Oecologia

, Volume 170, Issue 3, pp 789–798 | Cite as

Post-mortem ecosystem engineering by oysters creates habitat for a rare marsh plant

Community ecology - Original research

Abstract

Oysters are ecosystem engineers in marine ecosystems, but the functions of oyster shell deposits in intertidal salt marshes are not well understood. The annual plant Suaeda linearis is associated with oyster shell deposits in Georgia salt marshes. We hypothesized that oyster shell deposits promoted the distribution of Suaedalinearis by engineering soil conditions unfavorable to dominant salt marsh plants of the region (the shrub Borrichia frutescens, the rush Juncus roemerianus, and the grass Spartina alterniflora). We tested this hypothesis using common garden pot experiments and field transplant experiments. Suaedalinearis thrived in Borrichiafrutescens stands in the absence of neighbors, but was suppressed by Borrichiafrutescens in the with-neighbor treatment, suggesting that Suaedalinearis was excluded from Borrichiafrutescens stands by interspecific competition. Suaedalinearis plants all died in Juncusroemerianus and Spartinaalterniflora stands, regardless of neighbor treatments, indicating that Suaedalinearis is excluded from these habitats by physical stress (likely water-logging). In contrast, Borrichia frutescens, Juncusroemerianus, and Spartinaalterniflora all performed poorly in Suaedalinearis stands regardless of neighbor treatments, probably due to physical stresses such as low soil water content and low organic matter content. Thus, oyster shell deposits play an important ecosystem engineering role in influencing salt marsh plant communities by providing a unique niche for Suaeda linearis, which otherwise would be rare or absent in salt marshes in the southeastern US. Since the success of Suaedalinearis is linked to the success of oysters, efforts to protect and restore oyster reefs may also benefit salt marsh plant communities.

