Invasion History

First Non-native North American Tidal Record: 1924
First Non-native West Coast Tidal Record: 1924
First Non-native East/Gulf Coast Tidal Record:

General Invasion History:

Ocinebrellus inornatus is native to the Northwest Pacific, from the southern Kurile Islands in the Sea of Okhotsk through the Sea of Japan and the Yellow Sea, south to Jindo Island, South Korea (Golikov et al. 1976; Huang et al. 2001, Kil et al. 2005). It has been introduced to the Pacific Coast of North America (California to British Columbia) and the Atlantic Coast of Europe (France to Denmark). It has been transported around the world with Pacific Oyster (Crassostrea gigas) transplants.

North American Invasion History:

Invasion History on the West Coast:

Ocinebrellus inornatus was first collected on the West coast in 1924 in Samish Bay, Washington (WA) on newly transplanted Pacific Oysters (Crassostrea gigas) from Japan (Kincaid 1947, cited by Carlton 1979). It was subsequently found in many nearby areas where oysters were cultured, including Boundary Bay, British Columbia (BC) in 1931 (Sherwood 1931, cited by Carlton 1979), Puget Sound in 1932 (Galtsoff 1932, cited by Carlton 1979; Cohen et al. 1998), and Ladysmith, Vancouver Island, BC in 1934 (Elsey 1934, cited by Carlton 1979). In 1939, they appeared in Willapa Bay, WA (Hanna 1966, cited by Carlton 1979), where they are still abundant (Buhle and Ruesink 2009). They were found further south in Netarts Bay, Oregon in 1934 (Squire 1972, cited by Carlton 1979; Carlton 1992; Martel et al. 2004b), and in Tomales Bay, California (CA) in 1941 (Copeland 1941, cited by Carlton 1979), where its presence is reported to be variable (McLean, in Carlton 2007). In 1966, two live specimens of O. inornatus were collected in Morro Bay, CA (Carlton 1979), and in 2007, several live specimens were found in Humboldt Bay, CA (Mello, personal communication; Eberle, personal communication; Carlton, personal communication). This snail has direct development in egg capsules, and thus tends to have a localized distribution around oyster-growing areas (Garcia-Meunier et al. 2002).

Invasion History on the East Coast:

Invasion History on the Gulf Coast:

Invasion History in Hawaii:

Invasion History Elsewhere in the World:

In the Northeast Atlantic, Ocinebrellus inornatus was discovered in the Baie de Marennes-Oléron (Bay of Biscay), France in 1995 (Garcia-Meunier et al. 2002). Based on molecular analyses, O. inornatus was probably introduced to France with imports of Pacific Oysters from Washington State, with later genetic contributions of oysters imported directly from Japan (Martel et al. 2004a). By 2002, it had spread northward to at least nine other oyster-culture areas on the Atlantic Coast of France, as far as Quiberon in south Brittany (Martel et al. 2004b). Ocenebra inornatus was collected in Jutland, Denmark in 2006 (Lützen et al. 2011); Yerseke in the Oosterschelde estuary, Netherlands in 2007; and Tuttelhoek, Netherlands in 2008 (Faasse and Ligthart 2009). In the Netherlands, it was initially misidentified as O. erinacea (Faasse and Ligthart 2009).


Description

The shell of Ocinebrellus inornatus is dextrally coiled, with a large, oval aperture, and a spire formed of squared-off whorls. There are usually 6-7 whorls. The body whorl has 4-11 scalloped varices (thickened axial ridges) occurring at irregular intervals, and sometimes paired. The straight, short siphonal canal is open along its length. The shell has a spiral sculpture of alternating large and small cords, which may form nodes as they cross axial varices. The outer lip is thick, with a wide varix running along it. Adults are ~25-60 mm in size. The shell is chalky in texture, with colors varying from white to blue-gray and chestnut-brown (Abbott 1974; Houart and Sirenko 2003; Martel et al. 2004; Afonso 2011; McLean, in Carlton 2007). Eggs are laid in bottle-shaped, bright-yellow egg capsules, 10 x 4 mm in size, which hatch into 3-10 miniature juveniles (Quayle 1969; Houart and Sirenko 2003).

