Bugula neritina

Invasion History

First Galapagos Record: 1924

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General Invasion History:

Bugula neritina was described by Linnaeus from Europe in 1758, from the Mediterranean Sea. The Bugula 'neritina', widely identified in fouling communities is a widespread species complex of unknown tropical-warm-temperate origin, now widespread and cryptogenic in equatorial regions. It has been introduced to higher-latitude and more isolated ocean regions including the coast of northern Europe (Ryland 1960), the southwest Atlantic (Marcus 1937; Orensanz et al. 2002), the northeast Pacific (Carlton 1979; Wonham and Carlton 2005), Hawai'i (Carlton and Eldredge 2009), and the southwest Pacific (Keough and Ross 1999; Cranfield et al. 1998). In the English Channel and Long Island Sound, it appeared first near thermal effluents and gradually spread to other habitats (Ryland 1960; Carlton, personal communication 2004; Ryland 2011). In both the northeast Pacific and northwest Atlantic, B. 'neritina' has been extending its range northward, reaching Coos Bay, Oregon by 1986 (Wonham and Carlton 2005, and the Gulf of Maine (Boston and Salem Harbors, Massachusetts), by 2000 (MIT Sea Grant 2004). 
 
Many shallow-water populations around the world (England, Hong Kong, Hawaii, Australia, California, North Carolina, Curacao) share a single cytochrome oxidase (COI) haplotype (S1, McGovern and Hellberg 2002; Mackie et al. 2006). In California, a presumably native form 'D' is primarily found in more open marine waters (3-12 m) than the S 'shallow' form (0-8 m). The two forms have differing bryostatins, COI haplotypes, and endosymbionts Mackie et al. 2006; Davidson and Haygood 1999). 

Invasion History in the Galapagos:

'Bugula neritina' was first reported by Hastings (1930), from specimens collected in 1924. These specimens were collected from Santiago, Floreana, and Isabela Islands, in non-harbor habitats.The identity of these bryozoans is uncertain. Banta and Redden reported B. neritina from Santiago, Santa Cruz, Isabela, and Floreana Islands. McCann et al. (2019) found only one colony. 'Bugula neritina' from Galapagos harbors have not been tested genetically, but are suspected to be the widely introduced form Haplotype S ( McCann et al. 2019).
 

Invasion history elsewhere in the world:

Bugula neritina was described from the Mediterranean, where we consider it cryptogenic. It was first reported in Atlantic Europe in 1959, in a heated dock in Swansea, Wales (Ryland 1960). It apparently disappeared from British waters in the 1960s, possibly because of severe winters or cool summers, but reappeared or was rediscovered by 2004 in several locations on the south coast of England (Arenas et al. 2006). By 2011 it was widespread on Britain's south coast and present further north in the Irish Sea, to Wales, Scotland, and Ireland (Ryland et al. 2011). Elsewhere in Europe, it was found in Costa Lugo, Spain, on the Bay of Biscay (1997, Cesar-Aderiz et al. 1997), and subsequently found in many locations from the Netherlands to Cadiz, Spain (Ryland et al. 2011). Bugula neritina has also been found in the Azores (Ryland et al. 2011) 
 
In the southwest Atlantic, B. neritina was reported from Santos, near Sao Paulo by 1937 (Marcus 1937). On the subtropical-temperate Atlantic Coast of South America, B. neritina is reported from lha Grande Bay in Rio de Janeiro State, Brazil to Cabo Blanco, Argentina (47 S) and Port William in the Falkland Islands (52 S) (Gappa 2000; Orensanz et al. 2002; Vieira et al. 2008; Ignacio et al. 2010). In the mid-South Atlantic, it has been found on the remote island of Tristan da Cunha (37 S) (Ryland et al. 2011). On the west coast of South America, it was widespread in Chile in 1982, ranging from Arica (18 S) to Aruaco (37 S) (Moyano 1982, cited by Castilla et al. 2005). Bugula ‘neritina’ is considered an introduction to the Galapagos Islands, where it may have been first found in 1924 (Banta 1991, cited by Carlton 2019; McCann et al. 2019). 
 
Bugula neritina has been introduced to Pacific Island harbors, including those in American Samoa (Coles et al. 2002) and Palau (Marnie Campbell and Chad Hewitt 2009, personal observations). It was introduced to Port Philip Bay, Victoria, Australia by 1881 (Keough and Ross 1999) and is now widespread in harbors on the Australian coast (Brock 1983; Keough and Ross 1999; Wyatt et al. 2005; Mackie et al. 2006). In New Zealand, the first definite collection was at Wellington on the Cook Straits (1949, Ralph and Hurley 1952, cited by Gordon and Matawari 1992), but it is now widespread in New Zealand ports (Gordon and Matawari 1992).

Description

Colonies of Bugula neritina form bushy tufts 100 mm or more in height. The tips of the branches show slight spiral growth, and the bases consist of two parallel series of zooids (bifurcation type 4 of Ryland 1960, Hayward and Ryland 1998). The zooecia (zooids) are large, 600–800 µm, narrowing proximally. Spines are absent, but the distal margin forms an angular projection. This bryozoan has no avicularia. The polyps have 23–24 tentacles. The ooecia are attached to inner distal angles of the zooids, obliquely to the angle of the branch, and resemble 'miniature snail shells' (Hayward and Ryland 1998), and 'seem to form a series of small beads along the branches' (Osburn 1950). Colony color is 'purplish brown', or 'dark reddish purple' and translucent brown when preserved. The developing embryos are brown, and reach ~250 µm in diameter. The ancestrula is symmetrical, with a pedestal-like base, and lacks spines or rootlets. This description is based on information from Osburn (1940), Maturo (1957), Ryland (1960), Gordon and Mawatari (1992), Hayward and Ryland (1998) and Winston and Hayward (2012).