Keywords

Oyster shell Suaeda linearis Microhabitat Competition Salt marsh 

References

  1. Adam P (1990) Saltmarsh ecology. Cambridge University Press, New YorkCrossRefGoogle Scholar
  2. Anderson WD, Keith WJ, Tuten WR, Mills FH (1979) A survey of South Carolina’s washed shell recource. South Carolina Wildlife and Marine Resources Department, Technical Report No. 36. Charleston, SC, USAGoogle Scholar
  3. Andrews JD, Frierman M (1974) Epizootiology of Minchinia nelsoni in susceptible wild oysters in Virginia, 1959 to 1971. J Invertebr Pathol 24:127–140PubMedCrossRefGoogle Scholar
  4. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686CrossRefGoogle Scholar
  5. Auster PJ, Malatesta RJ, LaRosa SC, Cooper RA, Stewart LL (1991) Microhabitat utilization by the megafaunal assemblage at a low relief outer continental shelf site-Middle Atlantic Bight, USA. J Northwest Atl Fish Sci 11:59–69CrossRefGoogle Scholar
  6. Bahr LM, Lanier WP (1981) The ecology of intertidal oyster reefs of the South Atlantic Coast: a community profile. FWS/OBS-81/15. United States Fish and Wildlife Service, Washington, DC, USAGoogle Scholar
  7. Bakker JP, de Vries Y (1992) Germination and early establishment of lower salt-marsh species in grazed and mown salt marsh. J Veg Sci 3:247–252CrossRefGoogle Scholar
  8. Banks P et al (2007) Status review of the eastern oyster (Crassostrea virginica). Report to the National Marine Fisheries Service, Northeast Regional Office, Gloucester, MA, USAGoogle Scholar
  9. Bertness MD, Ellison AM (1987) Determinants of pattern in a New England salt marsh plant community. Ecol Monogr 57:129–147CrossRefGoogle Scholar
  10. Bertness MD, Gough L, Shumway SW (1992) Salt tolerances and the distribution of fugitive salt marsh plants. Ecology 73:1842–1851CrossRefGoogle Scholar
  11. Bigelow SW, Canham CD (2002) Community organization of tree species along soil gradients in a north-eastern USA forest. J Ecol 90:188–200CrossRefGoogle Scholar
  12. Brewer JS, Grace JB (1990) Plant community structure in an oligohaline tidal marsh. Vegetatio 90:93–107CrossRefGoogle Scholar
  13. Brewer JS, Levine JM, Bertness MD (1998) Interactive effects of elevation and burial with wrack on plant community structure in some Rhode Island salt marshes. J Ecol 86:125–136CrossRefGoogle Scholar
  14. Bruno JF (2000) Facilitation of cobble beach plant communities through habitat modification by Spartina alterniflora. Ecology 81:1179–1192Google Scholar
  15. Bruno JF (2002) Causes of landscape-scale rarity in cobble beach plant communities. Ecology 83:2304–2314CrossRefGoogle Scholar
  16. Carlsson R, Haeggstrom CA, Kraufvelin P (2008) The vascular plant flora of shell gravel deposits on the Aland Islands, SW Finland—community structure in relation to calcium. Boreal Environ Res 13:45–65Google Scholar
  17. Chapman VJ (1974) Salt marshes and salt deserts of the world. In: Reimold RJ, Queen WH (eds) Ecology of halophytes. Academic, New York, pp 3–19Google Scholar
  18. Coen L, Grizzle R (2007) The importance of habitat created by molluscan shellfish to managed species along the Atlantic Coast of the United States. In: Thomas J, Nygard J (eds) Atlantic states marine fisheries commission habitat management series No. 8. Atlantic States Marine Fisheries Commission, Washington, DC, USA, pp 1–108Google Scholar
  19. Coen LD, Luckenbach MW, Breitburg DL (1999) The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives. Am Fish Soc Symp 22:438–454Google Scholar
  20. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310PubMedCrossRefGoogle Scholar
  21. Cook T, Folli M, Klinck J, Ford S, Miller J (1998) The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar Coast Shelf Sci 46:587–597CrossRefGoogle Scholar
  22. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  23. Cuddington K, Hastings A (2004) Invasive engineers. Ecol Model 178:335–347CrossRefGoogle Scholar
  24. de Souza JP, Araujo GM, Haridasan M (2007) Influence of soil fertility on the distribution of tree species in a deciduous forest in the Triangulo Mineiro region of Brazil. Plant Ecol 191:253–263CrossRefGoogle Scholar
  25. Dittel A, Epifanio CE, Natunewicz C (1996) Predation on mud crab megalopae, Panopeus herbstii H. Milne Edwards: effect of habitat complexity, predator species and postlarval densities. J Exp Mar Biol Ecol 198:191–202CrossRefGoogle Scholar
  26. Drake BG (1989) Photosynthesis of salt marsh species. Aquat Bot 34:167–180CrossRefGoogle Scholar
  27. Ellison AM (1987) Effects of competition, disturbance, and herbivory on Salicornia europaea. Ecology 68:576–586CrossRefGoogle Scholar
  28. Etherington JR (1981) Limestone heaths in south-west Britain: their soils and the maintenance of their calcicole–calcifuge mixtures. J Ecol 69:277–294CrossRefGoogle Scholar
