Invasion History

First Non-native North American Tidal Record: 1996
First Non-native West Coast Tidal Record: 1996
First Non-native East/Gulf Coast Tidal Record:

General Invasion History:

Philine orientalis is native to the Western Pacific from Russia (Sea of Japan coast), Japan, China and south to the Gulf of Thailand, the Straits of Malacca, Java, and the Philippines (Golikov et al. 1976; Price et al. 2011). It was collected in Bodega Harbor, California in 1998, and later found in Tomales and San Francisco Bays (Michelle Chow, in Rudman 1999; Behrens 2004; Krug et al. 2012; California Academy of Sciences 2014).

North American Invasion History:

Invasion History on the West Coast:

Philine orientalis was first collected on the West Coast in Bodega Harbor, California in 1998. The discovery of P. orientalis occurred nearly simultaneously with the invasion of the New Zealand Sea Slug (P. auriformis), causing considerable confusion, which was increased by the muddled taxonomy of the genus. At one time, four species of introduced Philine: P. aperta, P. japonica, P. orientalis, and P. auriformis were listed for California waters (Behrens 2004). However, molecular and morphological analysis synonymized P. orientalis and P. japonica, and identified California P. aperta specimens as P. orientalis (Price et al. 2011; Krug et al. 2012). A graduate student, Michelle Chow, began studies of P. auriformis in Bodega Bay and found that at least two morphologically different species were present (Chow, in Rudman 1998-2014). By 2004, P. orientalis was collected in Tomales and San Francisco Bays (Behrens 2004; Krug et al. 2012). Within San Francisco Bay, P. orientalis, appears to be widely distributed, occurring in San Pablo Bay and the South Bay (Krug et al. 2012; California Academy of Sciences 2014). Although P. orientalis was first recognized in Bodega Harbor, as distinct from P. auriformis, it was most likely introduced to San Francisco Bay first, in ballast water, and then dispersed to Bodega and Tomales Bays. Philine spp. populations appeared to be ephemeral in Bodega and Tomales Bays in 2006-2010, and were not found some years. They were more stable in San Francisco and San Pablo Bays (Newsom and Williams 2014).


Description

Philine orientalis is a sea-slug with an internal shell, known as a bubble-shell. It has a well-developed head-shield, which is wedge-shaped, but rounded anteriorly, and comprising about 2/3 of the body length. The parapodial lobes are thick and muscular. The notch may be present or absent on the anterior end of the head shield. 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 gizzard plates are visible through the dorsal and ventral surfaces of the body. The shell occupies most of the body cavity immediately ventral to the dorsal portion of the posterior shield. The shell is loosely or tightly coiled, and its surface can be smooth or dotted. The buccal organ is small, but 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. The two paired plates fill most of the front end of the animal. Adult slugs are 25-40 mm in length. The body is translucent 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 Behrens (2004), Gosliner and Williams (in Carlton 2007), Rudman 2009, and Price et al. (2011).

When exotic Philine sp. invaded California waters, there was confusion over their identity. 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:   orientalis

Synonyms

Philine japonica (Lischke, 1872)
Philine argentata (Gould, 1859)
Philine striatella (Tapperone-Canefri, 1874)

Potentially Misidentified Species

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 (Price et al. 2011).

Philine auriformis
Philine auriformis, native to New Zealand, 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 orientalis is a sea-slug which inhabits sandy substrates, mudflats, and eelgrass beds (Golikov et al. 1976; Behrens 2004; California Academy of Sciences 2007). The animals are hermaphroditic and apparently do not self-fertilize. Fertilization is internal, and the individual lays 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 are likely planktotrophic.

Temperature and salinity tolerances of P. orientalis 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, within the polyhaline zone (18-30 PSU). The slug's habitat ranges from the lower intertidal to depths as deep as 180 m, on silty to sandy bottoms. It does occur in eelgrass beds (Price et al. 2011; California Academy of Sciences 2014). On the Pacific coast of Russia, it is often associated with scallops (Golikov et al. 1976). Philine orientalis is a carnivore and feeds primarily on small bivalves. In Hong Kong, major prey items were juveniles of Venerupis philippinarum (Morton and Chiu 1990). This slug has a muscular buccal mass and a gizzard with calcareous plates for crushing shells (Morton 1990). Glands in the mantle of Philine spp. secrete noxious acid compounds which discourage predators (Cadien and Ranasinghe 2003).

