Invasion History

First Non-native North American Tidal Record: 1992
First Non-native West Coast Tidal Record: 1992
First Non-native East/Gulf Coast Tidal Record:

General Invasion History:

Philine auriformis is thought to be native to New Zealand where it is common throughout coastal waters, both in the intertidal zone and in deeper water (Willan 1984; Gosliner 1995; Rudman 1999). It has been introduced to the West Coast of North America and ranges from San Diego, California to Barkley Sound, British Columbia.

North American Invasion History:

Invasion History on the West Coast:

In July 1992, a sea-slug collected from South San Francisco Bay was identified as this species. In 1994, it was collected in the central portion of the Bay (Cohen and Carlton 1995) and again in 2004, from Fruitvale Bridge, Oakland (Cohen et al. 2005). Beyond San Francisco Bay, it was collected in 1994 in Bodega Harbor (Gosliner 1995), Morro Bay in 1995 (Behrens 2004), Los Angeles-Long Beach Harbors in 1995 (Carver in Rudman 1999) and 1998 (Ranasinghe et al. 2005), and Elkhorn Slough in 1998 (Wasson et al. 2001). In 1998, P. auriformis was also collected in Mission Bay, Newport Bay, and Channel Islands Harbor (Ranasinghe et al. 2005). By 2000, P. auriformis ranged from San Diego, California to Coos Bay, Oregon (Goddard, in Rudman 1999; Ranasinghe et al. 2005). By 2004, it had been collected in Barkley Sound, on the West Coast of Vancouver Island, British Columbia (Behrens 2004). Ballast water is the most likely vector for the introduction of this animal, but planktonic larvae may have been partly responsible for the rapid dispersal along the coast.


Description

Philine auriformis is a sea-slug with an internal shell known as a bubble-shell. It has a well-developed head-shield, roughly quadrangular, comprising about 2/3 of the body length. Narrow parapodia extend from the foot, but do not meet in the midline of the body. The anterior end of the head shield is slightly indented. The posterior end of the body is rounded when the gills are extended and squarish when the gills are partially contracted. The posterior shield is short and roughly quadrangular, ending in two posterior lobes. Three spindle-shaped gizzard plates are visible through the dorsal and ventral surfaces of the body. There are two paired gizzard plates, roughly diamond-shaped. The shell occupies most of the body cavity immediately ventral to the dorsal portion of the posterior shield. The shell is broad, shallowly curved, with a short and narrow columella. The protoconch is tightly coiled and consists of three whorls. The surface of the shell is finely dotted. The buccal organ is large and muscular with the radular sac forming a postero-ventral lobe. The gizzard contains three similar calcareous spindle-shaped plates, which are convex on the ventral surface. Adult slugs are 15-30 mm in length. The body is translucent white to yellowish white. The shell is visible through the posterior tissue of the dorsal shield. Hancock's organs (i.e. paired chemosensory organs situated between the foot and the head-shield) are reddish brown and consist of 12 simple folds. Description based on Willan et al. (1984), Gosliner (1995), Behrens (2004), Gosliner and Williams (in Carlton 2007), and Price et al. (2011).

When exotic Philine sp. invaded California waters, there was much confusion about their identity. William Rudman (Rudman 1998) doubted the identification of P. auriformis, and one or more additional species were suspected. At one time, four species of introduced Philine: P. aperta, P. japonica, P. orientalis, and P. auriformis were listed for California waters (Behrens 2004). A recent molecular analysis has reduced the crowd to two, P. auriformis and P. orientalis (Krug et al. 2012).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Gastropoda
Subclass:   Opisthobranchia
Order:   Cephalaspidea
Family:   Philinidae
Genus:   Philine
Species:   auriformis

Synonyms

Potentially Misidentified Species

Philine albus
Native, Oregon to Channel Islands (Valdes et al.2016)

Philine aperta
Philine aperta Linneaus 1767 is native to the Atlantic coast of South Africa. This slug was erroneously reported to be present on the California coast (Behrens 2004; Krug et al. 2012). It was also lumped with the European species, P. quadripartita in the 20th century, and given a range from Britain to South Africa, but the two species are now treated as separate (Price et al. 2011).

