Short description of Ocinebrellus inornatus, Asian/Japanese oyster drill

Ocinebrellus inornatus, the Japanese oyster drill, is a predatory gastropod mollusc (snail). It grows to a maximum length of just under 50 mm. The shell is irregularly sculpted, with an oval aperture, thick outer lip, and a short straight siphonal canal, which is initially open but usually closes with age. The shell has 5-6 whorls, the last of which is sculpted with 4 to 12 axial ribs. The egg capsules are bright yellow, and approximately 10 x 4 mm. Differentiation of shells from the native oyster drill Ocenebra erinaceus is difficult and requires measurement of the shell spire angle to be certain. However, generally the shells of O. inornatus are more robust, with coarser ornamentation, and the ribs are more prominent and angulated around the shoulder than in O. erinaceus. The egg capsules, in cross-section, can be distinguished from those of O. erinaceus, as they are crescent-shaped rather than triangular.

Impact summary: Ocinebrellus inornatus, Asian/Japanese oyster drill

The Japanese oyster drill preys on a range of species, including commercially and environmentally important, and habitat/ reef forming bivalve species, particularly oysters. Considered a serious pest species on oyster growing operations in N. America, France and The Netherlands, where it is established.

Habitat summary: Ocinebrellus inornatus, Asian/Japanese oyster drill

Not currently found in GB. It would likely inhabit estuarine and benthic marine habitats in the intertidal and shallow subtidal zones, such as bivalve beds, biogenic reefs (particularly those associated with oysters), and other hard substratum.

Overview table

Environment	Marine
Species status	Non-Native
Native range	Northwestern Pacific
Functional type	Predator
Status in England	Non-Native
Status in Scotland	Non-Native
Status in Wales	Non-Native
Location of first record	No British records to date.
Date of first record	Unknown

Origin

Originally from the Northwestern Pacific, including Japan, Russia, China and Korea (Martel et al., 2004a; Fofonoff et al., 2021).

First Record

Not yet recorded in GB.

Pathway and Method

The N. American population was probably introduced with imports of Pacific Oysters (Magallana gigas) from the native range (Carlton, 1979). The initial introduction into Europe likely resulted from oysters imported from the US to France (Martel et al., 2004a), and the subsequent spread within Europe appears to have been via the unintentional co-transport of eggs, larvae and/or juveniles with bivalves and their substrates (Martel et al., 2004b; Faasse & Ligthart, 2009; Afonso, 2011). Net bags of cultured oysters also often contain juvenile and adult O. inornatus. These bags are not only moved from farm to farm within a local area, some are transported over long distances (Lutzen et al., 2012). Transport of other hard substrates e.g. rocks or driftwood, may also facilitate spread (Didderen & Gittenberger, 2013). The species lacks a planktonic phase, so natural spread is likely to be slow and any human-mediated spread will require collection directly from the benthos (Martel et al., 2004b).

Species Status

The Japanese oyster drill was first introduced to Puget Sound on the Pacific coast of N. America in the 1920s. Its range now extends from California to British Columbia (Fofonoff et al., 2021; GBIF, 2021). It is considered invasive in the US. The first European records were from the Atlantic coast of France in 1995 (Pigeot et al., 2000). It is now also present on the north coast of France, The Netherlands, Denmark and Portugal (Faase & Ligthart, 2009; Afonso, 2011; Lutzen et al., 2012; GBIF, 2021). It is considered to be invasive in the French part of the Bay of Biscay and the Dutch and Danish areas of the North Sea.

Dispersal Mechanisms

Natural dispersal is limited and slow as the species lacks a planktonic stage (Martel et al., 2004b). Adults are mobile but are unlikely to disperse naturally over distances of more than 1 km (Didderen & Gittenberger, 2013).

Reproduction

Ocinebrellus inornatus has separate sexes, with internal fertilization of the eggs. In its introduced range in Europe, mature adults congregate to breed in both Spring and Autumn, the females then lay clumps of 20-40 bright yellow egg capsules, over much of the year, on any hard substrate available (Pigeot et al., 2000; Buhle et al., 2004; Martel et al., 2004c; Faasse & Ligthart, 2009). Each egg capsule produces 10-15 viable embryos, which hatch as juvenile snails after three weeks (Lutzen et al., 2012). They mature when they reach 25-30 mm, after about a year of growth, and survive for 1-3 years (van den Brink & Wijsman, 2010; Fofonoff et al., 2021).

Known Predators/Herbivores

It is likely that the egg cases, larvae, juveniles and possibly small adults are consumed by crabs, birds, lobsters and fish (Thinkport, 2005; Grason & Miner, 2012; Fofonoff et al., 2021). Larger snails are less vulnerable to predation by these animals on account of their thick shell and cryptic appearance.

Resistant Stages

In The Netherlands, this species is known to survive winter temperatures of 0-1 C (Faasse & Ligthart, 2009). In addition, the thick shell likely provides adults with protection from predation, desiccation, and physical damage due to substrate movement and trampling.

