Skip to main content Accessibility help
×
Home

Co-occurrence of native Ostrea edulis and non-native Crassostrea gigas revealed by monitoring of intertidal oyster populations

  • Nadescha Zwerschke (a1), Judith Kochmann (a2), Elizabeth C. Ashton (a1), Tasman P. Crowe (a3), Dai Roberts (a1) (a4) and Nessa E. O'Connor (a1) (a4) (a5)...

Abstract

Coastal ecosystems are particularly vulnerable to alien invasions. Regular, standardized, targeted monitoring of coastal areas helps to detect the arrival of non-native species early, identify sites most vulnerable to invasion, and assess potential for further spread. This study quantified the spread and changes in distribution of non-native oyster, Crassostrea gigas, populations around the coast of Ireland. In total 37 sites were surveyed, in areas which either currently or previously harboured cultivated C. gigas, for the presence and abundance of ‘wild’ C. gigas. Wild populations were identified at 20 sites and at four additional sites C. gigas was observed as recently discarded from aquaculture activity. Five of the invaded sites were identified as being highly suitable for a population expansion based on their current population status. Importantly, we also identified individuals of C. gigas and native European oysters, Ostrea edulis, co-occurring within the same shore at five sites. This is the first record to our knowledge of such co-occurrence within Europe. This evidence of co-existing oyster species raises concerns regarding the potential impact of C. gigas on recovering O. edulis populations. In Ireland, however, C. gigas does not typically spread extensively from introduction points, and although self-containing populations exist, they are currently sustained at a much lower density than those observed in other regions such as the Wadden Sea or French Atlantic coasts. We suggest, therefore, that to protect native oyster populations, C. gigas should be eradicated where co-occurring with O. edulis and recommend continuous monitoring of invaded sites.

Copyright

Corresponding author

Correspondence should be addressed to: N. Zwerschke, Queen's University Marine Laboratory, 12–13 The Strand, Portaferry BT22 1PF, UK email: nzwerschke01@qub.ac.uk

