, Volume 158, Issue 4, pp 733–745 | Cite as

Reduced performance of native infauna following recruitment to a habitat-forming invasive marine alga

  • Paul E. Gribben
  • Jeffrey T. Wright
  • Wayne A. O’Connor
  • Martina A. Doblin
  • Bradley Eyre
  • Peter D. Steinberg
Global Change Ecology - Original Paper


Despite well-documented negative impacts of invasive species on native biota, evidence for the facilitation of native organisms, particularly by habitat-forming invasive species, is increasing. However, most of these studies are conducted at the population or community level, and we know little about the individual fitness consequences of recruitment to habitat-forming invasive species and, consequently, whether recruitment to these habitats is adaptive. We determined the consequences of recruitment to the invasive green alga Caulerpa taxifolia on the native soft-sediment bivalve Anadara trapezia and nearby unvegetated sediment. Initially, we documented the growth and survivorship of A. trapezia following a natural recruitment event, to which recruitment to C. taxifolia was very high. After 12 months, few clams remained in either habitat, and those that remained showed little growth. Experimental manipulations of recruits demonstrated that all performance measures (survivorship, growth and condition) were significantly reduced in C. taxifolia sediments compared to unvegetated sediments. Exploration of potential mechanisms responsible for the reduced performance in C. taxifolia sediments showed that water flow and water column dissolved oxygen (DO) were significantly reduced under the canopy of C. taxifolia and that sediment anoxia was significantly higher and sediment sulphides greater in C. taxifolia sediments. However, phytoplankton abundance (an indicator of food supply) was significantly higher in C. taxifolia sediments than in unvegetated ones. Our results demonstrate that recruitment of native species to habitat-forming invasive species can reduce growth, condition and survivorship and that studies conducted at the community level may lead to erroneous conclusions about the impacts of invaders and should include studies on life-history traits, particularly juveniles.


Anadara trapezia Bivalve Caulerpa taxifolia Fitness Growth Invasion biology Juveniles Maladaptive Soft sediment Survivorship 



We are grateful to Michael Clements for assistance with fieldwork and Louise McKenzie for assisting with fieldwork and video image analyses. Jeb Byers and two anonymous reviewers provided valuable comments which greatly improved the manuscript.


