Gracilaria vermiculophylla

Invasion History

First Non-native North American Tidal Record: 1979 First Non-native West Coast Tidal Record: 1979 First Non-native East/Gulf Coast Tidal Record: 1998

General Invasion History:

Gracilaria vermiculophylla is native to the Northwest Pacific, including the coasts of Japan, Korea, China, and Vietnam. It was first described from Hokkaido, Japan in 1956, by H. Ohmi (Rueness 2005; Guiry and Guiry 2016). Agarophyton species are widely cultured as a source of agar (Israel et al. 1999; Rueness 2005; Hommersand and Freshwater 2009) and there are a large number of studies reporting their physiology and growth characteristics. Species of the genera Gracilaria and Gracilariopsis are extraordinarily difficult to identify morphologically and molecular analyses are resulting in extensive revisions of their taxonomy and distribution (Gurgel and Frederiq 2004; Bellorin et al. 2004; Rueness 2005; Saunders 2009). Since 2000, G. vermiculophylla has been identified from the Eastern Pacific, near Ensenada, Mexico (Bellorin et. al. 2004); Elkhorn Slough, California (Rueness 2005); and British Columbia (Saunders 2009). In the Eastern Atlantic, it is known from Sweden to Spain (Rueness 2005), and in the Western Atlantic it ranges from Georgia to New Hampshire (Gurgel and Frederiq 2004; Rueness 2005; Tyler et al. 2005; Nettleton et al. 2013). Some of the invasion sites in Europe were near areas of Magallana gigas (Pacific Oyster) cultivation (Rueness 2005). The vast majority of introduced populations have genetic signatures similar to those of plants from northwest Japan, indicating their probable transport with Pacific Oysters (Crassostrea gigas) from that region. Secondary transport by currents, boat fouling, and ballast water has resulted in secondary introductions and genetic mixing (Krueger-Hadfield et al. 2017).

North American Invasion History:

Invasion History on the West Coast:

The full range of Gracilaria vermiculophylla on the West Coast of North America is unknown, as is the date of introduction, owing to confusion with G. pacifica and other similar species (Aguilar-Rosas et al. 2014; Kathy Ann Miller, personal communication). It was first reported from specimens collected in 1979 in Ensenada, Mexico and identified by molecular methods (Bellorin et al. 2004). The first specimens from US waters were collected in Elkhorn Slough, California in 1994 (Goff et al. 1994, cited by Bellorin 2004; Rueness 2005). RNA sequences were found to be nearly identical with Japanese G. vermiculophylla (Rueness 2005). In 2006-2008, specimens were collected at Bamfield and Courtenay on Vancouver Island, and at Port Moody on the British Columbia mainland near Vancouver, again identified through molecular methods (Saunders 2009). Additional collections were made in 2013-2015 from Tomales Bay, Bodega Bay, and Puget Sound and identified as G. vermiculophylla (Krueger-Hadfield et al. 2017). Possible vectors of introduction to the West Coast include hull fouling, ballast water, and Pacific Oyster transplants.

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Invasion History on the East Coast:

