Estuaries and Coasts

, Volume 42, Issue 1, pp 204–217 | Cite as

What Promotes the Recovery of Salt Marsh Infauna After Oil Spills?

  • J. W. Fleeger
  • M. R. Riggio
  • I. A. Mendelssohn
  • Q. Lin
  • D. R. Deis
  • D. S. Johnson
  • K. R. Carman
  • S. A. Graham
  • S. Zengel
  • A. Hou


Many factors influence the rate at which biotic communities recover from environmental disasters, and a thorough understanding of these factors is needed to formulate effective mitigation strategies. The importance of foundation species, soil environmental quality, and benthic microalgae to the long-term recovery of the salt marsh infaunal community following the 2010 Deepwater Horizon oil spill was examined in northern Barataria Bay, LA, from 2011 to 2016. The community of 12 abundant taxa of meiofauna and juvenile macroinfauna began to rebound from oiling in < 2 years, but did not fully recover after 6.5 years. The pace and intensity of recovery of nematodes, copepods, most polychaetes, tanaids, juvenile bivalves, and amphipods were significantly and positively related to the recovery of Spartina alterniflora and benthic microalgae. However, total petroleum hydrocarbon concentrations remained elevated over time, and live belowground plant biomass, bulk density, dead aboveground plant biomass, and live aboveground biomass of Juncus roemerianus were not resilient, indicating that soil quality at oiled sites was insufficient to foster the recovery of the infaunal community as a whole. Recovery of the kinorhynch Echinoderes coulli, the polychaete Manayunkia aestuarina, ostracods, and juvenile gastropods was suppressed in association with these factors. Foundation species enhance salt marsh infaunal recovery by modifying habitat in the short term and improving soil quality over the longer term. Therefore, efforts to enhance the recovery of foundation species (e.g., by plantings) should benefit the recovery of microalgal primary producers and benthic consumers after oiling in salt marshes.


Deepwater Horizon oil spill Resiliency Infauna Salt marsh Foundation species Benthic microalgae 



We thank Stefan Bourgoin for assistance with the creation of the sampling site map.

Funding Information

This research was made possible by a grant from The Gulf of Mexico Research Initiative.

Supplementary material

12237_2018_443_MOESM1_ESM.docx (382 kb)
ESM 1 (DOCX 382 kb)


