Oecologia

, Volume 159, Issue 4, pp 873–882 | Cite as

Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages

Conservation Ecology - Original Paper

Abstract

Studies examining the effects of invasive species have focussed traditionally on the direct/lethal effects of the invasive on the native community but there is a growing recognition that invasive species may also have non-lethal effects. In terrestrial systems, non-lethal effects of invasive species can disrupt early life-history phases (such as fertilisation, dispersal and subsequent establishment) of native species, but in the marine environment most studies focus on adult rather than early life-history stages. Here, we examine the potential for an introduced sessile marine invertebrate (Styela plicata) to exert both lethal and non-lethal effects on a native species (Microcosmus squamiger) across multiple early life-history stages. We determined whether sperm from the invasive species interfered with the fertilisation of eggs from the native species and found no effect. However, we did find strong effects of the invasive species on the post-fertilisation performance of the native species. The invasive species inhibited the settlement of native larvae and, in the field, the presence of the invasive species was associated with a ten-fold increase in the post-settlement mortality of the native species, as well as an initial reduction of growth in the native. Our results suggest that larvae of the native species avoid settling near the invasive species due to reduced post-settlement survival in its presence. Overall, we found that invasive species can have complex and pervasive effects (both lethal and non-lethal) across the early life-history stages of the native species, which are likely to result in its displacement and to facilitate further invasion.

Keywords

Fertilisation Invasive species Postmetamorphic performance Settlement Trait-mediated effects 

