Ciona intestinalis

Invasion History

First Non-native North American Tidal Record: 1838
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1838

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General Invasion History:

Ciona intestinalis was described from Sweden by Linnaeus in 1767, and was formerly regarded as a single cosmopolitan species, present in the coastal waters of every continent except Antarctica. The tunicates formerly regarded as C. intestinalis have been divided into at least 4 species, two of which, A and B, and widely distributed (Caputi et al. 2007), and two of which are confined to the Mediterranean and Black Seas (Species C and D, Zhan et al. 2015). Species B is now considered to be the true C. intestinalis, found from Norway to Spain, and from Newfoundland to Long Island Sound, with a few less certain reports from Delaware Bay, North Carolina, and Florida (Plough 1978; Carman et al. 2010; U.S. National Museum of Natural History 2019). Species A is widely distributed in southern Europe, the Mediterranean, the North Pacific, and in the Southern Hemisphere, is now recognized as a separate species, C. robusta (Brunetti et al. 2015).

The native range of Ciona intestinalis is difficult to determine, given its early discovery on both sides of the Atlantic, 1768 in Sweden by Linnaeus, and 1838 in Boston (Couthouy 1838). It has long been regarded as cryptogenic on each side of Atlantic, with a high potential for ship transport (Visscher 1927; Van Name 1945; Haydar 2012). C. intestinalis is strongly associated with human-made structures such as docks, ship hulls, and aquaculture facilities. Dramatic range expansions in Atlantic Canadian waters and recent genetic studies support the hypothesis of an invasion of the Northwest Atlantic by C. intestinalis (Carver et al. 2006; Nydam and Harrison 2008; Ramsay et al. 2008; Hudson et al. 2020). In the fall of 2004, specimens of C. intestinalis were identified in the Montague River, a branch of the Brudenell.

The presumed native range of Ciona intestinalis extends from Norway to the northern coast of Spain, and the outer Baltic Sea (Bouchemousse et. 2016). Occurrences in a few harbors in Iceland are introductions (Björnsson 2011, cited by Thorarinsdottir et al. 2014). In southern England and the coast of Normandy and Brittany, and southward, the ranges of C. intestinalis and C. robusta overlap (Sato et al. 2012; Bouchemousse et al. 2017). An introduced population of Ciona intestinalis has been reported in the Yellow and Bohai Seas, China (Zhan et al. 2010).

North American Invasion History:

Invasion History on the East Coast:

The earliest report of Ciona intestinalis is in Boston Harbor, Massachusetts, where it was found on old sunken logs in the harbor (Couthouy 1838). Other early records were from New Bedford, Massachusetts (Agassiz 1859, cited by Gould 1870), from Jamestown, Rhode Island (1880, US National Museum of Natural History 2009), and from Passamaquoddy Bay in Eastport, Maine (1868, Yale Peabody Museum 2019), and from Grand Manan Island, New Brunswick, Canada (Stimpson 1853). By 1912, it was reported from offshore waters in the Gulf of St. Lawrence, and from deep waters (242 m) off Nova Scotia (1885, US National Museum of Natural History 2019). There is some evidence for an expansion of the range of C. intestinalis beginning in the 19th century. Verrill and Smith (1874) did not report C. intestinalis (as C. tenella) in the Woods hole-Martha's Vineyard area, where Van Name (1912) later found it abundant. Verrill (1880) found it on rocks and pilings from low tide to ~37 m at Newport, Rhode Island. He noted that 'It seems to be very local in its distribution, for I have never seen it at any other locality upon our coast' (Verrill 1880). Van Name (1912, 1945) also gives Rhode Island as the southern limit. Plough (1978) shows locations in Long Island Sound, the New York Bight, and off Delaware, and Cape Hatteras. 

By 1987, C. intestinalis was abundant in Long Island Sound by 1987 (Osman 1995). Occurrences south of Long Island Sound are not well documented. Plough's (1978) maps do not give dates or precise locations. However, Carman et al. (2010) reported C. intestinalis at an aquaculture facility in North Carolina, based on a photograph, and a museum specimen from Florida is in the National Museum collections (USNM 1492383, U.S. National Museum of Natural History 2019, undated, ID by C. G. Messing, ~2000s). Ciona intestinalis has not been seen on SERC fouling plates from Chesapeake Bay or South Carolina (Kristen Larson, personal communication).