Habitat Occupied in GB

None currently occupied in GB. Ocinebrellus inornatus is usually found in estuarine and benthic marine habitats, in rocky, intertidal and shallow subtidal areas. It is typically found on substratum including gravel, mud, sand and shells, particularly biogenic reefs including bivalve beds (van den Brink & Wijsman, 2010). It can tolerate winter temperatures as low as -1 C, and salinities down to 23 psu (Faasse & Ligthart, 2009; Lutzen et al., 2012).

Not present in GB.

Environmental Impact

Ocinebrellus inornatus preys on oysters, scallops, mussels, clams, cockles, barnacles and other gastropods, by drilling through the shells with a radula, then secreting digestive enzymes that dissolve the prey’s tissues (Carlton, 1979; Afonso, 2011; Chiba & Arai, 2014; van den Brink & Wijsman, 2010; Babaran, 2017). If the prey species is fundamental to the local ecosystem, e.g. by providing habitats and food for other native species, then O. inornatus may have wider environmental impacts (van den Brink & Wijsman, 2010). Predation by O. inornatus has been implicated in the decline of oyster populations and slow recovery of previously over-exploited oyster populations. In GB and elsewhere around Europe, efforts are currently underway to re-establish populations of the native flat oyster, Ostrea edulis, for environmental enhancement in several locations. There is a risk that the presence of O. inornatus in high numbers may impact these efforts and the existing populations (Babaran, 2017). In W. France, Ocinebrellus inornatus competes successfully with the native Ocenebra erinaceus, which it now outnumbers (Lutzen et al., 2012).

Health and Social Impact

None known, although recreational harvesting of oysters may be affected in areas where O. inornatus becomes invasive.

Economic Impact

The Japanese oyster drill preys on a variety of commercially valuable bivalve species. In particular, it is known to target oysters of a saleable size, as well as their spat, representing a potential impact on oyster-growing operations and fisheries (Afonso, 2011; Babaran, 2017). An adult can consume small (20 mm) oysters at a rate of three per week, and the species has been found at densities exceeding 46 per sq. m (Buhle & Ruesink, 2009). This particularly affects oyster farmers that practice bottom culture techniques, as this creates greater opportunities for contact with, and predation from, Japanese oyster drills (Babaran, 2017). In Europe, oyster farmers in The Netherlands and France have experienced significant economic losses (Lutzen et al., 2012; Babaran, 2017). Elsewhere, along the west coast of N. America, the Japanese oyster drill is considered to be potentially the most serious predator of the native Olympic oyster and the imported Pacific oyster (van den Brink & Wijsman, 2010; Lutzen et al., 2012). The impact of infestations have been so severe in some areas that growers had to abandon and write-off infested beds (Buhle & Ruesink, 2009).

Identification

Amano, K., & Vermeij, G. J. (1998). Taxonomy and evolution of the genus Ocinebrellus (Gastropoda: Muricidae) in Japan. Paleontological Research, 2(3), 199-212.

Goud, J., Titselaar, F. F. L. M., & Mulder, G. (2008). Weer een ‘verstekeling’: de Japanse Stekelhoren Ocinebrellus inornatus (Recluz, 1851) (Gastropoda, Muricidae) levend aangetroffen in de Oosterschelde. Spirula, 365, 134-136.

Robert, S., Rossi, N., Le Moine, O., Soletchnik, P., Razet, D., Guilpain, P., Geairon, P., Blouin, F., & Sauriau, P-G. (2003). Research of biometric parameters differentiating the species Ocenebra erinacea and Ocinebrellus inornatus. Available from: https://archimer.ifremer.fr/doc/00134/24542/ Accessed on 2021-06-17.

van den Brink, A. M., & Wijsman, J. W. M. (2010). High risk exotic species with respect to shellfish transports from the Oosterschelde to the Wadden Sea. Available from: https://library.wur.nl/WebQuery/wurpubs/fulltext/143113 Accessed on 2021-06-17.

WoRMS (2021). Images of Ocinebrellus inornatus available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=578702#images Accessed on 2021-06-17.

Biology, ecology, spread, vectors

Afonso, C. (2011). Non-indigenous Japanese oyster drill Pteropurpura (Ocinebrellus) inornata (Recluz, 1851) (Gastropoda: Muricidae) on the South-west coast of Portugal. Aquatic Invasions, 6(1), 85-88.

Buhle, E., Margolis, M., & Ruesink, J. (2004). Bang for buck: cost-effective control of invasive species with different life histories. Ecological Economics, 52(3) 355-366.

Carlton, J. T. (1979). History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. University of California, Davis. Didderen, K., &

Gittenberger, A. (2013). Distribution and risk analysis of the American and Japanese oyster drill (Urosalpinx cinera, Ocenebra inornata) update 2013. Culemborg: Bureau Waardenburg bv. Faasse, M., &

Ligthart, M. (2009). American (Urosalpinx cinerea) and Japanese oyster drill (Ocinebrellus inornatus) (Gastropoda: Muricidae) flourish near shellfish culture plots in The Netherlands. Aquatic Invasions, 4(2), 321-326.

