Raffo et al. (2009) did not find evidence of competition between native Macrocystis pyrifera and U. pinnatifida when examining growth and density of the two species in Cracker Bay, Patagonia. However, this could be due to examining an earlier phase of invasion (Raffo et al. 2009).

Habitat Change- Reported impacts of U. pinnatifida on habitat quality vary regionally among different ecosystems, and have been rated as positive, negative, or neutral (Petrocelli and Cecere 2015). In habitats dominated by native kelps, U. pinnatifida is smaller than some native kelps and can be seasonal, dying off after reproducing, which results in a regular loss of habitat cover (Arnold et al. 2015). Suarez et al. (2017) found that morphology of seaweeds was the major factor affecting diversity of epibiota, in comparisons of U. pinnatida versus native species, with more structuarly complex species favoring higher diversity. In Wellington Harbor, New Zealand, the invasion of U. pinnatifida altered invertebrate communities and increased sediment deposition (Battershill et al. 1998, cited by Schaffelke and Hewitt 2007). In Patagonia, the diversity of fauna associated with the holdfast of U. pinnatifida was decreased, compared to that of the native kelp Macocystis pyrifera (Raffo et al. 2009). In reef areas, off northern Patagonia, reefs with a low degree of relief, which were invaded by Undaria, had a low diversity of fishes compared to similar uninvaded reefs. Reefs with higher relief were not noticeably affected by an Undaria invasion, because Undaria tended to colonize only the lower portions of the reefs, leaving many refuge areas unaltered (Irigoyen et al. 2011a).

However, impacts of Undaria pinnatifida on seaweed diversity or benthic invertebrate assemblages were not detected in a rigorously designed survey (BACI, before-after-control-impact) in Lyttleton Harbor, New Zealand, possibly because canopy-forming species, providing similar structure were already present (Forrest et al. 2002). Experimental plots covered by Undaria had higher algal biodiversity and greater abundance of several invertebrates than sites from which Undaria was removed (Irigoyen et al. 2011b). Similarly, in the Mar Piccolo, Italy, the invasion of U. pinnatifida improved habitat quality in a heavily polluted lagoon with little attached vegetation, providing habitat or epifauna and spawning habitat for squid (Cecere et al. 2000).

Food/Prey- The effects of U. pinnatifida on grazers and food webs has been studied only in a few localities. Experimental studies in Tasmania, New Zealand, and Patagonia indicate that it is avoided by some grazers, but grazed heavily by others (Valentine and Johnson 2005; Teso et al. 2009; South et al. 2015). In southern New Zealand, U. pinnatifida, during its peak of abundance, doubled the biomass and primary productivity of the lower intertidal community (South et al. 2015). Experiments in England also support mixed preferences by grazers, and the absence of 'enemy release' due to reduced grazing or relaxation of chemical defenses (Mabey et al. 2022).

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Regional Impacts

P080	Monterey Bay		Economic Impact	Aesthetic
A 10-year program to control Undaria pinnatifida through hand removal by divers in the Monterey Bay National Marine Sanctuary has an allocation of $160,000. The motivation is to slow the spread of U. pinnatifida and protect native kelp communities (Anderson 2006; Davidson et al. 2015).
NEP-V	Northern California to Mid Channel Islands		Economic Impact	Aesthetic
A 10-year program to control Undaria pinnatifida through hand removal by divers in the Monterey Bay National Marine Sanctuary has an allocation of $160,000. The motivation is to slow the spread of U. pinnatifida and protect native kelp communities. Evidence for negative impacts in California is unclear, but the native kelp community is highly valued (Anderson 2006; Davidson et al. 2015).
NEP-VI	Pt. Conception to Southern Baja California		Ecological Impact	Competition
Off Todos Santos Islands, Baja California, Mexico. a marine heatwave favored the partial replacement of the dominent native kelp Macrosysts pyrifera by the non-native seaweeds Sargaasum horneri and *Undaria pyrifera (Félix-Loaiza et al. 2022).
CA	California		Economic Impact	Aesthetic
A 10-year program to control Undaria pinnatifida through hand removal by divers in the Monterey Bay National Marine Sanctuary has an allocation of $160,000. The motivation is to slow the spread of U. pinnatifida and protect native kelp communities. Evidence for negative impacts in California is unclear, but the native kelp community is highly valued (Anderson 2006; Davidson et al. 2015)., A 10-year program to control Undaria pinnatifida through hand removal by divers in the Monterey Bay National Marine Sanctuary has an allocation of $160,000. The motivation is to slow the spread of U. pinnatifida and protect native kelp communities (Anderson 2006; Davidson et al. 2015).

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