Restoration Affects Sexual Reproductive Capacity in a Salt Marsh

  • Scott F. JonesEmail author
  • Erik S. Yando
  • Camille L. Stagg
  • Courtney T. Hall
  • Mark W. Hester


Plant sexual reproduction is an important driver of plant community maintenance, dispersal, and recovery from disturbance. Despite this, sexual reproduction in habitats dominated by clonally spreading perennial species, such as salt marshes, is often ignored. Communities dominated by long-lived perennial species can still depend on sexual reproduction for recolonizing large disturbed patches or for establishing in new patches, such as restored sites. We investigated the influence of restoration and elevation on flowering phenology, potential seed and seedling production, and insect flower damage of the dominant salt marsh grass, Spartina alterniflora, in reference and restored marshes in southeastern Louisiana, USA. We additionally tested whether elevation gradients or soil parameters could explain differences in sexual reproduction between sites. We demonstrate that sediment-slurry amendment restoration may not affect flowering phenology or insect flower damage at ecologically relevant levels, but that restoration activity increases sexual reproductive output at the patch scale. Restoration activity affected reproductive dynamics more often than changes in elevation alone. Restoration of subsiding salt marsh habitat by altering the soil environment may increase sexual reproductive capacity of these wetlands.


Salt marsh Spartina alterniflora Sediment amendment restoration Sexual reproduction Seed germination Flower phenology 



We would like to thank the Coastal Plant Ecology (J. Willis, M. McCoy) and Ecosystem Ecology (R. James, C. Laurenzano, J. Lesser, J. Nelson) labs at the University of Louisiana at Lafayette, K. Rogers, and O. Chapman for field and lab assistance. B. Chiviou at the USGS Wetland and Aquatic Research Center was instrumental in interpreting RTK data. Special thanks to L. Allain at the USGS WARC for starting us down the phenology path by lending us our first two time-lapse cameras, and to preliminary identification of Ischnodemus. V. Bayless at the LSU AgCenter identified I. conicus and provided copies of a genus-level key which was helpful. All data can be found at ScienceBase ( Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.


This research was partially funded by a grant to SFJ from the Ecology Center at ULL and the Society of Wetland Scientists.

Supplementary material

12237_2019_552_MOESM1_ESM.docx (6.4 mb)
ESM 1 (DOCX 6587 kb)


