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

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 West Coast:

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 on the Gulf Coast:

Invasion History in Hawaii:

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.


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).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Chordata
Subphylum:   Tunicata
Class:   Ascidiacea
Order:   Phlebobranchia
Family:   Cionidae
Genus:   Ciona
Species:   intestinalis

Synonyms

Ascidia virescens (Pennant, 1812)
Ascidia canina (Mueller, 1776)
Ascidia corrugata (Mueller, 1776)
Ascidia intestinalis (Linnaeus, 1767)
Ascidia membranosa (Renier, 1807)
Ascidia ocellata (Agassiz, 1850)
Ascidia pulchella (Alder, 1863)
Ascidia tenella (Stimpson, 1852)
Ascidia virens (Fabricius, 1779)
Ciona canina (Kupfer, 1875)
Ciona fascicularis (Hancock, 1870)
Ciona gelatinosa (Monniot, 1969)
Ciona ocellata (Dall, 1870)
Ciona tenella (Verrill, 1871)
Tethyum sociabile (Gunnerus, 1765)
Ciona sociabilis (Hartmeyer, 1915)
Ascidia viridescens (Brugiere, 1792)
Ciona intestinalis sp. B (Caputi, 2007)

Potentially Misidentified Species

Ciona robusta
Ciona robusta was formerly considered conspecific with C. intestinalis. Genetic studies in Europe found that two species were present, and overlapping in the English Channel (Caputi et al. (2007). The form widely distributed on the coast of southern Europe, Mediterranean Sea and the Pacific was initially designated 'Species A', and was found to correspond to C. robusta, described from Japan by Hoshino and Tokioka in 1967.

Ciona savigny
Ciona savignyi is native to the Northwest Pacific, introduced to the West Coast and New Zealand, but cryptogenic off Alaska-northern British Columbia.

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

Habitats

General HabitatMarinas & DocksNone
General HabitatCoarse Woody DebrisNone
General HabitatRockyNone
General HabitatUnstructured BottomNone
General HabitatVessel HullNone
General HabitatGrass BedNone
Salinity RangeMesohaline5-18 PSU
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEpibenthicNone

Life History


Tolerances and Life History Parameters

Minimum Temperature (ºC)0Gulmar Fjord, Sweden (Dybern 1965)
Maximum Temperature (ºC)27Experimental, animals from Brest, France (Kenworthy et al. 2018)
Minimum Salinity (‰)97 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 (‰)35Average Atlantic Ocean salinity
Minimum Reproductive Temperature8Field, Gulmarfjord, Sweden (Dybern et al. 1965).
Maximum Reproductive Temperature22Field, Gulmarfjord, Sweden (Dybern et al. 1965).
Minimum Reproductive Salinity10Field and experimental, zygotes, Baltic Sea populations (Dybern 1967)
Maximum Reproductive Salinity35Experimental, zygotes, Svenningesar, Sweden (Dybern 1967)
Minimum Duration1.5Egg + larva, Dybern 1965, 23C; Katz 1983
Maximum Duration7Dybern 1965, 8 C
Minimum Height (mm)50Maturity occurs at 50-80 mm height (Carver et al. 206).
Maximum Height (mm)150Van Name 1945
Broad Temperature RangeNoneCold temperate-Warm temperate
Broad Salinity RangeNoneMesohaline-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