  1. Anderson, M., R.N. Gorley, and R.K. Clarke. 2008. Permanova+ for primer: guide to software and statistical methods. Plymouth: Primer-E Limited 214 pp.Google Scholar
  2. Balthis, W.L., J.L. Hyland, C. Cooksey, P.A. Montagna, J.G. Baguley, R.W. Ricker, and C. Lewis. 2017. Sediment quality benchmarks for assessing oil-related impacts to the deep-sea benthos. Integrated Environmental Assessment and Management 13 (5): 840–851.CrossRefGoogle Scholar
  3. Bell, S.S. 1980. Meiofauna-macrofauna interactions in a high salt marsh habitat. Ecological Monographs 50 (4): 487–505.CrossRefGoogle Scholar
  4. Bonsdorff, E., A. Norkko, and E. Sandberg. 1995. Structuring zoobenthos: the importance of predation, siphon cropping and physical disturbance. Journal of Experimental Marine Biology and Ecology 192 (1): 125–144.CrossRefGoogle Scholar
  5. Brunner, C.A., K.M. Yeager, R. Hatch, S. Simpson, J. Keim, K.B. Briggs, and P. Louchouarn. 2013. Effects of oil from the 2010 Macondo well blowout on marsh foraminifera of Mississippi and Louisiana, USA. Environmental Science & Technology 47: 9115–9123.CrossRefGoogle Scholar
  6. Buffan-Dubau, E., and K.R. Carman. 2000. Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnology and Oceanography 45 (2): 381–395.CrossRefGoogle Scholar
  7. Carman, K.R., J.W. Fleeger, and S. Pomarico. 1997. Response of a benthic food web to hydrocarbon contamination. Limnology and Oceanography 42 (3): 561–571.CrossRefGoogle Scholar
  8. Carman, K.R., J.W. Fleeger, and S. Pomarico. 2000. Does historical exposure to hydrocarbon contamination alter the response of benthic communities to diesel contamination? Marine Environmental Research 49 (3): 255–278.CrossRefGoogle Scholar
  9. Clarke, K.R., and R.N. Gorley. 2006. PRIMER v6: User manual/tutorial. Plymouth: PRIMER-E 192 pp.Google Scholar
  10. Craft, C., and J. Sacco. 2003. Long-term succession of benthic infauna communities on constructed Spartina alterniflora marshes. Marine Ecology-Progress Series 257: 45–58.CrossRefGoogle Scholar
  11. Craft, C., J. Reader, J.N. Sacco, and S.W. Broome. 1999. Twenty-five years of ecosystem development of constructed Spartina alterniflora (Loisel) marshes. Ecological Applications 9 (4): 1405–1419.CrossRefGoogle Scholar
  12. Craft, C., P. Megonigal, S. Broome, J. Stevenson, R. Freese, J. Cornell, L. Zheng, and J. Sacco. 2003. The pace of ecosystem development of constructed Spartina alterniflora marshes. Ecological Applications 13 (5): 1417–1432.CrossRefGoogle Scholar
  13. Culbertson, J.B., I. Valiela, E.E. Peacock, C.M. Reddy, A. Carter, and R. van der Kruik. 2007. Long-term biological effects of petroleum residues on fiddler crabs in salt marshes. Marine Pollution Bulletin 54 (7): 955–962.CrossRefGoogle Scholar
  14. Culbertson, J.B., I. Valiela, M. Pickart, E.E. Peacock, and C.M. Reddy. 2008. Long-term consequences of residual petroleum on salt marsh grass. Journal of Applied Ecology 45 (4): 1284–1292.CrossRefGoogle Scholar
  15. Deegan, L.A., D.S. Johnson, R.S. Warren, B.J. Peterson, J.W. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490 (7420): 388–394.CrossRefGoogle Scholar
  16. Deepwater Horizon Trustees. 2016. Deepwater Horizon oil spill final programmatic damage assessment and restoration plan and final programmatic environmental impact statement.
  17. Deis, D.R., J.W. Fleeger, S.M. Bourgoin, I.A. Mendelssohn, Q. Lin, and A. Hou. 2017. Shoreline oiling effects and recovery of saltmarsh macroinvertebrates after the Deepwater Horizon oil spill. PeerJ 5: e3680. Scholar
