Abstract
Invasions by non-indigenous macroinvertebrates often cause ecological and economic problems, and commercial ships have been implicated as a principal mechanism for their dispersal. We explored the presence and species diversity of adult macroinvertebrates transported by transoceanic and coastal vessels arriving to ports on the Atlantic coast of Canada. We sampled 67 ballast tanks from 62 ships operating along discrete geographic pathways and tested whether mid-ocean exchange or voyage length affects the probability for translocation of macroinvertebrates. Additionally, we assessed the relationship between macroinvertebrate presence and the amount of sediment in ballast tanks. We document the presence of highly invasive European green crab (Carcinus maenas), mud crab (Rhithropanopeus harrisii), common periwinkle (Littorina littorea), soft shell clam (Mya arenaria) and blue mussel (Mytilus galloprovincialis) in ballast tanks of surveyed ships. Mid-ocean exchange did not affect macroinvertebrate occurrence, suggesting that current ballast water management regulations are ineffective for this taxonomic group. Viable individuals were recorded in vessels undertaking shorter voyages (average and maximum of 4.5 and 15 days, respectively) and presence was not related to the amount of sediment in tanks. While presence and densities of macroinvertebrates were low, invasion risk may nonetheless be significant during reproductive seasons owing to high fecundity of some taxa. The highest risk may be posed by decapods since gravid females may carry thousands to several million eggs per clutch, and after several weeks of brooding, two or more subsequent clutches may be fertilized by retained sperm from an earlier mating.
Similar content being viewed by others
References
Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215
Briski E, Bailey SA, Cristescu ME, MacIsaac HJ (2010) Efficacy of ‘saltwater flushing’ in protecting the Great Lakes from biological invasions by invertebrate eggs in ships’ ballast sediment. Freshw Biol 55:2414–2424
Briski E, Bailey SA, MacIsaac HJ (2011a) Invertebrates and their dormant eggs transported in ballast sediments of ships arriving to the Canadian coasts and the Laurentian Great Lakes. Limnol Oceanogr 56:1929–1939
Briski E, Cristescu ME, Bailey SA, MacIsaac HJ (2011b) Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biol Invas 13:1325–1340
Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol 23:313–371
Carver CE, Mallet AL (2004) Investigating potential ballast water management strategies for ships travelling from Chesapeake Bay to ports in Nova Scotia. Transport Canada. Atlantic Ballast water sub-committee report. URL: http://www.ceaa.gc.ca/B4777C6B-docs/WP-1785-052.pdf
Colautti RI, MacIsaac HJ (2004) A neutral terminology for defining invasive species. Divers Distrib 10:135–141
Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006a) Characterised and projected costs of nonindigenous species in Canada. Biol Invas 8:45–59
Colautti RI, Grigorovich IA, MacIsaac HJ (2006b) Propagule pressure: a null model for biological invasions. Biol Invas 8:1023–1037
Costlow JD, Bookhout CG, Monroe R (1966) Studies on the larval development of the crab, Rhithropanopeus harrisii (Gould). I. The effect of salinity and temperature on larval development. Physiol Zool 39:81–100
Creaser EP, Clifford DA (1982) Life history studies of the sandworm, Nereis virens Sars, in the Sheepscot estuary, Maine. Fish B-NOAA 80:735–743
Darling JA, Bagley MJ, Roman J, Tepolt CK, Geller JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007
Duggan IC, Bailey SA, van Overdijk CDA, MacIsaac HJ (2006) Invasion risk of active and diapausing invertebrates from residual ballast in ships entering Chesapeake Bay. Mar Ecol Prog Ser 324:57–66
Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299
Gollasch S, Leppäkoski E (1999) Initial risk assessment of alien species in Nordic coastal waters. Nordic Council of Ministers, Copenhagen
Goncalves F, Ribeiro R, Soares AMVM (1995) Laboratory study of effects of temperature and salinity on survival and larval development of a population of Rhithropanopeus harrisii from the Mondego River estuary, Portugal. Mar Biol 121:639–645
Government of Canada (2006) Ballast water control and management regulations. Can Gazette 140(13). URL: http://gazette.gc.ca/archives/p2/2006/2006-06-28/html/sor-dors129-eng.html#a
Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: Lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66
Grosholz ED, Ruiz GM (2002) Management plan for the European green crab. Aquatic nuisance species task force. URL: http://www.anstaskforce.gov/Species%20plans/GreenCrabManagementPlan.pdf. Accessed 7 July 2011
Howells R (2001) Introduced non-native fishes and shellfishes in Texas water: an updated list and discussion. Texas Parks and Wildlife Department, Management Data Series 188. URL: http://www.tpwd.state.tx.us/publications/pwdpubs/media/mds_inland/mds-188.pdf
