Invasion History

First Non-native North American Tidal Record: 1985
First Non-native West Coast Tidal Record: 1985
First Non-native East/Gulf Coast Tidal Record:

General Invasion History:

Haminoea japonica is native to the Northwest Pacific from northern Japan (Hakodate Bay, Hokkaido) to Hong Kong (Ito et al. 1996; Wu and Shin 1997; Huang 2001; Kil et al. 2005; Gosliner and Behrens 2006; Hanson et al. 2012). It has been reported from the Philippines (Poppe 2010, cited by Appeltans et al. 2014), but molecular analyses of Philippine specimens indicated that they belonged to several other species (Hanson et al. 2013). This snail inhabits shallow silt and mud bottoms, rocky shores, oyster beds, boat ramps, marinas and dock floats, where it grazes on algae (Gibson and Chia 1989a; Ito et al. 1996; Wu and Shin 1997; Gosliner and Behrens 2006).

Haminoea japonica was first found outside its native range before 1985, in the San Juan Islands, Washington, where it was described as a new species, H. callidegenita (Gibson and Chia 1989a). Established populations were later found in Spain (1992) and France (1993), and reported as H. callidegenita (Alvarez et al. 1993). On the West Coast of North America, its range extends from Boundary Bay, British Columbia to San Diego Bay, California (Gosliner and Behrens 2006; Hanson et al. 2012; Ruiz et al., unpublished data, Haizea Jimenez, personal communication 2013). Genetic analyses indicate that the likeliest source of West Coast and European populations is northeastern Japan. Since this region has few major international ports, but is a major source for transplanted Pacific Oyster (Crassostrea gigas) stocks, oyster plantings are the likeliest source of introduced populations (Hanson et al. 2012; Hanson et al. 2013).

North American Invasion History:

Invasion History on the West Coast:

Haminoea japonica was first reported on the West Coast in 1985 as a new species (H. callidegenita), found in oyster beds on Spencer Spit lagoon, Lopez Island, in the San Juan Islands, Washington. The snail had earlier been noticed by a scientist for its unusual mixture of planktotrophic and lecithotrophic reproductive modes, and may have been overlooked for a long time because of its similarity to the native species H. vesicula and H. virescens (Gibson and Chia 1989a). In 1999, it was seen in San Francisco bay, and initially identified as H. callidegenita, which was later found to be synonymous with H. japonica (Gosliner and Behrens 2006). It appears to be abundant in the south-central regions of the Bay from Oakland to Redwood City (California Academy of Sciences 2005; Cohen et al. 2005; Gosliner and Behrens 2006). It was found in Tomales Bay in 2008 (Hanson et al. 2012), and in San Diego Bay in 2013 (Ruiz et al., unpublished data, Haizea Jimenez, personal communication 2013). It is likely that this slug is present in other West Coast estuaries, and is being misidentified as one of the native Haminoea.

Invasion History Elsewhere in the World:

In Europe, Haminoea japonica was first identified (as H. callidegenita) in May 1992, in the Lagoon of Venice, Italy in the Adriatic Sea, although it is currently not established there (Alvarez et al. 1993; Zenetos et al. 2003, Occhipinti-Ambrogi et al. 2011; Crocetta 2012). In December 2002, it was reported from the Eo estuary, Spain on the Bay of Biscay. In 1993, this snail was found in Marennes-Oléron estuary, France, also on the Bay of Biscay (Alvarez et al. 1993). Subsequent introductions were reported from aquaculture tanks on the Bay of Cadiz, Spain in 1999 (Malaquias et al. 2006), and from oyster beds in Pléneuf-Val-André, Brittany, on the Gulf of St. Malo, France in 2003 (Hanson et al. 2013). The Venice populations have not been seen since (Zenetos et al. 2003), but established populations have been found in the lagoons of Fusaro and Sabàudia, Italy on the Tyrrhenian Sea in 2007 (Crocetta 2012; Crocetta et al. 2013; Hanson et al. 2013). These spotty occurrences throughout Europe, largely took place in areas of intense aquaculture, either Pacific Oyster (Crassostrea gigas) or Japanese Littleneck Clam (Venerupis philippinarum) (Hanson et al. 2013).