  18. DeLaune, R.D., C.J. Smith, W.H. Patrick Jr., J.W. Fleeger, and M.D. Tolley. 1984. Effect of oil on salt marsh biota: methods for restoration. Environmental Pollution 36: 207–227.CrossRefGoogle Scholar
  19. Duan, J., W. Liu, X. Zhao, Y. Han, S.E. O’Reilly, and D. Zhao. 2017. Study of residual oil in bay Jimmy sediment 5 years after the Deepwater Horizon oil spill: Persistence of sediment retained oil hydrocarbons and effect of dispersants on desorption. Science of the Total Environment 618: 1244–1253. Scholar
  20. Fertig, B., M.J. Kennish, G.P. Sakowicz, and L.K. Reynolds. 2014. Mind the data gap: identifying and assessing drivers of changing eutrophication condition. Estuaries and Coasts 37: S198–S221.CrossRefGoogle Scholar
  21. Fleeger, J.W., K.R. Carman, and R.M. Nisbet. 2003. Indirect effects of contaminants on aquatic ecosystems. Science of the Total Environment 317 (1-3): 207–233.CrossRefGoogle Scholar
  22. Fleeger, J.W., K.R. Carman, M.R. Riggio, I.A. Mendelssohn, Q. Lin, A. Hou, D.R. Deis, and S. Zengel. 2015. Recovery of saltmarsh benthic microalgae and meiofauna following the Deepwater Horizon oil spill linked to recovery of Spartina alterniflora. Marine Ecology-Progress Series 536: 39–54.CrossRefGoogle Scholar
  23. Fleeger, J.W., M.R. Riggio, I.A. Mendelssohn, Q. Lin, A. Hou, and D.R. Deis. 2018. Recovery of saltmarsh meiofauna six years after the Deepwater Horizon oil spill. Journal of Experimental Marine Biology and Ecology 502: 182–190.CrossRefGoogle Scholar
  24. Fry, B., D.M. Baltz, M.C. Benfield, J.W. Fleeger, A. Grace, H.L. Haas, and Z.J. Quiñones-Rivera. 2003. Chemical indicators of movement and residency for brown shrimp (Farfantepenaeus aztecus) in coastal Louisiana marshscapes. Estuaries 26 (1): 82–97.CrossRefGoogle Scholar
  25. Galván, K.A., J.W. Fleeger, and B. Fry. 2008. Stable isotope addition reveals dietary importance of phytoplankton and benthic microalgae to saltmarsh infauna. Marine Ecology-Progress Series 359: 37–49.CrossRefGoogle Scholar
  26. Galván, K.A., J.W. Fleeger, B.J. Peterson, D.C. Drake, L.A. Deegan, and D.S. Johnson. 2011. Natural abundance stable isotopes and dual isotope tracer additions help to resolve resources supporting a saltmarsh food web. Journal of Experimental Marine Biology and Ecology 410: 1–11.CrossRefGoogle Scholar
  27. Gesteira, J.L.G., and J.C. Dauvin. 2000. Amphipods are good bioindicators of the impact of oil spills on soft-bottom macrobenthic communities. Marine Pollution Bulletin 40 (11): 1017–1027.CrossRefGoogle Scholar
  28. Giere, O., 2009. Meiobenthology. The microscopic motile fauna of aquatic sediments. 2nd edition. Springer-Verlag, Berlin. 527 pp.Google Scholar
  29. Graham, S.A., and I.A. Mendelssohn. 2016. Contrasting effects of nutrient enrichment on below-ground biomass in coastal wetlands. Journal of Ecology 104 (1): 249–260.CrossRefGoogle Scholar
  30. Hentschel, B.T., N.T. Hayman, and T.W. Anderson. 2017. Hydrodynamic mediation of killifish predation on infaunal polychaetes. Limnology and Oceanography doi 63 (S1): S19–S29. Scholar
  31. Hester, M.W., J.M. Willis, S. Rouhani, M.A. Steinhoff, and M.C. Baker. 2016. Impacts of the Deepwater Horizon oil spill on the salt marsh vegetation of Louisiana. Environmental Pollution 216: 361–370.CrossRefGoogle Scholar
  32. Higgins, R.P., and J.W. Fleeger. 1980. Seasonal changes in the population structure of Echinoderes coulli (Kinorhyncha). Estuarine Coastal Marine Science 10 (5): 495–505.CrossRefGoogle Scholar