The Japanese Oyster-Drill has been known by several different names in very recent literature, including Ceratostoma inornata, Ocebra inornata and Pteropurpura inornata (Appeltans et al. 2013). Shell morphology in this species and genus is highly variable, which contributes to taxonomic confusion (Houart and Sirenko 2003).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Gastropoda
Subclass:   Prosobranchia
Order:   Neogastropoda
Family:   Muricidae
Genus:   Ocinebrellus
Species:   inornatus

Synonyms

Murex inornatus (Récluz, 1851)
Murex japonicus  (Dunker, 1860)
Murex talienwhanensis (Crosse, 1862)
Tritonalia japonica (Dunker, 1860)
Tritonium (Fusus) submuricatum (Schrenck, 1862)
Trophon incompta (Gould, 1860)
Ocinebrellus inornatus (Récluz, 1851)
Pteropurpura inornata (Récluz, 1851)
Ceratostoma inornatum (Récluz, 1851)
Murex crassus (Adams, 1853)
Tritonalia adunca (Nomura, 1938)
Ocenebra adunca (Kira, 1969)
Ocenebra endermonis (Habe & Ito, 1975)

Potentially Misidentified Species

Nucella lamellosa
Frilled Dogwinkle, native from Alaska to Santa Cruz, California

Ocenebra erinacea
European Oyster Drill, native to the Northeast Atlantic, ID aided by molecular methods (Garcia-Meunier et al. 2002).

Ecology

General:

Ocinebrellus inornatus is a marine snail found in shallow coastal waters. This species has separate sexes and internal fertilization. Eggs are laid in bright yellow bottle-shaped capsules. Martel et al. (2004c) report that capsules contain on average 1,291 eggs, most of which function as nurse eggs, so only about 3-10 juveniles hatch out per capsule (Quayle 1969; Duckwall 2009; Van den Brink and Wijsman 2010; Lutzen et al. 2011). Eggs hatch in about 3-8 weeks and hatchlings are about 2 mm long (Martel et al. 2004; Van den Brink and Wijsman 2010). They mature at about 25-30 mm, after about a year of growth, and survive for 1-3 years (Martel et al. 2004c; Duckwall 2009; McCoy and Tichenor 2013).

Ocinebrellus inornatus inhabis gravel, mud, and shell substrates, usually in oyster beds, from the intertidal zone to about 6 m depth (Buhle et al. 2009; Lützen et al. 2011). They have survived in estuaries in the Netherlands where temperatures fall to -1°C in winter (Faasse and Ligthart 2009). Snails from the Limfjord, Denmark, survived for several months at 23 PSU (Lützen et al. 2011). In Willapa Bay, Washington (WA), O. inornatus was most abundant in the more saline regions of the bay, while the Atlantic Oyster Drill (Urosalpinx cinerea) predominated in areas closer to rivers (Buhle et al. 2009).

Ocinebrellus inornatus is a carnivorous snail, best known as a predator of Pacific Oysters (Crassostrea gigas), European Oysters (Ostrea edulis), and Olympic Oysters (Ostrea lurida) (Buhle et al. 2009; Lützen et al. 2011). However, they also feed on mussels (Mytilus edulis), clams (Venerupis philippinarum), and barnacles (Chew and Eisler 1958; Duckwall 2009; Faasse and Ligthart 2009; Lützen et al. 2011). Oyster drills feed by grinding a hole into their prey's shell, with the animal secreting sulfuric acid to aid the penetration. When the hole is complete, the snail secretes digestive enzymes to digest the prey and slowly consume it. This can take up to a week. Oyster drills are limited to prey with a shell thickness less than the length of the radula, so they are limited to small prey, oyster spat, and juveniles of other bivalves (Duckwall 2009). In the Pacific Northwest O. inornatus competes with the native Frilled Dogwinkle (Nucella lamellosa) and the introduced Atlantic Oyster Drill (Urosalpinx cinerea) (Buhle et al. 2009; Williams and McDonald 2009). In France, it competes with O. erinacea (Martel et al. 2004c).

