Predation restricts black mangrove (Avicennia germinans) colonization at its northern range limit along Florida’s Gulf Coast


Climate change-driven range expansion of black mangroves (Avicennia germinans) is predicted along the northern Gulf of Mexico, where sea level rise is also driving conversion of freshwater forest islands to salt marsh. While climate-driven A. germinans range expansion has garnered considerable scientific attention, the role of top-down controls on colonization is largely overlooked. We investigated the effects of abiotic (flooding frequency, soil depth, soil salinity) and biotic (predation, herbivory) controls on A. germinans establishment at its northern range limit along Florida’s Gulf Coast by comparing fates of caged and non-caged propagules across four landscape positions (from creek edge to forest island interior) and at three sites along a tidal flooding frequency gradient. Within 12 days, grapsid crab, Sesarma reticulatum, consumed 99% of non-caged propagules. Among caged propagules, establishment increased with increasing flooding frequency; however, cages did not entirely prevent predation, which remained a primary cause of mortality, except in the rarely flooded island. Propagules that survived to seedlings experienced mild to fatal herbivory across landscape positions and sites. This study revealed that while relict forest islands and surrounding marshes can support A. germinans, predation and herbivory strongly suppress colonization, suggesting that mangrove expansion models should incorporate biotic controls.

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  1. Alongi, D. M., 2015. The impact of climate change on mangrove forests. Current Climate Change Reports 1: 30–39.

  2. Bertness, M. D., C. Holdredge & A. H. Altieri, 2009. Substrate mediates consumer control of salt marsh cordgrass on Cape Cod, New England. Ecology 90: 2108–2117.

  3. Bosire, J. O., J. G. Kairo, J. Kazungu, N. Koedam & F. Dahdouh-Guebas, 2005. Predation on propagules regulates regeneration in a high-density reforested mangrove plantation. Marine Ecology Progress Series 299: 149–155.

  4. Cannicci, S., D. Burrows, S. Fratini, T. J. Smith III, J. Offenberg & F. Dahdouh-Guebas, 2008. Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquatic Botany 89: 186–200.

  5. Castaneda, H. & F. Putz, 2007. Predicting sea-level rise effects on a nature preserve on the Gulf Coast of Florida: a landscape perspective. Florida Scientist 70: 166–175.

  6. Cavanaugh, K. C., J. R. Kellner, A. J. Forde, D. S. Gruner, J. D. Parker, W. Rodriguez & I. C. Feller, 2014. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences of USA 111: 723–727.

  7. Comeaux, R. S., M. A. Allison & T. S. Bianchi, 2012. Mangrove expansion in the Gulf of Mexico with climate change: implications for wetland health and resistance to rising sea levels. Estuarine, Coastal and Shelf Science 96: 81–95.

  8. Dahdouh-Guebas, F., M. Verneirt, J. Tack, D. Van Speybroeck & N. Koedam, 1998. Propagule predators in Kenyan mangroves and their possible effect on regeneration. Marine and Freshwater Research 49: 345–350.

  9. DeSantis, L. R., S. Bhotika, K. Williams & F. E. Putz, 2007. Sea-level rise and drought interactions accelerate forest decline on the Gulf Coast of Florida, USA. Global Change Biology 13: 2349–2360.

  10. Dunne, J. A., J. Harte & K. J. Taylor, 2003. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecological Monographs 73: 69–86.

  11. Farnsworth, E. J. & A. M. Ellison, 1997. Global patterns of pre-dispersal propagule predation in mangrove forests. Biotropica 29: 318–330.

  12. Fitter, A. H., R. S. R. Fitter, I. T. B. Harris & M. H. Williamson, 1995. Relationship between 1st flowering date and temperature in the flora of a locality in central England. Functional Ecology 9: 55–60.

  13. FNAI, 2015. Florida Land Cover Classification System Definitions for the Cooperative Land Cover Map v3.1.

  14. Giri, C. & J. Long, 2016. Is the geographic range of mangrove forests in the conterminous United States really expanding? Sensors 16: 2010.

  15. Grabherr, G., M. Gottfried & H. Pauli, 1994. Climate effects on mountain plants. Nature 369: 448.

  16. Guo, H., Y. Zhang, Z. Lan & S. C. Pennings, 2013. Biotic interactions mediate the expansion of black mangrove (Avicennia germinans) into salt marshes under climate change. Global Change Biology 19: 2765–2774.

  17. Guo, H., C. Weaver, S. P. Charles, et al., 2017. Coastal regime shifts: rapid responses of coastal wetlands to changes in mangrove cover. Ecology 98: 762–772.

  18. He, Q. & B. R. Silliman, 2016. Consumer control as a common driver of coastal vegetation worldwide. Ecological Monographs 86: 278–294.

  19. Holdredge, C., M. D. Bertness & A. H. Altieri, 2009. Role of crab herbivory in die-off of New England salt marshes. Conservation Biology 23: 672–679.

  20. Inouye, D. W., 2008. Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89: 353–362.

  21. Kelly, A. E. & M. L. Goulden, 2008. Rapid shifts in plant distribution with recent climate change. Proceedings of the National Academy of Sciences of USA 105: 11823–11826.