Regional Impacts

NA-ET1Gulf of St. Lawrence to Bay of FundyEconomic ImpactFisheries
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-S3NoneEconomic ImpactFisheries
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-S3NoneEcological ImpactCompetition
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-ET2Bay of Fundy to Cape CodEconomic ImpactFisheries
Ciona intestinalis was a dominant fouling organism at oyster and aquaculture sites in the Damariscotta River, Maine (Bullard et al. 2015)
N070Damariscotta RiverEconomic ImpactFisheries
Ciona intestinalis was a dominant fouling organism at oyster and aquaculture sites in the Damariscotta River, Maine (Bullard et al. 2015)
NA-ET3Cape Cod to Cape HatterasEconomic ImpactFisheries
On Matha's Vineyard, Ciona intestinalis was frequently found fouling aquacultural gear, though not attaching to shellfish (Carman et al. 2010).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NA-ET2 Bay of Fundy to Cape Cod 1838 Def Estab
NA-ET1 Gulf of St. Lawrence to Bay of Fundy 1885 Def Estab
NA-S3 None 1912 Def Estab
NA-ET3 Cape Cod to Cape Hatteras 1850 Def Estab
AR-IV None 2007 Def Estab
AR-V None 0 Native Estab
NEA-II None 0 Native Estab
NEA-III None 0 Native Estab
B-I None 1767 Native Estab
B-II None 0 Native Estab
NEA-IV None 0 Native Estab
NWP-4a None 2010 Def Estab
NEA-V None 0 Native Estab
B-III None 0 Native Estab
B-IV None 0 Native Estab
M040 Long Island Sound 1987 Def Estab
M020 Narragansett Bay 1880 Def Estab
M010 Buzzards Bay 1908 Def Estab
M090 Delaware Bay 1978 Def Unk
N100 Casco Bay 1873 Def Estab
N185 _CDA_N185 (Cape Cod) 1882 Def Estab
NA-ET2 Bay of Fundy to Cape Cod 1838 Def Estab
CAR-VII Cape Hatteras to Mid-East Florida 1978 Def Unk
N135 _CDA_N135 (Piscataqua-Salmon Falls) 1912 Def Estab
N165 _CDA_N165 (Charles) 1912 Def Estab
S020 Pamlico Sound 1978 Def Unk
N180 Cape Cod Bay 1879 Def Estab
N070 Damariscotta River 0 Def Estab
N010 Passamaquoddy Bay 1868 Def Estab
B-V None 0 Native Estab
SA-I None 1940 Def Estab
M023 _CDA_M023 (Narragansett) 2019 Prb Estab
N130 Great Bay 2018 Def Estab
NA-ET2 Bay of Fundy to Cape Cod 2018 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude

References

Aldred, Nick; Clare, Anthony S. (2014) Mini-review: Impact and dynamics of surface fouling by solitary and compound ascidians, Biofouling 30(3): 259-270

Altman, Safra; Whitlatch, Robert B. (2007) Effects of small-scale disturbance on invasion success in marine communities., Journal of Experimental Marine Biology and Ecology 342: 15-29

Ashton, Gail ; Boos, Karin; Shucksmith, Richard; Cook, Elizabeth (2006) Risk assessment of hull fouling as a vector for marine non-natives in Scotland, Aquatic Invasions 1(4): 214-218

Baldwin, Andy; Leason, Diane (2016) Potential Ecological impacts of Emerald Ash Borer on Maryland's Eastern Shore, In: None(Eds.) None. , <missing place>. Pp. <missing location>

Barnes, Robert D. (1983) Invertebrate Zoology, Saunders, Philadelphia. Pp. 883

Bastida-Zavala, Rolando J; Ten Hove, Harry A. (2003) Revision of Hydroides Gunnerus, 1758 (Polychaeta: Serpulidae) from the Eastern Pacific region and Hawaii, Beaufortia 53(4): 67-110

Bergström, Per; Thorngren, Linnea; Strand, Lisa; Lindegarth, Mats (2021) Identifying high-density areas of oysters using species distribution modeling: Lessons for conservation of the native Ostrea edulis and management of the invasive Magallana (Crassostrea) gigas in Sweden, Ecology and Evolution Published online: 1-21

Berrill, N. J. (1950) <missing title>, Ray Society, London. Pp. <missing location>

Bishop, John D.D.; Wood, Christine A.; Yunnie, Anna L. E.; Griffiths, Carly A. (2015a) Unheralded arrivals: non-native sessile invertebrates in marinas on the English coast, Aquatic Invasions 10: 249-264