Geacilaira vermiculophylla was probably introduced to the Atlantic Coast of North America some time before the year 2000. To date, the earliest reported collection is from 1998 at Hog Island Bay (identified as ‘G. aff. tenuistipitata) on the Atlantic Coast of Virginia (Gurgel and Frederiq 2004). In Hog Island Bay, just north of the mouth of the Chesapeake Bay, G. vermiculophylla was collected in 1999 (Gurgel and Frederiq 2004). Large blooms of Gracilaria spp had been observed in Hog Island Bay for some years previously (Tyler et al. 2005; Thomsen et al. 2005). In 2000, in Masonboro Sound, North Carolina an unidentified Gracilaria sp. was reported fouling nets and covering intertidal mudflats. By 2002, this alga was causing problems in power plants in the Cape Fear estuary and was distributed over a wide salinity range (Thompson 2002 personal communication). Reports of G. vermiculophylla fouling fishing gear were also widespread (Freshwater et al. 2006). By 2004, it ranged from the south side of Cape Fear (Brunswick County) to Beaufort and Bogue Sound, Carteret County, NC (Freshwater et al. 2006). The vectors of introduction to this region are not clear. Few transplants of Pacific oysters (C. gigas) were made in this area. During World War II, extensive aquaculture of Graciliaria sp. for agar was undertaken in North Carolina, but the cultured seaweed was presumed to be a native species, recently described as G. hummi, (Hommersand and Freshwater 2009). Deliberate transplants of G. vermiculophylla from Asian waters were unlikely under wartime conditions. This alga could have been introduced by ship fouling or ballast water, sometime after the war, and unrecognized due to its similarity with Gracilaria tikvahiae and Gracilariopsis longissima (‘Gracilaria verrucosa’). However, G. vermiculophylla gametes survive only briefly in the water column, and adult plants are rare in hull fouling. Alternatively, it could have been introduced with some of the scattered official or unofficial and unsuccessful plantings of Pacific Oysters (Crassostrea gigas)on the East Coast in the 1950s-1970s (Krueger-Hadfield et al. 2017). Genetic analyses suggest that G. vermiculophylla had two separate introductions during this period, one that stayed confined to southern New England, while the other spread north to Great Bay, New Hampshire, and south to Georgia (Krueger-Hadfield et al. 2017).Subsequent studies, using genetic methods, found that G. vermiculophylla has become widespread on the East Coast of North America, south to Wassaw Sound, Georgia (Byers et al. 2012; Kollars et al. 2015) and north as far as Great Bay, New Hampshire (Thomsen 2004; Thomsen et al. 2005; Thomsen and McGlathery 2006; MacIntyre et al. 2011; Nettleton et al. 2013). It was found to be abundant in the York River, Virginia in 2007 (Johnson and Lipcius 2012) and elsewhere in the Chesapeake Bay (James Norris, 2005, personal communication). The extent of G. vermiculophylla’s growth in Chesapeake Bay, Delaware Bay, and other Northeastern US estuaries is unknown, owing to the need for molecular identification. The difficulty of identification also makes documentation of its spread difficult. Specimens in South Carolina and Georgia were collected in 2009, where mats of the alga covered mudflats that historically lacked macrophytes (Byers et al. 2012). In 2000-2003, G. vermiculophylla was collected along the southern Gulf of Maine, from Provincetown, Massachusetts to Dover, on Great Bay, New Hampshire (Nettleton et al. 2013).

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Invasion History Elsewhere in the World:

The earliest reported collection of Gracilaria vermiculophylla in Europe was in the Netherlands in 1980. Blooms of a red alga were observed in Oostvoornse Meer, a lagoon in the Rhine Delta near Rotterdam. Specimens taken in 1994 were identified as G. vermiculophylla by molecular methods (Rueness 2005; Stegenga and Karremans 2015). Another early collection was in 1985, in the Ria de Aveiro lagoon, Portugal (Abreu et al. 2011). As in North America, this invasion was initially unrecognized, because of its similarity to native species. By 2004, this seaweed was known from many coastal and estuarine sites from the Oslofjord, Norway to the Bahia a Coruna, Spain, and the Ria Formosa, Portugal (Ruenss 2005). It continued to spread to new areas, including Northern Ireland in 2012 (Nunn and Minchin 2013), and the Baltic Sea coasts of Denmark and Germany in 2003-2007 (Thomsen et al. 2007; Hammann et al. 2013). In 2006-2009, G. vermiculophylla was found in lagoons of the Po Delta and in the Venice Lagoon, on the northern Adriatic Sea (Sfriso et al. 2012; Munari et al. 2015). Gracilaria vermiculophylla has spread south from Europe to lagoons on the Atlantic coast of Morocco, where it was first collected in 2002 (Guillemin et al. 2008).