Marine Biology

, Volume 157, Issue 9, pp 1929–1936 | Cite as

Interactions between two introduced species: Zostera japonica (dwarf eelgrass) facilitates itself and reduces condition of Ruditapes philippinarum (Manila clam) on intertidal flats

  • Chaochung Tsai
  • Sylvia Yang
  • Alan C. Trimble
  • Jennifer L. Ruesink
Original Paper


Dwarf eelgrass (duckgrass; Zostera japonica) and Manila clams (Ruditapes philippinarum) are two introduced species that co-occur on intertidal flats of the northeast Pacific. Through factorial manipulation of clam (0, 62.5, 125 clams m−2) and eelgrass density (present, removed by hand, harrowed), we examined intra- and interspecific effects on performance, as well as modification of the physical environment. The presence of eelgrass reduced water flow by up to 40% and was also observed to retain water at low tide, which may ameliorate desiccation and explain why eelgrass grew faster in the presence of conspecifics (positive feedback). Although shell growth of small (20–50 mm) clams was not consistently affected by either treatment in this 2-month experiment, clam condition improved when eelgrass was removed. Reciprocally, clams at aquaculture densities had no effect on eelgrass growth, clam growth and condition, or porewater nutrients. Overall, only Z. japonica demonstrated strong population-level interactions. Interspecific results support an emerging paradigm that invasive marine ecosystem engineers often negatively affect infauna. Positive feedbacks for Z. japonica may characterize its intraspecific effects particularly at the stressful intertidal elevation of this study (+1 m above mean lower low water).



We thank A. Norman and E. Wheat for help in the field. J. Heckes and W. Cowell kindly provided permission to work on their properties. We appreciate the hospitality of B. Kauffmann at the Washington Department of Fish and Wildlife Willapa Bay Field Office. CCT was funded through Howard Hughes Medical Institute Research Internship, Frye-Hotson-Riggs Endowment Fund (University of Washington Biology Department), and Program on the Environment Student Success Fund. He particularly thanks B. Buchwitz and M. Reese for help in project design and presentation. The manuscript benefitted substantially from comments by two anonymous reviewers. This project supports work on the ecological effects of shellfish aquaculture, Western Regional Aquaculture Center through Grant No. 2004-38500-14698 from the United States Department of Agriculture, Cooperative State Research, Education, and Extension Service. JLR and ACT were funded by the Andrew W. Mellon Foundation.