Philine bakeri
Native, Oregon to Mexico. 2 mm shell size, widespread but rarely collected (Valdes et al.2016)

Philine onatissima
Native, Channel Islands, Palos Verde Penisula, to 12 mm legth (Valdes et al.2016)

Philine orientalis
Philine orientalis, native to the Northwest Pacific, is introduced and established on the California Coast in San Francisco, Tomales, and Bodega Bays (Price et al. 2011; Krug et al. 2012).

Ecology

General:

Philine auriformis is a sea-slug which inhabits soft substrates, mudflats, and eelgrass beds (Willan et al. 1984; Gosliner 1995; Cadien and Ranasinghe 2003). The animals are hermaphroditic and apparently do not self-fertilize. Fertilization is internal, and individuals lay ovoid egg masses composed of spirals of capsules, each containing two eggs and attached to the substrate by a mucous thread (Gosliner 1995; Behrens 2004). The eggs hatch into veligers, which lack yolk, and so are probably planktotrophic.

Temperature and salinity tolerances of P. auriformis are not known, but its native and introduced range runs from warm- to cold-temperate climates. In San Francisco Bay, it ranges into San Pablo Bay, which has variable salinity (18-30 PSU) (Willan et al. 1984; Gosliner 1995; Krug et al. 2012; California Academy of Sciences 2014). The slug's habitat ranges from the lower intertidal to depths as deep as 300 m. It can occur in eelgrass beds, but is rare in areas heavily overgrown by green algae (Ulva spp., Gosliner 1995; Cadien and Ranasinghe 2003). Philine auriformis is a carnivore, which feeds primarily on small bivalves, such as Transenella spp., Parvilucina tenuisculpta, Axinopsida serricata and Gemma gemma (Gosliner 1995; Cadien and Ranasinghe 2003; Behrens 2004). It has a large, muscular buccal mass and a gizzard with calcareous plates for crushing shells (Gosliner 1995). Glands in the mantle of P. auriformis secrete noxious acid compounds which discourage predators (Cadien and Ranasinghe 2003).

Food:

Bivalves (Gemma, Transennella spp.)

Trophic Status:

Carnivore

Carn

Habitats

General HabitatUnstructured BottomNone
General HabitatGrass BedNone
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEpibenthicNone


Tolerances and Life History Parameters

Minimum Length (mm)15Gosliner 1995
Maximum Length (mm)50Cadien and Ranasinghe 2003. 30 mm is a more usual maximum (Gosliner 1995)
Broad Temperature RangeNoneCold Temperate-Warm Temperate
Broad Salinity RangeNonePolyhaline-Euhaline

General Impacts

There are no reported impacts of introduced Philine auriformis populations. However, in San Francisco Bay, this snail fed largely on the introduced clam Gemma gemma, while specimens in Bodega Harbor fed largely on Transennella spp. (Gosliner 1995). The feeding rate of this snail and its effect on bivalve populations are unknown (Cadien and Ranasinghe 2003).