Description

Haminoea japonica has a thin, fragile, ellipsoidal shell, which is almost completely covered by its mantle. The head extends anteriorly in front of the shell and the posterior of the foot trails behind the shell. The head-shield is notched at the posterior end, divided by a groove throughout its length, and extended to form two small horns anteriorly. A posterior lobe of the mantle partially covers the shell. The shell is oval and dextrally coiled, but with no spire. Living specimens are up to 33 mm long, but preserved ones only reach about 20 mm. The aperture lip is rounded and rises above the body whorl. The color is gray to light-brown with many dark pigment spots, especially on the protruding lobes. Orange pigment spots are scattered over the body. Some specimens have a reddish tinge. Description based on Gibson and Chia (1989a), Gosliner and Behrens (2006), and Gosliner and Williams (2007).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Gastropoda
Subclass:   Opisthobranchia
Order:   Cephalaspidea
Family:   Haminoeidae
Genus:   Haminoea
Species:   japonica

Synonyms

Haloa japonica (Pilsbry, 1895)
Haminoea callidegenita (Gibson & Chia, 1989)
Haminoea rotundata (Adams, 1850)
Haminoea japonica (Pilsbry, 1895)

Potentially Misidentified Species

Haminoea virescens
Puget Sound to the Gulf of California in rocky intertidal pools (Abbott 1974)

Haminoea vesicula
Puget Sound to the Gulf of California on boat landings and mudflats (Abbott 1974)

Ecology

General:

Haminoea japonica is a shelled sea-slug (bubble snail) inhabiting harbors and estuaries. Like most opisthobranchs, it is hermaphroditic with internal fertilization. Eggs are laid in a sausage-shaped gelatinous mass, containing 200-700 eggs. This species is unusual in having two modes of development (poecilogony). Some H. japonica eggs undergo direct development and hatch as miniature adults (Gibson and Chia 1989b), while others hatch as lecithotrophic larvae and remain swimming for up to 20 days, but then metamorphose successfully. The mode of development is affected by the thickness of jelly surrounding the egg. A thick, intact jelly mass induces direct development and metamorphosis inside the egg capsule, whereas a thin or broken one results in lecithotrophic development and metamorphosis outside the egg (Gibson and Chia 1989b).

Haminoea japonica prefers sheltered, shallow habitats, conducive to growth of the algae in which it feeds. It occurs on rocky and soft substrates, oyster beds, and on man-made structures including pilings and floats (Gibson and Chia 1989a; Ito et al. 1996; Wu and Shin 1997; Gosliner and Behrens 2006). In the San Juan Islands, Washington, it is confined to coves and lagoons, and appears to require warmer water than the native Haminoea spp. (Strathman et al. 2002). This snail's salinity tolerance is not known, but it has not been reported from strongly brackish habitats. It feeds on a variety of micro- and macroalgae, including diatoms, green (Ulva sp.; Monostroma angicava) and red seaweeds (Polysiphonia japonica). It grazes on any available surface, including seaweeds, mud, sand, rocks, dock floats, and aquarium glass, scraping off algae and detritus, with its radula (Gibson and Chia 1989a; Ito et al. 1996).

Food:

Macrolgae; diatoms; detritus

Trophic Status:

Herbivore

Herb

Habitats

General HabitatUnstructured BottomNone
General HabitatOyster ReefNone
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Tidal RangeMid IntertidalNone
Vertical HabitatEpibenthicNone


Tolerances and Life History Parameters

Minimum Duration0Some H. japonica eggs undergo direct development and hatch as miniature adults (Gibson and Chia 1989a)
Maximum Duration20Some H. japonica eggs hatch as lecithotrophic larvae, and remain swimming for 20 up to 20 days, but then metamorphose successfully (Gibson and Chia 1989a).
Minimum Length (mm)33Gibson and Chia 1989a
Broad Temperature RangeNoneCold temperate-Warm temperate
Broad Salinity RangeNonePolyhaline-Euhaline

General Impacts

Haminoea japonica has possible ecological impacts on native snails and more definite economic impacts on human health, as a host of an apparently exotic trematode which causes severe 'Swimmer's Itch' in bathers (Brant et al. 2010; Hanson 2012).

Economic Impacts

Health: In June 2005, many swimmers at Robert Crown Memorial Beach, in Alameda, California, reported skin irritation, which was recognized as 'Swimmers Itch', caused by cercariae (larvae) of schistosome trematodes, whose first host is snails. The larvae burrow into human skin, causing inflammation, but are unable to complete metamorphosis in humans. Their normal final hosts are shorebirds. Possible host snails were examined and the source of the cercariae was found to be H. japonica. The trematode belonged to the genus Gigantobilharzia, previously known only from freshwater snails. The trematode appears to be exotic to North America, and first began infecting people in the late 1990s, most likely introduced with H. japonica (Anonymous 2005; Cohen 2005; Brant et al. 2010).

Ecological Impacts

Competition: The native H. vesicula is reported to have declined in areas invaded by H. japonica (Hanson 2012). However, the details and locations of these observations were not given.