Bugula neritina constitutes a widespread species complex of forms which can only be distinguished by molecular methods. At least three cryptic species are present, designated as 'Type S' (shallow-water, cosmopolitan), ‘Type D’ (open water, California, presumed native), and a ‘North Atlantic lineage’ (Connecticut and Delaware) (Davidson and Haygood 1999; McGovern and Hellberg 2003; Mackie et al. 2006). A recent analysis (Fehlman-Ale et al. 2014) supports this general picture, but found haplotype N, the 'Northwest Atlantic genotype' occurring in Queensland, Australia, and central California).

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Taxonomy

Ecology

General:

Life History- Bugula neritina is a bush-like, calcified bryozoan, composed of many individual zooids. The zooids feed by extending the ciliated tentacles of the lophophore as a funnel, creating a current, and driving food particles into their mouths. The food is guided along the tentacles and through the pharynx by the cilia. Larger food particles can be moved or captured by flicking or contracting the tentacles. The zooids are hermaphroditic and produce large yolky eggs that hatch into lecithotrophic larvae, which are planktonic for short periods (less than 1 day). Larvae settle on a substrate and metamorphose into the first zooid of a colony, an ancestrula (Barnes 1983).

Ecology- Bugula neritina attaches to stones, wood, pilings, floats, buoys, ship hulls, seaweed, seagrasses, oysters, other bryozoans, and other hard substrates (Ryland 1965; Gordon and Mawatari 1992; Hayward and Ryland 1998; Ryland et al. 2011).

Food:

Phytoplankton, detritus

Trophic Status:

Suspension Feeder

SusFed

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Habitats

General Habitat	Grass Bed	None
General Habitat	Coarse Woody Debris	None
General Habitat	Oyster Reef	None
General Habitat	Marinas & Docks	None
General Habitat	Rocky	None
General Habitat	Vessel Hull	None
General Habitat	Coral reef	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)	2.2	Field, based on coldest site in geographical range, Boston MA (Zerebecki and Sorte 2011); 9 C Experimental, Japan (Kitamura and Hirayama 1984)
Maximum Temperature (ºC)	30	Experimental, Japan (Kitamura and Hirayama 1984). Temperature tolerances vary with acclimation and geographical location. For B. neritina, from Lynn Harbor MA, acclimated at 17 C, the median lethal 24 h temperature (LT50) was 26.4 C, but significantly lower (24.4) for this species from Bodega Bay CA (Sorte et al. 2013).
Minimum Salinity (‰)	18	Field observations, Italian coastal lagoons (Occhipinti Ambrogi and D'Hondt 1981).
Maximum Salinity (‰)	40	Field salinity (Shark Bay, Western Australia) (Wyatt et al. 2005)
Minimum Duration	0	Larval period (Wendt 2000)
Maximum Duration	0.5	Larval period (Wendt 2000)
Maximum Height (mm)	98	New Zealand, Gordon and Mawatari 1992
Broad Temperature Range	None	Warm temperate-Tropical
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

Economic Impacts 

Shipping, Industry- Bugula 'neritina' is a frequent fouling organism and has been found on fixed structures, ship hulls, in ships' internal water systems, and in power plants using seawater in warm waters worldwide (Ryland 1971). Bugula 'neritina' collected in Botany Bay, Australia, proved highly resistant as larvae and adults to dissolved copper, an active agent in many antifouling paints, and therefore have the potential to foul coated hulls (Piola and Johnston 2006).

Fisheries- Bugula 'neritina' has fouled aquaculture nets and cages (Hodson et al. 1997). This bryozoan also contributed to fouling which slowed the growth of cultured mussels (Perna perna) in Brazil (de Sá et al. 2007).

Human Health- Bugula 'neritina' has a positive economic impact, as a source of bryostatins, potential anticancer compounds (Davidson and Haygood 1999). The extracted, purified compounds can be worth $380,000 per pound (Lovell et al. 2008).

Ecological Impacts 

Competition- Bugula 'neritina' in subtropical-tropical waters worldwide is a major competitor in the fouling community (Sutherland and Karlson 1977; Winston 1982). The tolerance of Bugula 'neritina' to copper-based antifouling paints (Piola and Johnston 2006) may give it a competitive advantage over more sensitive species, such as Schizoporella errata and Tricellaria occidentalis (Piola and Johnston 2006). Bugula neritina was one of several invasive fouling species which showed increased growth (zooid number) at temperatures 3.5 and 4.5 °C above the ambient temperature in Bodega Harbor (13.5 °C), while the native colonial tunicate Distaplia occidentalis showed reduced survival (Sorte et al. 2010). Bugula 'neritina' was one of a group of seven non-native species in Bodega Harbor, most of which were rare or absent in 1970–1971, but were among the eight most abundant species in 2006. Spawning periods and the abundance of species in this group appeared to be favored by a 1 °C increase in average temperatures at this site over a 30-year period (Sorte and Stachowicz 2011).

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