Regional Impacts

P056_CDA_P056 (Los Angeles)Ecological ImpactPredation
The increase in populations of P. aurifornis off the Palos Verde peninsula was accompanied by a decrease in the abundance of the small bivalves Parvilucina tenuisculpta and Axinopsida serricata (Cadien and Ranasinghe 2003).
NEP-VIPt. Conception to Southern Baja CaliforniaEcological ImpactPredation
The increase in populations of P. aurifornis off the Palos Verde peninsula was accompanied by a decrease in the abundance of the small bivalves Parvilucina tenuisculpta and Axinopsida serricata (Cadien and Ranasinghe 2003).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NZ-IV None 1909 Native Estab
NEP-V Northern California to Mid Channel Islands 1992 Def Estab
NEP-IV Puget Sound to Northern California 1998 Def Estab
NEP-VI Pt. Conception to Southern Baja California 1994 Def Estab
NEP-III Alaskan panhandle to N. of Puget Sound 2004 Def Unk
P170 Coos Bay 1998 Def Estab
P050 San Pedro Bay 1998 Def Estab
P030 Mission Bay 2004 Def Estab
P040 Newport Bay 1998 Def Estab
P062 _CDA_P062 (Calleguas) 1998 Def Estab
P070 Morro Bay 1995 Def Estab
P080 Monterey Bay 1996 Def Estab
P090 San Francisco Bay 1992 Def Estab
P112 _CDA_P112 (Bodega Bay) 1994 Def Estab
P111 _CDA_P111 (Tomales-Drakes Bay) 2004 Def Estab
NZ-VI None 1998 Native Estab
P020 San Diego Bay 1995 Def Estab
P056 _CDA_P056 (Los Angeles) 1995 Def Estab
P065 _CDA_P065 (Santa Barbara Channel) 1998 Def Estab
P058 _CDA_P058 (San Pedro Channel Islands) 1998 Def Estab
AUS-VIII None 1969 Def Unk
P069 _CDA_P069 (Central Coastal) 1998 Def Estab
P064 _CDA_P064 (Ventura) 1994 Def Estab
P130 Humboldt Bay 2015 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude
27489 Foss 2011 2011 2011-04-21 Draw Bridge, Los Angeles-Long Beach Harbor Def 33.7645 -118.2428
27526 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-24 Fruitvale Bridge, Oakland, San Francisco Bay Def 37.7690 -122.2296
27948 Wasson et al, 2001 (Elkhorn Slough Survey) 1998 1998-03-01 Elkhorn Slough Station 8 Def 36.8290 -121.7429
28459 California Department of Fish and Wildlife 2014 2011 2011-05-04 Dana Inn Marina, Mission Bay Def 32.7671 -117.2362
28725 Foss 2011 2010 2010-06-03 Treasure Island Def 37.8149 -122.3702
28877 Foss 2009 2005 2005-07-06 Coyote Point, South San Francisco Bay Def 37.5920 -122.3210
29206 California Department of Fish and Wildlife 2014 2011 2011-05-04 Seaforth Landing, Mission Bay Def 32.7621 -117.2365
29642 Introduced Species Study 2006 2006-07-26 Commercial Fishing Fleet Dock, Port Hueneme Def 34.1482 -119.2020
29683 California Department of Fish and Wildlife 2014 2011 2011-04-22 Marina del Rey Harbor Entrance Def 33.9702 -118.4496
29754 Gosliner 1995; Behrens 2004) 1994 1994-04-01 Bodega Harbor Def 38.3262 -123.0495
30063 Los Angeles/Long Beach Baseline Study (2000) 2000 2000-01-01 Los Angeles/Long Beach Harbor Complex Def 33.7632 -118.2526
30333 Cohen and Carlton, 1995 1992 1992-06-01 South San Francisco Bay Def 37.5457 -122.1645
31656 California Department of Fish and Wildlife 2014 2011 2011-04-20 Loading Dock at Bumper Pad #51, Los Angeles Harbor Def 33.7410 -118.2746
31700 Foss 2009 2005 2005-10-21 Ayala Cove, San Franicsco Bay Def 37.8680 -122.4350
32169 California Department of Fish and Wildlife 2914 2011 2011-04-20 LA/Long Beach Coast Guard Pier Def 33.7233 -118.2685
32342 Foss 2009 2005 2005-08-25 China Basin, San Pablo Bay Def 37.7780 -122.3881
33331 California Department of Fish and Wildlife 2014 2011 2011-04-20 Slip D-50, Los Angeles Harbor Def 33.7165 -118.2801
33545 California Department of Fish and Wildlife 2014 2011 2011-04-19 Pump-A-Head Dock Def 33.7026 -118.0542
33647 California Department of Fish and Wildlife 2014 2011 2011-04-21 Super Mexico Pier Def 33.7708 -118.2113

