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:

Haloaa 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Bay, British Columbia to San Diego Bay, California (Gosliner and Behrens 2006; Hanson et al. 2012; Ruiz et al., unpublished data, Haizea Jimenez, personal communication 2013).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:

Haloa 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, Haloa 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

Haloa 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:   Haloa
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:

Haloa 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 tolerates salinities of 20-25 PSU Trkov et al. 2024). 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

Life History

Haloa 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).

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.
CACaliforniaEcological 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.
CACaliforniaEconomic 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)., 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).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
P020 San Diego Bay 2013 Non-native Established
NEP-VI Pt. Conception to Southern Baja California 2013 Non-native Established
P110 Tomales Bay 2008 Non-native Established
NEP-V Northern California to Mid Channel Islands 2000 Non-native Established
P090 San Francisco Bay 1999 Non-native Established

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude
697261 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-27 Pete's Harbor, San Francisco Bay Non-native 37.5006 -122.2242
698015 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 Fruitvale Bridge, San Francisco Bay Non-native 37.7690 -122.2296
698605 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-27 Coyote Point Marina, San Francisco Bay Non-native 37.5907 -122.3180
698919 Introduced Species Study 2010 2010-07-14 Point San Pablo Yacht Harbor Non-native 37.9643 -122.4185
699326 Introduced Species Study 2010 2010-07-15 San Pablo Bay Pumphouse Non-native 38.0446 -122.4326
699414 Introduced Species Study 2005 2005-07-06 Coyote Point Non-native 37.5920 -122.3210
699894 Introduced Species Study 2010 2010-05-31 Redwood Creek - Marina Non-native 37.5021 -122.2130
700465 Introduced Species Study 2010 2010-06-01 Coyote Point Marina Non-native 37.5905 -122.3177
700805 Introduced Species Study 2010 2010-06-01 Sea Plane Harbor Non-native 37.6349 -122.3848
701113 Gosliner and Behrens 2006 1999 Brisbane Harbor [Sierra Point Marina] Non-native 37.6732 -122.3807
702139 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 San Leandro Marina, San Francisco Bay Non-native 37.6966 -122.1932
702965 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Sierra Point Marina, San Francisco Bay Non-native 37.6732 -122.3807
704289 Cohen et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Brisbane Lagoon, San Francisco Bay Non-native 37.6862 -122.3906
704592 Introduced Species Study 2010 2010-06-01 Sierra Point Marina Non-native 37.6740 -122.3792
760261 California Academy of Sciences Invertebrate Zoology Collections Database 2001 2001-03-21 Brisbane Marina [Sierra Point Marina] Non-native 37.6732 -122.3807
760262 California Academy of Sciences Invertebrate Zoology Collections Database 2001 2001-09-24 Oyster Point Marina Non-native 37.6632 -122.3818
760263 California Academy of Sciences Invertebrate Zoology Collections Database 2001 2001-11-15 Brisbane Marina [Sierra Point Marina] Non-native 37.6767 -122.3808
760264 California Academy of Sciences Invertebrate Zoology Collections Database 2002 2002-03-08 Oyster Point Marina Non-native 37.6631 -122.3817
760265 California Academy of Sciences Invertebrate Zoology Collections Database 2003 2003-05-07 Redwood City Yacht Harbor Non-native 37.5023 -122.2114
760266 California Academy of Sciences Invertebrate Zoology Collections Database 2003 2003-10-10 Redwood City Yacht Harbor Non-native 37.5024 -122.2133
760267 California Academy of Sciences Invertebrate Zoology Collections Database 2003 Lake Merritt Non-native 37.8025 -122.2578
760268 Brant et al. 2010 2005 Crab Cove (northern end of Robert Crown Memorial State Beach) Non-native 37.7678 -122.2777
760269 Brant et al. 2010 2006 Robert Crown Memorial State Beach, southern end Non-native 37.7525 -122.2493
760270 Brant et al. 2010 2007 Damon Slough (Lion Creek) Non-native 37.7539 -122.2060
760271 Brant et al. 2010 2008 Lake Merritt Non-native 37.8062 -122.2563
767393 Ruiz et al., 2015 2012 2012-08-16 Tomales-SNPS, Bodega Bay, California, USA Non-native 38.1359 -122.8719
768057 Ruiz et al., 2015 2012 2012-09-11 Ballena Isle Marina, San Francisco Bay, CA, California, USA Non-native 37.7676 -122.2869
768229 Ruiz et al., 2015 2012 2012-09-13 San Leandro Marina, San Francisco Bay, CA, California, USA Non-native 37.6962 -122.1919
768270 Ruiz et al., 2015 2013 2013-08-15 Ballena Isle Marina, San Francisco Bay, CA, California, USA Non-native 37.7656 -122.2858
770944 Ruiz et al., 2021a 2017 2017-09-25 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5023 -122.2124
771087 Ruiz et al., 2021a 2017 2017-09-19 Richmond Marina Bay Yacht Harbor, San Francisco Bay, California, USA Non-native 37.9129 -122.3494
771148 Ruiz et al., 2021a 2017 2017-09-27 Oakland Yacht Club, San Francisco Bay, California, USA Non-native 37.7837 -122.2640
771526 Ruiz et al., 2021a 2017 2017-09-20 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.5048 -122.2574