  33. Hooper, D.U., F.S. Chapin, J.J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J.H. Lawton, D.M. Lodge, M. Loreau, S. Naeem, and B. Schmid. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75 (1): 3–35.CrossRefGoogle Scholar
  34. Husseneder, C., J.R. Donaldson, and L.D. Foil. 2016. Impact of the 2010 Deepwater Horizon oil spill on population size and genetic structure of horse flies in Louisiana marshes. Scientific Reports 6.Google Scholar
  35. Johnson, D.S., J.W. Fleeger, K.A. Galván, and E.B. Moser. 2007. Worm holes and their space-time continuum: Spatial and temporal variability of macroinfaunal annelids in a northern New England salt marsh. Estuaries and Coasts 30 (2): 226–237.CrossRefGoogle Scholar
  36. Johnson, D.S., J.W. Fleeger, M.R. Riggio, I.A. Mendelssohn, Q. Lin, S.A. Graham, D.R. Deis, and A. Hou. 2018. Saltmarsh plants, but not fertilizer, facilitate benthic invertebrate recolonization after an oil spill. Ecosphere 9 (1): e02082.CrossRefGoogle Scholar
  37. Kovach, R.P., C.C. Muhlfeld, R. Al-Chokhachy, J.B. Dunham, B.H. Letcher, and J.L. Kershner. 2016. Impacts of climatic variation on trout: a global synthesis and path forward. Reviews in Fish Biology and Fisheries 26 (2): 135–151.CrossRefGoogle Scholar
  38. Levin, L.A., and T.S. Talley. 2002. Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecological Applications 12 (6): 1785–1802.CrossRefGoogle Scholar
  39. Levine, B.M., J.R. White, R.D. DeLaune, and K. Maiti. 2017. Crude oil effects on redox status of salt marsh soil in Louisiana. Soil Science Society of America Journal 81 (3): 647–653.CrossRefGoogle Scholar
  40. Lin, Q.X., and I.A. Mendelssohn. 2012. Impacts and recovery of the Deepwater Horizon oil spill on vegetation structure and function of coastal salt marshes in the northern Gulf of Mexico. Environmental Science & Technology 46 (7): 3737–3743.CrossRefGoogle Scholar
  41. Lin, Q., I.A. Mendelssohn, S. Graham, A. Hou, J.W. Fleeger, and D.R. Deis. 2016. Response of salt marshes to oiling from the Deepwater Horizon spill: implications for plant growth, soil surface-erosion, and shoreline stability. Science of the Total Environment 557–558: 369–377.CrossRefGoogle Scholar
  42. McCall, B.D., and S.C. Pennings. 2012. Disturbance and recovery of salt marsh arthropod communities following BP Deepwater Horizon oil spill. PLoS One 7 (3): e32735. Scholar
  43. McCann, M.J., K.W. Able, R.R. Christian, F.J. Fodrie, O.P. Jensen, J.J. Johnson, P.C. Lopez-Duarte, C.W. Martin, J.A. Olin, M.J. Polito, B.J. Roberts, and S.L. Ziegler. 2017. Key taxa in food web responses to stressors: the Deepwater Horizon oil spill. Frontiers in Ecology and the Environment 15 (3): 142–149.CrossRefGoogle Scholar
  44. McGlathery, K.J., L.K. Reynolds, L.W. Cole, R.J. Orth, S.R. Marion, and A. Schwarzschild. 2012. Recovery trajectories during state change from bare sediment to eelgrass dominance. Marine Ecology-Progress Series 448: 209–221.CrossRefGoogle Scholar
  45. Mendelssohn, I.A., I.C. Anderson, D.M. Baltz, R. Caffey, K.R. Carman, J.W. Fleeger, S.B. Joye, Q. Lin, E. Maltby, E.B. Overton, and L. Rozas. 2012. Oil impacts to coastal wetlands: implications for the Mississippi River Delta ecosystem after the Deepwater Horizon oil spill. Bioscience 62 (6): 562–574.CrossRefGoogle Scholar
  46. Michel, J., and N. Rutherford. 2014. Impacts, recovery rates, and treatment options for spilled oil in marshes. Marine Pollution Bulletin 82 (1-2): 19–25.CrossRefGoogle Scholar
