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Marine Biology

, Volume 156, Issue 6, pp 1311–1320 | Cite as

Susceptibility of non-indigenous ascidian species in British Columbia (Canada) to invertebrate predation

  • A. Epelbaum
  • C. M. Pearce
  • D. J. Barker
  • A. Paulson
  • T. W. Therriault
Original Paper

Abstract

Non-indigenous ascidians are known to significantly alter the structure and composition of benthic communities and adversely affect shellfish aquaculture by fouling both the cultured species and the infrastructure. The ability of these species to persist in new locations and their current and potential distributions are dependent upon physiological tolerances to environmental factors and biotic resistance to competition and predation. Despite significant data on global invasion patterns, potential biotic resistance to non-indigenous ascidians is poorly understood. We identified potential predators of four non-indigenous ascidians (Styela clava, Botryllus schlosseri, Botrylloides violaceus, and Didemnumvexillum) in British Columbia (BC), Canada in order to: (1) assess the potential for biotic interference to limit the establishment and/or spread of these ascidian species in BC, and (2) identify candidate species to be used as ascidian biofouling control agents in shellfish aquaculture. Using a series of single- and multiple-choice laboratory experiments, potential benthic predators (including various species of molluscs, echinoderms, and arthropods) were offered non-indigenous ascidians as prey. The sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus franciscanus, the sea stars Dermasterias imbricata and Evasterias troschelii, the nudibranch Hermissenda crassicornis, and the crabs Cancer productus and Carcinus maenas were found to consume one or more species of non-indigenous ascidians in single-choice experiments. However, when provided a choice, all predators chose their respective preferred food over ascidians. Thus, predation alone is unlikely to prevent large-scale establishment and spread of non-indigenous ascidians in BC, but it may have the potential to significantly reduce localized populations of ascidians. Green sea urchins, S. droebachiensis, were found to be efficient grazers of all four ascidian species, consuming 12.7 ± 5.14 cm2 (mean ± SD) of adult B. violaceus over a 3-day period, 15 ± 3.7 juvenile colonies of B. violaceus over a 2-day period, and 63 ± 28.8 juvenile colonies of B. schlosseri over a 2-day period. Using sea urchins as biological control organisms may significantly reduce ascidian fouling in shellfish aquaculture.

Keywords

British Columbia Shellfish Aquaculture Ascidian Coloni Ascidian Species Strongylocentrotus Droebachiensis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank J. Blackburn, L. Keddy, and R. Marshall (Fisheries and Oceans Canada) for their assistance in various aspects of the experiments, as well as Marine Biology editors and reviewers for their helpful suggestions that improved the manuscript. Support for the project was provided by funds from the Aquatic Invasive Species program of Fisheries and Oceans Canada. A. Epelbaum was funded through the Visiting Fellowship in Canadian Governmental Laboratories program of the Natural Sciences and Engineering Research Council of Canada (NSERC). A. Paulson and D. Barker were funded by Undergraduate Student Research Awards and a Discovery Grant (to C. Pearce) provided by NSERC. All experiments comply with the current laws of Canada.