771551 Ruiz et al., 2021a 2017 2017-09-20 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.5048 -122.2574
771569 Ruiz et al., 2021a 2017 2017-09-20 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.5048 -122.2574
771721 Ruiz et al., 2021a 2018 2018-09-19 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.8047 -122.2573
771727 Ruiz et al., 2021a 2018 2018-09-19 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.8047 -122.2573
771735 Ruiz et al., 2021a 2018 2018-09-19 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.8047 -122.2573
771743 Ruiz et al., 2021a 2018 2018-09-19 Lake Merritt Boat House, San Francisco Bay, California, USA Non-native 37.8047 -122.2573
771903 Ruiz et al., 2021a 2018 2018-09-24 Ballena Isle Marina, San Francisco Bay, California, USA Non-native 37.7654 -122.2845
771927 Ruiz et al., 2021a 2018 2018-09-24 Ballena Isle Marina, San Francisco Bay, California, USA Non-native 37.7654 -122.2845
771940 Ruiz et al., 2021a 2018 2018-09-24 Ballena Isle Marina, San Francisco Bay, California, USA Non-native 37.7654 -122.2845
771982 Ruiz et al., 2021a 2018 2018-09-24 Ballena Isle Marina, San Francisco Bay, California, USA Non-native 37.7654 -122.2845
772011 Ruiz et al., 2021a 2018 2018-09-21 Oakland Yacht Club, San Francisco Bay, California, USA Non-native 37.7843 -122.2648
772304 Ruiz et al., 2021a 2018 2018-09-18 Richmond Marina Bay Yacht Harbor, San Francisco Bay, California, USA Non-native 37.9139 -122.3461
775481 Ruiz et al., 2022 2014 2014-09-09 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775482 Ruiz et al., 2022 2014 2014-09-09 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775483 Ruiz et al., 2022 2014 2014-09-16 Coyote Point Marina, San Francisco Bay, California, USA Non-native 37.5895 -122.3160
775484 Ruiz et al., 2022 2014 2014-09-11 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5024 -122.2134
775485 Ruiz et al., 2022 2014 2014-09-11 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5024 -122.2134
775486 Ruiz et al., 2022 2014 2014-09-15 Loch Lomond Marina, San Francisco Bay, California, USA Non-native 37.9723 -122.4829
775487 Ruiz et al., 2022 2015 2015-09-21 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5022 -122.2129
775488 Ruiz et al., 2022 2015 2015-09-21 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5022 -122.2129
775489 Ruiz et al., 2022 2015 2015-09-21 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5022 -122.2129
775490 Ruiz et al., 2022 2015 2015-09-17 Ballena Isle Marina, San Francisco Bay, California, USA Non-native 37.7679 -122.2863
775491 Ruiz et al., 2022 2015 2015-09-22 Coyote Point Marina, San Francisco Bay, California, USA Non-native 37.5887 -122.3164
775492 Ruiz et al., 2022 2015 2015-09-16 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775493 Ruiz et al., 2022 2015 2015-09-16 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775494 Ruiz et al., 2022 2015 2015-09-16 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775495 Ruiz et al., 2022 2016 2016-09-22 Coyote Point Marina, San Francisco Bay, California, USA Non-native 37.5898 -122.3165
775496 Ruiz et al., 2022 2016 2016-09-22 Coyote Point Marina, San Francisco Bay, California, USA Non-native 37.5898 -122.3165
775497 Ruiz et al., 2022 2016 2016-09-26 Redwood City Marina, San Francisco Bay, California, USA Non-native 37.5027 -122.2138
775498 Ruiz et al., 2022 2016 2016-09-14 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775499 Ruiz et al., 2022 2016 2016-09-14 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
775500 Ruiz et al., 2022 2016 2016-09-14 San Leandro Marina, San Francisco Bay, California, USA Non-native 37.6978 -122.1928
819490 Ruiz GM and JB Geller (2015) 2013 Marriott Marina None 32.7065 -117.1695
819491 Ruiz GM and JB Geller (2015) 2013 Cabrillo Isle None 32.7249 -117.2063
819492 Ruiz GM and JB Geller (2015) 2013 Imperial Beach None 32.6141 -117.1273
819493 Ruiz GM and JB Geller (2015) 2013 Point Loma None 32.6912 -117.2390
819494 Ruiz GM and JB Geller (2015) 2013 Chula Vista None 32.6407 -117.1251
819495 Ruiz GM and JB Geller (2015) 2013 National City None 32.6750 -117.1348
819496 Ruiz GM and JB Geller (2015) 2013 Fiddler's cove None 32.6483 -117.1402
819497 Ruiz GM and JB Geller (2015) 2013 None None
819498 Ruiz GM and JB Geller (2015) 2013 Coronado None 32.6843 -117.1606
819499 Ruiz GM and JB Geller (2015) 2013 Coronado Cays None 32.6339 -117.1332
820423 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oracle Park None 37.7780 -122.3843
820424 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Tiburon Ferry None 37.8724 -122.4540
820425 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Point Richmond None 37.9082 -122.3941
820426 Ruiz GM, Chang AL, and JB Geller (2023) 2022 San Francisco Marina None 37.8076 -122.4332
820427 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Hunter's Point None 37.7058 -122.3750
820428 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oyster Point None 37.6797 -122.3774
820429 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Richardson Bay None 37.8624 -122.4636
820430 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Albany None 37.8648 -122.3229
820431 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oakland None 37.6977 -122.2501
820432 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Ballena Isle None 37.7637 -122.3002

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