Biological Invasions

, Volume 11, Issue 10, pp 2303–2316 | Cite as

Distribution and ecological role of the non-native macroalga Gracilaria vermiculophylla in Virginia salt marshes

  • M. S. Thomsen
  • K. J. McGlathery
  • A. Schwarzschild
  • B. R. Silliman
Original Paper

Abstract

Intertidal salt marshes are considered harsh habitats where relatively few stress-resistant species survive. Most studies on non-native species in marshes describe terrestrial angiosperms. We document that a non-native marine macroalga, Gracilaria vermiculophylla, is abundant throughout Virginia’s Atlantic coastline. We sampled eight marshes, characterized by low slopes and by the presence of the tube-building polychaete Diopatracuprea on adjacent mudflats, which have been shown previously to be associated with G. vermiculophylla. G. vermiculophylla was found in 71% of the sampled quadrats on the border between the mudflat and tall Spartina alterniflora, 51% within the tall S. alterniflora zone, and 12% further inland. We also tagged G. vermiculophylla from two habitats: (1) unattached G. vermiculophylla within marshes and (2) G. vermiculophylla ‘incorporated’ onto D.cuprea tubes on the adjacent mudflats. Of the incorporated thalli, 3–9% ended up in the marsh, demonstrating connectivity between habitats. In addition, 21% of unattached thalli remained for 2 weeks within the marsh, suggesting that entanglement around marsh plants reduces tidal drift. Growth experiments in mesh bags indicate that most of the G. vermiculophylla transferred from the lagoon to the marsh decomposed there, potentially enhancing local nutrient levels. Finally, we document that G. vermiculophylla in marshes had a reduced associated flora and fauna compared to G. vermiculophylla on the adjacent Diopatra mudflats. In conclusion, unattached G. vermiculophylla is abundant along marsh borders in the tall S. alterniflora zone in Virginia, and we hypothesize that this non-native species has significant impacts in terms of marsh habitat complexity, species abundance and diversity, nutrient dynamics, productivity, and trophic interactions.

Keywords

Non-native macroalgae Salt marsh Gracilaria vermiculophylla Spartina alterniflora 

References

  1. Able KW, Ragan SM (2003) Impact of common reed, Phragmites australis, on essential fish habitat: influence on reproduction, embryological development, and larval abundance of mummichog (Fundulus heteroclitus). Estuaries 26:40–50CrossRefGoogle Scholar
  2. Adam P (1990) Saltmarsh ecology. Cambridge University Press, CambridgeGoogle Scholar
  3. Amsberry L, Baker MA, Ewanchuk PJ, Bertness MD (2000) Clonal integration and the expansion of Phragmites australis. Ecol Appl 10:1110–1118. doi:10.1890/1051-0761(2000)010[1110:CIATEO]2.0.CO;2 CrossRefGoogle Scholar
  4. Anderson MJ (2004) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance using permutation tests. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  5. Bart D, Burdick DM, Chambers R, Hartman JM (2006) Human facilitation of Phragmites australis invasion in tidal marshes: a review and synthesis. Wetlands Ecol Manage 14:53–65. doi:10.1007/s11273-005-2566-z CrossRefGoogle Scholar
  6. Benoit LK, Askins RA (1999) Impact of the spread of Phragmites on the distribution of birds in Connecticut tidal marshes. Wetlands 19:194–208CrossRefGoogle Scholar
  7. Boyer KE, Fong P (2005) Macroalgal-mediated transfers of water column nitrogen to intertidal sediments and salt marsh plants. J Exp Mar Biol Ecol 321:59–69. doi:10.1016/j.jembe.2005.01.005 CrossRefGoogle Scholar
  8. Brinkhuis BH (1977) Comparisons of salt-marsh fucoid production estimated from three different indices. J Phycol 13:328–335Google Scholar
  9. Brinkhuis BH, Tempel NR, Jones RF (1976) Photosynthesis and respiration of exposed salt-marsh fucoids. Mar Biol (Berl) 34:349–359. doi:10.1007/BF00398128 CrossRefGoogle Scholar
  10. Brusati ED, Grosholz ED (2006) Native and introduced ecosystem engineers produce contrasting effects on estuarine infaunal communities. Biol Invasions 8:683–695. doi:10.1007/s10530-005-2889-y CrossRefGoogle Scholar
  11. Brusati ED, Grosholz ED (2007) Effect of native and invasive cordgrass on Macoma petalum density, growth, and isotopic signatures. Estuar Coast Shelf Sci 71:517–522. doi:10.1016/j.ecss.2006.08.026 CrossRefGoogle Scholar
  12. Buschmann A, Chapman AS, Saier B (2006) How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar Biol (Berl) 148:743–754. doi:10.1007/s00227-005-0128-9 CrossRefGoogle Scholar
  13. Chambers RM, Osgood DT, Bart DJ, Montalto F (2003) Phragmites australis invasion and expansion in tidal wetlands: interactions among salinity, sulfide, and hydrology. Estuaries 26:398–406CrossRefGoogle Scholar
  14. Chapman VJ (1974) Salt marshes and salt deserts of the world. Cramer, LehreGoogle Scholar
  15. Chen HL, Li B, Hu JB, Chen JK, Wu JH (2007) Effects of Spartina alterniflora invasion on benthic nematode communities in the Yangtze Estuary. Mar Ecol Prog Ser 336:99–110. doi:10.3354/meps336099 CrossRefGoogle Scholar
  16. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  17. Cottet M, de Montaudouin X, Blanchet H, Lebleu P (2007) Spartina anglica eradication experiment and in situ monitoring assess structuring strength of habitat complexity on marine macrofauna at high tidal level. Estuar Coast Shelf Sci 71:629–640. doi:10.1016/j.ecss.2006.09.014 CrossRefGoogle Scholar
  18. Cowper SW (1978) The drift algae community of seagrass beds in Redfish Bay, Texas. Contrib Mar Sci 21:125–132Google Scholar
  19. Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp invasions in Pacific estuaries, USA. Biol Conserv 78:51–58. doi:10.1016/0006-3207(96)00017-1 CrossRefGoogle Scholar
  20. Daiber F (1982) Animals of the tidal marsh. Van Nostrand Reinhold Company, New YorkGoogle Scholar
  21. Fong P, Boyer KE, Zedler JB (1998) Developing an indicator of nutrient enrichment in coastal estuaries and lagoons using tissue nitrogen content of the opportunistic alga, Enteromorpha intestinalis (L. Link). J Exp Mar Biol Ecol 231:63–79. doi:10.1016/S0022-0981(98)00085-9 CrossRefGoogle Scholar
  22. Freshwater DW, Montgomery F, Greene JK, Hamner RM, Williams M, Whitfield PE (2006) Distribution and identification of an invasive Gracilaria species that is hampering commercial fishing operations in southeastern North Carolina, USA. Biol Invasions 8:631–637. doi:10.1007/s10530-005-1809-5 CrossRefGoogle Scholar
  23. Gabriela P, Juan A, Marta BC (2000) Spatial micro-patterns in the steppe of Tierra del Fuego induced by sheep grazing. J Veg Sci 11:43–50. doi:10.2307/3236774 CrossRefGoogle Scholar
  24. Grimm V, Reise K, Strasser M (2003) Marine metapopulations: a useful concept? Helgol Mar Res 56:222–228Google Scholar
  25. Hanski I (1998) Metapopulation dynamics. Nature 396:41–49. doi:10.1038/23876 CrossRefGoogle Scholar
  26. Hay ME, Renaud PE, Fenical W (1988) Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia 75:246–252. doi:10.1007/BF00378605 CrossRefGoogle Scholar
  27. Hay ME, Duffy JE, Fenical W (1990) Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology 71:733–743. doi:10.2307/1940326 CrossRefGoogle Scholar
  28. Hedge P, Kriwoken LK (2000) Evidence for effects of Spartina anglica invasion on benthic macrofauna in Little Swanport estuary, Tasmania. Austral Ecol 25:150–159. doi:10.1046/j.1442-9993.2000.01016.x Google Scholar
  29. Heinz W (1999) Photosynthesis yield analyzer mini-PAM, Portable Chlorophyll Fluorometer, Handbook of Operation 2. Edition, AugustGoogle Scholar
  30. Holmquist JG (1992) Disturbance, dispersal, and patch insularity in a marine benthic assemblage: influence of a mobile habitat on seagrasses and associated fauna. PhD Dissertation, Department of Biology, Florida State University, Florida, USAGoogle Scholar
  31. Holmquist JG (1994) Benthic macroalgae as a dispersal mechanism for fauna: influence of a marine tumbleweed. J Exp Mar Biol Ecol 180:235–251. doi:10.1016/0022-0981(94)90069-8 CrossRefGoogle Scholar
  32. Humm HJ (1979) The marine algae of Virginia. The University Press of Virginia, VirginiaGoogle Scholar
  33. Keddy PA (2000) Wetland ecology—principles and conservation. Cambridge Press, Cambridge, UKGoogle Scholar
  34. Lipcius RN, Stockhausen WT (2002) Concurrent decline of the spawning stock, recruitment, larval abundance, and size of the blue crab Callinectes sapidus in Chesapeake Bay. Mar Ecol Prog Ser 226:45–61. doi:10.3354/meps226045 CrossRefGoogle Scholar
  35. Lippson AJ, Lippson RL (1997) Life in the Chesapeake Bay. The John Hopkins University Press, BaltimoreGoogle Scholar
  36. Macinnis CMO, Ralph PJ (2001) Short-term response and recovery of Zostera capricorni photosynthesis after herbicide exposure. Aquat Bot 76:1–15. doi:10.1016/S0304-3770(03)00014-7 CrossRefGoogle Scholar
  37. Mangum CP, Santos SL, Rhodes WR (1968) Distribution and feeding in the onuphid polychaete, Diopatra cuprea (BOSC). Mar Biol (Berl) 2:33–40. doi:10.1007/BF00351635 CrossRefGoogle Scholar
  38. Moseman SM, Levina LA, Curri C, Forder C (2004) Colonization, succession, and nutrition of macrobenthic assemblages in a restored wetland at Tijuana Estuary, California. Estuar Coast Shelf Sci 60:755–770. doi:10.1016/j.ecss.2004.03.013 CrossRefGoogle Scholar
  39. Mouget JL, Tremblin G (2002) Suitability of the Fluorescence Monitoring Systems (FMS, Hansatech) for measurement of photosynthetic characteristics in algae. Aquat Bot 74:219–231. doi:10.1016/S0304-3770(02)00104-3 CrossRefGoogle Scholar
  40. Neira C, Grosholz ED, Levin LA, Blake R (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecol Appl 16:1391–1404. doi:10.1890/1051-0761(2006)016[1391:MGMOBF]2.0.CO;2 CrossRefPubMedGoogle Scholar
  41. Nieva FJJ, Castillo JM, Luque CJ, Figueroa ME (2003) Ecophysiology of tidal and non-tidal populations of the invading cordgrass Spartina densiflora: seasonal and diurnal patterns in a Mediterranean climate. Estuar Coast Shelf Sci 57:919–928. doi:10.1016/S0272-7714(02)00422-5 CrossRefGoogle Scholar
  42. Nyberg CD (2006). Attributes of non-indigenous seaweeds with special emphasis on Gracilaria vermiculophylla. Licenciate thesis, Gøteborg University, Gøteborg, SwedenGoogle Scholar
  43. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  44. Raikar S, Lima M, Fujita Y (2001) Effect of temperature, salinity and light intensity on the growth of Gracilaria spp. (Gracilariales, Rhodophyta) from Japan, Malaysia and India. Indian J Mar Sci 30:98–104Google Scholar
  45. Rueness J (2005) Life history and molecular sequences of Gracilaria vermiculophylla (Gracilariales, Rhodophyta), a new introduction to European waters. Phycologia 44:120–128. doi:10.2216/0031-8884(2005)44[120:LHAMSO]2.0.CO;2 CrossRefGoogle Scholar
  46. Schneider CW, Searles RB (1991) Seaweeds of the southeastern United States—Cape Hatteras to Cape Caneveral. Duke University Press, Durham, NCGoogle Scholar
  47. Silliman BR, Bertness MD (2004) Shoreline development drives invasion of Phragmites australis and the loss of New England salt marsh plant diversity. Conserv Biol 18:1424–1434. doi:10.1111/j.1523-1739.2004.00112.x CrossRefGoogle Scholar