References

  1. Brunetti R, Beghi L, Bressan M, Marin MG (1980) Combined effects of temperature and salinity on colonies of Botryllus schlosseri and Botrylloides leachi (Ascidiacea) from the Venetian Lagoon. Mar Ecol Prog Ser 2:303–314. doi: https://doi.org/10.3354/meps002303 CrossRefGoogle Scholar
  2. Carver CE, Chisholm A, Mallet AL (2003) Strategies to mitigate the impact of Ciona intestinalis (L.) biofouling on shellfish production. J Shellfish Res 22:621–631Google Scholar
  3. Cayer D, MacNeil M, Bagnall AG (1999) Tunicate fouling in Nova Scotia aquaculture: a new development. J Shellfish Res 18:327Google Scholar
  4. Connell JH (1983) On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am Nat 122:661–696. doi: https://doi.org/10.1086/284165 CrossRefGoogle Scholar
  5. Dijkstra J, Harris LG, Westerman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68. doi: https://doi.org/10.1016/j.jembe.2006.10.015 CrossRefGoogle Scholar
  6. Enright C, Krailo D, Staples L, Smith M, Vaughan C, Ward D, Gaul P, Borgese E (1983) Biological control of fouling algae in oyster aquaculture. J Shellfish Res 3:41–44Google Scholar
  7. Epelbaum A, Herborg L-M, Therriault TW, Pearce CM (2009a) Temperature and salinity effects on growth, survival, reproduction, and potential distribution of two non-indigenous botryllid ascidians in British Columbia. J Exp Mar Biol Ecol 369:43–52. doi: https://doi.org/10.1016/j.jembe.2008.10.028 CrossRefGoogle Scholar
  8. Epelbaum A, Therriault TW, Paulson A, Pearce CM (2009b) Botryllid tunicates: culture techniques and experimental procedures. Aquat Invasion 4:111–120. doi: https://doi.org/10.3391/ai.2009.4.1.12 CrossRefGoogle Scholar
  9. Fretter V (1951) Some observations on the British cypraeids. Proc Malacol Soc Lond 29:14–20Google Scholar
  10. Hintze J (2001) NCSS and PASS. Number Cruncher Statistical Systems, Kaysville. Available at: www.ncss.com
  11. Karayucel S (1997) Mussel culture in Scotland. World Aquac 28:4–10Google Scholar
  12. Kashenko SD (1996) Effects of desalination on the larval settlement and metamorphosis of the ascidian Styela clava. Biol Morya (Vladivost) 2:174–178Google Scholar
  13. Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56:291–298. doi: https://doi.org/10.1353/psc.2002.0026 CrossRefGoogle Scholar
  14. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4. doi: https://doi.org/10.1016/j.jembe.2006.10.009 CrossRefGoogle Scholar
  15. Lambert G (2009) Adventures of a sea squirt sleuth: the remarkable story of Didemnum vexillum, a global ascidian invader. Aquat Invasion 4:5–28. doi: https://doi.org/10.3391/ai.2009.4.1.2 CrossRefGoogle Scholar
  16. Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol (Berl) 130:675–688. doi: https://doi.org/10.1007/s002270050289 CrossRefGoogle Scholar
  17. Lambert CC, Lambert G (2003) Persistence and differential distribution of non-indigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161. doi: https://doi.org/10.3354/meps259145 CrossRefGoogle Scholar
  18. LeBlanc N, Davidson J, Tremblay R, McNiven M, Landry T (2007) The effect of anti-fouling treatments for the clubbed tunicate on the blue mussel, Mytilus edulis. Aquaculture 264:205–213. doi: https://doi.org/10.1016/j.aquaculture.2006.12.027 CrossRefGoogle Scholar
  19. Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adult vs. larval chemical defenses. Ecol Monogr 62:547–568. doi: https://doi.org/10.2307/2937316 CrossRefGoogle Scholar
  20. Lodeiros C, Garcia N (2004) The use of sea urchins to control fouling during suspended culture of bivalves. Aquaculture 231:293–298. doi: https://doi.org/10.1016/j.aquaculture.2003.10.022 CrossRefGoogle Scholar
  21. Lopez-Legentil S, Turon X, Schupp P (2006) Chemical and physical defenses against predators in Cystodytes (Ascidiacea). J Exp Mar Biol Ecol 332:27–36. doi: https://doi.org/10.1016/j.jembe.2005.11.002 CrossRefGoogle Scholar
  22. McCarthy A, Osman RW, Whitlatch RB (2007) Effects of temperature on growth rates of colonial ascidians: a comparison of Didemnum sp. to Botryllus schlosseri and Botrylloides violaceus. J Exp Mar Biol Ecol 342:172–174. doi: https://doi.org/10.1016/j.jembe.2006.10.036 CrossRefGoogle Scholar
  23. Millar RH (1971) The biology of ascidians. Adv Mar Biol 9:1–100. doi: https://doi.org/10.1016/S0065-2881(08)60341-7 CrossRefGoogle Scholar
  24. Osman RW, Whitlatch RB (1995a) Influence of resident adults on larval settlement: a comparison to settlement. J Exp Mar Biol Ecol 190:169–198. doi: https://doi.org/10.1016/0022-0981(95)00035-P CrossRefGoogle Scholar