Boffelli, Dario; Weer, Claire V.; Weng, Li; Lewis, Keith D.; Shoukry, Malak I.; Pachter, Lior; Keys, David N.; Rubin, Edward M. (2004) Intraspecies sequence comparisons for annotating genomes, Genome Research 14: 2406-2411

Bouchemousse, Sarah; Bishop, John D. D.; Viard, Frédérique (2016) Contrasting global genetic patterns in two biologically similar, widespread and invasive Ciona species (Tunicata, Ascidiacea), Scientific Reports 6: 24875

Bouchemousse, Sarah; Leveque, Laurent; Dubois, Guillaume; Viard, Frederique (2016) Co-occurrence and reproductive synchrony do not ensure hybridization between an alien tunicate and its interfertile native congener, Evolutionary Ecology 30: 69-87

Brunetti, Riccardo and 5 authors 1, CARMELA GISSI 2, ROBERTA PENNATI 2, FEDERICO CAICCI 3, FABIO GASPARINI 3 and LUCIA MANNI 3 (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis, Zoological Systematics and Evolutionary Research 53(3): 186--193

Brunetti, Riccardo; Gissi, Carmela; Pennati, Roberta; Caicci, Federico; Gasparini, Fabio; Manni, Lucia (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis, Journal of Zoological Systematics and Evolutionary Research Published online: <missing location>

Cacabelos, Eva and 10 auhtors (2019) First record of Caulerpa prolifera in the Azores (NE Atlantic), Botanica Marina 62(2): 155-160

Caputi, Luigi ; Andreakis, Nikos; Mastrototaro, Francesco; Cirino, Paola; Vassillo, Mauro; Sordino, Paolo (2007) Cryptic speciation in a model invertebrate chordate., Proceedings of the National Academy of Sciences 104(22): 9364-9369

Caputi, Luigi; Crocetta, Fabio; Toscano, Francesco; Sordino, Paolo; Cirino, Paola (2015) Long-term demographic and reproductive trends in Ciona intestinalis sp. A, Marine Ecology 36: 118-128

Carman, M. R.; Morris, J. A.; Karney, R. C.; Grunden, D. W. (2010) An initial assessment of native and invasive tunicates in shellfish aquaculture of the North American east coast, Journal of Applied Ichthyology 26(Suppl. 2): 8-11

Carman, Mary R. and 13 authors (2016) Distribution and diversity of tunicates utilizing eelgrass as substrate in the western North Atlantic between 39° and 47° north latitude (New Jersey to Newfoundland), Management of Biological Invasions Published online: <missing location>

Carman, Mary R.; Bullard, S.G.; Donnelly, J.P. (2007) Water quality, nitrogen pollution, and ascidian diversity in coastal waters of southern Massachusetts, USA., Journal of Experimental Marine Biology and Ecology 342: 175-178

Carver, C. E.; Chisholm A; Mallet, A. L. (2003) Strategies to mitigate the impacts of Ciona intestinalis biofouling on shellfish production., Journal of Shellfish Research 22: 521-631

Collin, Samuel B.; Edwards, Paul K.; Leung, Brian; Johnson, Ladd E. (2013) Optimizing early detection of non-indigenous species: Estimating the scale of dispersal of a nascent population of the invasive tunicate Ciona intestinalis (L.), Marine Pollution Bulletin 73: 64-69

Collin, Samuel B.; Johnson, Ladd E. (2014) Invasive species contribute to biotic resistance: negative effect of caprellid amphipods on an invasive tunicate, Biological Invasions 16: 2209-2219

Comeau, Luc A.; Filgueira, Ramon; Guyondet, Thomas; Somier, Remi (2015) The impact of invasive tunicates on the demand for phytoplankton in longline mussel farms, Aquaculture 441: 91-105