Food:

Oysters, other shelled mollusks

Consumers:

Crabs, birds

Competitors:

Other oyster drills and carnivorous snails

Trophic Status:

Carnivore

Carn

Habitats

General HabitatOyster ReefNone
General HabitatRockyNone
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEpibenthicNone

Life History


Tolerances and Life History Parameters

Minimum Temperature (ºC)-1Field data. Oosterschelde, Netherlands (Faasse and Ligthart 2009)
Minimum Salinity (‰)23Snails from Denmark survived and fed for 2 months at 23 PSU, the lowest salinity tested (Lutzen et al. 2011).
Minimum Length (mm)25adult snails, Abbott 1974
Maximum Height (mm)33Abbott 1974
Broad Temperature RangeNoneCold temperate-Warm temperate
Broad Salinity RangeNonePolyhaline-Euhaline

General Impacts

The Japanese Oyster Drill (Ocinebrellus inornatus) is a carnivorous snail, which feeds on a variety of shelled invertebrates, including mussels, clams, barnacles and other gastropods (Williams and McDonald's 2009; Lützen et al. 2011). However, its biggest ecological and economic impacts come from predation on oysters (Galtsoff 1932; Quayle 1969; Martel et al. 2004c; Buhle et al. 2009).

Economic Impacts

Fisheries: The predatory snail Ocinebrellus inornatus was regarded as major pest of oyster-culture in its native waters and 'very destructive to native oysters in Puget Sound' within 8 years of its discovery (Galtsoff 1932). Similarly, it was discovered in Atlantic France in 1995, and regarded as a pest species on the introduced Pacific Oyster (C. gigas) in culture operations (Buhle et al. 2009). Its effects on cultured oysters are greatest on newly planted 'seed oysters', because of the snail’s preference for small prey (Carl and Giguet 1972; Goulletquer et al. 2002; Buhle et al. 2009). Drill infestations can be prevented by inspection and removal of drills on seed oysters, and inspection and regulation of oyster transfers and culture equipment. Control of drills in infested areas involves raking the ground, removing debris, and other labor-intensive tasks (Quayle 1969).

Ecological Impacts

Predation: In Willapa Bay, Washington, O. inornatus was a predator on 'wild' reefs of introduced Pacific Crassostrea gigas and native Olympia Oysters (O. lurida), preferring the former in feeding experiments (Buhle and Ruesink 2009). Its feeding rate is higher than the native West Coast Frilled Dogwinkle (Nucella lamellosa) (Wlliams and McDonald 2009) and the European Oyster Drill (Ocenebra erinacea) (Martel et al. 2004c.). In Williams and McDonald's (2009) experiments, O. inornatus was fed mussels, but the extent of its feeding and impacts away from oysters and oyster-culture areas is not clear.

Competition: Ocinebrellus inornatus may compete with native and introduced predatory snails, but these impacts have not been fully evaluated. Ocinebrellua inornatus has higher feeding rates than N. lamellosa in Puget Sound (Williams and McDonald 2009) and O. erinacea in France. In the former case, it is not clear how often the two species co-occur and compete for prey in the field. In the latter case, in oyster-culture operations, both snails have unlimited food and did not exhibit interference behavior. However, competition might occur in 'wild' oyster populations with multiple predators, diseases, and higher oyster mortality (Martel et al. 2004c). In Willapa Bay, the Japanese and Atlantic Oyster Drills (Urosalpinx cinerea) had similar feeding rates but were spatially separated, with U. cinerea occurring in the inner, less saline part of the bay, and O. inornatus in the lower bay (Buhle et al. 2009).

