Botryllus schlosseri

Invasion History

General Invasion History:

The origin of Botryllus schlosseri is currently unknown. In the Northeast Atlantic, it ranges from Norway to the Mediterranean (Hayward and Ryland 1991; Rinkevich et al. 1995; Ben-Shlomo et al. 2001; Lejeusne et al. 2010). On the coast of Asia, it ranges from Peter the Great Bay, Russia to Hong Kong and southern China (Nishikawa 1991; Huang 2001). It is now widespread on temperate coasts on both sides of the North and South Atlantic and Pacific, and oceanic islands such as Bermuda, the Azores, and New Zealand. It is a common component of fouling communities and has likely been spread largely by shipping and aquaculture transfers. A recent genetic analysis indicates that 'B. schlosseri' is a complex of at least five cryptic species (A-E), but only one, clade A, had a widespread distribution in the Northeast and Northwest Atlantic, and Northeast Pacific. The other clades had restricted distributions in Europe (Bock et al. 2012). However, Yund et al. (2015) have identified at least one subclade which appears to be native to the Northwest Atlantic. This subclade is most genetically diverse in that region, and 9 of its 12 haplotypes are unique. The divergence between the prevailing Northwest Atlantic haplotype and those from European waters is too great to be accounted for by evolution (Yund et al. 2015). We cannot exclude the occurrence of European genotypes or cryptic species in East Coast waters, and so we will treat B. schlosseri as a single cryptogenic species. A recent analysis of Clade A (Nydam et al. 2017) suggests a Pacific origin for Clade A, with highest genetic diversity in specimens from the Northeast Pacific. However these populations are introduced (Carlton 1979). Northwest Pacific populations were not included in Nydam et al.'s (2017) study, and could be a possible source of Clade A.

North American Invasion History:

Invasion History on the West Coast:

Botryllus schlosseri was first collected on the West Coast at Mare Island Naval Yard, in San Francisco Bay, California in 1947 (Carlton 1979) and has since spread to the north and south through ship-fouling, and aquaculture transfers. It was reported in San Diego, CA in 1965 (Lambert and Lambert 1998), and reached Humboldt Bay, CA by the 1970s and Coos Bay, OR by 1978 (Boyd et al. 2002, Carlton 1989). In surveys conducted between 1994 and 2003 it was collected in 16 embayments between San Francisco and Mexico (Lambert and Lambert 1998; Wasson et al. 2001; Cohen et al. 2002; Fairey et al. 2002; deRivera et al. 2005). In 2013, it was also reported in Morro Bay, CA (Smithsonian surveys). Further south, it was reported from Ensenada, Mexico in 2000 (Lambert and Lambert 2003) and Bahia San Quintin, Mexico in 2005 (Rodriguez and Ibarra-Obando 2008). It has been found in several areas north of San Francisco Bay including Tomales Bay (in 2001, Fairey et al. 2002), Bodega Harbor (in 1997, Stoner et al. 2002), San Juan Islands, WA (in the late 1960s or early 1970s, Lambert et al. 1987 cited in Lambert and Lambert, 1998), Vancouver Island, British Columbia (prior to 1998; Lambert and Lambert, 1998) and at its current northern limit, Sitka, AK in 2000 (Ruiz et al., unpublished data).  Zwahleb et al. (2022), consider records from Puget Sound before the 1990s to be doubtful, but found this tunicate tp be increasingly abundant after 1999.  Puget Sound populations have a low genetic diversity, indicative of recnet establishment (Zwahleb et al. (2022),

Invasion History on the East Coast:

Recent genetic analysis suggests that Botryllus schlosseri includes genotypes native to the Northwest Atlantic (Yund et al. 2015), although the presence of genotypes or cryptic species from elsewhere in the world cannot be excluded at this time. Consequently, we will treat it as a cryptogenic species in the Gulf of Mexico and and most of the East Coast. It should be noted, though that it has apparently recently expanded its range into Atlantic Canada, most likely by human transport, so that we will treat it as introduced in those bioregions (NA-ET1, NA-S2, NA-S3, comprising the Atlantic coast of Newfoundland and Nova Scotia, and the Gulf of St. Lawrence).

