Diplosoma listerianum

Invasion History

First Non-native North American Tidal Record: 1899
First Non-native West Coast Tidal Record: 1899
First Non-native East/Gulf Coast Tidal Record: 1975

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General Invasion History:

Diplosoma listerianum was first described from the English Channel by Milne-Edwards in 1841. Initially, this species was described, under different names, from many different places around the world, such as Australia (D. rayneri Macdonald 1859) Brazil (D. macdonaldi Herdman 1886), and Japan (D. mitsukurii Oka 1892). These and many other names were synonymized by Kott (1990; 2001). This tunicate is now said to have a cosmopolitan distribution but represents a species complex (Perez-Portela et al. 2013). In most of these regions, D. listerianum was already established when researchers began surveying tunicates and, as a result, many populations have not been recognized as true introductions. One cryptic species (clade A) occurred in most of the sites sampled worldwide, while three other clades had more local distributions (Perez-Portela et al. 2013). We consider this species complex to be cryptogenic (of unknown origin) through most of its range. However, it appears to be a definite introduction in several locations, including the Northeast Pacific (California to British Columbia), the Northeast Atlantic (north of Cape Hatteras, North Carolina), Hawaii, New Zealand, and South Africa. In European waters, near the site of first description, range expansions have been noted in the North Sea (UK, Vance et al. 2008) and in the Netherlands (1st Record 1977, Gittenberger et al. 2007).

North American Invasion History:

Invasion History on the West Coast:

Diplosoma listerianum was collected in San Diego Bay, California in 1917. It was described by Ritter and Forsyth as D. pizoni from a single colony (Van Name 1945). Five additional colonies collected in 1899 were also identified as D. pizoni by Ritter (Eldredge 1966). Diplosoma listerianum apparently expanded its range northward, reaching Monterey Bay by 1939 (Van Name 1945; Eldredge 1966). In 1948, D. listerianum was found in San Francisco Bay, California (Eldredge 1966). In 1960, it was collected on Vancouver Island, British Columbia and by 1966 it was common in Puget Sound, Washington (Lambert 1966). 
 
Since D. listerianum was treated as a native species, we have not been able to find first dates of record for many West Coast water bodies. By 1980, it was considered common from San Diego, California to British Columbia, Canada (Abbott and Newberry 1980). In Southern California, Lambert and Lambert (1998) described it as occurring in 'all harbors, at all times of year' and subsequent surveys have confirmed this (Fairey et al. 2001; de Rivera et al. 2006; Ruiz et al., unpublished data). Further north, it occurs in Humboldt Bay, CA (Fairey et al. 2003; Ruiz et al. unpublished data) and Coos Bay, Oregon (1988, Hewitt 1993, 2001, Ruiz et al., unpublished data). It is widespread throughout Puget Sound (Ruiz et al., unpublished data) and has been collected at as far north as Bamfield, Vancouver Island, British Columbia (Mackie and Singla 1987). 

Invasion History on the East Coast:

Diplosoma listerianum was first collected in 1880 in the Atlantic Ocean off South Carolina, and subsequently found from Cape Fear, NC to Biscayne Bay, FL (U.S. National Museum of Natural History 2002; Van Name 1921; Ruiz et al. unpublished data). We consider it cryptogenic in these southern US waters. The first reported occurrence of D. listerianum north of Cape Hatteras, NC was in Long Island Sound, CT in the 1970s (R. Whitlatch to James T. Carlton, personal communication, 2002). In 1981, it was found at the east end of the Cape Cod Canal, in the Gulf of Maine (R. Whittaker to James T. Carlton, personal communication, 1984). In 1997, it was found in Great Bay, near Portsmouth, New Hampshire (Blezard 1999). In 1998, it was found in Narragansett Bay, Rhode Island and Vineyard Sound, Massachusetts (Whitlatch and Osman 2000). In 1999, it was found near Cape Neddick, Maine (ME) (Harris and Tyrell 2001), and in 2003 it was found in Casco Bay, ME (MIT Sea Grant 2003). It was found in the Gulf of St. Lawrence, in the Magdalene Islands, Quebec in 2008 and in Lunenburg Harbour, Nova Scotia in 2012; however establishment in both locations is uncertain (Willis et al. 2011; Moore et al. 2014).  The northward range expansion fluctuates with the variability of winter weather. and the presence of thermal refugia. It is predicted to colonize most of the Atlantic coast of Nova Scotia by 2075 (Lowen and DiBacco 2023).  There are no published records of this tunicate south of Long Island Sound, CT. However, in 2001 and 2002, specimens were found on fouling plates in lower Chesapeake Bay near Cape Charles, VA. Since there were concerns about identifications, specimens were confirmed as D. listerianum by Gretchen Lambert. Colonies in Cape Charles, Virginia (VA) appeared to be abundant (Ruiz et al. unpublished data).