Food:

Bivalves

Trophic Status:

Carnivore

Carn

Habitats

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


Tolerances and Life History Parameters

Minimum Length (mm)25Behrens 2004; Price et al. 2011
Maximum Length (mm)40Behrens 2004; Price et al. 2011
Broad Temperature RangeNoneCold temperate-Tropical

General Impacts

In its native range, P. orientalis is a significant predator on small bivalves, including juveniles of the commercially important Venerupis philippinarum (Japanese Littlenecks) (Morton and Chiu 1990). Philine orientalis secretes a highly acidic mucus which can discourage feeding by other predators such as the native Dungeness Crab (Metacarcinus magister) and the introduced Green Crab (Carcinus maenas). This effect was found to reduce foraging rates by these predators in laboratory experiments but was not seen in field experiments in San Francisco Bay. Modeling suggested that interference would only occur under specific abundance levels of P. orientalis (Newsom and Williams 2014).

Regional Impacts

P112_CDA_P112 (Bodega Bay)Ecological ImpactCompetition
Under some conditions Philine orientalis interfered with predation on small clams by Dungeness Crabs (Metacarcinus magister) and Green Crabs (Carcinus maenas), but only when both crab species were present, and only at certain levels of density of the three predators (Newsom and Williams 2014).
P112_CDA_P112 (Bodega Bay)Ecological ImpactPredation
Phiiline orientalis was a significant predator on small bivalves in Bodega Harbor, CA (Newsom and Williams 2014).
CACaliforniaEcological ImpactCompetition
Under some conditions Philine orientalis interfered with predation on small clams by Dungeness Crabs (Metacarcinus magister) and Green Crabs (Carcinus maenas), but only when both crab species were present, and only at certain levels of density of the three predators (Newsom and Williams 2014).
CACaliforniaEcological ImpactPredation
Phiiline orientalis was a significant predator on small bivalves in Bodega Harbor, CA (Newsom and Williams 2014).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
P130 Humboldt Bay 2015 Def Estab
NEP-IV Puget Sound to Northern California 2015 Def Estab
P090 San Francisco Bay 2004 Def Estab
P110 Tomales Bay 2004 Def Estab
P112 _CDA_P112 (Bodega Bay) 1998 Def Estab
NEP-V Northern California to Mid Channel Islands 1996 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude
699554 Introduced Species Study 2005 2005-09-07 Redwood Creek - Shipping Def 37.5120 -122.2109
699928 Introduced Species Study 2005 2005-09-07 Dumbarton Bridge Def 37.5070 -122.1168
700282 M. Chow and T. Gosliner, pers. comm., in Behrens 2004 1998 1998-07-01 Bodega Bay Def 38.3262 -123.0495
703286 Introduced Species Study 2010 2010-06-12 China Camp Def 38.0025 -122.4617
703778 Introduced Species Study 2005 2005-06-08 Crown Beach Def 37.7603 -122.2737
704402 T. Gosliner, pers. comm., in Behrens 2004 1998 Tomales Bay Def 38.2100 -122.9400
819030 Ruiz GM and JB Geller (2015) 2012 San Leandro None 37.6580 -122.2217
819031 Ruiz GM and JB Geller (2015) 2012 Redwood City None 37.5574 -122.1755
819032 Ruiz GM and JB Geller (2015) 2012 Coyote Point None 37.5987 -122.3252
819033 Ruiz GM and JB Geller (2015) 2012 None None
819034 Ruiz GM and JB Geller (2015) 2012 Corte Madera None 37.9309 -122.4819
819035 Ruiz GM and JB Geller (2015) 2012 Oyster Point None 37.6805 -122.3731
819036 Ruiz GM and JB Geller (2015) 2012 Richardson Bay None 37.8788 -122.4759
819037 Ruiz GM and JB Geller (2015) 2012 Emeryville None 37.8596 -122.3152
819038 Ruiz GM and JB Geller (2015) 2012 Ballena Isle None 37.7643 -122.2978
819440 Ruiz GM and JB Geller (2018) 2015 Fairhaven terminal None 40.7842 -124.1983
819441 Ruiz GM and JB Geller (2018) 2015 Eureka marina None 40.8026 -124.1810
819442 Ruiz GM and JB Geller (2018) 2015 Schneider dock None 40.7992 -124.1848
819443 Ruiz GM and JB Geller (2018) 2015 Redwood marine terminal None 40.8078 -124.1869
819444 Ruiz GM and JB Geller (2018) 2015 Woodley island None 40.8097 -124.1538
819445 Ruiz GM and JB Geller (2018) 2015 Sierra pacific None 40.8155 -124.1822
819446 Ruiz GM and JB Geller (2018) 2015 Redwood chip export None 40.7999 -124.1915