References

Hide All
AFBI (2015) Coastal monitoring. Available at: https://www.afbini.gov.uk/articles/coastal-monitoring#toc-3 (accessed 19 June 2015).
Allen, S.K. and Guo, X. (1996) Triploids for biological containment. The risk of heteroploid mosaics. In Levin, M., Angle, J., McIntyre, T. and Yu, H. (eds) Proceedings of the Third International Conference on Risk Assessment Methodologies. http://www.nbiap.vt.edu/brarg/brasym96/allen96.htm.
Ball, B., Raine, R. and Douglas, D. (1997) Phytoplankton and particulate matter in Carlingford Lough, Ireland: an assessment of food availability and the impact of bivalve culture. Estuaries 20, 430440.
Blanchard, M. (2009) Recent expansion of the slipper limpet population (Crepidula fornicata) in the Bay of Mont-Saint-Michel (Western Channel, France). Aquatic Living Resources 22, 1119.
Brandt, G., Wehrmann, A. and Wirtz, K. (2008) Rapid invasion of Crassostrea gigas into the German Wadden Sea dominated by larval supply. Journal of Sea Research 59, 279296.
Bromley, C., McGonigle, C., Ashton, E.C. and Roberts, D. (2016) Restoring degraded European native oyster, Ostrea edulis, habitat: is there a case for harrowing? Hydrobiologia 768, 151165.
Chapin, F.S., Zavaleta, E.S., Eviner, V.T., Naylor, R.L., Vitousek, P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., Hobbie, S.E., Mack, M.C. and Díaz, S. (2000) Consequences of changing biodiversity. Nature 405, 234242.
Connor, D.W., Allen, J.H., Golding, N., Howell, K.L., Lieberknecht, L.M., Northern, K.O. and Reker, J.B. (2004) The marine habitat classification for Britain and Ireland. Version 03.02. Peterborough: Joint Nature Conservation Committee.
Cuff, W. and Coleman, N. (1979) Optimal survey design: lessons from a stratified random sample of macrobenthos. Journal of the Fisheries Research Board of Canada 36, 351361.
Dutertre, M., Beninger, P.G., Barillé, L., Papin, M. and Haure, J. (2010) Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast. Marine Environmental Research 69, 19.
Eno, N.C., Clark, R.A. and Sanderson, W.G. (1997) Non-native marine species in British waters: a review and directory. Peterborough: Joint Nature Conservation Committee.
Escapa, M., Isacch, J.P., Daleo, P., Alberti, J., Iribarne, O., Borges, M., Dos Santos, E.P., Gagliardini, D.A. and Lasta, M. (2004) The distribution and ecological effects of the introduced Pacific oyster Crassotrea gigas (Thunberg, 1793) in northern Patagonia. Journal of Shellfish Research 23, 765772.
European Commission (2017) European commission at work: infringement procedure. Available at: https://ec.europa.eu/info/infringement-procedure_en (accessed 15 June 2017).
Ferreira, J.G., Duarte, P. and Ball, B. (1997) Trophic capacity of Carlingford Lough for oyster culture – analysis by ecological modelling. Aquatic Ecology 31, 361378.
Ferreira, J.G., Hawkins, A.J.S., Monteiro, P., Moore, H., Service, M., Pascoe, P.L., Ramos, L. and Sequeira, A. (2008) Integrated assessment of ecosystem-scale carrying capacity in shellfish growing areas. Aquaculture 275, 138151.
Fey, F., Dankers, N., Steenbergen, J. and Goudswaard, K. (2009) Development and distribution of the non-indigenous Pacific oyster (Crassostrea gigas) in the Dutch Wadden Sea. Aquaculture International 18, 4559.
Guy, C. and Roberts, D. (2010) Can the spread of non-native oysters (Crassostrea gigas) at the early stages of population expansion be managed? Marine Pollution Bulletin 60, 10591064.
Harding, J.M., Mann, R. and Southworth, M.J. (2008) Shell length-at-age relationships in James River, Virginia, oysters (Crassostrea virginica) collected four centuries apart. Journal of Shellfish Research 27, 11091115.
Hayward, P.J. and Ryland, J.S. (2008) Marine fauna of North-West Europe. New York, NY: Oxford University Press.
Herbert, R.J.H., Humphreys, J., Davies, C.J., Roberts, C., Fletcher, S. and Crowe, T.P. (2016) Ecological impacts of non-native Pacific oysters (Crassostrea gigas) and management measures for protected areas in Europe. Biodiversity and Conservation 25, 28352865.
Hiscock, K. (ed.) (1996) Marine nature conservation review: rationale and methods. Peterborough: Joint Nature Conservation Committee.