Regional Impacts

NEP-VNorthern California to Mid Channel IslandsEconomic ImpactHealth
Cercaria of an unidentified schistosome trematode Gigantobilharzia sp. associated with H. japonica have been a cause of swimmers itch (cercarial dermatitis) among bathers in San Francisco Bay. The larvae burrow into human skin, causing inflammation, but are unable to complete metamorphosis. Their normal hosts are shorebirds. The trematode appears to be exotic to North America, and first began infecting people in the late 1990s, most likely introduced from elsewhere (Anonymous 2005; Cohen 2005; Brant et al. 2010).
P090San Francisco BayEconomic ImpactHealth
Cercaria of an unidentified schistosome trematode Gigantobilharzia sp. associated with H. japonica have been a cause of swimmers itch (cercarial dermatitis) among bathers in San Francisco Bay. The larvae burrow into human skin, causing inflammation, but are unable to complete metamorphosis. Their normal hosts are shorebirds. The trematode appears to be exotic to North America, and first began infecting people in the late 1990s, most likely introduced from elsewhere (Anonymous 2005; Cohen 2005; Brant et al. 2010).
NEP-VNorthern California to Mid Channel IslandsEcological ImpactCompetition
The native H. vesicula is reported to have declined in areas invaded by H. japonica. (Hanson 2012). However, the details and locations of these observations were not given.
NEP-IIIAlaskan panhandle to N. of Puget SoundEcological ImpactCompetition
The native H. vesicula is reported to have declined in areas invaded by H. japonica. (Hanson 2012). However, the details and locations of these observations were not given.

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NWP-4b None 0 Native Estab
NWP-3b None 0 Native Estab
EAS-III None 0 Native Estab
NWP-2 None 0 Native Estab
NWP-3a None 0 Native Estab
NEP-V Northern California to Mid Channel Islands 2000 Def Estab
NEP-III Alaskan panhandle to N. of Puget Sound 1985 Def Estab
P090 San Francisco Bay 1999 Def Estab
MED-VII None 1992 Def Unk
NEA-V None 1992 Def Estab
NWP-4a None 0 Native Estab
P292 _CDA_P292 (San Juan Islands) 1985 Def Estab
P290 Puget Sound 2006 Def Estab
NEA-IV None 2003 Def Estab
P297 _CDA_P297 (Strait of Georgia) 2011 Def Estab
P110 Tomales Bay 2008 Def Estab
NEP-VI Pt. Conception to Southern Baja California 2013 Def Estab
P020 San Diego Bay 2013 Def Estab
MED-III None 2007 Def Estab
MED-II None 0 Def Estab
EAS-VI None 1997 Def Unk
MED-I None 2018 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude
26800 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-27 Petes Harbor, South San Francisco Bay Def 37.5006 -122.2242
27543 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 Fruitvale Bridge, Oakland, San Francisco Bay Def 37.7690 -122.2296
28118 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-27 Coyote Point Marina, South San Francisco Bay Def 37.5907 -122.3180
28425 Foss 2011 2010 2010-07-14 Point San Pablo Yacht Harbor Def 37.9643 -122.4185
28825 Foss 2011 2010 2010-07-15 San Pablo Bay Pumphouse Def 38.0446 -122.4326
28913 Foss 2009 2005 2005-07-06 Coyote Point Def 37.5920 -122.3210
29378 Foss 2011 2010 2010-05-31 Redwood Creek - Marina Def 37.5021 -122.2130
29924 Foss 2011 2010 2010-06-01 Coyote Point Marina Def 37.5905 -122.3177
30254 Foss 2011 2010 2010-06-01 Sea Plane Harbor Def 37.6349 -122.3848
30553 Gosliner and Behrens 2006) 1999 1999-09-01 San Francisco Bay Def 37.8494 -122.3681
31550 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 San Leandro Marina, San Francisco Bay Def 37.6966 -122.1932
32315 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Sierra Point Marina, San Francisco Bay Def 37.6732 -122.3807
33608 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Brisbane Lagoon, San Francisco Bay Def 37.6862 -122.3906
33888 Foss 2011 2010 2010-06-01 Sierra Point Marina Def 37.6740 -122.3792
767393 Ruiz et al., 2015 2012 2012-08-16 Tomales-SNPS, Bodega Bay, California, USA Def 38.1359 -122.8719
768057 Ruiz et al., 2015 2012 2012-09-11 Ballena Isle Marina, San Francisco Bay, CA, California, USA Def 37.7676 -122.2869
768229 Ruiz et al., 2015 2012 2012-09-13 San Leandro Marina, San Francisco Bay, CA, California, USA Def 37.6962 -122.1919
768270 Ruiz et al., 2015 2013 2013-08-15 Ballena Isle Marina, San Francisco Bay, CA, California, USA Def 37.7656 -122.2858

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