  29. Gough L, Grace JB (1998) Herbivore effects on plant species density at varying productivity levels. Ecology 79:1586–1594CrossRefGoogle Scholar
  30. Grabowski JH, Peterson CH (2007) Restoring oyster reefs to recover ecosystem services. In: Cuddington K, Byers JE, Wilson WG, Hastings A (eds) Theoretical ecology series, vol 4. Academic, Waltham, pp 281–298Google Scholar
  31. Gutiérrez J, Iribarne O (1999) Role of Holocene beds of the stout razor clam Tagelus plebeius in structuring present benthic communities. Mar Ecol Prog Ser 185:213–228CrossRefGoogle Scholar
  32. Gutiérrez 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
  33. Harding JM, Mann R (2001) Oyster reefs as fish habitat: opportunistic use of restored reefs by transient fishes. J Shellfish Res 20:951–959Google Scholar
  34. Hargis WJ Jr, Haven DS (1999) Chesapeake oyster reefs, their importance, destruction, and guidelines for restoring them. In: Luckenbach MW, Mann R, Wesson JA (eds) Oyster reef habitat restoration: a synopsis, and a synthesis of approaches. Virginia Institute of Marine Science, Gloucester Point, pp 329–358Google Scholar
  35. Hastings A et al (2007) Ecosystem engineering in space and time. Ecol Lett 10:153–164PubMedCrossRefGoogle Scholar
  36. He Q, Cui BS, Cai YZ, Deng JF, Sun T, Yang ZF (2009) What confines an annual plant to two separate zones along coastal topographic gradients? Hydrobiologia 630:327–340CrossRefGoogle Scholar
  37. Hessini K, Ghandour M, Albouchi A, Soltani A, Werner K, Abdelly C (2008) Biomass production, photosynthesis, and leaf water relations of Spartina alterniflora under moderate water stress. J Plant Res 121:311–318PubMedCrossRefGoogle Scholar
  38. Hik DS, Jefferies RL, Sinclair ARE (1992) Foraging by geese, isostatic uplift and asymmetry in the development of salt marsh plant communities. J Ecol 80:395–406CrossRefGoogle Scholar
  39. Huston MA (1994) Biological diversity. The coexistence of species on changing landscapes. Cambridge University Press, CambridgeGoogle Scholar
  40. Ingold A, Havill DC (1984) The influence of sulphide on the distribution of higher plants in salt marshes. J Ecol 72:1043–1054CrossRefGoogle Scholar
  41. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  42. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  43. Jones CG, Gutierrez JL, Byers JE, Crooks JA, Lambrinos JG, Talley TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119:1862–1869CrossRefGoogle Scholar
  44. Krantz GE, Jordan SJ (1996) Management alternatives for protecting Crassostrea virginica fisheries in Perkinsus marinus enzootic and epizootic areas. J Shellfish Res 15:167–176Google Scholar
  45. Larsen PF (1985) The benthic macrofauna associated with the oyster reefs of the James River Estuary, Virginia, USA. Int Rev Gesamten Hydrobiol Hydrogr 70:797–814CrossRefGoogle Scholar
  46. Lee CH, Lee DK, Ali MA, Kim PJ (2008) Effects of oyster shell on soil chemical and biological properties and cabbage productivity as a liming materials. Waste Manag 28:2702–2708PubMedCrossRefGoogle Scholar
  47. Lehnert R, Allen D (2002) Nekton use of subtidal oyster shell habitat in a southeastern US estuary. Estuaries 25:1015–1024CrossRefGoogle Scholar
  48. Lenihan HS (1999) Physical–biological coupling on oyster reefs: how habitat structure influences individual performance. Ecol Monogr 69:251–275Google Scholar
  49. Linthurst RA, Seneca ED (1981) Aeration, nitrogen and salinity as determinants of Spartina alterniflora Loisel. growth response. Estuaries 4:53–63CrossRefGoogle Scholar
  50. MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598CrossRefGoogle Scholar
  51. McDonald J (1982) Divergent life history patterns in the co-occurring intertidal crabs Panopeus herbstii and Eurypanopeus depressus (Crustacea: Brachyura: Xanthidae). Mar Ecol Prog Ser 8:173–180CrossRefGoogle Scholar
  52. Meade RH (1982) Sources, sinks, and storage of river sediment in the Atlantic drainage of the United States. J Geol 90:235–252CrossRefGoogle Scholar
  53. Meyer DL (1994) Habitat partitioning between the xanthid crabs Panopeus herbstii and Eurypanopeus depressus on intertidal oyster reefs (Crassostrea virginica) in Southeastern North Carolina. Estuaries 17:674–679CrossRefGoogle Scholar
  54. Meyer DL, Townsend EC, Thayer GW (1997) Stabilization and erosion control value of oyster cultch for intertidal marsh. Restor Ecol 5:93–99CrossRefGoogle Scholar
  55. Milliman J, Pilkey O, Ross D (1972) Sediments of the continental margin off the eastern United States. Geol Soc Am Bull 83:1315–1334CrossRefGoogle Scholar
  56. NCDENR (2001) North Carolina oyster fishery management plan. North Carolina Department of Environment and Natural Resources, North Carolina Division of Marine Fisheries, Morehead City, NC, USAGoogle Scholar
  57. Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 289–316Google Scholar