References

Behrens, David W. (2004) Pacific coastal nudibranchs, supplement II: new species to the information on the oldies., Proceedings of the California Academy of Sciences, Third Series 55(2): 11-54

Burn, Robert (2006) A checklist and bibliography of the Opisthobranchia (Mollusca: Gastropoda) of Victoria and the Bass Strait area, south-eastern Australia, Museum Victoria Science Reports 10: 1-42

Cadien, Donald B.; Ranasinghe, J. Ananda (2003) Southern California Coastal Water Research Project 2001-02 Biennial Report, Southern California Coastal Water Research Project 2001-02 Biennial Report, Westminster CA. Pp. 253-267

2005-2015 Invertebrate Zoology Collection Database. http://research.calacademy.org/research/izg/iz_coll_db/index.asp

California Department of Fish and Wildlife (2014) Introduced Aquatic Species in California Bays and Harbors, 2011 Survey, California Department of Fish and Wildlife, Sacramento CA. Pp. 1-36

Carlton, James T. (Ed.) (2007) <missing title>, University of California Press, Berkeley. Pp. <missing location>

Cigarria, Juan, Valdes, Angel (1996) Anadara inaequivalvis (Bruguiere, 1789) in the North Atlantic., Journal of Conchology 35(4): 378-379

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

Cohen, Andrew N.; Carlton, James T. (1995) Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta., U.S. Fish and Wildlife Service and National Sea Grant College Program (Connecticut Sea Grant), Washington DC, Silver Spring MD.. Pp. <missing location>

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

Goddard, Jeffrey H. R. (2001) An identification guide to larval marine invertebrates of the Pacific Northwest, Oregon State University Press, Corvallis OR. Pp. 86-128

Gosliner, T. M. (1995) Introduction and spread of Philine auriformis (Gastropoda: Opisthobranchia) from New Zealand to San Francisco Bay and Bodega Harbor, Marine Biology 122: 249-255

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

Krug, Patrick J.; Asif, Jamal H.; Baeza, Isabel; Morley, Margaret S.; Blom, Wilma M.; Gosliner, Terry M. (2012) Molecular identification of two species of the carnivorous sea slug Philine, invaders of the US west coast, Biological Invasions 14(11): 2447-2459

Price, Rebecca M.; Gosliner, Terrence M.; Valdes, Angel (2011) Systematics and phylogeny of Philine (Gastropoda: Opisthobranchia) with emphasis on the Philine aperta species complex, Veliger 51: 1-58

Ranasinghe, J. Ananda and 6 authors. (2005) The prevalence of non-indigenous species in southern California embayments and their effects on benthic macroinvertebrate communities, Biological Invasions 7: 679-686

1997-2016 Sea Slug Forum. http://www.austmus.gov.au/seaslugs/philcali.htm

Rudman, William B. (1972) The genus of Philine (Opisthobranchia: Gastropoda), Proceedings of the Malacological Society of London 40: 171-181

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>

Valdés, Ángel;; Cadien, Donald B.; Gosliner, Terrence M. (2016) Philinidae, Laonidae and Philinorbidae (Gastropoda: Cephalaspidea: Philinoidea) from the northeastern Pacific Ocean and the Beaufort Sea (Arctic Ocean), Zootaxa 4147(5): 501-537

Wasson, Kerstin; Zabin, C. J.; Bedinger, L.; Diaz, M. C.; Pearse J. S. (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport, Biological Conservation 102: 143-153

Willan, Richard C. (1976) The opisthobranch Thecacera pennigera in New Zealand, with a discussion of the genus., Veliger 18(4): 347-352

Willan, Richard; Morton, John; Walsby, J. R.; Ballantine, W. J. (1984) <missing title>, Leigh Marine Laboratory, University of Auckland, Auckland, New Zealand. Pp. 106