Hughes RN, Roberts DJ (1980) Reproductive effort of winkles (Littorina spp.) with contrasted methods of reproduction. Oecologia 47:130–136
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18
Humphrey DB (2008) Characterizing ballast water as a vector for non-indigenous zooplankton transport. MSc Thesis, Univ. of British Columbia, Vancouver, B.C. Canada
Invasive Species Specialist Group (ISSG). (2011) Global invasive species database. IUCN Species Survival Commission. URL: http://www.issg.org. Consulted on 12 Aug 2011
Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invas 11:2009–2019
Kelly DW, Muirhead JR, Heath DD, MacIsaac HJ (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol Ecol 15:3641–3653
Klein G, MacIntosh K, Kaczmarska I, Ehrman JM (2010) Diatom survivorship in ballast water during trans-Pacific crossings. Biol Invas 12:1031–1044
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Lockwood JL, Cassey P, Blackburn T (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910
McMahon RF (2002) Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Can J Fish Aquat Sci 59:1235–1244
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492
Morgan SG, Goy JW, Costlow JD (1983) Multiple ovipositions from single matings in the mud crab Rhithropanopeus harrisii. J Crustacean Biol 3:542–547
Palumbi S (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis D, Mable B, Moritz C (eds) Molecular systematics. Sinauer, Sunderland, pp 205–247
Payen GG, Bonami J-R (1979) Mise en evidence de particules d’allure virale associees aux noyaux des cellules mesodermiques de la zone germinative testiculaire du crabe Rhithropanopeus harrisii (Gould) (Brachyoure, Xanthide). Rev Trav Inst Pech Marit 43:361–365
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Reid DF, Johengen T, MacIsaac HJ, Dobbs FC, Doblin M, Drake L, Ruiz GM, Jenkins PT, Santagata S, van Overdijk CDA, Gray D, Ellis S, Hong Y, Tang Y, Thomson F, Heinemann S, Rondon S (2007) A final report for the project “Identifying, verifying, and establishing options for best management practices for NOBOB vessels”. National Oceanic and Atmospheric Administration, Great Lakes Environmental Research Laboratory, and University of Michigan Cooperative Institute for Limnology and Ecosystems Research, Ann Arbor. URL: http://www.glerl.noaa.gov/res/Task_rpts/2004/aisreid04-1.html
Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433
Ricciardi A, MacIsaac HJ (2000) Recent mass invasions of the North American Great Lakes by Ponto-Caspian species. Trends Ecol Evol 15:62–65
Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B 273:2453–2459
Rossong MA, Quijón PA, Snelgrove PVR, Barrett TJ, McKenzie CH, Locke A (2011) Regional differences in foraging behaviour of invasive green crab (Carcinus maenas) populations in Atlantic Canada. Biol Invas. doi:10.1007/s10530-011-0107-7
Samuel NJ, Soundarapandian P (2010) Embryology of commercially important portunid crab Scylla serrata (Forskal). Curr Res J Biol Sci 2:38–41
Shields JD, Okazaki RK (1991) Fecundity and the reproductive potential of the yellow rock crab Cancer Anthonyi. Fish B-NOAA 89:299–305
Simard N, Plourde S, Gilbert M, Gollasch S (2011) Net efficacy of open ocean ballast water exchange on plankton communities. J Plankton Res 33:1378–1395
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102
Stickney AP (1963) Histology of the reproductive system of the soft-shell clam (Mya arenaria). Biol Bull 125:344–351
Sylvester F, Kalaci O, Leung B, Lacoursière-Roussel A, Murray CC, Choi FM, Bravo MA, Therriault TW, MacIsaac HJ (2011) Hull fouling as an invasion vector: can simple models explain a complex problem? J Appl Ecol 48:415–423
Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invas 3:333–345
Ward JM, Ricciardi A (2007) Impacts of Dreissena invasions on benthic macroinvertebrate communities: a meta-analysis. Divers Distrib 13:155–165
Acknowledgments
We thank participating shipping companies and crews, the Shipping Federation of Canada, multiple port authorities and our sampling team: A.M. Weise, O. Casas-Monroy, N. Simard, J.-Y. Couture, M. Huot, O. Lacasse, D. Humphrey, C.Owens, S. Ross, C.D.A. van Overdijk and Dr. C. McKindsey. We are grateful to R. Tedla, S. Ross and H. Coker for laboratory support and to Dr. M. Cristescu for making available her laboratory resources. Great thanks to Dr. Paul Valentich-Scott for taxonomic assistance, and to Dr. Andrea Locke and an anonymous reviewer for helpful comments. This research was supported by NSERC’s Canadian Aquatic Invasive Species Network, Transport Canada, Fisheries and Oceans Canada, by NSERC Discovery Grants to SAB and HJM, and by a DFO Invasive Species Research Chair to HJM.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Briski, E., Ghabooli, S., Bailey, S.A. et al. Invasion risk posed by macroinvertebrates transported in ships’ ballast tanks. Biol Invasions 14, 1843–1850 (2012). https://doi.org/10.1007/s10530-012-0194-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0194-0