  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42Google Scholar
  2. Allen BJ, Williams SL (2003) Native eelgrass Zostera marina controls growth and reproduction of an invasive mussel through food limitation. Mar Ecol Prog Ser 254:57–67CrossRefGoogle Scholar
  3. Anderson LW (2005) California’s reaction to Caulerpa taxifolia: a model for invasive species rapid response. Biol Invasions 7:1003–1006CrossRefGoogle Scholar
  4. Bellan-Santini D, Arnaud P, Bellan G, Verlaque M (1996) The influence of the introduced alga, Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota. J Mar Biol Assoc UK 76:235–237Google Scholar
  5. Bologna PAX, Heck KL (1999) Differential predation and growth rates of bay scallops within a seagrass habitat. J Exp Mar Bio Ecol 239:299–314Google Scholar
  6. Breitburg DL (1992) Episodic hypoxia in Chesapeake Bay: interacting effects of recruitment, behavior, and physical disturbance. Ecol Monogr 62:525–546CrossRefGoogle Scholar
  7. Carmichael RH, Shriver AC, Valiela I (2004) Changes in shell and soft tissue growth, tissue composition, and survival of quahogs, Mercenaria mercenaria, and softshell clams, Mya arenaria, in response to eutrophic-driven changes in food supply and habitat. J Exp Mar Biol Ecol 313:75–104CrossRefGoogle Scholar
  8. Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130CrossRefGoogle Scholar
  9. Ceccherelli G, Cinelli F (1997) Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymedocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. J Exp Mar Biol Ecol 217:165–177CrossRefGoogle Scholar
  10. Chisholm JRM, Moulin P (2003) Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 48:787–794Google Scholar
  11. Cline J (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458CrossRefGoogle Scholar
  12. Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710–723CrossRefGoogle Scholar
  13. Creese RG, Davies AR, Glasby TM (2004) Eradicating and preventing the spread of the invasive alga Caulerpa taxifolia in NSW. NSW Fish Final Rep Ser 64:110Google Scholar
  14. Crone EE (2001) Is survivorship a better surrogate than fecundity? Oikos 55:2611–2614Google Scholar
  15. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152CrossRefGoogle Scholar
  16. Crooks JA (2001) Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon. Biol Invasions 3:23–36CrossRefGoogle Scholar
  17. Crooks JA (2002) Characterizing eco-system consequences of biological invasions: the role of ecosystem engineers. Oikos 97:137–152CrossRefGoogle Scholar
  18. Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75CrossRefGoogle Scholar
  19. Cummins SP, Roberts DE, Ajani P, Underwood AJ (2004) Comparisons of assemblages of phytoplankton between open water and seagrass habitats in a shallow coastal lagoon. Mar Freshw Res 55:447–456CrossRefGoogle Scholar
  20. D’Avanzo C, Kremer JN (1994) Diel oxygen dynamics and anoxic events in an eutrophic estuary of Waquoit Bay, Massachusetts. Estuaries 17:131–139CrossRefGoogle Scholar
  21. Decker MB, Breitburg DL, Marcus NH (2003) Geographical differences in behavioral responses to hypoxia: local adaptation to an anthropogenic stressor? Ecol Appl 14:1104–1109CrossRefGoogle Scholar
  22. Deegan LA, Wright A, Ayvazian SG, Finn JT, Golden H, Rand Merson R, Harrison J (2002) Nitrogen loading alters seagrass ecosystem structure and support of higher trophic levels. Aquat Conserv Mar Freshw Ecosyst 12:193–212CrossRefGoogle Scholar
  23. Doty MS (1971) Measurements in water movement in reference to benthic algae growth. Bot Mar 14:32–35CrossRefGoogle Scholar
  24. Edgar GJ (2000) Australian marine life: the plants and animals of temperate waters. Reed New Holland, SydneyGoogle Scholar
  25. Fossing H, Jorgensen BB (1989) Measurement of bacterial sulfate reduction in sediments: evaluation of single-step chromium reduction method. Biogeochemistry 8:205–222CrossRefGoogle Scholar
  26. Glasby TM, Creese RG (2007) Invasive marine species management and research. In: Connell SD, Gillanders BM (eds) Marine ecology. Oxford University Press, Melbourne, pp 569–594Google Scholar
  27. Gribben PE, Wright JT (2006a) Invasive seaweed enhances recruitment of a native bivalve: roles of refuge from predation and habitat choice. Mar Ecol Prog Ser 318:177–185CrossRefGoogle Scholar
  28. Gribben PE, Wright JT (2006b) Sublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion? Oecologia 149:352–361PubMedCrossRefGoogle Scholar
  29. Hacker SD, Dethier MN (2006) Community modification by a grass invader has differing impacts for marine habitats. Oikos 113:279–286CrossRefGoogle Scholar
  30. Hedge P, Kriwoken Lk (2000) Evidence for effects of Spartina anglica invasion on benthic macrofauna in Little Swanport Estuary, Tasmania. Austral Ecol 25:150–159Google Scholar
  31. Howerton RD, Boyd CE (1992) Measurements of water circulation in ponds with gypsum blocks. Aquac Eng 11:141–155CrossRefGoogle Scholar
  32. Irlandi EA, Peterson CH (1991) Modification of animal habitat by large plants: mechanisms by which seagrasses influence clam growth. Oecologia 87:307–318CrossRefGoogle Scholar
  33. Keck RT, Maurer D, Lind H (1975) A comparative study of the hard clam gonad development cycle. Biol Bull 148:243–258PubMedCrossRefGoogle Scholar
  34. Levi F, Francour P (2004) Behavioural response of Mullus surmuletus to habitat modification by the invasive macroalga Caulerpa taxifolia. J Fish Biol 64:55–64CrossRefGoogle Scholar