Invasion History on the Gulf Coast:

Diplosoma listerianum was first found at Cedar Key, FL in 1885 (U.S. National Museum of Natural History 2002; Van Name 1921). It has been collected from Cape Sable, FL to Laguna Madre, Texas (U.S. National Museum of Natural History 2002; Van Name 1921, Lambert et al. 2005; Ruiz et al. unpublished data). We regard it as cryptogenic in the Atlantic Ocean south of Cape Hatteras, NC.

Invasion History in Hawaii:

Diplosoma listerianum was collected in Honolulu, Oahu as early as 1900. It has also been found on Maui and on remote islands, such as Midway Island and Johnston Atoll (Eldredge 1967, Coles et al. 1999; Coles et al. 2001; Carlton and Eldredge 2009).

Invasion History Elsewhere in the World:

Diplosoma listerianum has been reported worldwide from tropical to cold-temperate regions. Among locations where it is considered a recent invader are Guam (1998, Lambert 2002), New Zealand (1946, Cranfield et al. 1998), and South Africa (1st Record 1949, now found from Saldanha Bay to Durban, Monniot et al. 2001; Mead et al. 2011b). In 2018, one specimen was found in a harbor on the southwest coast of Iceland (Ramos-Espla et al. 2020). Genetic studies may result in changes to cryptogenic/introduced status of D. listerianum populations.

We consider Diplosoma listerianum to be broadly cryptogenic in the East Atlantic and tropical continental waters around the world, but introduced to more isolated regions and islands. In the Eastern Pacific, we regard D. listerianum as introduced to the Galapagos Islands (Lambert 2019) and on Cocos Island, Costa Rica, where it was found on fouling plates in 2018 (Ruiz et al., unpublished data).

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Description

Diplosoma listerianum is a colonial ascidian species forming extensive thin, delicate encrusting sheets, rarely more than 2 mm thick and up to 50 mm wide. It can overgrow seagrasses, pilings, crab shells, and other sessile organisms such as corals, gorgonians, and other tunicates. Its tunic is transparent and may have white or yellowish granular bodies suspended in the tunic material. Zooids (individual animals) underneath the tunic may be white, brown, green, or black due to pigment on the abdomen, and sometimes the thoracic epithelium. Other tissues are usually light-colored ranging from white to yellowish or rusty (Van Name 1945; Kott 2001). The colonies have a variable but extensive common cloacal cavity that is subdivided by thin connective tissue in which the zooids are embedded. Each zooid is enclosed by a branch or strip of tunic material (Van Name 1945; Kott 2001). Zooids are small, about 1 mm long. The oral siphon is conspicuous and divided into six deeply divided lobes around the opening. The atrial opening is large and oval, with no atrial tube or languet. This opening has plain edges and exposes most of the branchial sac to the cloacal cavity. There are four rows of stigmata, 10 in the anterior row, and eight in the posterior row. The stomach is rounded and smooth-walled, leading to an intestine of large diameter. Conspicuous stolonic vessels extend from the ventral side of the abdomen where the post-pyloric part of the gut is bent ventrally at right angles to the vertical axis of the zooid. Two oval testis follicles lie against the dorsal side of the gut loop. The vas deferens is hooked around between them, extending anteriorly around the ascending limb of the gut loop. The ovaries and eggs are found behind the intestinal loop (Van Name 1945; Kott 2001). The larvae have a trunk 0.4–6 mm long, with three fixatory papillae (Hayward and Ryland 1990).