Ciona intestinalis has had a more dramatic range and population expansion at the northern end of its East Coast range. In the late 1800s, it had already been collected at the mouth of the Bay of Fundy and Passamaquoddy Bay, and in deep water (232 m) off Halifax (Stimpson 1852; US National Museum of Natural History 2019; Yale Peabody Museum 2019). Low to high densities were found in New Brunswick estuaries off the lower Bay of Fundy (LeGresley et al. 2008). Van Name (1912 lists it as occurring in the Gulf of St. Lawrence, Canada, but with no details. Off Nova Scotia and in the Gulf of St. Lawrence, it was apparently restricted to deep water. However, in 2004, C. intestinalis was found in the Montague River, a branch of the Brudenell River estuary, on Prince Edward Island. From 2004 to 2005, numbers increased from 1 or 2 per 10 cm-2 collector plate to ~500 per plate. This tunicate spread throughout the estuary, replacing the previous dominant fouler- Styela clava (Ramsay et al. 2008). In 2006 it was found in the adjacent Cardigan River (Carver et al. 2006). By 2018, many scattered populations were found in the southwest corner of the Gulf of St. Lawrence on Prince Edward Island and Nova Scotia (Department of Fisheries and Oceans 2018). In Gulf of Maine and the adjacent Atlantic coast of Nova Scotia occurrences of C. intestinalis were localized, from Yarmouth to Cape Sable, Mahone Bay, and Chedabucto Bay (Carver et al. 2006). In 1997, heavy infestations at mussel farms were first observed near Lunenburg, Nova Scotia (Carver et al. 2003). In 2012, C. intestinalis was detected on the Atlantic coast of Newfoundland, at Buring, in Placentia Bay, nearby Little Bay, and the nearby French Islands of St. Pierre and Miquelon (Sargent et al. 2013).

Hudson et al. (2020) found evidence that Atlantic Canada populations contain a combination of English Channel and Swedish shallow-water genotypes. They suggest that hybridization between English Channel and Swedish populations resulted in a population well-adapted to colonization of artificial structures in shallow water. Previous high-resolution genetic studies in the English Channel indicate both genetic similarity due to anthropogenic transport, but also some local differentiation resulting from limited natural dispersal (Hudson et al. 2016). Studies in Sweden indicate genetic differentiation between deep-water and shallow-water populations, though both populations favor natural substrates (Johannesson et al. 2018). Although Hudson et al. (2020) sampled only populations in Atlantic Canada, historic the records cited above indicated an early 18th or early 19th-century introduction of shallow-water populations of Ciona intestinalis in New England waters, followed by a range expansion. The early museum records of deep-water specimens (100-270 m) could represent genotypically differentiated populations, as seen in Sweden (Johannesson et al 2018.). Genetic sampling of shallow and deep-water populations is desirable because multiple introductions of different genotypes of C. intestinalis that are adapted to different conditions are possible. An example is seen in the invasion history of the Green Crab (Carcinus maenas), where the range of the species originally introduced from Spain rapidly extended northward after a second introduction from Scandinavia (Roman 2006; Blakeslee et al. 2010).

Invasion History Elsewhere in the World:

Ciona intestinalis (Species B) has been morphologically and genetically identified from Iceland (Thorarinsdottir et al. 2014), and from the Northwest Pacific, on the coasts of China and South Korea (Zhan et al. 2010). In Iceland this tunicate has been found in a harbor in Straumsvík, south-western Iceland, and in three other small harbors in 2008 (2007, Svavarsson and Dungal 2008, cited by Thorarinsdottir et al. 2014). This tunicate was abundant in six harbors (Akranes, Reykjavík, Hafnarfjörður, Keflavík, Sandgerði and Grindavík) on the southwest coast of Iceland where they were identified by molecular methods. Sequences from Iceland clustered with samples from England, Denmark, and Nova Scotia, but did not pinpoint a specific location of origin (Araola 2019). Fishing boats seems to be the likeliest vector for smaller harbors. In the Northwest Pacific, Ciona intestinalis (Type B) has been identified by molecular methods at Liaoning China, in the Bohai Sea, in China and in the Yellow Sea (Shandong, China, Zhan et al. 2010). The extent of the range of C. intestinalis in the Northwest Pacific is not known. All the specimens identified from South Korean waters were identified as C. robusta (Type A, Lee and Shin 2014). Ciona intestinalis was probably introduced with hull fouling of ships from Europe, but the timing of this introduction is unknown.

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Description

The tunicate Ciona intestinalis, described from Sweden by Linnaeus in 1767, is a solitary tunicate with an elongated, cylindrical or vase-shaped body that can reach a length of 150 mm long. It is widest near the permanently attached posterior end and tapers toward the anterior end. The tunic can be transparent, translucent, or white. Much of the tunic is soft, flexible, and gelatinous, except for the posterior end where it can be tough, mostly opaque, white or yellowish-white. The muscle bands and organs are often visible beneath the tunic. The siphons are short and directed forward, with the oral siphon larger than the atrial siphon. The oral siphon has 8 lobes, each with a yellow margin containing 8 reddish-orange spots, but these spots are not always apparent. The atrial siphon has 6 lobes, each with a yellow margin containing 6 reddish-orange spots. There are 5-7 conspicuous longitudinal muscle bands on each side of the body that extend nearly the entire length of the body (Van Name 1945; Sato et al. 2012).