Hollander, J., Blomfeldt, J., Carlsson, P. and Strand, Å. (2015) Effects of the alien Pacific oyster (Crassostrea gigas) on subtidal macrozoobenthos communities. Marine Biology 162, 547555.
Hulme, P.E. and Barrett, S.C.H. (2013) Integrating trait- and niche-based approaches to assess contemporary evolution in alien plant species. Journal of Ecology 101, 6877.
IPCC (2014) Climate Change 2014 Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Core Writing Team, Pachauri, R.K. and Meyer, L.A. (eds). Geneva: IPCC.
Kater, B.J. and Baars, J.M.D.D. (2004) The potential of aerial photography for estimating surface areas of intertidal pacific oyster beds (Crassostrea gigas). Journal of Shellfish Research 23, 773779.
Knights, A.M., Firth, L.B. and Russell, B.D. (2017) Ecological responses to environmental change in marine systems. Journal of Experimental Marine Biology and Ecology 492, 36. http://dx.doi.org/10.1016/j.jembe.2017.01.016.
Kochmann, J., O'Beirn, F., Yearsley, J. and Crowe, T.P. (2013) Environmental factors associated with invasion: modelling occurrence data from a coordinated sampling programme for Pacific oysters. Biological Invasions 15, 22652279.
Krassoi, F.R., Brown, K.R., Bishop, M.J., Kelaher, B.P. and Summerhayes, S. (2008) Condition-specific competition allows coexistence of competitively superior exotic oysters with native oysters. Journal of Animal Ecology 77, 515.
Laing, I., Walker, P. and Areal, F. (2006) Return of the native: is European oyster (Ostrea edulis) stock restoration in the UK feasible? Aquatic Living Resources 19, 283287.
Lewin, W.-C., Arlinghaus, R. and Mehner, T. (2006) Documented and potential biological impacts of recreational fishing: insights for management and conservation. Reviews in Fisheries Science 14, 305367. http://dx.doi.org/10.1080/10641260600886455.
Markert, A., Wehrmann, A. and Kröncke, I. (2009) Recently established Crassostrea-reefs versus native Mytilus-beds: differences in ecosystem engineering affects the macrofaunal communities (Wadden Sea of Lower Saxony, southern German Bight). Biological Invasions 12, 1532.
McGonigle, C., Cavanagh, M. and Santiago, R. (2011) Native oyster stock assessment Lough Foyle. The Loughs Agency (Foyle, Carlingford and Irish Lights Commission), Londonderry, Carlingford, Report Reference LA/0Y0211.
Mieszkowska, N., Firth, L. and Bentley, M. (2013) Impacts of climate change on intertidal habitats. MCCIP Science Review 4, 180192.
Miossec, L., le Deuff, R.-M. and Goulletquer, P. (2009) Alien species alert Crassostrea gigas (Pacific oyster) ICES Cooperative Research Report.
Nehring, S. (2006) NOBANIS – Invasive Alien Species Fact Sheet Crassostrea gigas.
Nelson, T.C. (1924) The attachment of oyster larvae. Biological Bulletin 46, 143151.
Post, J.R., Sullivan, M., Cox, S., Lester, N.P., Walters, C.J., Parkinson, E.A., Paul, A.J., Jackson, L. and Shuter, B.J. (2002) Canada's recreational fisheries: the invisible collapse. Fisheries Management 27, 617.
Pyšek, P. and Richardson, D.M. (2010) invasive species, environmental change and management, and health. Annual Review of Environment and Resources 35, 2555.
R Core Team (2016) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Reise, K. (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Senckenbergiana Maritima 28, 167175.
Rico-Villa, B., Pouvreau, S. and Robert, R. (2009) Influence of food density and temperature on ingestion, growth and settlement of Pacific oyster larvae, Crassostrea gigas. Aquaculture 287, 395401.
Rilov, G. and Crooks, J.A. (eds) (2009) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Berlin: Springer Verlag.
Rinde, E., Tjomsland, T., Hjermann, D.Ø., Kempa, M., Norling, P. and Kolluru, V.S. (2016) Increased spreading potential of the invasive Pacific oyster (Crassostrea gigas) at its northern distribution limit in Europe due to warmer climate. Marine and Freshwater Research 68, 252262.
Rohfritsch, A., Bierne, N., Boudry, P., Heurtebise, S., Cornette, F. and Lapègue, S. (2013) Population genomics shed light on the demographic and adaptive histories of European invasion in the Pacific oyster, Crassostrea gigas. Evolutionary Applications 6, 10641078.