Fofonoff, P. W., Ruiz, G. M., Steves, B., Simkanin, C., & Carlton, J. T. (2021). National Exotic Marine and Estuarine Species Information System. Available from: http://invasions.si.edu/nemesis. Accessed on 2021-06-18.

GBIF (2021). Ocinebrellus inornatus (Recluz, 1851) in GBIF Secretariat (2021). GBIF Backbone Taxonomy. Checklist dataset https://doi.org/10.15468/39omei Accessed via GBIF.org on 2021-06-17.

Grason, E. W., & Miner, B. G. (2012). Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs. Oecologia, 169(1), 105-115.

Lutzen, J., Faasse, M., Gittenberger, A., Glenner. H., & Hoffmann, E. (2012). The Japanese oyster drill Ocinebrellus inornatus (Recluz, 1851) (Mollusca, Gastropoda, Muricidae), introduced to the Limfjord, Denmark. Aquatic Invasions 7(2), 181–191.

Martel, C., Viard, F., Bourguet, D., & Garcia-Meunier, P. (2004a). Invasion by the marine gastropod Ocinebrellus inornatus in France: I. Scenario for the source of introduction. Journal of Experimental Marine Biology and Ecology, 305(2), 155-170.

Martel, C., Viard, F., Bourguet, D., & Garcia-Meunier, P. (2004b). Invasion by the marine gastropod Ocinebrellus inornatus in France. II. Expansion along the Atlantic coast. Marine Ecology Progress Series 273, 163-172.

Martel, C., Guarini, J. M., Blanchard, G., Sauriau, P. G., Trichet, C., Robert, S., & Garcia-Meunier, P. (2004c). Invasion by the marine gastropod Ocinebrellus inornatus in France. III. Comparison of biological traits with the resident species Ocenebra erinacea. Marine Biology 146, 93-102.

Pigeot, J., Miramand, P., Garcia-Meunier, P., Guyot, T., & Seguignes, M. (2000). Presence d’un nouveau predateur de l’huitre creuse, Ocinebrellus inornatus (Recluz, 1851), dans le bassin conchylicole de Marennes-Oleron. Comptes Rendus de l'Academie des Sciences - Series III - Sciences de la Vie, 323(8), 697-703.

Thinkport (2005). Maryland Bayville Factsheet – Oyster drills – the oyster’s enemy. Available from: https://pdf4pro.com/view/oyster-drills-the-oyster-s-enemy-thinkport-org-4689e3.html Accessed on 2021-06-29.

van den Brink, A. M., & Wijsman, J. W. M. (2010). High risk exotic species with respect to shellfish transports from the Oosterschelde to the Wadden Sea. Available from: https://library.wur.nl/WebQuery/wurpubs/fulltext/143113 Accessed on 2021-06-17.

Management and impact

Afonso, C. (2011). Non-indigenous Japanese oyster drill Pteropurpura (Ocinebrellus) inornata (Recluz, 1851) (Gastropoda: Muricidae) on the South-west coast of Portugal. Aquatic Invasions, 6(1), 85-88.

Babaran, D. (2017). Japanese Oyster Drills (Ocinebrellus inornatus): exploring prey size and species preference in the Netherlands. HZ University of Applied Sciences. Final Project Report. Available from: https://www.deltaexpertise.nl/images/4/4f/Babaran_2017_Japanese_oyster_drill_prey_preference.pdf

Buhle, E., Margolis, M., & Ruesink, J. (2004). Bang for buck: cost-effective control of invasive species with different life histories. Ecological Economics, 52(3) 355-366.

Buhle, E., & Ruesink, J. (2009). Impacts of invasive oyster drills on Olympia Oyster, Ostrea lurida (Carpenter, 1864) recovery in Willapa Bay, Washington, United States. Journal of Shellfish Research, 28(1), 87-96.

Chiba, S., & Arai, Y. (2014). Predation impact of small drilling gastropods on the Japanese scallop Mizuhopecten yessoensis. Journal of Shellfish Research, 33(1), 137-144.

Lutzen, J., Faasse, M., Gittenberger, A., Glenner. H., & Hoffmann, E. (2012). The Japanese oyster drill Ocinebrellus inornatus (Recluz, 1851) (Mollusca, Gastropoda, Muricidae), introduced to the Limfjord, Denmark. Aquatic Invasions 7(2), 181–191.

van den Brink, A. M., & Wijsman, J. W. M. (2010). High risk exotic species with respect to shellfish transports from the Oosterschelde to the Wadden Sea. Available from: https://library.wur.nl/WebQuery/wurpubs/fulltext/143113 Accessed on 2021-06-17.

General

Fofonoff, P. W., Ruiz, G. M., Steves, B., Simkanin, C., & Carlton, J. T. (2021). National Exotic Marine and Estuarine Species Information System. Available from: http://invasions.si.edu/nemesis. Accessed on 2021-06-18.

van den Brink, A. M., & Wijsman, J. W. M. (2010). High risk exotic species with respect to shellfish transports from the Oosterschelde to the Wadden Sea. Available from: https://library.wur.nl/WebQuery/wurpubs/fulltext/143113 Accessed on 2021-06-17.