Couthouy, Joseph P. (1838) Descriptions of new species of Mollusca and shells, and remarks on several polypi found in Massachusetts Bay, Boston Journal of Natural History 2: 53-111

Daigle, Rémi M.; Herbinger, Christophe M. (2009) Ecological interactions between the vase tunicate (Ciona intestinalis) and the farmed blue mussel (Mytilus edulis) in Nova Scotia, Canada, Aquatic Invasions 4(1): 177-187

Davidson, John D. P.; Landry, Thomas; Johnson, Gerald R.; Ramsay, Aaron; Quijón, Pedro A. (2015) A field trial to determine the optimal treatment regime for Ciona intestinalis on mussel socks, Management of Biological Invasions In press: <missing location>

Dybern, Bernt I. (1965) The life cycle of Ciona intestinalis (L.) F. typic in relation to the environmental temperature, Oikos 16: 109-131

Dybern, Bernt I. (1967) The distribution and salinity tolerence of Ciona intestinalis typica with special reference to the waters around souhern scaninavia., Ophelia 4: 207-226

Dybern, Bernt I. (1969) Distribution and ecology of ascidians in Kvirturdvikpollen and Vagsbopollen on the west coast of Norway, Sarsia 37: 21-40

Fairey, Russell; Dunn, Roslyn; Sigala, Marco; Oliver, John (2002) <missing title>, California Department of Fish and Game, Sacramento. Pp. <missing location>

Fay, R. C.; Vallee, J. A. (1979) A survey of the littoral and sublittoral ascidians of southern California, including the Channel Islands., Bulletin of the Southern California Academy of Sciences 78(2): 122-135

Gauff, Robin P. M.; Lejeusne, Christophe; Arsenieff, Laure ; Bohner, Olivier; Coudret , Jerome; Desbordes, Florian; Jandard, Alise; Loisel, Gaetan (2022) Alien vs. predator: influence of environmental variability and predation on the survival of ascidian recruits of a native and alien species, Biological Invasions Published online: Published online

Gittenberger, Adriaan (2009) Invasive tunicates on Zeeland and Prince Edward Island mussels, and management practices in The Netherlands., Aquatic Invasions 4(1): 279-281

Gosner, Kenneth L. (1978) A field guide to the Atlantic seashore., In: (Eds.) . , Boston. Pp. <missing location>

Gould, Augustus A. (1870) <missing title>, Wright and Potter, State Printers, Boston. Pp. <missing location>

Harris, Larry G.; Irons, Katherine P. (1982) Artificial Substrates, <missing publisher>, <missing place>. Pp. 131-174

Haydar, Deniz (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean, Diversity and Distributions 18: 101-110

Hoshino, Z.; Nishikawa, T. (1985) Taxonomic Studies of Ciona intestinalis, Publication of the Seto Marine Biological Laboratory 30(1/3): 61-79

Hoshino, Zen'ichiro; Tokioka, Takasi (1967) An unusually robust Ciona from the northeastern coast of Honsyu island, Japan, Publications of the Seto Marine Biological Laboratory 15(4): 275-290

Kanary, Lisa and 5 authors (2011) Predicting larval dispersal of the vase tunicate Ciona intestinalis in a Prince Edward Island estuary using a matrix population model, Aquatic Invasions 6(4): 491-506

Kanary, Lisa; Locke, Andrea; Watmough, James (2010) Evaluating the effectiveness of SCUBA-based visual searches for an invasive tunicate, Ciona intestinalis, in a Prince Edward Island estuary, Aquatic Invasions 5(2): <missing location>

Katz, Michael J. (1983) Comparative anatomy of the tunicate tadpole, Ciona intestinalis, Biological Bulletin 164: 1-27

Kott, P. (1998) Tunicata, Zoological Catalogue of Australia 34: 51-252

Lee, Taekjun; Shin, Sook (2014) Morphological and molecular identification of an introduced alien sea squirt (Tunicata: Ascidiacea) in Korea, Proceedings of the Biological Society of Washington 127(1): 284-297