Food/Prey: As mid-size predators, O. inornatus are potential prey for larger predators, such as crabs and fishes. In Samish Bay, Washington, O. inornatus and Uroosalpinx cinerea are prey for the Red Rock Crab, Cancer productus, but the crab shows a strong preference for juvenile Pacific Oysters over the two species of introduced oyster drills. Both species of drills show behavioral responses (hiding and reduced feeding), based on chemical clues (Grason and Miner 2012a; Grason and Miner 2012b).


Regional Impacts

NEP-IIIAlaskan panhandle to N. of Puget SoundEconomic ImpactFisheries
Ocinebrellus inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932). 'Considerable destruction of seed oysters' occurred in Ladysmith Harbour, British Columbia (Carl and Giguet 1972). However, O. inornatus prefers small individuals of the introduced Pacific Oyster (Crassostrea gigas) to juveniles of the native O. lurida (Olympia Oyster) (Buhle and Ruesink 2009; Grason and Miner 2012a). Permits (and presumably inspection and cleaning) are required for the movement of oysters and culture equipment between bays in Washington and British Columbia. Drill damage in an infested oysterbed can be controlled by tilling the ground, removing debris, and planting older oysters, less likely to be eaten. Drills can be buried by dragging dredges over the bottom.  Coordination between growers on adjacent grounds is essential for control (Quayle 1969).
NEP-IIIAlaskan panhandle to N. of Puget SoundEcological ImpactPredation
The Japanese Oyster Drill's feeding rate on mussels is about 2X that of native Nucella lamellosa (Frilled Dogwinkle) and O. inornatus from Samish Bay (Wlliams and McDonald 2009). Ocinebrellusr inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932). However, O. inornatus prefers small individuals of the introduced Pacific Oyster (Crassostrea gigas) to juvenile native O. lurida (Olympia Oyster) (Buhle and Ruesink 2009; Grason and Miner 2012a). The Red Rock Crab (Cancer productus) is a predator on Oyster Drills, both the Japanese O. inornata and the Atlantic Urosalpinx cinerea, and prefers juvenile drills to adults. However, the crabs prefer juvenile oysters (specifically C. gigas) to both species of snails, and so may contribute to oyster mortality, rather than reducing it (Grason and Miner 2012a). The two introduced snails both show behavioral responses, hiding and reduced feeding, in the presence of the native crabs (Grason and Miner 2012b). In experiments, Ocinebrellus inornatus was a more significant predator on Olympia oysters, than native rock crabs (Cancridae), and suffered little predation from the crabs (Grason and Buhle 2016).
P290Puget SoundEconomic ImpactFisheries
Ocinebrellus inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932). However, O. inornatus prefers small individuals of the introduced Pacific Oyster (Crassostrea gigas) to same-sized juveniles of the native O. lurida (Olympia Oyster) (Buhle and Ruesink 2009; Grason and Miner 2012a).
P290Puget SoundEcological ImpactPredation
Ocenebrellus inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932). However, O. inornatus prefers small individuals of the introduced Pacific Oyster (Crassostrea gigas) to same-sized juveniles of the native O. lurida (Olympia Oyster) (Buhle and Ruesink 2009; Grason and Miner 2012a). However, O. inornatus was a more significant predator on Olympia oysters, than native rock crabs (Cancridae), and suffered little predation from the crabs (Grason and Buhle 2016).
P293_CDA_P293 (Strait of Georgia)Economic ImpactFisheries
Ocinebrellus inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932).
P293_CDA_P293 (Strait of Georgia)Ecological ImpactPredation
Ocinebrellus inornatus is 'very destructive to native oysters in Puget Sound' (Galtsoff 1932). The feeding rate on mussels is about 2X that of the native Nucella lamellosa (Wlliams and McDonald 2009, O. inornatus from Samish Bay.)
NEP-IVPuget Sound to Northern CaliforniaEconomic ImpactFisheries