While we consider B. schlosseri cryptogenic in the Gulf of Maine and southward, it apparently a recent invader on the Atlantic coast of the Maritime Provinces, and the Gulf of St. Lawrence. Many of these populations have been identified as having Northwest Atlantic genotypes (Yund et al. 2015), so they may have been introduced from harbors futher south along the East Coast. Botryllus schlosseri is now abundant on the Atlantic coast of Nova Scotia at Lunenburg, and other locations, and in the Bras d'Or Lakes estuary on Cape Breton Island (Locke et al. 200; Sephton et al. 2011). It was collected in the Gulf of St. Lawrence by Hooper (cited by Callahan et al. 2010), on the west coast of Newfoundland in 1975 , but its occurrence in the Gulf was not widely published until it was found on Prince Edward Island in the Gulf of St. Lawrence by 2001 (Locke et al. 2007). In 2011, it was found on floating docks in Conception Bay, on the outer Atlantic coast of Newfoundland, but was removed as a control measure (Robinson 12/8/2011).

Botryllus schlosseri was first recorded in North America in about 1838 simultaneously from both Boston, Massachusetts (at a meeting of January 17, 1838, and thus almost certainly based upon 1837 collections; Couthouy 1838), and New York City (in a publication dated January 1, 1839, and thus based upon material collected no later than 1838) (James T. Carlton, personal communication). It was later described as B. gouldii from New York circa 1870 (Verrill 1871). Later accounts gave wider ranges: Portland, Maine southward to New Jersey. The current northern range includes the Gulf of Maine from Massachusetts Bay to Cobscook Bay, Maine (Yund and Feldgarden 1992; Blezard 1999; Dijkstra et al. 2007; MIT Sea Grant 2009); Passamaquoddy Bay, New Brunswick (LeGresley et al. 2008); the Atlantic coast of Nova Scotia at Lunenburg; the Bras d'Or lakes estuary on Cape Breton Island (Locke et al. 2007); and Placentia Bay, Newfoundland (Callahan et al. 2010). It was collected in the Gulf of St. Lawrence by Hooper, on the west coast of Newfoundland (in 1975, cited by Callahan et al. 2010), but its occurrence in the Gulf was not widely publicized until it was found on Prince Edward Island in the Gulf of St. Lawrence by 2001 (Locke et al. 2007).

It is now found as far south as Florida, but records between New Jersey and Florida are spotty. It has been reported in Beaufort and other areas of North Carolina (Van Name 1945, Sutherland and Karlson 1977, USNM 15481, U.S. Museum of Natural History 2003) and Chesapeake Bay (Gosner 1978). Plough (1978) collected it off Sapelo Island, GA and it was reported by Mook (1983) from the Indian River Lagoon, FL, but was not found in recent late summer surveys (e.g. Ruiz et al. unpublished data), but this species may grow best in winter and spring at lower latitudes.

In Chesapeake Bay, B. schlosseri was not reported in the course of an extensive survey of Chesapeake benthos in 1915-1922 (Cowles 1930) or in shoreline surveys near Norfolk, VA by Ferguson et al. (1949). However, it was reported as fouling the dredge, “Chinook”, in Hampton Roads, VA in 1923 (Visscher 1928). It was listed as a ‘rare species’ in deeper waters of the lower Bay by Wass (1965). A colony was collected at Virginia Institute of Marine Science (Gloucester Point, VA) in 1962 (Calder 1972), and it was common to abundant on piers in Norfolk, VA in 1964-1965 (Calder and Brehmer 1967). 'For nearly twenty years, it was a rare inhabitant of deep waters near the mouth of Chesapeake Bay’, as indicated in the checklist by Wass (1963). During the drought years of the mid 1960’s, B. schlosseri suddenly appeared at Gloucester Point on oyster trays and eventually erupted to cover nearly all tufts of eelgrass (Zostera marina) and widgeongrass (Ruppia maritima) inhabiting shallow waters in the lower York River and Mobjack Bay, VA. In 1973 Andrews reported: ‘It is a fast-growing pernicious pest on trays in the cool months of spring and fall but barely survives hot summers in Virginia...B. schlosseri was not vigorous in the wet year of 1971, but it was still present on trays of oysters in the spring of 1972. After Agnes it disappeared and no trace has been found at any fouling stations. It may not recover its distribution of the 1960's until another series of droughts occurs'. Botryllus schlosseri was abundant on fouling panels in Lynnhaven Bay, VA in 1977 (Otsuka and Dauer 1980) and common on settling plates (1994-95) in all of the major lower Bay regions sampled except Norfolk, VA (15-18ppt), and not at all sites. Botryllus schlosseri is much more common on spring-early summer plates than summer-fall plates (Ruiz et al. unpublished data). The spread of B. schlosseri in the lower Bay region in the 1960’s suggests a recent introduction, either from Europe or from further north along the East Coast. However, this pattern could also represent population fluctuations in response to long-term salinity or temperature changes.