References

  1. Almany GR (2003) Priority effects in coral reef fish communities. Ecology 84:1920–1935CrossRefGoogle Scholar
  2. Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Biol Ecol 342:15–29CrossRefGoogle Scholar
  3. Bando KJ (2006) The roles of competition and disturbance in a marine invasion. Biol Invasions 8:755–763CrossRefGoogle Scholar
  4. Bjerknes AL, Totland O, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12CrossRefGoogle Scholar
  5. Bullard SG, Whitlatch RB, Osman RW (2004) Checking the landing zone: do invertebrate larvae avoid settling near superior spatial competitors? Mar Ecol Prog Ser 280:239–247CrossRefGoogle Scholar
  6. Bullard SG, Sedlack B, Reinhardt JF, Litty C, Gareau K, Whitlatch RB (2007) Fragmentation of colonial ascidians: differences in reattachment capability among species. J Exp Mar Biol Ecol 342:166–168CrossRefGoogle Scholar
  7. Butman CA, Grassle JP, Webb CM (1988) Substrate choices made by marine larvae settling in still water and in a flume flow. Nature 333:771–773CrossRefGoogle Scholar
  8. Byers JE, Goldwasser L (2001) Exposing the mechanism and timing of impact of nonindigenous species on native species. Ecology 82:1330–1343Google Scholar
  9. Byrd J, Lambert CC (2000) Mechanism of the block to hybridisation and selfing between the sympatric ascidians Ciona intestinalis and Ciona savignyi. Mol Reprod Dev 55:109–116PubMedCrossRefGoogle Scholar
  10. Carlton JT (1999) The scale and ecological consequences of biological invasions in the world’s oceans. In: Sandlund OT (ed) Invasive species and biodiversity management. Kluwer, Dordrecht, pp 195–212Google Scholar
  11. Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639PubMedCrossRefGoogle Scholar
  12. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–557PubMedCrossRefGoogle Scholar
  13. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  14. Davis AR, Butler AJ, van Altena I (1991) Settlement behaviour of ascidian larvae: preliminary evidence for inhibition by sponge allelochemicals. Mar Ecol Prog Ser 72:117–123CrossRefGoogle Scholar
  15. Edlund AF, Koehl MAR (1998) Adhesion and reattachment of compound ascidians to various substrata: weak glue can prevent tissue damage. J Exp Biol 201:2397–2402PubMedGoogle Scholar
  16. Elkin C, Marshall DJ (2007) Desperate larvae: influence of deferred costs and habitat requirements on habitat selection. Mar Ecol Prog Ser 335:143–153CrossRefGoogle Scholar
  17. Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (Cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265CrossRefGoogle Scholar
  18. Galil BS (2007) Loss or gain? invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55:314–322PubMedCrossRefGoogle Scholar
  19. Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282CrossRefGoogle Scholar
  20. Gribben PE, Wright JT (2006) Sublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion? Oecologia 149:352–361PubMedCrossRefGoogle Scholar
  21. Grosberg RK (1981) Competitive ability influences habitat choice in marine invertebrates. Nature 290:700–702CrossRefGoogle Scholar
  22. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  23. Harper FM, Hart MW (2005) Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars. Biol Bull 209:113–126PubMedCrossRefGoogle Scholar
  24. Hewitt CL (2002) Distribution and biodiversity of Australian tropical marine bioinvasions. Pac Sci 56:213–222CrossRefGoogle Scholar
  25. Hollebone AL, Hay ME (2007) Propagule pressure of an invasive crab overwhelms native biotic resistance. Mar Ecol Prog Ser 342:191–196CrossRefGoogle Scholar
  26. Kott P (1985) The Australian Ascidiacea, Part 1. Phlebobranchia and Stolidobranchia. Mem Queensl Mus 23:1–438Google Scholar
  27. Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated. Proc Natl Acad Sci USA 105:3800–3804PubMedCrossRefGoogle Scholar
  28. Lambert C (2000) Germ-cell warfare in ascidians: sperm from one species can interfere with the fertilisation of a second species. Biol Bull 198:22–25PubMedCrossRefGoogle Scholar
  29. Lambert CC (2001) Fertilization-induced glycosidase release and interspecific sperm competition in ascidians. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 24–29Google Scholar
  30. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4CrossRefGoogle Scholar
  31. Levitan DR (1995) The ecology of fertilization in free-spawning invertebrates. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 123–156Google Scholar
  32. Levitan DR, Petersen C (1995) Sperm limitation in the sea. Trends Ecol Evol 10:228–231CrossRefGoogle Scholar
  33. Mack MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol Evol 13:195–198CrossRefGoogle Scholar
  34. Mack RP, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  35. Maldonado M, Young CM (1999) Effects of the duration of larval life on post-larval stages of the demosponge Sigmadocia caerulea. J Exp Mar Biol Ecol 232:9–21CrossRefGoogle Scholar
  36. Marshall DJ, Styan CA, Keough MJ (2000) Intraspecific co-variation between egg and body size affects fertilisation kinetics of free-spawning marine invertebrates. Mar Ecol Prog Ser 195:305–309CrossRefGoogle Scholar
  37. Marshall DJ, Bolton TF, Keough MJ (2003a) Offspring size affects the post-metamorphic performance of a colonial marine invertebrate. Ecology 84:3131–3137CrossRefGoogle Scholar
  38. Marshall DJ, Pechenik JA, Keough MJ (2003b) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser 246:153–162CrossRefGoogle Scholar
  39. Meyer JJ, Byers JE (2005) As good as dead? Sublethal predation facilitates lethal predation on an intertidal clam. Ecol Lett 8:160–166CrossRefGoogle Scholar
  40. Morgan S (1995) Life and death in the plankton: larval mortality and adaptation. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 279–322Google Scholar
  41. Nystrom P, Svensson O, Lardner B, Bronmark C, Graneli W (2001) The influence of multiple introduced predators on a littoral pond community. Ecology 82:1023–1039Google Scholar
  42. Osman RW, Whitlatch RB (1995) The influence of resident adults on recruitment: a comparison to settlement. J Exp Mar Biol Ecol 190:169–190CrossRefGoogle Scholar
  43. Pangle KL, Peacor SD (2006) Non-lethal effect of the invasive predator Bythotrephes longimanus on Daphnia mendotae. Freshwater Biol 51:1070–1078CrossRefGoogle Scholar
  44. Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333CrossRefGoogle Scholar
  45. Piazzi L, Ceccherelli G (2002) Effects of competition between two introduced Caulerpa. Mar Ecol Prog Ser 225:189–195CrossRefGoogle Scholar
  46. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UKGoogle Scholar
  47. Reusch TBH, Williams SL (1999) Macrophyte canopy structure and the success of an invasive marine bivalve. Oikos 84:398–416CrossRefGoogle Scholar
  48. Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828CrossRefGoogle Scholar
  49. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632Google Scholar
  50. Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972Google Scholar
  51. Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739CrossRefGoogle Scholar
  52. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Syst 37:95–122CrossRefGoogle Scholar
  53. Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590CrossRefGoogle Scholar
  54. Stoner DS (1994) Larvae of a colonial ascidian use a non-contact mode of substratum selection on a coral reef. Mar Biol 121:319–326CrossRefGoogle Scholar
  55. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651PubMedCrossRefGoogle Scholar
  56. Trussell GC, Ewanchuk PJ, Bertness MD (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245CrossRefGoogle Scholar
  57. Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84:629–640CrossRefGoogle Scholar
  58. Trussell GC, Ewanchuk PJ, Bertness MD, Silliman BR (2004) Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects. Oecologia 139:427–432PubMedCrossRefGoogle Scholar
  59. Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252PubMedCrossRefGoogle Scholar
  60. Underwood AJ, Keough MJ (2001) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 183–200Google Scholar
  61. Veen T, Borge T, Griffith SC, Saetre G-P, Bures S, Gustafsson L, Sheldon BC (2001) Hybridization and adaptive mate choice in flycatchers. Nature 411:45–50PubMedCrossRefGoogle Scholar
  62. Wendt DE (1998) Effect of larval swimming duration on growth and reproduction of Bugula neritina (Bryozoa) under field conditions. Biol Bull 195:126–135CrossRefGoogle Scholar
  63. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  64. Wieczorek SK, Todd CD (1997) Inhibition and facilitation of bryozoan and ascidian settlement by natural multi-species biofilms: effects of film age and the roles of active and passive larval attachment. Mar Biol 128:463–473CrossRefGoogle Scholar
  65. Wonham MJ, Walton WC, Ruiz GM, Frese AN, Galil BS (2001) Going to the source: role of the invasion pathway in determining potential invaders. Mar Ecol Prog Ser 215:1–12CrossRefGoogle Scholar
  66. Wyatt ASJ, Hewitt CL, Walker DI, Ward TJ (2005) Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment. Divers Distrib 11:33–44CrossRefGoogle Scholar
  67. Young CM, Svane I (1989) The ecology and behaviour of ascidian larvae. Oceangr Mar Biol Annu Rev 27:45–90Google Scholar
  68. Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:10–13PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Departament de Biologia Animal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Centre for Advanced Studies of Blanes (CEAB, CSIC)Blanes (Girona)Spain
  3. 3.School of Integrative Biology, University of QueenslandBrisbaneAustralia

Personalised recommendations