  1. Arganda-Carreras, I., V. Kaynig, C. Rueden, K.W. Eliceiri, J. Schindelin, A. Cardona, and H. Sebastian Seung. 2017. Trainable Weka segmentation: A machine learning tool for microscopy pixel classification. Bioinformatics 33 (15): 2424–2426.CrossRefGoogle Scholar
  2. Barbier, E.B., S.D. Hacker, C. Kennedy, E.W. Koch, A.C. Stier, and B.R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81 (2): 169–193.CrossRefGoogle Scholar
  3. Barrett, S.C. 2015. Influences of clonality on plant sexual reproduction. Proceedings of the National Academy of Sciences 112 (29): 8859–8866.CrossRefGoogle Scholar
  4. Bater, C.W., N.C. Coops, M.A. Wulder, T. Hilker, S.E. Nielsen, G. McDermid, and G.B. Stenhouse. 2011. Using digital time-lapse cameras to monitor species-specific understorey and overstorey phenology in support of wildlife habitat assessment. Environmental Monitoring and Assessment 180 (1-4): 1–13.CrossRefGoogle Scholar
  5. Bertness, M.D., and S.W. Shumway. 1992. Consumer driven pollen limitation of seed production in marsh grasses. American Journal of Botany 79 (3): 288–293.CrossRefGoogle Scholar
  6. Bertness, M., C. Wise, and A. Ellison. 1987. Consumer pressure and seed set in a salt marsh perennial plant community. Oecologia 71 (2): 190–200.CrossRefGoogle Scholar
  7. Biber, P.D., and J.D. Caldwell. 2008. Seed germination and seedling survival of Spartina alterniflora Loisel. American Journal of Agricultural and Biological Sciences 3: 633–638.CrossRefGoogle Scholar
  8. Blake, G.R., and K.H. Hartge. 1986. Bulk density. Methods of Soil Analysis: Part 1- Physical and Mineralogical Methods. 363–375Google Scholar
  9. Bradley, P.M., and J.T. Morris. 1990. Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71 (1): 282–287.CrossRefGoogle Scholar
  10. Bradley, P., and J. Morris. 1991. The influence of salinity on the kinetics of NH4 + uptake in Spartina alterniflora. Oecologia 85 (3): 375–380.CrossRefGoogle Scholar
  11. Callaway, J.C., and M.N. Josselyn. 1992. The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries and Coasts 15 (2): 218–226.CrossRefGoogle Scholar
  12. Crosby, S.C., M. Ivens-Duran, M.D. Bertness, E. Davey, L.A. Deegan, and H.M. Leslie. 2015. Flowering and biomass allocation in US Atlantic coast Spartina alterniflora. American Journal of Botany 102 (5): 669–676.CrossRefGoogle Scholar
  13. Daehler, C.C., and D.R. Strong. 1994. Variable reproductive output among clones of Spartina alterniflora (Poaceae) invading San Francisco Bay, California: The influence of herbivory, pollination, and establishment site. American Journal of Botany 81 (3): 307–313.CrossRefGoogle Scholar
  14. Derksen-Hooijberg, M., C. Angelini, L.P. Lamers, A. Borst, A. Smolders, J.R. Hoogveld, H. Paoli, J. de Koppel, B.R. Silliman, and T. der Heide. 2018. Mutualistic interactions amplify salt marsh restoration success. Journal of Applied Ecology 55 (1): 405–414.CrossRefGoogle Scholar
  15. Duarte, C.M., A. Borja, J. Carstensen, M. Elliott, D. Krause-Jensen, and N. Marbà. 2015. Paradigms in the recovery of estuarine and coastal ecosystems. Estuaries and Coasts 38 (4): 1202–1212.CrossRefGoogle Scholar
  16. Eleuterius, L.N., and J.D. Caldwell. 1984. Flowering phenology of tidal marsh plants in Mississippi. Castanea 1: 172–179.Google Scholar
  17. Fang, X. 2002. Reproductive biology of smooth cordgrass (Spartina alterniflora). LSU Master's Theses, 750.Google Scholar
  18. Fang, X., P.K. Subudhi, B.C. Venuto, and S.A. Harrison. 2004a. Mode of pollination, pollen germination, and seed set in smooth cordgrass (Spartina alterniflora, Poaceae). International Journal of Plant Sciences 165 (3): 395–401.CrossRefGoogle Scholar
  19. Fang, X., P.K. Subudhi, B.C. Venuto, S.A. Harrison, and A.B. Ryan. 2004b. Influence of flowering phenology on seed production in smooth cordgrass (Spartina alterniflora Loisel.). Aquatic Botany 80 (2): 139–151.CrossRefGoogle Scholar
  20. Feher, L.C., M.J. Osland, K.T. Griffith, J.B. Grace, R.J. Howard, C.L. Stagg, N.M. Enwright, K.W. Krauss, C.A. Gabler, R.H. Day, and K. Rogers. 2017. Linear and nonlinear effects of temperature and precipitation on ecosystem properties in tidal saline wetlands. Ecosphere 8 (10): e01956.CrossRefGoogle Scholar