  35. Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87:419–432PubMedCrossRefGoogle Scholar
  36. Longepierre S, Robert A, Levi F, Francour P (2005) How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems. Biodivers Conserv 14:365–376CrossRefGoogle Scholar
  37. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  38. Malouf RE, Bricelj VM (1989) Comparative biology of clams: environmental tolerances, feeding, and growth. In: Manzi J, Castagna M (eds) Clam mariculture in North America. Elsevier, Amsterdam, pp 23–73Google Scholar
  39. Meinesz A, Belsher T, Thibaut T, Antolic B, Ben Mustapha K, Bourdouresque C-F, Chiaverini D, Cottalorda J-M, Djellouli A, El Abed A, Orestano C, Grau AM, Ivesa L, Jaklin L, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, de Vaugelas J, Zavodnik N, Zuljevic A (2001) The introduced marine alga Caulerpa taxifolia in the Medtiterranean. Biol Invasions 38:499–508Google Scholar
  40. Neira C, Levin LA, Grosholz ED (2005) Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Mar Ecol Prog Ser 292:111–126CrossRefGoogle Scholar
  41. Neira C, Grosholz ED, Levin LA, Blake R (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecol Appl 16:1391–1404PubMedCrossRefGoogle Scholar
  42. Nell JA, O’Connor WA, Heasman MP, Goard LJ (1994) Hatchery production for the venerid clam Katelysia rhytiphora (Lamy) and the Sydney cockle Anadara trapezia (Deshayes). Aquaculture 119:149–156CrossRefGoogle Scholar
  43. Patterson K, Nell J (1996) Estuarine clam farming in NSW. Austasia Aquac 10:52–53Google Scholar
  44. Peterson CH, Estes JA (2001) Conservation and management of marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinuaer, Sunderland, pp 469–507Google Scholar
  45. Posey MH (1988) Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69:974–983CrossRefGoogle Scholar
  46. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  47. Reusch TBH, Williams SL (1999) Macrophyte canopy structure and the success of an invasive marine bivalve. Oikos 84:398–416CrossRefGoogle Scholar
  48. Robertson BA, Hutto RL (2006) A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87:1075–1085PubMedCrossRefGoogle Scholar
  49. Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939CrossRefGoogle Scholar
  50. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  51. Sullivan LA, Bush RT, McConchie DM (2000) A modified chromium-reducible sulfur method for reduced inorganic sulfur: optimum reaction time for acid sulfate soil. Aust J Soil Res 38:729–734CrossRefGoogle Scholar
  52. Swanson RL, Williamson JE, De Nys R, Kumar N, Bucknall MP (2004) Induction of settlement of larvae of the sea urchin Holopneustes purpurascens by histamine from its host plant. Biol Bull 206:161–172PubMedCrossRefGoogle Scholar
  53. Thompson TL, Glenn EP (1994) Plaster standards to measure water motion. Limnol Oceanogr 39:1768–1779Google Scholar
  54. Ulstrup KE, Hill R, Ralph PJ (2005) Photosynthetic impact of hypoxia on in hospite zooxanthellae in the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 286:125–132Google Scholar
  55. Underwood AJ (1997) Experiments in ecology. Cambridge University Press, CambridgeGoogle Scholar
  56. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  57. Williamson JE, Carson DG, De Nys R, Steinberg PD (2004) Demographic consequences of an ontogenetic shift by a sea urchin in response to host plant chemistry. Ecology 85:1355–1371CrossRefGoogle Scholar
  58. Winter JE (1978) A review of the knowledge of suspension-feeding in lamellibranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13:1–33CrossRefGoogle Scholar
  59. Wonham MJ, O’Connor M, Harley CDG (2005) Positive effects of a dominant invader on introduced and native mudflat species. Mar Ecol Prog Ser 289:109–116CrossRefGoogle Scholar
  60. Wright JT (2005) Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations. Mar Biol 147:559–569CrossRefGoogle Scholar
  61. Wright JT, Davies AR (2006) Demographic feedback between clonal growth and fragmentation in an invasive seaweed. Ecology 87:1744–1754PubMedCrossRefGoogle Scholar
  62. Wright JT, Gribben PE (2008) Fitness response of fauna to an invasive seaweed: predictions of impact based on community structure alone are insufficient. J Appl Ecol 45:1540–1549CrossRefGoogle Scholar
  63. Wright JT, McKenzie LA, Gribben PE (2007) A decline in the density and health of a native bivalve associated with Caulerpa taxifolia invasion. Mar Freshw Res 58:263–277CrossRefGoogle Scholar
  64. York PH, Booth DJ, Glasby TM, Pease BC (2006) Fish assemblages in habitats dominated by Caulerpa taxifolia and native seagrasses in south-eastern Australia. Mar Ecol Prog Ser 312:223–234CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Paul E. Gribben
    • 1
  • Jeffrey T. Wright
    • 2
  • Wayne A. O’Connor
    • 3
  • Martina A. Doblin
    • 1
  • Bradley Eyre
    • 4
  • Peter D. Steinberg
    • 5
  1. 1.Department of Environmental SciencesUniversity of TechnologySydneyAustralia
  2. 2.Institute for Conservation Biology and School of Biological SciencesUniversity of WollongongWollongongAustralia
  3. 3.NSW Department of Primary Industries Port Stephens Fisheries CentreTaylors BeachAustralia
  4. 4.School of Environmental Science and ManagementSouthern Cross UniversityLismoreAustralia
  5. 5.Centre for Marine Biofouling and Bio-Innovation and School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia

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