  58. Pennings SC, Callaway RM (1996) Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation. Ecology 77:1410–1419CrossRefGoogle Scholar
  59. Pennings SC, Moore DJ (2001) Zonation of shrubs in western Atlantic salt marshes. Oecologia 126:587–594CrossRefGoogle Scholar
  60. Pennings SC, Richards CL (1998) Effects of wrack burial in salt-stressed habitats: Batis maritima in a southwest Atlantic salt marsh. Ecography 21:630–638CrossRefGoogle Scholar
  61. Pennings SC, Grant MB, Bertness MD (2005) Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J Ecol 93:159–167CrossRefGoogle Scholar
  62. Pezeshki SR (1997) Photosynthesis and root growth in Spartina alterniflora in relation to root zone aeration. Photosynthetica 34:107–114CrossRefGoogle Scholar
  63. Powell EN, Klinck JM (2007) Is oyster shell a sustainable estuarine resource? J Shellfish Res 26:181–194CrossRefGoogle Scholar
  64. Powell EN, Ashton-Alcox KA, Kraeuter JN, Ford SE, Bushek D (2008) Long-term trends in oyster population dynamics in Delaware Bay: Regime shifts and response to disease. J Shellfish Res 27:729–755CrossRefGoogle Scholar
  65. R Development Core Team (2010) R: A language and environment for statistical computing. Version 2.12.0. Vienna, AustriaGoogle Scholar
  66. Rothschild BJ, Ault JS, Goulletquer P, Heral M (1994) Decline of the Chesapeake Bay oyster populations: a century of habitat destruction and overfishing. Mar Ecol Prog Ser 111:29–39CrossRefGoogle Scholar
  67. Saunders R (2002) The Fig Island Ring Complex (38CH42): coastal adaptation and the question of ring function in the Late Archaic. Report prepared for the South Carolina Department of Archives and History, Columbia, SC, USAGoogle Scholar
  68. Szedlmayer ST, Howe JC (1997) Substrate preference in age-0 red snapper, Lutjanus campechanus. Environ Biol Fishes 50:203–207CrossRefGoogle Scholar
  69. Tessier M, Gloaguen JC, Lefeuvre JC (2000) Factors affecting the population dynamics of Suaeda maritima at initial stages of development. Plant Ecol 147:193–203CrossRefGoogle Scholar
  70. Tessier M, Gloaguen JC, Bouchard V (2002) The role of spatio-temporal heterogeneity in the establishment and maintenance of Suaeda maritima in salt marshes. J Veg Sci 13:115–122Google Scholar
  71. Thibodeau PM, Gardner LR, Reeves HW (1998) The role of groundwater flow in controlling the spatial distribution of soil salinity and rooted macrophytes in a southeastern salt marsh, USA. Mangroves Salt Marshes 2:1–13CrossRefGoogle Scholar
  72. Thompson V, Worth J (2011) Dwellers by the sea: native American adaptations along the southern coasts of eastern North America. J Archaeol Res19 (1):51–101Google Scholar
  73. Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJ, USAGoogle Scholar
  74. USDA (2004) Soil survey laboratory methods manual. Version 4. United States Department of Agriculture, Natural Resources Conservation Service. Washington, DC, USAGoogle Scholar
  75. van de Koppel J, Altieri AH, Silliman BR, Bruno JF, Bertness MD (2006) Scale-dependent interactions and community structure on cobble beaches. Ecol Lett 9:45–50PubMedGoogle Scholar
  76. van Wesenbeeck BK, Crain CM, Altieri AH, Bertness MD (2007) Distinct habitat types arise along a continuous hydrodynamic stress gradient due to interplay of competition and facilitation. Mar Ecol Prog Ser 349:63–71CrossRefGoogle Scholar
  77. Varty AK, Zedler JB (2008) How waterlogged microsites help an annual plant persist among salt marsh perennials. Estuaries Coasts 31:300–312CrossRefGoogle Scholar
  78. Vivian-Smith G (1997) Microtopographic heterogeneity and floristic diversity in experimental wetland communities. J Ecol 85:71–82CrossRefGoogle Scholar
  79. Walker DA, Bockheim JG, Chapin FS, Eugster W, Nelson FE, Ping CL (2001) Calcium-rich tundra, wildlife, and the “Mammoth Steppe”. Quat Sci Rev 20:149–163CrossRefGoogle Scholar
  80. Watkinson AR, Davy AJ (1985) Population biology of salt marsh and sand dune annuals. Plant Ecol 62:487–497CrossRefGoogle Scholar
  81. Whitaker JD et al (2004) An ecological characterization of coastal hammock islands in South Carolina. Ocean and Coastal Resources Management, South Carolina Department of Health and Environmental Control. Charleston, SC, USAGoogle Scholar
  82. Wiegert RG, Freeman BJ (1990) Tidal salt marshes of the southeast Atlantic coast: A community profile. US Fish and Wildlife Service Biological Report 85:1–80Google Scholar
  83. Woods H, Hargis WJ, Hershner CH, Mason P (2005) Disappearance of the natural emergent 3-dimensional oyster reef system of the James River, Virginia, 1871–1948. J Shellfish Res 24:139–142Google Scholar
  84. Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. Bioscience 56:203–209CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Biology and BiochemistryUniversity of HoustonHoustonUSA

Personalised recommendations