Philine orientalis

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

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 Habitat	Unstructured Bottom	None
General Habitat	Grass Bed	None
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Vertical Habitat	Epibenthic	None
Vertical Habitat	Endobenthic	None

---

---

Tolerances and Life History Parameters

Minimum Length (mm)	25	Behrens 2004; Price et al. 2011
Maximum Length (mm)	40	Behrens 2004; Price et al. 2011
Broad Temperature Range	None	Cold 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 Impact	Competition
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 Impact	Predation
Phiiline orientalis was a significant predator on small bivalves in Bodega Harbor, CA (Newsom and Williams 2014).
CA	California		Ecological Impact	Competition
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).
CA	California		Ecological Impact	Predation
Phiiline orientalis was a significant predator on small bivalves in Bodega Harbor, CA (Newsom and Williams 2014).

References

2015 Maryland Emerald Ash Borer (Agrilus planipennis) Trap Results (2015) <missing title>, <missing publisher>, <missing place>. Pp. <missing location>

Academy of Natural Sciences of Philadelphia 2002-2024a Malacology Collection Search. <missing URL>



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

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

California Academy of Sciences 2005-2015 Invertebrate Zoology Collection Database. <missing URL>



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

Golikov, A. N. and 7 other editors. (1976) <missing title>, Nauk, Leningrad. Pp. <missing location>

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

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

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

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

Morton, Brian; Chiu, S. T. (1990) The diet, prey size, and consumption of Philine orientalis (Opisthobranchia; Philinidae) in Hong Kong, Journal of Molluscan Studies 56: 289-299

Natural History Museum Rotterdam 2010-2014 Mollusks. <missing URL>



Newsom, Amanda J.; Williams, Susan L. (2014) Predation and functional responses of Carcinus maenas and Cancer magister in the presence of the introduced cephalaspidean nPhiline orientalis, Estuaries and Coasts 37: 1284-1294

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

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>

U.S. National Museum of Natural History 2002-2021 Invertebrate Zoology Collections Database. http://collections.nmnh.si.edu/search/iz/



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

---