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Bay, British Columbia to San Diego Bay, California (Gosliner and Behrens 2006; Hanson et al. 2012; Ruiz et al., unpublished data, Haizea Jimenez, personal communication 2013).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.
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.
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
NWP-4b None 0 Native Established
NWP-3b None 0 Native Established
EAS-III None 0 Native Established
NWP-2 None 0 Native Established
NWP-3a None 0 Native Established
NEP-V Northern California to Mid Channel Islands 2000 Non-native Established
NEP-III Alaskan panhandle to N. of Puget Sound 1985 Non-native Established
P090 San Francisco Bay 1999 Non-native Established
MED-VII None 1992 Non-native Unknown
NEA-V None 1992 Non-native Established
NWP-4a None 0 Native Established
P292 _CDA_P292 (San Juan Islands) 1985 Non-native Established
P290 Puget Sound 2006 Non-native Established
NEA-IV None 2003 Non-native Established
P297 _CDA_P297 (Strait of Georgia) 2011 Non-native Established
P110 Tomales Bay 2008 Non-native Established
NEP-VI Pt. Conception to Southern Baja California 2013 Non-native Established
P020 San Diego Bay 2013 Non-native Established
MED-III None 2007 Non-native Established
MED-II None 0 Non-native Established
EAS-VI None 1997 Non-native Unknown
MED-I None 2018 Non-native Established

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 Non-native 37.5006 -122.2242
27543 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 Fruitvale Bridge, Oakland, San Francisco Bay Non-native 37.7690 -122.2296
28118 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-27 Coyote Point Marina, South San Francisco Bay Non-native 37.5907 -122.3180
28425 Foss 2011 2010 2010-07-14 Point San Pablo Yacht Harbor Non-native 37.9643 -122.4185
28825 Foss 2011 2010 2010-07-15 San Pablo Bay Pumphouse Non-native 38.0446 -122.4326
28913 Foss 2009 2005 2005-07-06 Coyote Point Non-native 37.5920 -122.3210
29378 Foss 2011 2010 2010-05-31 Redwood Creek - Marina Non-native 37.5021 -122.2130
29924 Foss 2011 2010 2010-06-01 Coyote Point Marina Non-native 37.5905 -122.3177
30254 Foss 2011 2010 2010-06-01 Sea Plane Harbor Non-native 37.6349 -122.3848
30553 Gosliner and Behrens 2006) 1999 1999-09-01 San Francisco Bay Non-native 37.8494 -122.3681
31550 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 San Leandro Marina, San Francisco Bay Non-native 37.6966 -122.1932
32315 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Sierra Point Marina, San Francisco Bay Non-native 37.6732 -122.3807
33608 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-23 Brisbane Lagoon, San Francisco Bay Non-native 37.6862 -122.3906
33888 Foss 2011 2010 2010-06-01 Sierra Point Marina Non-native 37.6740 -122.3792
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

References

Abbott, R. Tucker (1974) American Seashells, Van Nostrand Reinhold, New York. Pp. <missing location>

Alvarez, L. A., Martinez, E., Cigarria, J., Rolan, E., Villani, G. (1993) Haminaea callidegenita Gibson and Chia, 1989 (Opisthobranchia: Cephalaspidea), a Pacific species introduced in European coasts, Iberus 11(2): 59-65

Anonymous (2005) Invaders cause rash of problems for swimmers, Nature 436: 616

Appeltans, W. et al. 2011-2015 World Registry of Marine Species. <missing URL>



Brant, Sara V.; Cohen, Andrew N.; James, David; Hui, Lucia; Hom, Albert; Loker, Eric S. (2010) Cercarial dermatitis transmitted by exotic marine snail, Emerging Infectious Diseases 16(9): 1357-1365

California Academy of Sciences 2005 <i>Haminoea japonica</i> (Pilsbry, 1895). <missing URL>



Carlton, James T. (Ed.) (2007) The Light and Smith Manual: Intertidal Invertebrates from Central California to Oregon Fourth Edition, Completely Revised and Expanded, University of California Press, Berkeley. Pp. <missing location>

Cohen, Andrew N. 2005-2024 Exotics Guide- Non-native species of the North American Pacific Coat. https://www.exoticsguide.org/



Cohen, Andrew N. and 10 authors (2005) <missing title>, San Francisco Estuary Institute, Oakland CA. Pp. <missing location>

Crocetta, Fabio (2012) Marine alien Mollusca in Italy: a critical review and state of the knowledge, Journal of the Marine Biological Association of the United Kingdom 92(6): 1357-1365