  47. Mills, C.G., and K.S. McNeal. 2014. Salt marsh sediment biogeochemical response to the BP Deepwater Horizon blowout. Journal of Environmental Quality 43 (5): 1813–1819.CrossRefGoogle Scholar
  48. Nixon, Z., S. Zengel, M. Baker, M. Steinhoff, G. Fricano, S. Rouhani, and J. Michel. 2016. Shoreline oiling from the Deepwater Horizon oil spill. Marine Pollution Bulletin 107 (1): 170–178.CrossRefGoogle Scholar
  49. Nordstrom, M.C., A.W. Demopoulos, C.R. Whitcraft, A. Rismondo, P. McMillan, J.P. Gonzalez, and L.A. Levin. 2015. Food web heterogeneity and succession in created saltmarshes. Journal of Applied Ecology 52: 1343–1354.CrossRefGoogle Scholar
  50. Okoro, D., P. Oviasogie, and F. Oviasogie. 2011. Soil quality assessment 33 months after crude oil spillage and clean-up. Chemical Speciation and Bioavailability 23 (1): 1–6.CrossRefGoogle Scholar
  51. Pascal, P.-Y., J.W. Fleeger, H.T.S. Boschker, H.M. Mitwally, and D.S. Johnson. 2013. Response of the benthic food web to short- and long-term nutrient enrichment in saltmarsh mudflats. Marine Ecology-Progress Series 474: 27–41.CrossRefGoogle Scholar
  52. Pennings, S.C., B.D. McCall, and L. Hooper-Bui. 2014. Effects of oil spills on terrestrial arthropods in coastal wetlands. Bioscience 64 (9): 789–795.CrossRefGoogle Scholar
  53. Pennings, S.C., S. Zengel, J. Oehrig, M. Alber, T.D. Bishop, D.R. Deis, D. Devlin, A.R. Hughes, J.J. Hutchens, W.M. Kiehn, C.R. McFarlin, C.L. Montague, S. Powers, C.E. Proffitt, N. Rutherford, C.L. Stagg, and K. Walters. 2016. Marine ecoregion and Deepwater Horizon oil spill affect recruitment and population structure of a salt marsh snail. Ecosphere 7 (12): e01588.CrossRefGoogle Scholar
  54. Peterson, C.H., S.D. Rice, J.W. Short, D. Esler, J.L. Bodkin, B.E. Ballachey, and D.B. Irons. 2003. Long-term ecosystem response to the Exxon Valdez oil spill. Science 302 (5653): 2082–2086.CrossRefGoogle Scholar
  55. Rabalais, N.N., and R.E. Turner. 2016. Effects of the Deepwater Horizon oil spill on coastal marshes and associated organisms. Oceanography 29 (3): 150–159.CrossRefGoogle Scholar
  56. Schratzberger, M., and J. Ingels. 2017. Meiofauna matters: the roles of meiofauna in benthic ecosystems. Journal of Experimental Marine Biology and Ecology 502: 12–25. Scholar
  57. Silliman, B.R., J. van de Koppel, M.W. McCoy, J. Diller, G.N. Kasozi, K. Earl, P.N. Adams, and A.R. Zimmerman. 2012. Degradation and resilience in Louisiana salt marshes after the BP-Deepwater Horizon oil spill. Proceedings of the National Academy of Sciences of the United States of America 109 (28): 11234–11239.CrossRefGoogle Scholar
  58. Thomas, Z., and K.M. Waring. 2015. Enhancing resiliency and restoring ecological attributes in second-growth Ponderosa pine stands in northern New Mexico, USA. Forest Science 61 (1): 93–104.CrossRefGoogle Scholar
  59. Thorne, R.E., and G.L. Thomas. 2008. Herring and the “Exxon Valdez” oil spill: an investigation into historical data conflicts. ICES Journal of Marine Science 65: 44–50.CrossRefGoogle Scholar
  60. Trujillo-Narcia, A., M. del Carmen Rivera-Cruz, L. del Carmen Lagunes-Espinoza, D. Jesus Palma-Lopez, S. Soto-Sanchez, and G. Ramirez-Valverde. 2012. Effects of restoration of riverine sediments contaminated with crude-oil. Revista Internacional de Contaminacion Ambiental 28: 361–374.Google Scholar