Very few records are known from the Atlantic Coast south of Cape Hatteras, NC. Aside from the Pearse et al. record from Beaufort, NC cited by Van Name (1945), it was reported from Beaufort in 1971 by Sutherland and Karlson (1977) and collected off North Carolina in 1981 (USNM 15481, U.S. Museum of Natural History 2003). Plough (1978) collected it off Sapelo Island, GA. It was reported by Mook (1983) from the Indian River Lagoon, FL, but was not found in later surveys (e.g. Ruiz et al. unpublished data). However, it was not found on SERC plates deployed in summer months (June-Sept) in Charleston, SC and Jacksonville, FL harbors, or the Indian River Lagoon, FL (Ruiz et al. unpublished data). As noted for the Gulf, this species may grow best in winter and spring at lower latitudes.

Invasion History on the Gulf Coast:

Botryllus schlosseri was collected in the Gulf of Mexico in 1887 off Cedar Key, FL (USNMNH 6993, US. National Museum of Natural History 2003; Van Name 1921; Van Name 1945), and was collected from the Tortugas northwest to St. Andrew Sound, FL. Most USNMNH collections were made between December and April, though two were made in June. This temperate species may be most abundant in winter months in the Gulf. Botryllus schlosseri was never found on SERC settling plates deployed in this region during the summer (Ruiz et al. unpublished data).

Invasion History Elsewhere in the World:

Botryllus schlosseri has been introduced to many remote parts of the world by shipping. It was reported as absent from Bermuda by Van Name (1921), but was listed as being present in Bermuda by Berrill (1932). It was first collected in the Azores Islands in 1971 (Morton and Britton 2000). In the Southern Hemisphere, it is known from Chile (in 1948, Valdivia et al. 2005; Ben-Shlomo et al. 2010), Argentina (in 1964, Orensanz et al. 2002; Ben-Shlomo et al. 2010), South Africa (in 1955, Monniot et al. 2001), Australia (in 1905, Kott 1985), and New Zealand (in 1922, Cranfield et al. 1998).

Description

Botryllus schlosseri is a colonial tunicate that can form colonies as large as 25 mm x 150 mm and up to 2 mm thick. Color is highly variable within and among colonies, and can be yellow, dark purple, red, brown or black. Colonies consist of many radial clusters of 5-20 zooids forming star-shaped systems. Individual zooids can be 1.75 mm - 5 mm long. There are 12-16 oral tentacles around the oral siphon and 7-9 stigmatal rows. The stomach has 8-10 folds and is somewhat spirally deflected with a prominent pyloric caecum. On each side of peribranchial cavity are 1-4 ovaries which are located above prominent testis. Tailed larvae, about 400 µm long, with eight ampullae, may be present in the cavity (Van Name 1945; Nishikawa 1991; Lambert and Lambert 1998).

A recent genetic analysis indicates 'Botryllus schlosseri' is probably a complex of cryptic species. Five clades (A-E) were identified in Europe, but only one of these (A) was found at sites in the Northwest Atlantic and Northeast Pacific. The other clades had restricted distributions on the coasts of Europe (Bock et al. 2012). However, Yund et al. (2015) have found that clade A is comprised of several subclades, at least one (BS2) of which is native to the Northwest Atlantic.

Taxonomy

Ecology

General:

Life History- A colonial (or compound) tunicate consists of many zooids, bearing most or all of the organs of a solitary tunicate, but modified to varying degrees for colonial life. Colonial tunicates of the genera Botryllus have small zooids, arranged in systems, and fully embedded in a mass of tunic material. Each zooid has an oral siphon and an atrial canal, an opening to a shared cloacal chamber. Water is pumped into the oral siphon, through finely meshed ciliated gills on the pharynx, where phytoplankton and detritus is filtered, and passed on mucus strings to the stomach and intestines. Excess waste is expelled in the outgoing atrial water (Van Name 1945; Barnes 1983).