Crocetta, Fabio; Macali, Armando; Furfaro, Giulia; Cooke, Samantha; Villani, Guido; Valdés, Ángel (2013) Alien molluscan species established along the Italian shores: an update, with discussions on some Mediterranean 'alien species' categories, ZooKeys 277: 91:108

Foss, Stephen (2009) <missing title>, California Department of Fish and Game, Sacramento CA. Pp. <missing location>

Foss, Stephen (2011) <missing title>, California Department of Fish and Game, Office of Spill Prevention and Response, Sacramento. Pp. 54

Gibson, Glenys D.; Chia, Fu-Shiang (1989a) Description of a new species of Haminoea, Haminoea callidegenita (Mollusca: Opisthobranchia), with two other Haminoea species found in the northeast Pacific., Canadian Journal of Zoology 67: 914-922

Gibson, Glenys D.; Chia, Fu-Shiang (1989b) Developmental variability (pelagic and benthic) in Haminoea callidegenita (Opisthobranchia: Cephalaspidea) is influenced by egg mass jelly, Biological Bulletin 176(2): 103-110

Gosliner, Terrence M.; Behrens, David W. (2006) Anatomy of an invasion: Systematics and distribution of the introduced opisthobranch snail Haminoea japonica Pilsbry 1895 (Gastropoda: Opisthobranchia; Haminoeidae), Proceedings of the California Academy of Sciences 57(37): 1003-1010

Gosliner, Terrence; Williams, Gary C. (2007) The Light and Smith Manual: Intertidal Invertebrates from Central California to Oregon, University of California Press, Berkeley CA. Pp. 783-788

Hanson, Dieta; Hirano, Yayoi; Valdes, Angel (2012) Population genetics of Haminoea (Haloa) japonica Pilsbry, 1895, a widespread non-indigenous sea slug (Mollusca: Opisthobranchia) in North America and Europe, Biological Invasions 15(2): 395-406

Hanson, Dieta (2012) Alien invaders: Haminoea japonica in North America and Europe, American Conchologist 40: 19

Hanson, Dieta and 5 authors (2013) Slipping through the cracks: The taxonomic impediment conceals the origin and dispersal of Haminoea japonica, an invasive species with impacts to human health, PLOS ONE 8(10): e77457

Huang, Zongguo (Ed.), Junda Lin (Translator) (2001) Marine Species and Their Distributions in China's Seas, Krieger, Malabar, FL. Pp. <missing location>

Ito, K.; Goshima, S.; Nakao, S. (1996) Growth and reproduction of the generalist opisthobranch Haloa japonica: effect of algal seasonality on growth rate, Marine Biology 126: 395-401

Kil, Hyun Jong; Yoon, Sook Hee; Kim, Won; Choe, Byung Lae; Sohn, Hyun Joon; Park, Joong-Kee (2005) Faunistic investigation for marine mollusks in Jindo Island., Korean Journal of Systematic Zoology Special Issue 5: 29-46

Kim, Daemin; Taylor, Andrew T.; Near, Thomas J. (2022) Phylogenomics and species delimitation of the economically important Black Basses (Micropterus), Scientific Reports 12(9113): Published online
https://doi.org/10.1038/s41598-022-11743-2

Malaquias, Manuel Antonio E.; Cervera, Juan Lucas (2006) The genus Haminoea (Gastropoda: Cephalaspidea) in Portugal, with a review of the European species., Journal of Molluscan Studies 72: 89-103

Occhipinti-Ambrogi, Anna and 15 authors (2011) Alien species along the Italian coasts: an overview, Biological Invasions 13: 215–237

Rudman, W. B. 1997-2016 Sea Slug Forum. http://www.seaslugforum.net/



Ruiz, Gregory M.; Geller, Jonathan (2018) Spatial and temporal analysis of marine invasions in California, Part II: Humboldt Bay, Marina del Re, Port Hueneme, and San Francisco Bay, Smithsonian Environmental Research Center & Moss Landing Laboratories, Edgewater MD, Moss Landing CA. Pp. <missing location>

Strathmann, Richard; Staver, Jennifer M.; Hoffman, Jennifer R. (2002) Risk and the evolution of cell-cycle durations of embryos, Evolution 56(4): 708-720

Trkov, Domen; Praprotnik, Eva; Lipej, Lovrenc (2023) Salinity tolerance of non-native heterobranch sea slug Haloa japonica, Malacologia 66(1/2): 115-126
https://doi.org/10.4002/040.066.0105

Wu, R. S. S.; Shin, P. K. S. (1997) Sediment characterization and colonization by soft-bottom benthos: A field manipulation experiment, Marine Biology 128: 475-487