  22. Kilkenny, F. F. & L. F. Galloway, 2016. Evolution of marginal populations of an invasive vine increases the likelihood of future spread. New Phytologist 209: 1773–1780.

  23. Krauss, K. W., A. S. From, T. W. Doyle, T. J. Doyle & M. J. Barry, 2011. Sea-level rise and landscape change influence mangrove encroachment onto marsh in the Ten Thousand Islands region of Florida, USA. Journal of Coastal Conservation 15: 629–638.

  24. Lancaster, L. T., G. Morrison & R. N. Fitt, 2016. Life history trade-offs, the intensity of competition, and coexistence in novel and evolving communities under climate change. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160046.

  25. Lewis, R. & F. Dunstan, 1975. The possible role of Spartina alterniflora Loisel in establishment of mangroves in Florida. Proceedings for Second Annual Conference on the Restoration of Coastal Vegetation in Florida May 17, 1975. Hillsborough Community College, Tampa: 82–100.

  26. Lugo, A. E. & C. Patterson-Zucca, 1977. The impact of low temperature stress on mangrove structure and growth. Tropical Ecology 18: 149–161.

  27. McGuinness, K. A., 1997. Seed predation in a tropical mangrove forest: a test of the dominance-predation model in northern Australia. Journal of Tropical Ecology 13: 293–302.

  28. McKee, K. L., 1995. Mangrove species distribution and propagule predation in Belize: an exception to the dominance-predation hypothesis. Biotropica 27: 334–345.

  29. McKee, K. L. & J. E. Rooth, 2008. Where temperate meets tropical: multi-factorial effects of elevated CO2, nitrogen enrichment, and competition on a mangrove-salt marsh community. Global Change Biology 14: 971–984.

  30. McKee, K. L., J. E. Rooth & I. C. Feller, 2007. Mangrove recruitment after forest disturbance is facilitated by herbaceous species in the Caribbean. Ecological Applications 17: 1693.

  31. McKee, K., K. Rogers & N. Saintilan, 2012. Response of salt marsh and mangrove wetlands to changes in atmospheric CO2, climate, and sea level. In Middleton, B. A. (ed.), Global Change and the Function and Distribution of Wetlands. Springer, Dordrecht: 63–96.

  32. Minchinton, T. E., 2006. Consequences of pre-dispersal damage by insects for the dispersal and recruitment of mangroves. Oecologia 148: 70–80.

  33. Møller, A. P., D. Rubolini & E. Lehikoinen, 2008. Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences of USA 105: 16195–16200.

  34. Nitto, D. D., G. Neukermans, N. Koedam, H. Defever, F. Pattyn, J. Kairo & F. Dahdouh-Guebas, 2014. Mangroves facing climate change: landward migration potential in response to projected scenarios of sea level rise. Biogeosciences 11: 857–871.

  35. Osborne, K. & T. Smith III, 1990. Differential predation on mangrove propagules in open and closed canopy forest habitats. Vegetatio 89: 1–6.

  36. Osland, M. J., N. Enwright, R. H. Day & T. W. Doyle, 2013. Winter climate change and coastal wetland foundation species: salt marshes vs. mangrove forests in the southeastern United States. Global Change Biology 19: 1482–1494.

  37. Osland M. J., R. H. Day, A. S. From, M. L. McCoy, J. L. McLeod & J. J. Kelleway, 2015. Life stage influences the resistance and resilience of black mangrove forests to winter climate extremes. Ecosphere 6: 1–15.

  38. Osland, M. J., N. M. Enwright, R. H. Day, C. A. Gabler, C. L. Stagg & J. B. Grace, 2016a. Beyond just sea-level rise: considering macroclimatic drivers within coastal wetland vulnerability assessments to climate change. Global Change Biology 22: 11.

  39. Osland, M. J., L. C. Feher, K. T. Griffith, et al., 2016b. Climatic controls on the global distribution, abundance, and species richness of mangrove forests. Ecological Monographs. doi:10.1002/ecm.1248.

  40. Osland, M. J., R. H. Day, C. T. Hall, M. D. Brumfield, J. L. Dugas & W. R. Jones, 2017. Mangrove expansion and contraction at a poleward range limit: climate extremes and land–ocean temperature gradients. Ecology 98: 125–127.

  41. Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37: 637–669.

  42. Parmesan, C. & G. Yohe, 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42.

  43. Parson, K. A. & A. A. De La Cruz, 1980. Energy flow and grazing behavior of conocephaline grasshoppers in a Juncus roemerianus marsh. Ecology 61: 1045–1050.

  44. Patterson, C. S., I. A. Mendelssohn & E. M. Swenson, 1993. Growth and survival of Avicennia germinans seedlings in a mangal/salt marsh community in Louisiana, USA. Journal of Coastal Research 9: 801–810.

  45. Patterson, S., K. L. McKee & I. A. Mendelssohn, 1997. Effects of tidal inundation and predation on Avicennia germinans seedling establishment and survival in a sub-tropical mangal/salt marsh community. Mangroves and Salt Marshes 1: 103–111.