  21. Fine, G. and G. Thomassie. 2000. Vermilion smooth cordgrass. NRCS Publication ID, 5830.Google Scholar
  22. Gedan, K.B., B. Silliman, and M. Bertness. 2009. Centuries of human-driven change in salt marsh ecosystems. Annual Review of Marine Science 1 (1): 117–141.CrossRefGoogle Scholar
  23. Grace, J.B. 1993. The adaptive significance of clonal reproduction in angiosperms: An aquatic perspective. Aquatic Botany 44 (2-3): 159–180.CrossRefGoogle Scholar
  24. Grime, J. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist 111 (982): 1169–1194.CrossRefGoogle Scholar
  25. Hartman, J.M. 1988. Recolonization of small disturbance patches in a New England salt marsh. American Journal of Botany 75 (11): 1625–1631.CrossRefGoogle Scholar
  26. Jones, S.F., C.L. Stagg, K.W. Krauss, and M.W. Hester. 2016. Tidal saline wetland regeneration of sentinel vegetation types in the Northern Gulf of Mexico: An overview. Estuarine, Coastal and Shelf Science 174: A1–A10.CrossRefGoogle Scholar
  27. Kettenring, K.M., and D.F. Whigham. 2009. Seed viability and seed dormancy of non-native Phragmites australis in suburbanized and forested watersheds of the Chesapeake Bay, USA. Aquatic Botany 91 (3): 199–204.CrossRefGoogle Scholar
  28. Kettenring, K.M., and D.F. Whigham. 2018. The role of propagule type, resource availability, and seed source in Phragmites invasion in Chesapeake Bay wetlands. Wetlands. 38 (6): 1259–1268. Scholar
  29. Kettenring, K.M., M.K. McCormick, H.M. Baron, and D.F. Whigham. 2010. Phragmites australis (common reed) invasion in the Rhode River subestuary of the Chesapeake Bay: Disentangling the effects of foliar nutrients, genetic diversity, patch size, and seed viability. Estuaries and Coasts 33 (1): 118–126.CrossRefGoogle Scholar
  30. Kettenring, K.M., M.K. McCormick, H.M. Baron, and D.F. Whigham. 2011. Mechanisms of Phragmites australis invasion: Feedbacks among genetic diversity, nutrients, and sexual reproduction. Journal of Applied Ecology 48 (5): 1305–1313.CrossRefGoogle Scholar
  31. Liu, W., K. Maung-Douglass, D.R. Strong, S.C. Pennings, and Y. Zhang. 2016. Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China. Journal of Ecology 104 (1): 173–181.CrossRefGoogle Scholar
  32. McCormick, M.K., K.M. Kettenring, H.M. Baron, and D.F. Whigham. 2010. Extent and reproductive mechanisms of Phragmites australis spread in brackish wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30 (1): 67–74.CrossRefGoogle Scholar
  33. Mendelssohn, I.A., and N.L. Kuhn. 2003. Sediment subsidy: Effects on soil-plant responses in a rapidly submerging coastal salt marsh. Ecological Engineering 21 (2-3): 115–128.CrossRefGoogle Scholar
  34. Mendelssohn, I.A., and K.L. McKee. 1988. Spartina alterniflora die-back in Louisiana: Time-course investigation of soil waterlogging effects. Journal of Ecology 76 (2): 509–521.CrossRefGoogle Scholar
  35. Mobberley, D.G. 1953. Taxonomy and distribution of the genus Spartina. Iowa State Dissertations, 12794.Google Scholar
  36. Mooring, M.T., A.W. Cooper, and E.D. Seneca. 1971. Seed germination response and evidence for height ecophenes in Spartina alterniflora from North Carolina. American Journal of Botany 58 (1): 48–55.CrossRefGoogle Scholar
  37. NOAA. 2016. Tides & Currents - Station Info. for Port Fourchon, Belle Pass, LA - Station ID: 8762075. Accessed May 2017.
  38. Obeso, J.R. 2002. The costs of reproduction in plants. New Phytologist 155 (3): 321–348.CrossRefGoogle Scholar
  39. Osland, M., N. Enwright, and C.L. Stagg. 2014. Freshwater availability and coastal wetland foundation species: Ecological transitions along a rainfall gradient. Ecology 95 (10): 2789–2802.CrossRefGoogle Scholar
  40. Pennings, S.C., C.K. Ho, C.S. Salgado, K. Więski, N. Davé, A.E. Kunza, and E.L. Wason. 2009. Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90 (1): 183–195.CrossRefGoogle Scholar
  41. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2016. Nlme: Linear and nonlinear mixed effects models.Google Scholar
  42. R Core Team. 2016. R: A language and environment for statistical computing. Vienna, Austria.Google Scholar