  61. U.S. District Court. 2015. Oil spill by the oil rig “Deepwater Horizon” in the Gulf of Mexico, on April 20, 2010, findings of fact and conclusions of law: phase two trial. New Orleans: United States District court for the Eastern District of Louisiana. Available at files/ OilSpill/ orders/1152015FindingsPhaseTwo.pdf. Accessed on 3 March 2016.
  62. van der Zee, E.M., C. Angelini, L.L. Govers, M.J.A. Christianen, A.H. Altieri, K.J. van der Reijden, B.R. Silliman, J.V. De Koppel, M. van der Geest, J.A. van Gils, H.W. van der Veer, T. Piersma, P.C. de Ruiter, H. Olff, and T. van der Heide. 2016. How habitat-modifying organisms structure the food web of two coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences 283: 20152326. Scholar
  63. Wagg, C., S.F. Bender, F. Widmer, and M.G.A. van der Heijden. 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America 111: 5266–5270.CrossRefGoogle Scholar
  64. Warren, R.S., P.E. Fell, R. Rozsa, A.H. Brawley, A.C. Orsted, E.T. Olson, V. Swamy, and W.A. Niering. 2002. Salt marsh restoration in Connecticut: 20 years of science and management. Restoration Ecology 10 (3): 497–513.CrossRefGoogle Scholar
  65. Whanpetch, N., M. Nakaoka, H. Mukai, T. Suzuki, S. Nojima, T. Kawai, and C. Aryuthaka. 2010. Temporal changes in benthic communities of seagrass beds impacted by a tsunami in the Andaman Sea, Thailand. Estuarine Coastal and Shelf Science 87 (2): 246–252.CrossRefGoogle Scholar
  66. Whipple, S.A., J.W. Fleeger, and L.L. Cook. 1981. The influence of tidal flushing, light exposure and natant macrofauna on edaphic chlorophyll a in a Louisiana salt marsh. Estuarine, Coastal and Shelf Science 13 (6): 637–643.CrossRefGoogle Scholar
  67. Whitcraft, C.R., and L.A. Levin. 2007. Regulation of benthic algal and animal communities by salt marsh plants: Impact of shading. Ecology 88 (4): 904–917.CrossRefGoogle Scholar
  68. Zengel, S., B.M. Bernik, N. Rutherford, Z. Nixon, and J. Michel. 2015. Heavily oiled salt marsh following the Deepwater Horizon oil spill, ecological comparisons of shoreline cleanup treatments and recovery. Plos One.
  69. Zengel, S., C.L. Montague, S.C. Pennings, S.P. Powers, M. Steinhoff, G. Fricano, C. Schlemme, M.N. Zhang, J. Oehrig, Z. Nixon, S. Rouhani, and J. Michel. 2016a. Impacts of the Deepwater Horizon oil spill on salt marsh periwinkles (Littoraria irrorata). Environmental Science & Technology 50 (2): 643–652.CrossRefGoogle Scholar
  70. Zengel, S., S.C. Pennings, B. Silliman, C. Montague, J. Weaver, D.R. Deis, M.O. Krasnec, N. Rutherford, and Z. Nixon. 2016b. Deepwater Horizon oil spill impacts on salt marsh fiddler crabs (Uca spp.). Estuaries and Coasts 39 (4): 1154–1163.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2018

Authors and Affiliations

  • J. W. Fleeger
    • 1
  • M. R. Riggio
    • 1
  • I. A. Mendelssohn
    • 2
  • Q. Lin
    • 2
  • D. R. Deis
    • 3
  • D. S. Johnson
    • 4
  • K. R. Carman
    • 5
  • S. A. Graham
    • 6
  • S. Zengel
    • 7
  • A. Hou
    • 8
  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  2. 2.Department of Oceanography and Coastal SciencesLouisiana State UniversityBaton RougeUSA
  3. 3.AtkinsJacksonvilleUSA
  4. 4.Department of Biological Sciences, Virginia Institute of Marine ScienceCollege of William & MaryGloucester PointUSA
  5. 5.Department of BiologyUniversity of Nevada-RenoRenoUSA
  6. 6.Department of Biological SciencesNicholls State UniversityThibodauxUSA
  7. 7.Research Planning, Inc. (RPI)TallahasseeUSA
  8. 8.Department of Environmental SciencesLouisiana State UniversityBaton RougeUSA

Personalised recommendations