LeGresley, Murielle M.; Martin, Jennifer L.; McCurdy, Paul; Thorpe, Bruce; Chang, Blythe D. (2008) Nonindigenous tunicate species in the Bay of Fundy, eastern Canada, ICES Journal of Marine Science 65: 770-774

Lin, Yaping; Chen, Yiyong; Xiong, Wei; Zhan, Aibin (2016) Genomewide gene-associated microsatellite markers for the model invasive ascidian, Ciona intestinalis species complex, Molecular Ecology Resources 16: 784-793

Locke, Andrea (2009) A screening procedure for potential tunicate invaders of Atlantic Canada., Aquatic Invasions 4(1): 71-79

Locke, Andrea; Doe, Kenneth G.; Fairchild, Wayne L.; Jackman, Paula M.; Reese, Erica J. (2009) Preliminary evaluation of effects of invasive tunicate management with acetic acid and calcium hydroxide on non-target marine organisms in Prince Edward Island, Canada., Aquatic Invasions 4(1): 221-236

Lutz-Collins, Vanessa; Ramsay, Aaron; Quijón, Pedro A.; Davidson, Jeffrey (2009) Invasive tunicates fouling mussel lines: evidence of their impact on native tunicates and other epifaunal invertebrates., Aquatic Invasions 4(1): 213-220

Martin, Jennifer L.; LeGresley, Murielle M.; Thorpe, Bruce; McCurdy, Paul (2011) Non-indigenous tunicates in the Bay of Fundy, eastern Canada (2006-2009), Aquatic Invasions 6(4): corrected proof

McKenzie, Cynthia H.; Matheson, Kyle; Caines, Scott; Wells, Terri (2016) Surveys for non-indigenous tunicate species in Newfoundland, Canada (2006-2014): a first step towards understanding impact and control, Management of Biological Invasions 7(1): 21-32

McKenzie, Cynthia H.; Matheson, Kyle; Reid, Vanessa; Wells, Terri; Mouland, Derek; Green, Darrell; Pilgrim, Brooks; Perry, Geoff (2016) The development of a rapid response plan to control the spread of the solitary invasive tunicate, Ciona intestinalis (Linnaeus, 1767), in Newfoundland and Labrador, Canada, Management of Biological Invasions 7(1): 87-100

McLaughlin, Janelle; Bourque, Daniel; LeBlanc, Angeline R.; Fortin, Guillaume (2013) Effect of suspended inorganic matter on fertilization success, embryonic development, larval settlement, and juvenile survival of the vase tunicate Ciona intestinalis (Linnaeus, 1767), Aquatic Invasions 8(4): 375-388

Mead, A.; Carlton, J. T.; Griffiths, C. L. Rius, M. (2011b) Introduced and cryptogenic marine and estuarine species of South Africa, Journal of Natural History 39-40: 2463-2524

Millar, R. H. (1954) The annual growth and reproductive cycle of four ascidians, Journal of the Marine Biological Association of the United Kingdom 31(1): 41-61

Millar, R.H. (1971) Ascidians as fouling organisms., In: Jones, E.B. Gareth; Eltringham S.K.(Eds.) Marine borers, fungi and fouling organisms of wood. , Brussels. Pp. 185-195

2003-2008 Introduced and cryptogenic species of the North Atlantic. http://massbay.mit.edu/exoticspecies/exoticmaps/introduced.html

Moura, Carlos J.; Collins, Allen G.; Santos, Ricardo S.; Lessios, Harilaos (2019) Predominant east to west colonizations across major oceanic barriers: Insights into the phylogeographic history of the hydroid superfamily Plumularioidea, suggested by a mitochondrial DNA barcoding marker, Ecology and Evolution 9: :13001–13016.