Ciona intestinalis was formerly regarded as a species widely distributed in the North Pacific and Atlantic, probably introduced in the Northeast Pacific, and the Southern Hemisphere, and was considered native or cryptogenic on the coasts of the North (Van Name 1945). Genetic analyses indicated that there were at least four cryptic species, with two genotypes, C and D, restricted to the Mediterranean and Black Seas, respectively. Genotype A was eventually identified as Ciona robusta  (Hoshino & Tokioka 1967) and is widley distributed in southern Europe, the Mediterranean, the North Pacific, and the Southern Hemisphere (Caputi et al. 2007; Zhan et al. 2010; Zhan et al. 2015; Sato et al. 2012; Brunetti et al. 2015). Genotype B was identified as the true Ciona intestinalis described by Linnaeus, and a neotype, from Roscoff, France, was designated (Brunetti et al. 2015). Ciona intestinalis was largely limited to the northern North Atlantic (Caputi et al. 2007; Brunetti et al. 2015), although a population in the Bohai and Yellow Seas, China is an apparent introduction (Zhan et al. 2010). Sato et al. (2012) found species 'A' (C. robusta and 'B' (C. intestinalis) living in symapatry within Plymouth Harbor, England, as indicated by genetic analysis. Ciona robusta specimens have little pigment on the margins of the oral siphons, while most tunicates have strong yellow, orange, or red pigmentation on the margins. Most 'A' (Ciona robusta) have small tubercles on the siphon, while most 'B' (C. intestinalis) specimens lacked them. The two types also tended to differ in the color of papillae on the gonoducts, with more intense coloration in most 'robusta' specimens. These differences are heritable in culture, and intermediate in hybrids (Sato et al. 2012). Hybrids of the two species are asymmetrically infertile. C. intestinalis can be fertilized by C. robusta sperm, but the reverse cross had very low fertility (Caputi et al. 2007; Malfant et al. 2017). Hybrids are rare in the wild (Bouchemousse et al. 2016b; Malfant et al. 2017).

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Taxonomy

Ecology

General:

Life History- Ciona intestinalis is a vase-shaped solitary tunicate, attached at its base to a substrate with two openings or siphons, an oral and an atrial siphon. Water is pumped in through the oral siphon, where phytoplankton and detritus are filtered by the gills, and passed on mucus strings to the stomach and intestines. Waste is then expelled in the outgoing atrial water. Solitary ascidians are hermaphroditic, meaning that both eggs and sperm are released to the atrial chamber. Eggs may be self-fertilized or fertilized by sperm from nearby animals, but Ciona spp. have a partial block to self-fertilization. Eggs are externally fertilized. Eggs and sperm are released through the atrial siphon into the surrounding water column where fertilization takes place. Fertilized eggs 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 settle immediately after release, but the larval period can be longer at lower temperatures (Dybern 1965). Modelling indicates that dispersal distances are limited, less than 6 km per generation (Kanary et al. 2011; Collin et al. 2013). Once settled, the tail is absorbed, the gill basket expands, and the tunicate begins to feed by filtering (Barnes 1983). Ciona intestinalis near Millport, Scotland, has an annual life cycle, but more rapid growth and more frequent reproduction are likelier in warmer climates (Millar 1954; Carver et al. 2006).

Ciona intestinalis (sensu stricto, Species B) is a tunicate associated with cooler, northern waters, in contrast with C. robusta (Species A), which is widely introduced in warm-temperate regions. Temperature and salinity tolerances for survival and reproduction wary with habitats. Scandinavian populations survive temperatures of 0° C or lower in winter (Dybern 1965), while populations from the southern end of the range (Brittany, France) have an upper limit of ~27°C (Kenworthy et al. 2018). Populations from the Baltic Sea, Germany, tolerate salinities as low as 9 PSU, while those from the Gullmarfjord, Sweden, have a lower limit of 17 PSU, and those from Brittany had a lower limit of 22 PSU (Dybern 1965; Kenworthy et al. 2018). Since larval dispersal is limited, it is likely that some of these differences are genetic. Ciona intestinalis, like other tunicates, is a filter-feeder, and are capable of retaining particles as small as 1 um. It may have the ability to select larger particles, but this is unclear (Carver et a1. 2006). Predators in Nova Scotia include Green and Rock Crabs (Carcinus maenas and Cancer irroratus (Carver et al. 2004).