  1. Abbe GR, Albright BW (2003) An improvement to the determination of meat condition index for the eastern oyster Crassostrea virginica (Gmelin 1791). J Shellfish Res 22:747–752Google 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. Baldwin JR, Lovvorn JR (1994) Expansion of seagrass habitat by the exotic Zostera japonica and its use by dabbling ducks and brant in Boundary Bay, British Columbia. Mar Ecol Prog Ser 103:119–127CrossRefGoogle Scholar
  4. Bartoli M, Nizzoli D, Viaroli P, Turolla E, Castaldelli G, Fano EA, Rossi R (2001) Impacts of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455:203–212CrossRefGoogle Scholar
  5. Booth DM, Heck KL (2009) Effects of the American oyster Crassostrea virginica on growth rates of the seagrass Halodule wrightii. Mar Ecol Prog Ser 389:117–126CrossRefGoogle Scholar
  6. Bos AR, Bouma TJ, de Kort GLJ, van Katwijk MM (2007) Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuar Coast Shelf Sci 74:344–348CrossRefGoogle Scholar
  7. Bulleri F, Bruno JF, Benedetti-Cecchi L (2008) Beyond competition: incorporating positive interactions between species to predict ecosystem invasibility. PLoS Biol 6(6):e162. doi: 10.1371/journal.pbio.0060162
  8. Carroll J, Gobler CJ, Peterson BJ (2008) Resource-restricted growth of eelgrass in New York estuaries: light limitation, and alleviation of nutrient stress by hard clams. Mar Ecol Prog Ser 369:51–62CrossRefGoogle Scholar
  9. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  10. Dumbauld BR, Ruesink JL, Rumrill SS (2009) The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290:196–223CrossRefGoogle Scholar
  11. Fonseca MS, Calahan JA (1992) A preliminary evaluation of wave attenuation by four species of seagrass. Est Coast Shelf Sci 35:565–576CrossRefGoogle Scholar
  12. Gribben PE, Wright JT (2006) Invasive seaweed enhances recruitment of a native bivalve: roles of refuge from predation and the habitat choice of recruits. Mar Ecol Prog Ser 318:177–185CrossRefGoogle Scholar
  13. Gribben PE, Wright JT, O’Connor WA, Doblin MA, Eyre B, Steinberg PD (2009) Reduced performance of native infauna following recruitment to a habitat-forming invasive marine alga. Oecologia 158:733–745. doi: 10.1007/s00442-008-1181-0 CrossRefPubMedGoogle Scholar
  14. Guttierez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90CrossRefGoogle Scholar
  15. Haag WR (2009) Extreme longevity in freshwater mussels revisited: sources of bias in age estimates derived from mark-recapture experiments. Freshwater Biol 54:1474–1486CrossRefGoogle Scholar
  16. Han J, Zhang Z, Yu Z, Widdows J (2001) Differences in the benthic-pelagic particle flux biodeposition and sediment erosion at intertidal sites with and without clam (Ruditapes philippinarum) cultivation in eastern China. J Exp Mar Biol Ecol 261:245–261CrossRefGoogle Scholar
  17. Irlandi EA (1996) The effects of seagrass patch size and energy regime on growth of a suspension-feeding bivalve. J Mar Res 54:161–185CrossRefGoogle Scholar
  18. Irlandi EA, Peterson CH (1991) Modification of animal habitat by large plants: mechanisms by which seagrasses influence clam growth. Oecologia 87:307–318CrossRefGoogle Scholar
  19. Kaldy JE (2006) Production ecology of the non-indigenous seagrass, dwarf eelgrass (Zostera japonica Ascher. & Graeb.), in a Pacific Northwest estuary, USA. Hydrobiologia 553:201–217CrossRefGoogle Scholar
  20. Kimbro DL, Grosholz ED, Baukus AJ, Nesbitt NJ, Travis NM, Attoe S, Coleman-Hulbert C (2009) Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades. Oecologia 160:563–575CrossRefPubMedGoogle Scholar
  21. Koshikawa Y, Hagiwara K, Lim BK, Sakurai N (1997) A new marking method for short necked clam Ruditapes philippinarum with rust. Fisheries Science 63:533–538Google Scholar
  22. Kowalski JL, DeYoe HR, Allison TC, Kaldy JE (2001) Productivity estimation in Halodule wrightii: comparison of leaf-clipping and leaf-marking techniques and the importance of clip height. Mar Ecol Prog Ser 220:131–136CrossRefGoogle Scholar
  23. Magni P, Montani S (2006) Seasonal patterns of pore-water nutrients, benthic chlorophyll a and sedimentary AVS in a macrobenthos-rich tidal flat. Hydrobiologia 571:297–311CrossRefGoogle Scholar
  24. McKinnon JG, Gribben PE, Davis AR, Jolley DF, Wright JT (2009) Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Mar Ecol Prog Ser 380:59–71CrossRefGoogle Scholar
  25. 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
  26. Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61Google Scholar
  27. Nizzoli D, Bartoli M, Viaroli P (2006) Nitrogen and phosphorus budgets during a farming cycle of the Manila clam Ruditapes philippinarum: an in situ experiment. Aquaculture 261:98–108CrossRefGoogle Scholar
  28. Nizzoli D, Bartoli M, Viaroli P (2007) Oxygen and ammonium dynamics during a farming cycle of the bivalve Tapes philippinarum. Hydrobiologia 587:25–36CrossRefGoogle Scholar
  29. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva P, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Inv 1:3–19CrossRefGoogle Scholar
  30. Peterson BJ, Heck KL (2001) An experimental test of the mechanism by which suspension feeding bivalves elevate seagrass productivity. Mar Ecol Prog Ser 218:115–125CrossRefGoogle Scholar
  31. Posey M (1988) Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69:974–983CrossRefGoogle Scholar
  32. Powell GVN, Schaffner FC (1991) Water trapping by seagrasses occupying bank habitats in Florida Bay. Estuar Coast Shelf Sci 32:43–60CrossRefGoogle Scholar
  33. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  34. Ruckelshaus MH, Wissmar RC, Simenstad CA (1993) The importance of autotroph distribution to mussel growth in a well-mixed, temperate estuary. Estuaries 16:898–912CrossRefGoogle Scholar
  35. Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay M (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643–689CrossRefGoogle Scholar
  36. Ruesink JL, Feist BE, Harvey CJ, Hong JS, Trimble AC, Wisehart LM (2006) Changes in productivity associated with four introduced species: Ecosystem transformation of a “pristine” estuary. Mar Ecol Prog Ser 311:203–215CrossRefGoogle Scholar
  37. Ruesink JL, Hong JS, Wisehart L, Hacker SD, Dumbauld BR, Trimble AC, Hessing-Lewis M (2010) Congener comparison of native (Zostera marina) and introduced (Z. japonica) eelgrass at multiple scales within a Pacific Northwest estuary. Biological Invasions doi: 10.1007/s10530-009-9588-z
  38. Shafer DJ, Sherman TD, Wyllie-Echeverria S (2007) Do desiccation tolerances control the vertical distribution of intertidal seagrasses? Aquat Bot 87:161–166CrossRefGoogle Scholar
  39. Shafer DJ, Wyllie-Echeverria S, Sherman TD (2008) The potential role of climate in the distribution and zonation of the introduced seagrass Zostera japonica in North America. Aquat Bot 89:297–302CrossRefGoogle Scholar
  40. Simberloff D, von Holle B (1999) Positive interactions of non-indigenous species: invasional meltdown? Biol Inv 1:21–32CrossRefGoogle Scholar
  41. Spencer BE, Kaiser MJ, Edwards DB (1997) Ecological effects of intertidal Manila clam cultivation: observations at the end of the cultivation phase. J Appl Ecol 34:444–452CrossRefGoogle Scholar
  42. Thompson T, Glenn E (1994) Plaster standards to measure water motion. Limnol Oceanogr 39:1768–1779CrossRefGoogle Scholar
  43. Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819CrossRefGoogle Scholar
  44. UNESCO (1994) Protocols for the Joint Global Ocean Flux Study (JGOFS) Core Measurements. IOC Manual and Guides 29. Intergovernmental Oceanographic Commission of UNESCOGoogle Scholar
  45. Vinther HF, Laursen JS, Holmer M (2008) Negative effects of blue mussel (Mytilus edulis) presence in eelgrass (Zostera marina) beds in Flensborg fjord, Denmark. Est Coast Shelf Sci 77:91–103CrossRefGoogle Scholar
  46. Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Poll Bull 55:323–332CrossRefGoogle Scholar
  47. Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Inv 7:369–392CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Chaochung Tsai
    • 1
    • 2
  • Sylvia Yang
    • 1
  • Alan C. Trimble
    • 1
  • Jennifer L. Ruesink
    • 1
  1. 1.Department of BiologyUniversity of WashingtonSeattleUSA
  2. 2.Program on the EnvironmentUniversity of WashingtonSeattleUSA

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