Colonial tunicates reproduce both asexually, by budding, and sexually, from fertilized eggs developing into larvae. Buds can form from the body wall of the zooid. Colonies vary in size and can range from small clusters of zooids to huge spreading masses. The zooids are hermaphroditic, with eggs and sperm being produced by a single individual. Eggs may be self-fertilized or fertilized by sperm from nearby animals, but many species have a partial block to self-fertilization. Eggs are internally fertilized and embryos are incubated in the atrial cavity. Once mature, they hatch into a tadpole larva with a muscular tail, notochord, eyespots, and a set of adhesive papillae. The lecithotrophic (non-feeding, yolk-dependent) larva swims briefly before settlement. Swimming periods are usually less than a day, and some larvae can settle immediately after release, but the larval period can be longer at lower temperatures. Once settled, the tail is absorbed, the gill basket expands, and the tunicate begins to feed by filtering (Van Name 1945; Barnes 1983). At Millport Scotland, B. schlosseri had only one generation per year, while at Plymouth, England, there were at least two (Millar 1954).

In all part of its native and introduced range, B. schlosseri is more frequently reported from anthropogenic stuctures than from natural surfaces, (Simkanin et al. 2012). Dock floats are especially favored habitats, probably because their motion provides rapid water exchange, and a fresh supply of food-laden water (Glasby 2001). Other colonized man-made structures include pilings, piers, aquaculture structures, and boat hulls (Carman et al. 2010; Davidson et al. 2010; Simkanin et al. 2012). Natural habitats include rocky reefs, bivalve colonies, seaweeds, and eelgrass (White and Orr 2011; Simkanin et al. 2012; Wong and Vercaemer 2012; Carman et al. 2016).

Food:

Phytoplankton

Consumers:

Crabs, snails, urchins, starfish

Competitors:

Other fouling organisms

Trophic Status:

Suspension Feeder

Habitats

Life History

Tolerances and Life History Parameters

General Impacts

Economic Impacts

Shipping and Industry: The colonial ascidian Botryllus schlosseri is a common fouling organism in temperate harbors and on ships (Visscher 1927; Milkman 1967) and has been called 'a fast-growing pernicious pest' on oyster trays in lower Chesapeake Bay, but is absent or rare on natural oyster beds, presumably because of siltation (Andrews 1973). However, it is an important experimental organism in embryology, genetics, and immunology (Milkman 1967; Rinkevich et al. 1995).

Ecological Impacts

Competition: Bancroft (1903) listed hydroids, bryozoans, and 'worms' as competitors for space with B. schlosseri at Woods Hole, MA and Naples, Italy. Botryllus schlosseri is abundant and occasionally dominant in spring-early summer fouling communities in the lower Chesapeake Bay (Andrews 1973; Ruiz et al. unpublished data). When fouling plates in Lynnhaven Bay, VA were covered with wire mesh to exclude larger predators, B. schlosseri became the dominant fouling organism during December-March (Otsuka and Dauer 1982). In Long Island Sound, NY, recruitment of other fouling organisms, including native Spirorbis spp., was reduced in the vicinity of B. schlosseri colonies (Osman and Whitlatch 1995), and on colonial tunicates including B. schlosseri in Portsmouth Harbor, NH (Dijkstra et al. 2007). However, in Humboldt Bay (CA), fouling plate experiments (Nelson 2009) found that colonial tunicates (Botryllus schlosseri and Botrylloides violaceus), growing in sheets, were able to quickly occupy space on fouling plates, but did not decrease recruitment or species richness. In Langstone Harbor, Hampshire, England, Schmidt and Warner (1986) found that B. schlosseri paired with Trididemnum tenerum or Botrylloides leachii, on plexiglass panels resulted in stand-offs, colonies touching without overgrowth. However, B. schlosseri and the other species were always overgrown when paired with Diplosoma listerianum. In experiments in Wells Harbor, Maine, Botryllus schlosseri grew rapidly on some artificial substrates (rubber and metal), outcompeting native organisms, but grew more slowly on natural substrates (shell, marble, slate) (Tyrell and Byers 2007). In Bodega Harbor, California, Botryllus schlosseri was one of the eight most abundant fouling organisms both in 1969-1971 and in 2005-2009 (Sorte and Stachowicz 2011). Spawning periods and 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).

Botryllus schlosseri, Botrylloides violaceus, and a native sponge Halichrondria panicea were found to adversely affect native eelgrass Zostera marina in southeastern Nova Scotia by fouling the leaves of the grass, and reducing the availability of light. Fouling increased the mortality of the plants (Wong and Vercaemer 2012). Negative effects on eelgrass are likely to be widespread.

Habitat Change:

Based on experiments on fouling of eelgrass plants in Nova Scotia, the spread of Botrylloides violaceus and Botryllus schlosseri is likely to have an adverse impact on eelgrass beds, increasing mortality of the plants and decreasing their productivity (Wong and Vercaemer 2012).

Regional Impacts