A recent study has shown that 'Diplosoma listerianum' consists of at least 4 cryptic species. One of these, clade A, is extremely widespread, occurring in the northeast Atlantic (Plymouth, England; Atlantic and Mediterranean Spain); western Atlantic (Panama); southeast Atlantic-Indian Ocean (South Africa); western Pacific (Japan; Melbourne Australia), and eastern Pacific (Washington, California; Chile) (Perez-Portela et al. 2013). Other clades (B, C, and D) have a more limited distribution, but overlap with clade A. The genetic structure of local populations of clade A is suggestive of anthropogenic dispersal along historic shipping routes but does not indicate a region of origin. The distribution of the clades does not easily correspond with the many historic synonyms (eg., 'D. macdonaldi, D. mitsakurii, etc.). Additional genetic surveys will be needed to determine the identity of populations in many regions of the world.

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Taxonomy

Ecology

General:

Life History- A colonial tunicate consists of many zooids, bearing most or all the organs of a solitary tunicate, but modified to varying degrees for colonial life. Colonial tunicates of the family Didemnidae have small zooids, completely embedded in an encrusting and thin tunic. Each zooid has an oral siphon and an atrial aperture which opens to a shared local chamber. Water is pumped into the oral siphon, through finely meshed ciliated gills on the pharynx, where phytoplankton and detritus are 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 that develop into larvae. Buds can form from the body wall of the zooids. Colonies vary in size ranging from small clusters of zooids to huge spreading masses. The zooids are hermaphroditic, which means both eggs and sperm are released into the atrial chamber. Eggs may be self-fertilized or fertilized by sperm from nearby animals, but some species have a partial block to self-fertilization. Fertilized eggs are brooded within the tunic until they hatch into lecithotrophic (non-feeding, yolk-dependent) tadpole larvae. The larva has a muscular tail and a notochord, eyespots, and a set of adhesive papillae. The larvae are expelled upon hatching and swim briefly before settlement. Swimming periods are usually less than a day, but some larvae settle immediately after release or swim for longer periods if the water temperature is low. On settlement the tail is absorbed, the gill basket expands, and the tunicate begins to feed by filtering (Van Name 1945; Barnes 1983). Populations of D. listerianum in Millport, Scotland had 1–2 generations per year, while those in Plymouth, England had up to 3 generations per year, and could produce larvae in 2–4 weeks after settlement (Millar 1954). 

Food:

Phytoplankton

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	Mangroves	None
General Habitat	Vessel Hull	None
General Habitat	Unstructured Bottom	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
Maximum Temperature (ºC)	30	Field, based on warmest site in geographical range, Miami FL (Zerebecki and Sorte 2011) Temperature tolerances vary with acclimation and geographical location. For D. listerianum, from Lynn Harbor MA, acclimated at 17 C, the median lethal 24 h temperature (LT50) was 29.41C, but signficantly lower (27.9) for this species from Bodega Bay CA (Sorte et al. 2013).
Minimum Salinity (‰)	18	Typical salinity, Black Sea. In Great Bay NH, D. listerianum occurred at a station where salinity dropped to 24 ppt in spring, but not further upstream (Blezard 1999). A population from Holyhead Harbour, Wales (Irish Sea) showed dramatic mortality when transferred from 34 to 27 and 20 PSU (Gröner et al. 2011).
Maximum Salinity (‰)	40	Field salinity (Shark Bay, Australia, Wyatt et al. 2005)
Minimum Reproductive Temperature	15	Field, larval release, Mediterranean (Brunetti et al. 1988)
Minimum Duration	0	Brunetti et al. 1988 (80% settlement within 24 hours in the light)
Maximum Duration	3	Brunetti et al. 1988 (only 40% settlement with 3 days in the dark)
Broad Temperature Range	None	Cold temperate-Tropical
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