The Japanese Oyster Drill is a pest of cultured Pacific oysters, especially seed oysters in Willapa Bay (Buhle and Ruesink 2009)
NEP-IVPuget Sound to Northern CaliforniaEcological ImpactPredation
Ocinebrellus inornata is a predator on introduced Pacific (Crassostrea gigas) and native Olympia Oysters (O. lurida) in Willapa Bay, preferring the former in feeding experiments (Buhle and Ruesink 2009).
P270Willapa BayEconomic ImpactFisheries
A pest of cultured Pacific oysters, especially seed oysters in Willapa Bay (Buhle and Ruesink 2009)
P270Willapa BayEcological ImpactPredation
Predator on introduced Pacific Oysters (Crassostrea gigas) and native Olympia Oysters (O. lurida) in Willapa Bay, preferring the former in feeding experiments (Buhle and Ruesink 2009).
NEA-IVNoneEconomic ImpactFisheries
Ocinebrellus inornatus is an important predator on seed-oysters in Pacific Oyster aquaculture in Atlantic France (Goulletquer et al. 2002). Although it has a lower feeding rate than the native European Oyster Drill (O. erinacea), it has a higher reproductive output and a longer breeding season than the native, and the potential to consume more oysters (Martel et al. 2004c). In newly colonized areas, eradication was attempted, but appears to have been unsuccesful. The methods included: '1) destruction of the ovigerous capsules using propane burners; 2) incentive harvest operations in the intertidal zone; and 3) pot fishing using oyster meat like bait. Today, the species is present from Brittany, except perhaps for Finistère, to Arcachon Bay' (Stiger-Pouvreau and Thouzeau 2015).
P290Puget SoundEcological ImpactFood/Prey
The Red Rock Crab (Cancer productus) is a predator on Oyster Drills, both the Japanese O. inornatus and the Atlantic Urosalpinx cinerea, and prefers juvenile drills to adults. However, the crabs prefer juvenile C. gigas to both species of snail, and so may contribute to oyster mortality, rather than reducing it (Grason and Miner 2012a). The two introduced snails both show behavioral responses, hiding and reduced feeding, in the presence of the native crabs (Grason and Miner 2012b).
P110Tomales BayEcological ImpactPredation
Ocinebrellus inornatus was a major predator on Olympia Oysters (Ostrea lurida), especially on the eastern side of the Bay, when low salinities and high temperatures, reduced predation by native Rock Crabs (Cancer productus). Climate warming my increase predatpory impacts by this snail (Cheng et al. 2016). Native predatory snails (Acanthinucella spirata) appeared to have little impact on Olymbic Oyster populations (Cheng and Grosholz 2016).
NEP-VNorthern California to Mid Channel IslandsEcological ImpactPredation
Ocinebrellus inornatus was a major predator on Olympia Oysters (Ostrea lurida), especially on the eastern side of the Bay, when low salinities and high temperatures, reduced predation by native Rock Crabs (Cancer productus). Climate warming my increase predatpory impacts by this snail (Cheng et al. 2016). Native predatory snails (Acanthinucella spirata) appeared to have little impact on Olymbic Oyster populations (Cheng and Grosholz 2016).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NWP-4a None 0 Native Estab
NEP-III Alaskan panhandle to N. of Puget Sound 1924 Def Estab
NEP-IV Puget Sound to Northern California 1934 Def Estab
NEP-V Northern California to Mid Channel Islands 1941 Def Estab
NEA-IV None 1995 Def Estab
P070 Morro Bay 1966 Def Unk
P110 Tomales Bay 1941 Def Estab
P230 Netarts Bay 1934 Def Estab
P270 Willapa Bay 1939 Def Estab
P297 _CDA_P297 (Strait of Georgia) 1931 Def Estab
P293 _CDA_P293 (Strait of Georgia) 1924 Def Estab
P290 Puget Sound 1932 Def Estab
P130 Humboldt Bay 2007 Def Unk
NWP-3a None 0 Native Estab
NEA-II None 2007 Def Estab
NWP-5 None 0 Native Estab
NWP-3b None 0 Native Estab
NEA-V None 1999 Def Estab
NWP-4b None 0 Native Estab
NWP-2 None 0 Native Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude

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