  25. Osman RW, Whitlatch RB (1995b) Ecological factors controlling the successful invasion of three species of ascidians into marine subtidal habitats in New England. In: Balcom NC (ed) Proceedings of the northeast conference on non-indigenous aquatic nuisance species, 25 January 1997. Publication no: CT-SG-95-04. Connecticut Sea Grant College Program, Cromwell, pp 49–60Google Scholar
  26. Osman RW, Whitlatch RB (1999) Ecological interaction of invading ascidians within epifaunal communities of southern New England. In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference, January 24–27, 1999. Sea Grant College Program, Massachusetts Institute of Technology, Cambridge, pp 164–174Google Scholar
  27. Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145. doi: https://doi.org/10.1016/j.jembe.2004.05.001 CrossRefGoogle Scholar
  28. Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270:203–214. doi: https://doi.org/10.1016/S0022-0981(02)00023-0 CrossRefGoogle Scholar
  29. Ross KA, Thorpe JP, Brand AR (2004) Biological control of fouling in suspended scallop cultivation. Aquaculture 229:99–116. doi: https://doi.org/10.1016/S0044-8486(03)00328-4 CrossRefGoogle Scholar
  30. Sebens KP (1999) Marine bioinvasions in the rocky subtidal zone (Massachusetts 1977–1998). In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference, January 24–27, 1999. Sea Grant College Program, Massachusetts Institute of Technology, Cambridge, p 414Google Scholar
  31. Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect–host associations. Nature 366:681–683. doi: https://doi.org/10.1038/366681a0 CrossRefGoogle Scholar
  32. Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling patterns and processes. Ecology 83:2575–2590CrossRefGoogle Scholar
  33. Stefaniak L, Lambert G, Gittenberger A, Zhang H, Lin S, Whitlatch RB (2009) Genetic conspecificity of the worldwide populations of Didemnum vexillum Kott, 2002. Aquat Invasion 4:29–44. doi: https://doi.org/10.3391/ai.2009.4.1.3 CrossRefGoogle Scholar
  34. Stoecker D (1980) Chemical defenses of ascidians against predators. Ecology 61:1327–1334. doi: https://doi.org/10.2307/1939041 CrossRefGoogle Scholar
  35. Tabashnik BE (1983) Host range evolution: the shift from native legume hosts to alfalfa by the butterfly, Colias philodice eriphyle. Evolution 37:150–162. doi: https://doi.org/10.2307/2408183 CrossRefGoogle Scholar
  36. Uribe E, Etchepare I (2002) Effects of biofouling by Ciona intestinalis on suspended culture of Argopecten purpuratus in Bahia Inglesa, Chile. Bull Aquac Assoc Can 102:93–94Google Scholar
  37. Valentine PC, Collie JS, Reid RN, Asch RG, Guida VG, Blackwood DS (2007a) The occurrence of the colonial ascidian Didemnum sp. on Georges Bank gravel habitat—ecological observations and potential effects on groundfish and scallop fisheries. J Exp Mar Biol Ecol 342:179–181. doi: https://doi.org/10.1016/j.jembe.2006.10.038 CrossRefGoogle Scholar
  38. Valentine PC, Carman MR, Blackwood DS, Heffron EJ (2007b) Ecological observations on the colonial ascidian Didemnum sp. in a New England tide pool habitat. J Exp Mar Biol Ecol 342:109–121. doi: https://doi.org/10.1016/j.jembe.2006.10.021 CrossRefGoogle Scholar
  39. Waddell BJ, Perry RI (2007) Survey results of green sea urchin (Strongylocentrotus droebachiensis) populations in Queen Charlotte Strait, British Columbia, October 2006. Can Tech Rep Fish Aquat Sci 2742:47Google Scholar
  40. Whitlatch R, Osman R, Frese A, Malatesta R, Mitchell P, Sedgewick L (1995) The ecology of two introduced marine ascidians and their effects on epifaunal organisms in Long Island Sound. In: Balcom NC (ed) Proceedings of the northeast conference on non-indigenous aquatic nuisance species, 25 January 1997. Publication no: CT-SG-95-04. Connecticut Sea Grant College Program, Cromwell, pp 29–48Google Scholar
  41. Yamaguchi M (1975) Growth and reproductive cycles of the marine fouling ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (Central Japan). Mar Biol (Berl) 29:253–259. doi: https://doi.org/10.1007/BF00391851 CrossRefGoogle Scholar
  42. Young CM (1986) Defenses and refuges: alternative mechanisms of coexistence between a predatory gastropod and its ascidian prey. Mar Biol (Berl) 91:513–522. doi: https://doi.org/10.1007/BF00392603 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • A. Epelbaum
    • 1
    • 3
  • C. M. Pearce
    • 1
    • 2
  • D. J. Barker
    • 2
  • A. Paulson
    • 2
  • T. W. Therriault
    • 1
  1. 1.Fisheries and Oceans CanadaPacific Biological StationNanaimoCanada
  2. 2.Department of Fisheries and AquacultureVancouver Island UniversityNanaimoCanada
  3. 3.Centre for Shellfish ResearchVancouver Island UniversityNanaimoCanada

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