Economic Impacts

Fisheries: Diplosoma listerianum has been reported to foul cultured shellfish in the United Kingdom (Isle of Man), Croatia, Japan, and Hong Kong (Ross et al. 2004, Igic 1972, Arakawa 1990, Huang 2003, cited by da Rocha et al. 2009). Da Rocha et al. (2009) suggest that because of the thinness of D. listerianum colonies, its impacts on mussel growth might be small, but this hypothesis still needs to be tested.

Shipping and Industry: In many parts of the world, the colonial tunicate Diplosoma listerianum is an abundant fouling organism (Lambert 2002), known from docks, buoys, floats, and ship hulls (Woods hole Oceanographic Institution 1951).

Ecological Impacts

Competition: In experiments in Long Island Sound, Diplosoma listerianum significantly reduced recruitment of native Spirorbis spp, Bugula spp, and Balanus spp, mostly through overgrowth of newly settled individuals (Osman and Whitlatch 1995). Diplosoma listerianum also significantly reduced recruitment of Botryllus schlosseri and non-indigenous Botrylloides violaceus, mostly through overgrowth of newly settled individuals (Osman and Whitlatch 1995). Disturbance enhanced the spread of D. listerianum (Altman and Whitlatch 2007). Diplosoma listerianum was a strong competitor in utilizing empty space on fouling plates (Stachowicz et al. 2002). In Eel Pond, Woods Hole, Massachusetts, Diplosoma listerianum outgrew Botrylloides violaceus and other organisms on fouling plates, covering ~72% of the plates at the end of the experiment. In cooler water, north of Cape Cod, in Lynn Harbor, Massachusetts Bay, D. listerianum achieved a stand-off with B. violaceus, becoming co-dominant, covering ~37% of the plates at the peak of its growth (Agius 2007). While working in the English Channel, Schmidt and Warner (1986) found that D. listerianum outcompeted Trididemnum tenerum, Botryllus schlosseri and Botrylloides leachii in 39% of trials on fouling plates and reached stand-offs in 61%.  Vance et al. (2008) observed that D. listerianum rapidly overgrew other fouling organisms on plates in newly colonized regions on the North Sea coast of England. Diplosoma listerianum was one of several invasive fouling species which showed increased growth (% coverage) at temperatures 3.5 and 4.5°C above the ambient temperature in Bodega Harbor (13.5°C), while the native Distaplia occidentalis showed reduced survival (Sorte et al. 2010). 

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Regional Impacts

NEP-V	Northern California to Mid Channel Islands		Ecological Impact	Competition
Diplosoma listerianum was one of several invasive fouling species which showed increased growth (% coverage) at temperatures 3.5 and 4.5°C above the ambient temperature in Bodega Harbor (13.5°C), while the native Distaplia occidentalis showed reduced survival (Sorte et al. 2010).
P112	_CDA_P112 (Bodega Bay)		Ecological Impact	Competition
Diplosoma listerianum was one of several invasive fouling species which showed increased growth (% coverage) at temperatures 3.5 and 4.5°C above the ambient temperature in Bodega Harbor (13.5°C), while the native Distaplia occidentalis showed reduced survival (Sorte et al. 2010).
CA	California		Ecological Impact	Competition
Diplosoma listerianum was one of several invasive fouling species which showed increased growth (% coverage) at temperatures 3.5 and 4.5°C above the ambient temperature in Bodega Harbor (13.5°C), while the native Distaplia occidentalis showed reduced survival (Sorte et al. 2010)., Diplosoma listerianum was one of several invasive fouling species which showed increased growth (% coverage) at temperatures 3.5 and 4.5°C above the ambient temperature in Bodega Harbor (13.5°C), while the native Distaplia occidentalis showed reduced survival (Sorte et al. 2010).

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