Nydam, Marie L.; Harrison, Richard G. (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea)., Marine Biology 151: 1839-1847

Nydam, Marie L.; Harrison, Richard G. (2010) Polymorphism and divergence within the ascidian genus Ciona, Molecular Phylogenetics and Evolution 56: 718-726

Nydam, Marie L.; Harrison, Richard G. (2011) Introgression despite substantial divergence in a broadcast spawning marine invertebrate, Evolution 65(3): 429-442

Occhipinti-Ambrogi, Anna; Galil, Bella S. (2004) A uniform terminology on bioinvasions: a chimera or an operative tool?, Marine Pollution Bulletin 49: 688-694

Osman, Richard W.; Whitlatch, Robert B. (1995) The influence of resident adults on recruitment: a comparison to settlement., Journal of Experimental Marine Biology and Ecology 190: 169-198

Pante, Eric and 11 authors (2015) Species are hypotheses: avoid connectivity assessments based on pillars of sand, Molecular Ecology 34: 525-544

Pascoe, P. L.; Parry, H. E.; Hawkins, A. J. S. (2007) Dynamic filter-feeding responses in fouling organisms, Aquatic Biology 1: 177-185

Patanasatienkul, Thitiwan; Revie, Crawford W.; Davidson, Jeff; Sanchez, Javier (2014) Mathematical model describing the population dynamics of Ciona intestinalis, a biofouling tunicate on mussel farms in Prince Edward Island, Canada, Management of Biological Invasions 5: in press

Pederson, Judith, and 13 authors (2021) 2019 Rapid Assessment Survey of marine bioinvasions of southern New England and New York, USA, with an overview of new records and range expansions, Bioinvasions Records 10(2): 22-–237

Plough, Harold H. (1978) <missing title>, Johns Hopkins University Press, Baltimore. Pp. <missing location>

Rajbanshi, Rubi; Pederson, Judith (2007) Competition among invading ascidians and a native mussel., Journal of Experimental Marine Biology and Ecology 342: 163-165

Ramsay, Aaron; Davidson, Jeff; Landry, Thomas; Arsenault, Garth (2008) Process of invasiveness among exotic tunicates in Prince Edward Island, Canada., Biological Invasions 10(8): 1311-1316

Reid, Vanessa; McKenzie, Cynthia; Matheson, Kyle; Wells, Terri; Couturier, Cyr (2016) Post-metamorphic attachment by solitary ascidian Ciona intestinalis (Linnaeus, 1767) juveniles from Newfoundland and Labrador, Canada, Management of Biological Invasions 7(1): 67-76

Roman, Joe. (2006) Diluting the founder effect: cryptic invasions expand a marine invader's range., Marine Ecology Progress Series 311: 251-262

Rosa, M. and 6 authors (2013) Biofouling ascidians on aquaculture gear as potential vectors of harmful algal introductions, Harmful Algae 23: 1-7

Roux, Camille; Tsagkogeorga, Georgia; Bierne, Nicolas; Galtier, Nicolas (2013) Crossing the species barrier: Genomic hotspots of introgression between two highly divergent Ciona intestinalis species, Molecular Biology and Evolution 30(7): 1574-1587

Sargent, Philip S.; Wells, Terri; Matheson, Kyle; McKenzie, Cynthia H.; Deibel, Don (2013) First record of vase tunicate, Ciona intestinalis (Linnaeus, 1767) in coastal Newfoundland waters, Bioinvasions Records 2(2): in press

Sato, Atsuko; Satoh, Nori; Bishop, John D. D. (2012) Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry, Marine Biology 159: 1611-1619

Silva, Nathan; Smith, William C. (2008) Inverse correlation of population similarity and introduction date for invasive ascidians, PLOSOne 3(6): available online

Stachowicz, John J.; Byrnes, Jarrett E. (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors., Marine Ecology Progress Series 311: 251-262

Stachowicz, John J.; Fried, Heather; Osman, Richard W.; Whitlatch, Robert B. (2002a) Biodiversity, invasion resistence, and marine ecosystem function: reconciling pattern and process., Ecology 83(9): 2575-2590