  43. Richards, C.L., J. Hamrick, L.A. Donovan, and R. Mauricio. 2004. Unexpectedly high clonal diversity of two salt marsh perennials across a severe environmental gradient. Ecology Letters 7 (12): 1155–1162.CrossRefGoogle Scholar
  44. Richardson, A.D., A.S. Bailey, E.G. Denny, C.W. Martin, and J. O'Keefe. 2006. Phenology of a northern hardwood forest canopy. Global Change Biology 12 (7): 1174–1188.CrossRefGoogle Scholar
  45. Richardson, A.D., B.H. Braswell, D.Y. Hollinger, J.P. Jenkins, and S.V. Ollinger. 2009. Near-surface remote sensing of spatial and temporal variation in canopy phenology. Ecological Applications 19 (6): 1417–1428.CrossRefGoogle Scholar
  46. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona. 2012. Fiji: An open-source platform for biological-image analysis. Nature Methods 9 (7): 676–682.CrossRefGoogle Scholar
  47. Silvertown, J. 2008. The evolutionary maintenance of sexual reproduction: Evidence from the ecological distribution of asexual reproduction in clonal plants. International Journal of Plant Sciences 169 (1): 157–168.CrossRefGoogle Scholar
  48. Slater, J.A. and R.M. Baranowski. 1990. Lygaeidae of Florida (Hemiptera: Heteroptera), in Florida Dept. Agric and Consumer Serv., Arthropods of Florida and Neighboring Land Areas, Vol. 14, Div. Plant Industry, Gainesville, FL.Google Scholar
  49. Slocum, M.G., I.A. Mendelssohn, and N.L. Kuhn. 2005. Effects of sediment slurry enrichment on salt marsh rehabilitation: Plant and soil responses over seven years. Estuaries 28 (4): 519–528.CrossRefGoogle Scholar
  50. Sokolov, I.M., X. Chen, R.M. Strecker, and L.M. Hooper-Bùi. 2018. An annotated list of Auchenorrhyncha and Heteroptera collected in the coastal salt marshes of the Mississippi Delta in Louisiana. Psyche: A Journal of Entomology 2018: 1808370.Google Scholar
  51. Somers, G.F., and D. Grant. 1981. Influence of seed source upon phenology of flowering of Spartina alterniflora Loisel. and the likelihood of cross pollination. American Journal of Botany 68 (1): 6–9.CrossRefGoogle Scholar
  52. Sparks, E.L., and J. Cebrian. 2015. Effects of fertilization on grasshopper grazing of northern Gulf of Mexico salt marshes. Estuaries and Coasts 38 (3): 988–999.CrossRefGoogle Scholar
  53. Stagg, C.L., and I.A. Mendelssohn. 2010. Restoring ecological function to a submerged salt marsh. Restoration Ecology 18: 10–17.CrossRefGoogle Scholar
  54. Stephenson, A. 1981. Flower and fruit abortion: Proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12 (1): 253–279.CrossRefGoogle Scholar
  55. Travis, S.E., and M.W. Hester. 2005. A space-for-time substitution reveals the long-term decline in genotypic diversity of a widespread salt marsh plant, Spartina alterniflora, over a span of 1500 years. Journal of Ecology 93 (2): 417–430.CrossRefGoogle Scholar
  56. Travis, S.E., C.E. Proffitt, and K. Ritland. 2004. Population structure and inbreeding vary with successional stage in created Spartina alterniflora marshes. Ecological Applications 14 (4): 1189–1202.CrossRefGoogle Scholar
  57. Wolkovich, E.M., B.I. Cook, and T.J. Davies. 2014. Progress towards an interdisciplinary science of plant phenology: Building predictions across space, time and species diversity. New Phytologist 201 (4): 1156–1162.CrossRefGoogle Scholar
  58. Wolters, M., A. Garbutt, R.M. Bekker, J.P. Bakker, and P.D. Carey. 2008. Restoration of salt-marsh vegetation in relation to site suitability, species pool and dispersal traits. Journal of Applied Ecology 45: 904–912.CrossRefGoogle Scholar
  59. Zuur, A.F., E.N. Ieno, N.J. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. ed. Gail, M., K. Krickeberg, J.M. Samet, A. Tsiatis, and W. Wong. New York, NY: Spring Science and Business Media.Google Scholar

Copyright information

©  This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection  2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Louisiana at LafayetteLafayetteUSA
  2. 2.Western Ecological Research CenterU.S. Geological SurveyDavisUSA
  3. 3.Department of GeographyNational University SingaporeSingaporeSingapore
  4. 4.Wetland and Aquatic Research CenterU.S. Geological SurveyLafayetteUSA

Personalised recommendations