Rohfritsch, A., Bierne, N., Boudry, P., Heurtebise, S. and Lapegue, S. (2010) Genomic of adaptation of the Pacific cupped oyster, Crassostrea gigas, in the context of its geographic expansion. ICES CM 2010/ K:02.
Ruesink, J.L., Lenihan, H.S., Trimble, A.C., Heiman, K.W., Micheli, F., Byers, J.E. and Kay, M.C. (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annual Review of Ecology, Evolution, and Systematics 36, 643689.
Schmidt, A., Wehrmann, A. and Dittmann, S. (2008) Population dynamics of the invasive Pacific oyster Crassostrea gigas during the early stages of an outbreak in the Wadden Sea (Germany). Helgoland Marine Research 62, 367376.
Seebens, H., Gastner, M.T. and Blasius, B. (2013) The risk of marine bioinvasion caused by global shipping. Ecology Letters 16, 29.
Smaal, A.C., Kater, B.J. and Wijsman, J. (2009) Introduction, establishment and expansion of the Pacific oyster Crassostrea gigas in the Oosterschelde (SW Netherlands). Helgoland Marine Research 63, 7583.
Smyth, D., Kregting, L., Elsäßer, B., Kennedy, R. and Roberts, D. (2016) Using particle dispersal models to assist in the conservation and recovery of the overexploited native oyster (Ostrea edulis) in an enclosed sea lough. Journal of Sea Research 108, 5059.
Smyth, D. and Roberts, D. (2010) The European oyster (Ostrea edulis) and its epibiotic succession. Hydrobiologia 655, 2536.
Steele, S. and Mulcahy, M.F. (1999) Gametogenesis of the oyster Crassostrea gigas in southern Ireland. Journal of the Marine Biological Association of the United Kingdom 79, 673686.
Syvret, M., Fitzgerald, A. and Hoare, P. (2008) Development of a Pacific oyster aquaculture protocol for the UK – technical report (FIFG Project No: 07/Eng/46/04). Sea Fish Industry Authority.
The Irish Meterological Service Online (2016). Climate of Ireland. Available at: http://www.met.ie/marine/marine_map.asp (accessed 23 May 2016).
The Marine Institute (2015) Weather buoy network real time data. Available at: http://data.marine.ie/Dataset/Details/20972# (accessed 10 September 2015).
Thomas, Y., Pouvreau, S., Alunno-Bruscia, M., Barillé, L., Gohin, F., Bryère, P. and Gernez, P. (2016) Global change and climate-driven invasion of the Pacific oyster (Crassostrea gigas) along European coasts: a bioenergetics modelling approach. Journal of Biogeography 43, 568579.
Troost, K. (2010) Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. Journal of Sea Research 64, 145165.
Tully, O. and Clarke, S. (2012) The status and management of oyster (Ostrea edulis) in Ireland. Irish fisheries investigations. Galway: Marine Institute.
Underwood, A.J. (1997) Experiments in ecology. Cambridge: Cambridge University Press.
Vitousek, P.M. (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57, 713.
Went, A.E.J. (1962) Historical notes on the oyster fisheries of Ireland. Proceedings of the Royal Irish Academy Section C: Archaeology, Celtic Studies, History, Linguistics, Literature 62, 195223.
Wilkie, E.M., Bishop, M.J. and O'Connor, W.A. (2013) The density and spatial arrangement of the invasive oyster Crassostrea gigas determines its impact on settlement of native oyster larvae. Ecology and Evolution 3, 48514860.
Williamson, M. (2006) Explaining and predicting the success of invading species at different stages of invasion. Biological Invasions 8, 15611568.
Wolff, W. and Reise, K. (2002) Oyster imports as a vector for the introduction of alien species into northern and western European coastal waters. In Leppäkoski, E., Gollasch, S. and Olenin, S. (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Amsterdam: Springer, pp. 193205.
Wrange, A.-L., Valero, J., Harkestad, L.S., Strand, Ø., Lindegarth, S., Christensen, H.T., Dolmer, P., Kristensen, P.S. and Mortensen, S. (2009) Massive settlements of the Pacific oyster, Crassostrea gigas, in Scandinavia. Biological Invasions 12, 11451152.
Zwerschke, N., Emmerson, M., Roberts, D. and O'Connor, N. (2016) Benthic assemblages associated with native and non-native oysters are similar. Marine Pollution Bulletin 111, 305310.

Keywords

Type Description Title
WORD
Supplementary materials

Zwerschke et al supplementary material
Zwerschke et al supplementary material 1

 Word (17 KB)
17 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed