Biological Invasions

, Volume 11, Issue 2, pp 225–239 | Cite as

Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions

  • Serena M. Moseman
  • Rui Zhang
  • Pei Yuan Qian
  • Lisa A. Levin
Original Paper


Impacts of invasive species on microbial components of wetland ecosystems can reveal insights regarding functional consequences of biological invasions. Nitrogen fixation (acetylene reduction) rates and diversity of nitrogen fixers, determined by genetic fingerprinting (T-RFLP) of the nifH gene, were compared between native and invaded sediments in three systems. Variable responses of nitrogen fixing microbes to invasion by a non-native mussel, Musculista senhousia, and mangrove, Avicennia marina, in Kendall Frost-Northern Wildlife Preserve (Mission Bay) and salt cedar, Tamarisk (Tamarix spp.) in Tijuana Estuary suggest microbes respond to both species- and site-specific influences. Structurally similar invaders (the mangrove and salt cedar) produced different effects on activity and diversity of nitrogen fixers, reflecting distinct environmental contexts. Despite relative robustness of microbial community composition, subtle differences in total diversity or activity of nitrogen fixers reveal that microbes are not immune to impacts of biological invasions, and that functional redundancy of microbial diversity is limited, with significant consequences for functional dynamics of wetlands.


Asian mussel Diazotroph Mangrove Salt cedar Functional redundancy 



The authors thank Christine R. Whitcraft, Jeffrey A. Crooks, and Amanda J. Demopolous for providing environmental data. Generous support from Pei-Yuan Qian of the Hong Kong University of Science and Technology enabled T-RFLP applications and collaborations. Funding for this research was provided by the National Science Foundation, the National Estuarine Research Reserve System (Graduate Research Fellowships for Serena Moseman), and the University of California Natural Reserve System (Mildred Mathias Student Research Grant). The Michael M. Mullin and Mia Tegner Memorial Funds and the Graduate Department of Scripps Institution of Oceanography also provided financial support. Helpful comments and guidance were provided by Carolyn Currin, and James Leichter. Facilities and gas chromatography equipment were provided by Lihini Aluwihare. Equipment for DNA extractions were provided by the Center for Marine Biodiversity and Conservation at Scripps Institution of Oceanography. Guillermo Mendoza provided guidance with Primer software operation and applications. Pat McMillan gave valuable formatting assistance. Tracy Washington and Maria del Carmen Rivero assisted with laboratory analyses.


  1. Allen JA (1998) Mangroves as alien species: the case of Hawaii. Glob Ecol Biogeogr Lett 7(1):61–71CrossRefGoogle Scholar
  2. Bagwell CE, Dantzler M, Bergholz PW, Lovell CR (2001) Host-specific ecotype diversity of rhizoplane diazotrophs of the perennial glasswort Salicornia virginica and selected salt marsh grasses. Aquat Microb Ecol 23(3):293–300CrossRefGoogle Scholar
  3. Bartoli M, Nizzoli D, Viaroli P, Turolla E, Castaldelli G, Fano EA, Rossi R (2001) Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455:203–212CrossRefGoogle Scholar
  4. Baum BR (1978) The genus Tamarix. Israel Academy of Sciences and the Humanities, JerusalemGoogle Scholar
  5. Bertness M (1984) Habitat and community modification by an introduced herbivorous snail. Ecology 65(2):370–381CrossRefGoogle Scholar
  6. Boyer KE, Zedler JB (1999) Nitrogen addition could shift plant community composition in a restored California salt marsh. Restor Ecol 7(1):74–85CrossRefGoogle Scholar
  7. Brown MM, Friez MJ, Lovell CR (2003) Expression of nifH genes by diazotrophic bacteria in the rhizosphere of short form Spartina alterniflora. FEMS Microbiol Ecol 43:411–417CrossRefPubMedGoogle Scholar
  8. Brusati ED, Grosholz ED (2006) Native and introduced ecosystem engineers produce contrasting effects on estuarine infaunal Communities. Biol Invasions 8:683–695CrossRefGoogle Scholar
  9. Capone DG (1988) Benthic nitrogen fixation. In: Blackburn TH, Sorensen J (eds) Nitrogen cycling in coastal marine environments. Wiley, New York, pp 85–123Google Scholar
  10. Capone DG, Montoya JP (2001) Nitrogen fixation and denitrification. In: Paul JH (ed) Methods in microbiology. Academic Press, San Diego, pp 271–288Google Scholar
  11. Chisholm JRM, Moulin P (2003) Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 48(2):787–794CrossRefGoogle Scholar
  12. Clarke KR, Gorley RN (2001) Primer v5: user manual/tutorial. Primer-E Ltd, Plymouth, UKGoogle Scholar
  13. Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council and Plymouth Marine Laboratory, Plymouth, UKGoogle Scholar
  14. Covin JD, Zedler JB (1988) Nitrogen effects on Spartina foliosa and Salicornia virginica in the salt marsh at Tijuana Estuary. Wetlands 8:51–65Google Scholar
  15. Crooks JA (1996) The population ecology of an exotic mussel, Musculista senhousia, in a southern California bay. Estuaries 19(1):42–50CrossRefGoogle Scholar
  16. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152CrossRefGoogle Scholar
  17. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. OIKOS 97:153–166CrossRefGoogle 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. Crooks JA, Ruiz GM (2001) Biological invasions of marine ecosystems. In: Gallaugher P, Bendell-Young L (eds) Waters in peril. Kluwer, Norwell, MA, pp 3–18Google Scholar
  20. Currin C, Paerl H (1998) Epiphytic nitrogen fixation associated with standing dead shoots of smooth cordgrass, Spartina alterniflora. Estuaries 21(1):106–117CrossRefGoogle Scholar
  21. Di Tomaso JM (1998) Impact, biology, and ecology of salt cedar (Tamarix spp.) in the southwestern United States. Weed Technol 12:326–336Google Scholar
  22. Ehrenfield JG (2006) A potential novel source of information for screening and monitoring the impact of exotic plants on ecosystems. Biol Invasions 8:1511–1521CrossRefGoogle Scholar
  23. Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243CrossRefGoogle Scholar
  24. Gribsholt B, Kristensen E (2002) Effects of bioturbation and plant roots on salt marsh biogeochemistry: a mesocosm study. Mar Ecol Prog Ser 241:71–87CrossRefGoogle Scholar
  25. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRefGoogle Scholar
  26. Holguin G, Vasquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fert Soils 33:265–278CrossRefGoogle Scholar
  27. Kay IS, Demopoulos AJ, Levin LA (2007) Halting an invasion surge of non-native mangroves in a Southern California tidal salt marsh while engaging the local community. Paper presented at the joint meeting of the Ecological Society of America, 92nd Annual Meeting and Society for Ecological Restoration, San Jose, CA, 10 August 2007Google Scholar
  28. Larned ST (2003) Effects of the invasive, nonindigenous seagrass Zostera japonica on nutrient fluxes between the water column and benthos in a NE Pacific estuary. Mar Ecol Prog Ser 254:69–80CrossRefGoogle Scholar
  29. Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87(2):419–432PubMedCrossRefGoogle Scholar
  30. Livingstone DC, Patriquin DG (1980) Nitrogenase activity in relation to season, carbohydrates and organic acids in a temperate zone root association. Soil Biol Biogeochem 12:543–546CrossRefGoogle Scholar
  31. Lovell CR (2002) Plant-microbe interactions in the marine environment. Encyclopedia Environ Microbiol 5:2539–2554Google Scholar
  32. McKane RB, Johnson LC, Shaver SR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71PubMedCrossRefGoogle Scholar
  33. Morton B (1974) Some aspects of the biology, population dynamics, and functional morphology of Musculista senhousia Benson (Bivalvia, Mytilidae). Pac Sci 28:19–33Google Scholar
  34. Reusch TBH, Williams S (1998) Variable response of native Zostera marina to a non-indigenous bivalve Musculista senhousia. Oecologia 113:428–441CrossRefGoogle Scholar
  35. Reusch TBH, Chapman ARO, Groger JP (1994) Blue mussels Mytilus edulis do not interfere with eelgrass Zostera marina but fertilize shoot growth through biodeposition. Mar Ecol Prog Ser 108:265–282CrossRefGoogle Scholar
  36. Sjoling S, Mohammed SM, Lyimo TJ, Kyaruzi JJ (2005) Benthic bacterial diversity and nutrient processes in mangroves: impact of deforestation. Estuar Coast Shelf Sci 63:397–406CrossRefGoogle Scholar
  37. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14(5):799–800CrossRefGoogle Scholar
  38. Steinquest S (2000) Salt cedar integrated weed management and the Endangered Species Act. In: Spencer N (ed) Proceedings of the X international symposium on biological control of weeds. Montana State University, Bozeman, Montana, USA, pp 407–504, 4–14 July 1999Google Scholar
  39. Strong JA, Dring MJ, Maggs CA (2006) Colonization and modification of soft substratum habitats by the invasive macroalga Sargassum muticum. Mar Ecol Prog Ser 321:87–97CrossRefGoogle Scholar
  40. Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80(5):1455–1474Google Scholar
  41. Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5(3):240–245PubMedCrossRefGoogle Scholar
  42. Tyler AC, Grosholz ED (2007) Spartina invasion changes intertidal ecosystem metabolism in San Francisco Bay. In: Proceedings of the third annual invasive spartina conference. Cambridge Inc, Cambridge, UK (in review)Google Scholar
  43. Valiela I, Teal JM (1974) Nutrient limitation in salt marsh vegetation. In: Reimold RJ, Queen WH (eds) Ecology of halophytes. Academic Press Inc, New York, pp 547–563Google Scholar
  44. Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Pollut Bull 55:323–332PubMedCrossRefGoogle Scholar
  45. Welsh DT (2000) Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions, and significance to primary productivity. Ecol Lett 3:58–71CrossRefGoogle Scholar
  46. Whitcraft CR (2007) Wetland plant influence on sediment ecosystem structure and trophic function. Dissertation, University of California, San DiegoGoogle Scholar
  47. Whitcraft CR, Talley DM, Crooks JA, Boland J, Gaskin J (2007) Invasion of tamarisk (Tamarisk spp.) in a southern California salt marsh. Biol Invasions 9:875–879CrossRefGoogle Scholar
  48. Whiting G, Gandy E, Yoch D (1986) Tight coupling of root-associated nitrogen fixation and plant photosynthesis in the salt marsh grass Spartina alterniflora and carbon dioxide enhancement of nitrogenase activity. Appl Environ Microbiol 52:108–113PubMedGoogle Scholar
  49. Zani S, Mellon MT, Collier JL, Zehr JP (2000) Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected with RT-PCR. Appl Environ Microbiol 66:3119–3124PubMedCrossRefGoogle Scholar
  50. Zedler JB, Nordby CS, Kus BE (1992) The ecology of Tijuana Estuary: A National Estuarine Research Reserve. NOAA Office of Coastal Resource Management, Sanctuaries and Reserves Division, Washington DCGoogle Scholar
  51. Zedler JB, Callaway JC, Sullivan G (2001) Declining biodiversity – why species matter and how their functions might be restored in Californian tidal marshes. Bioscience 51(12):1005–1017CrossRefGoogle Scholar
  52. Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 55(10):2522–2526PubMedGoogle Scholar
  53. Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW (1995) Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl Environ Microbiol 61(7):2527–2532PubMedGoogle Scholar
  54. Zehr JO, Montoya JP, Jenkens BD, Hewson I, Mondragon E, Short CM, Church MJ, Hansen A, Karl DM (2007). Experiments linking nitrogenase gene expression to nitrogen fixation in the North Pacific subtropical gyre. Limnol Oceanogr 52(1):169–183CrossRefGoogle Scholar
  55. Zhaoyong S, Zhang L, Feng G, Peter C, Changyan T, Xiaolin L (2006) Diversity of arbuscular mycorrhizal fungi associated with desert ephemerals growing under and beyond the canopies of Tamarisk shrubs. Chin Sci Bull 51:132–139CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Serena M. Moseman
    • 1
  • Rui Zhang
    • 2
    • 3
  • Pei Yuan Qian
    • 3
  • Lisa A. Levin
    • 1
  1. 1.Scripps Institution of OceanographyLa JollaUSA
  2. 2.National University of SingaporeSingaporeSingapore
  3. 3.Coastal Marine LaboratoryHong Kong University of Science and TechnologyKowloonHong Kong

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