Food:

Phytoplankton, detritus

Consumers:

fish, crabs, starfish

Competitors:

other tunicates

Trophic Status:

Suspension Feeder

SusFed

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Habitats

General Habitat	Marinas & Docks	None
General Habitat	Coarse Woody Debris	None
General Habitat	Rocky	None
General Habitat	Unstructured Bottom	None
General Habitat	Vessel Hull	None
General Habitat	Grass Bed	None
Salinity Range	Mesohaline	5-18 PSU
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Epibenthic	None

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Life History

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	0	Gulmar Fjord, Sweden (Dybern 1965)
Maximum Temperature (ºC)	27	Experimental, animals from Brest, France (Kenworthy et al. 2018)
Minimum Salinity (‰)	9	7 day survival, Baltic Sea populations; 17 PSU for 6 days, Gulmar Fjord, Sweden (Dybern 1967); 22 PSU, Brest, France (Kenworthy et al. 2018)
Maximum Salinity (‰)	35	Average Atlantic Ocean salinity
Minimum Reproductive Temperature	8	Field, Gulmarfjord, Sweden (Dybern et al. 1965).
Maximum Reproductive Temperature	22	Field, Gulmarfjord, Sweden (Dybern et al. 1965).
Minimum Reproductive Salinity	10	Field and experimental, zygotes, Baltic Sea populations (Dybern 1967)
Maximum Reproductive Salinity	35	Experimental, zygotes, Svenningesar, Sweden (Dybern 1967)
Minimum Duration	1.5	Egg + larva, Dybern 1965, 23C; Katz 1983
Maximum Duration	7	Dybern 1965, 8 C
Minimum Height (mm)	50	Maturity occurs at 50-80 mm height (Carver et al. 206).
Maximum Height (mm)	150	Van Name 1945
Broad Temperature Range	None	Cold temperate-Warm temperate
Broad Salinity Range	None	Mesohaline-Euhaline

General Impacts

Shipping and Industry:

Ciona intestinalis is widely known as a fouling organism of ships and docks (Visscher 1927; Woods Hole Oceanographic Institution 1951; Millar 1971), and laboratory seawater systems (Fofonoff, pers. obs.).

Fisheries:

Its most serious economic impacts have been on shellfish aquaculture in Nova Scotia where tunicates are said to reduce the growth rates of mussels and foul culturing ropes (Carver et al. 1999; Ramsay et al. 2008). These aquaculture industries are likely affected economically as well. Another negative potential impact of C. intestinalis and other tunicates is that when they foul aquaculture gear and boats they can retain and transport viable cells and cysts of toxic phytoplankton (Rosa et al. 2013).

Ecological Impacts

Competition:

Ciona intestinalis is a formidable competitor since it can quickly erupt and replace other species in fouling communities, both in its native and introduced ranges (Millar 1971; Lambert and Lambert 2003). On mussel socks (plastic net tubes) in Montague-Brudenell River, Prince Edward Island, abundances of native Molgula spp. and sedentary polychaetes were inversely correlated with C. intestinalis (Lutz-Collins et al. 2009

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Regional Impacts

NA-ET1	Gulf of St. Lawrence to Bay of Fundy		Economic Impact	Fisheries
Ciona intestinalis has negative impacts due to fouling, and competition for phytoplankton, on farmed mussels and oysters in Nova Scotia, Canada (Carver et al. 2003; Daigle and Hersnberger 2009).
NA-S3	None		Economic Impact	Fisheries
Ciona intestinalis is considered a threat to mussel culture operations in Prince Edward Island (Carver et al. 2003; Ramsay et al. 2008, Gittenberger 2009). Large biomasses of C. intestinalis in Prince Edward Island estuaries have a high clearance rate, decreasing available food for cultured mussels (Comeau et al. 2015).
NA-S3	None		Ecological Impact	Competition
Abundances of native Molgula spp. and sedentary polychaetes were inversely correlated with Ciona intestinalis settling on mussel socks in the Montague-Brudenell River, Prince Edward Island (Lutz-Collins et al. 2009). Ciona intestinalis competedwith, and eventually largely replaced Styela clava in Prince Edward Island estuaries (Ramsay et al. 2008).
NA-ET2	Bay of Fundy to Cape Cod		Economic Impact	Fisheries
Ciona intestinalis was a dominant fouling organism at oyster and aquaculture sites in the Damariscotta River, Maine (Bullard et al. 2015)
N070	Damariscotta River		Economic Impact	Fisheries
Ciona intestinalis was a dominant fouling organism at oyster and aquaculture sites in the Damariscotta River, Maine (Bullard et al. 2015)
NA-ET3	Cape Cod to Cape Hatteras		Economic Impact	Fisheries
On Matha's Vineyard, Ciona intestinalis was frequently found fouling aquacultural gear, though not attaching to shellfish (Carman et al. 2010).
ME	Maine		Economic Impact	Fisheries
Ciona intestinalis was a dominant fouling organism at oyster and aquaculture sites in the Damariscotta River, Maine (Bullard et al. 2015)

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