Stewart-Clark, Sarah E.; Davidson, Jeffrey; Greenwood, Spencer J. (2013) Monitoring for propagules of Ciona intestinalis in marine water samples: the development of temporal gene expression markers for viability and life stage specific assays, Management of Biological Invasions 4(3): 207-217

Stimpson, William (1852) Several new ascidians from the coast of the United States, Proceedings of the Boston Society of Natural History 4: 228-238

Sumner, Francis B., Osburn, Raymond C., Davis, Bradley M. (1913a) A biological survey of the waters of Woods Hole and vicinity. Part I. Section I. Physical and Zoological. Section II. Botanical, Bulletin of the Bureau of Fisheries 31: 1-544

Suzuki, Miho M.; Nishikawa, Teruaki ; Bird, Adrian (2005) Genomic approaches reveal unexpected genetic divergence within Ciona intestinalis., Journal of Molecular Evolution 61: 627-635

Therriault, Thomas W.; Herborg, Leif-Matthias (2008) Predicting the potential distribution of the vase tunicate Ciona intestinalis in Canadian waters: Informing a risk assessment., ICES Journal of Marine Science 65: 788-794

Therriault, Thomas; Herborg, Leif-Matthias (2008) A qualitiative biological risk assessment for vase tunicate Ciona intestinalis in Canadian waters: using expert knowledge., ICES Journal of Marine Science 65: 781-787

Thorarinsdottir, Gudrun G.; Gunnarsson, Karl; Gíslason, Ó. Sindri (2014) Marine invasive species in the Arctic, Nordic Council of Ministers, Copenhagen, Denmark. Pp. 83-109

2002-2021 Invertebrate Zoology Collections Database. <missing description>

Ulman, Aylin and 17 authors (2017) A massive update of non-indigenous species records in Mediterranean marinas, PeerJ 5( e3954): <missing location>

Van Name, Willard G. (1912) Simple ascidians of the coasts of New England and neighboring British provinces., Proceedings of the Boston Society of Natural History 34: 439-619

Van Name, Willard G. (1945) The North and South American ascidians, Bulletin of the American Museum of Natural History 84: 1-462

Vazquez, E.; Urgorri, V. (1992) [Fouling ascidians in the inlet of A Grana, Ria de Ferrol, (Galicia, Spain)], Nova Acta Cientifica Compostelana (Bioloxia) 3: 161-167

Vercaemer, Benedikte; Sephton, Dawn; Nicolas, Jean M.; Howes, Stephanie; Keays, Joanne (2011) Ciona intestinalis environmental control points: Field and laboratory investigations, Aquatic Invasions 6(4): 477-490

Verrill, A.E.; Smith, S.I. (1873) <missing title>, 1 Report of the United States Commission of Fish and Fisheries, <missing place>. Pp. 1-757

Visscher, J. Paul (1927) Nature and extent of fouling of ship's bottoms., Bulletin of the Bureau of Fisheries 43: 193-252

Whitlatch, Robert B.; Osman, Richard W. (2009) Post-settlement predation on ascidian recruits: predator responses to changing prey density., Aquatic Invasions 4(1): 121-131

Woods Hole Oceanographic Institution, United States Navy Dept. Bureau of Ships (1952) Marine fouling and its prevention., United States Naval Institute., Washington, D.C.. Pp. 165-206

2008-2016 YPM Invertebrate Zoology - Online Catalog. http://peabody.yale.edu/collections/search-collections?iz

Zhan, Aibin; Briski, Elizabeta; Bock, Dan G.; Ghabooli, Sara; MacIsaac, Hugh J. (2015) Ascidians as models for studying invasion success, Marine Biology 162: 2449-2470

Zhan, Aibin; MacIsaac, Hugh J .; Cristescu, Melania E. (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity complex: from regional endemism to global homogeneity, Molecular Ecology 19: 4678-4694