819447 Ruiz GM and JB Geller (2018) 2015 US Coast guard None 40.7750 -124.2090
819448 Ruiz GM and JB Geller (2018) 2015 Forest products None 40.7304 -124.2193
819449 Ruiz GM and JB Geller (2018) 2015 Fields landing None 40.7378 -124.2218
819616 Ruiz GM and JB Geller (2015) 2013 Emeryville None 37.8602 -122.3000
819617 Ruiz GM and JB Geller (2015) 2013 Corte Madera None 37.9364 -122.4833
819618 Ruiz GM and JB Geller (2015) 2013 Richardson bay None 37.8737 -122.4667
819619 Ruiz GM and JB Geller (2015) 2013 None None
819620 Ruiz GM and JB Geller (2015) 2013 Ballena isle None 37.7578 -122.2500
819621 Ruiz GM and JB Geller (2015) 2013 Oyster Point None 37.6788 -122.3667
819622 Ruiz GM and JB Geller (2015) 2013 Redwood city None 37.5588 -122.2000
819623 Ruiz GM and JB Geller (2015) 2013 Coyote Point None 37.5926 -122.2667
819624 Ruiz GM and JB Geller (2015) 2013 San Leandro None 37.6602 -122.2167
819773 Ruiz GM and JB Geller (2018) 2014 Oyster Point None 37.6937 -122.3689
819774 Ruiz GM and JB Geller (2018) 2014 SF marina None 37.8075 -122.4347
819775 Ruiz GM and JB Geller (2018) 2014 Hayward None 37.6485 -122.2184
819776 Ruiz GM and JB Geller (2018) 2014 Ballena Isle None 37.7583 -122.2841
819777 Ruiz GM and JB Geller (2018) 2014 San Mateo None 37.5938 -122.3036
819778 Ruiz GM and JB Geller (2018) 2014 San Bruno None 37.6479 -122.3662
819779 Ruiz GM and JB Geller (2018) 2014 Richmond None 37.9187 -122.3919
819780 Ruiz GM and JB Geller (2018) 2014 Albany None 37.8877 -122.3247
819781 Ruiz GM and JB Geller (2018) 2014 San Quentin None 37.9372 -122.4787
819782 Ruiz GM and JB Geller (2018) 2014 Richardson bay None 37.8715 -122.4790
819983 Ruiz GM and JB Geller (2018) 2015 Oakland None 37.7056 -122.2473
819984 Ruiz GM and JB Geller (2018) 2015 Ballena Isle None 37.7588 -122.2834
819985 Ruiz GM and JB Geller (2018) 2015 SF marina None 37.8074 -122.4345
819986 Ruiz GM and JB Geller (2018) 2015 Richardson bay None 37.8705 -122.4797
819987 Ruiz GM and JB Geller (2018) 2015 Smithsonian None 37.8981 -122.4623
819988 Ruiz GM and JB Geller (2018) 2015 Hunters Point None 37.7088 -122.3691
819989 Ruiz GM and JB Geller (2018) 2015 Oyster Point None 37.6747 -122.3753
819990 Ruiz GM and JB Geller (2018) 2015 Union City None 37.5865 -122.1743
819991 Ruiz GM and JB Geller (2018) 2015 Albany None 37.8879 -122.3245
819992 Ruiz GM and JB Geller (2018) 2015 San Lorenzo None 37.6480 -122.2159
820203 Ruiz GM and JB Geller (2018) 2016 SF marina None 37.8071 -122.4345
820204 Ruiz GM and JB Geller (2018) 2016 Bay Farm None 37.7237 -122.2632
820205 Ruiz GM and JB Geller (2018) 2016 Brisbane None 37.6560 -122.3697
820206 Ruiz GM and JB Geller (2018) 2016 Mission Bay None 37.7553 -122.3790
820207 Ruiz GM and JB Geller (2018) 2016 Albany None 37.8773 -122.3241
820208 Ruiz GM and JB Geller (2018) 2016 El Cerrito None 37.8885 -122.3367
820209 Ruiz GM and JB Geller (2018) 2016 Richardson bay None 37.8669 -122.4751
820210 Ruiz GM and JB Geller (2018) 2016 Paradise Cay None 37.9044 -122.4684
820211 Ruiz GM and JB Geller (2018) 2016 Oyster Point None 37.6688 -122.3741
820212 Ruiz GM and JB Geller (2018) 2016 Ballena Isle None 37.7516 -122.2878
820413 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oracle Park None 37.7780 -122.3843
820414 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Tiburon Ferry None 37.8724 -122.4540
820415 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Point Richmond None 37.9082 -122.3941
820416 Ruiz GM, Chang AL, and JB Geller (2023) 2022 San Francisco Marina None 37.8076 -122.4332
820417 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Hunter's Point None 37.7058 -122.3750
820418 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oyster Point None 37.6797 -122.3774
820419 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Richardson Bay None 37.8624 -122.4636
820420 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Albany None 37.8648 -122.3229
820421 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Oakland None 37.6977 -122.2501
820422 Ruiz GM, Chang AL, and JB Geller (2023) 2022 Ballena Isle None 37.7637 -122.3002

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