  48. Stæhr P, Pedersen MF, Thomsen MS, Wernberg T, Krause-Jensen D (2000) Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar Ecol Prog Ser 207:79–88. doi:10.3354/meps207079 CrossRefGoogle Scholar
  49. Theodose TA, Martin J (2003) Microclimate and substrate quality controls on nitrogen mineralization in a New England high salt marsh. Plant Ecol 167:213–221. doi:10.1023/A:1023974109113 CrossRefGoogle Scholar
  50. Thomsen MS (2004a) Macroalgal distribution patterns and ecological performances in a tidal coastal lagoon, with emphasis on the non-indigenous Codium fragile ssp. tomentosoides. PhD thesis, Department of Environmental Sciences, University of Virginia, Charlottesville, 315 pGoogle Scholar
  51. Thomsen MS (2004b) Species, thallus size and substrate determine macroalgal break forces and break places in a low-energy soft-bottom lagoon. Aquat Bot 80:153–161. doi:10.1016/j.aquabot.2004.08.002 CrossRefGoogle Scholar
  52. Thomsen MS, McGlathery KJ (2005) Facilitation of macroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuar Coast Shelf Sci 62:63–73. doi:10.1016/j.ecss.2004.08.007 CrossRefGoogle Scholar
  53. Thomsen MS, McGlathery KJ (2006) Effects of accumulations of sediments and drift algae on recruitment of sessile organisms associated with oyster reefs. J Exp Mar Biol Ecol 328:22–34. doi:10.1016/j.jembe.2005.06.016 CrossRefGoogle Scholar
  54. Thomsen MS, McGlathery KJ (2007) Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biol Invasions 9:499–513. doi:10.1007/s10530-006-9043-3 CrossRefGoogle Scholar
  55. Thomsen MS, McGlathery KJ, Tyler AC (2006) Macroalgal distribution pattern in a shallow, soft-bottom lagoon, with emphasis on the nonnative Gracilaria vermiculophylla and Codium fragile. Estuaries Coasts 29:470–478Google Scholar
  56. Thomsen MS, Silliman BR, McGlathery KJ (2007a) Spatial variation in recruitment of native and invasive sessile species onto oyster reefs in a temperate soft-bottom lagoon. Estuar Coast Shelf Sci 72:89–101. doi:10.1016/j.ecss.2006.10.004 CrossRefGoogle Scholar
  57. Thomsen MS, Stæhr P, Nyberg CD, Krause-Jensen D, Schwærter S, Silliman BR (2007b) Gracilaria vermiculophylla in northern Europe, with focus on Denmark, and what to expect in the future. Aquat Invasions 3:1–12Google Scholar
  58. Virnstein RW, Carbonara PA (1985) Seasonal abundance and distribution of drift algae and seagrasses in the Mid-Indian River Lagoon, Florida. Aquat Bot 23:67–82. doi:10.1016/0304-3770(85)90021-X CrossRefGoogle Scholar
  59. Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Pollut Bull 55:323–332. doi:10.1016/j.marpolbul.2006.11.010 CrossRefPubMedGoogle Scholar
  60. Wernberg T, Thomsen MS, Staerh PA, Pedersen MF (2004) Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Denmark). Helgol Mar Res 58:154–161. doi:10.1007/s10152-004-0180-8 CrossRefGoogle Scholar
  61. Wernberg T, Vanderklift MA, How J, Lavery PS (2006) Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147:692–701. doi:10.1007/s00442-005-0318-7 CrossRefPubMedGoogle Scholar
  62. Wikstrom SA, Kautsky L (2004) Invasion of a habitat-forming seaweed: effects on associated biota. Biol Invasions 6:141–150. doi:10.1023/B:BINV.0000022132.00398.14 CrossRefGoogle Scholar
  63. Williams SL, Grosholz ED (2008) The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries Coasts 31:3–20CrossRefGoogle Scholar
  64. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359. doi:10.1146/annurev.ecolsys.38.091206.095543 CrossRefGoogle Scholar
  65. Wittenberg R, Cock MJ (2001) Invasive alien species. How to address one of the greatest threats to biodiversity: a toolkit of best prevention and management practices. CAB International, WallingfordGoogle Scholar
  66. Yokoya NS, Kakita H, Obika H, Kitamura T (1999) Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island, Japan. Hydrobiologia 398/399:339–347. doi:10.1023/A:1017072508583 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • M. S. Thomsen
    • 1
    • 2
  • K. J. McGlathery
    • 3
  • A. Schwarzschild
    • 3
  • B. R. Silliman
    • 4
  1. 1.Marine Department, National Environmental Research InstituteUniversity of AarhusRoskildeDenmark
  2. 2.School of Natural Sciences, Faculty of Computing, Health and ScienceEdith Cowan UniversityJoondalupAustralia
  3. 3.Department of Environmental SciencesUniversity of VirginiaCharlottesvilleUSA
  4. 4.Department of ZoologyUniversity of FloridaGainesvilleUSA

Personalised recommendations