  46. Perry, L., P. J. Low, J. R. Ellis & J. D. Reynolds, 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912–1915.

  47. R Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

  48. Reddy, K. R., M. W. Clark, R. D. DeLaune & M. Kongchum, 2013. Physicochemical characterization of wetland soils. In Delaune, R. D., K. R. Reddy, C. J. Richardson & J. P. Megonigal (eds), Methods in Biogeochemistry of Wetlands. Soil Science Society of America, Madison: 41–53.

  49. Rhoades, J., 1996. Salinity: electrical conductivity and total dissolved solids. Methods of Soil Analysis, Part 3: Chemical Methods. Soil Science Society of America and American Society of Agronomy, Madison: 417–435.

  50. Robertson, A., R. Giddins & T. Smith, 1990. Seed predation by insects in tropical mangrove forests: extent and effects on seed viability and the growth of seedlings. Oecologia 83: 213–219.

  51. Saintilan, N., N. C. Wilson, K. Rogers, A. Rajkaran & K. W. Krauss, 2014. Mangrove expansion and salt marsh decline at mangrove poleward limits. Global Change Biology 20: 147–157.

  52. Smith, T. J., 1987. Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68: 266–273.

  53. Smith, T. J., H. T. Chan, C. C. McIvor & M. B. Robblee, 1989. Comparisons of seed predation in tropical, tidal forests from three continents. Ecology 70: 146–151.

  54. Sousa, W. P. & B. J. Mitchell, 1999. The effect of seed predators on plant distributions: Is there a general pattern in mangroves? Oikos 86: 55–66.

  55. Sousa, W. P., P. G. Kennedy & B. J. Mitchell, 2003. Propagule size and predispersal damage by insects affect establishment and early growth of mangrove seedlings. Oecologia 135: 564–575.

  56. Souza, M. M. A. & E. V. S. B. Sampaio, 2011. Predation on propagules and seedlings in mature and regenerating mangroves in the Coast of Ceará, Brazil. Hydrobiologia 661: 179–186.

  57. Sparks, E. L. & J. Cebrian, 2015. Does bird removal affect grasshopper grazing on Juncus roemerianus (black needlerush) marshes? Wetlands Ecology and Management 23: 1083–1089.

  58. Sparks, T. H. & T. J. Yates, 1997. The effect of spring temperature on the appearance dates of British butterflies 1883–1993. Ecography 20: 368–374.

  59. Steele, O. C., K. C. Ewel & G. Goldstein, 1999. The importance of propagule predation in a forest of nonindigenous mangrove trees. Wetlands 19: 705–708.

  60. Stevens, P., S. Fox & C. Montague, 2006. The interplay between mangroves and saltmarshes at the transition between temperate and subtropical climate in Florida. Wetlands Ecology and Management 14: 435–444.

  61. Travers, S. E., B. Marquardt, N. J. Zerr, J. B. Finch, M. J. Boche, R. Wilk & S. C. Burdick, 2015. Climate change and shifting arrival date of migratory birds over a century in the northern Great Plains. The Wilson Journal of Ornithology 127: 43–51.

  62. Van Nedervelde, F., S. Cannicci, N. Koedam, J. Bosire & F. Dahdouh-Guebas, 2015. What regulates crab predation on mangrove propagules? Acta Oecologica 63: 63–70.

  63. Vince, S. W., S. R. Humphrey & R. W. Simons, 1989. The Ecology of Hydric Hammocks: A Community Profile. U.S. Department of the Interior, Fish and Wildlife Service, Research and Development.

  64. Walther, G.-R., E. Post, P. Convey, et al., 2002. Ecological responses to recent climate change. Nature 416: 389–395.

  65. Ward, R. D., D. A. Friess, R. H. Day & R. A. MacKenzie, 2016. Impacts of climate change on mangrove ecosystems: a region by region overview. Ecosystem Health and Sustainability 2: e01211.

  66. Williams, K., M. V. Meads & D. A. Sauerbrey, 1998. The roles of seedling salt tolerance and resprouting in forest zonation on the west coast of Florida, USA. American Journal of Botany 85: 1745–1752.

  67. Williams, K., K. C. Ewel, R. P. Stumpf, F. E. Putz & T. W. Workman, 1999. Sea-level rise and coastal forest retreat on the west coast of Florida, USA. Ecology 80: 2045–2063.

  68. Williams, K., M. MacDonald, K. McPherson & T. H. Mirti, 2007. Ecology of the coastal edge of hydric hammocks on the Gulf Coast of Florida. In: Ecology of Tidal Freshwater Forested Wetlands of the Southeastern United States. Springer, Dordrecht: 255–289.

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We thank Waccasassa Bay Preserve State Park for permission to conduct research at Turtle Creek. We also thank University of Florida Seahorse Key Marine Lab for providing transportation support, especially Captain Kenny and Rose McCain. We acknowledge Shawn Taylor and Nathan Reaver for much appreciated field assistance. AL acknowledges funding from the University of Florida Graduate School Fellowship and H. T. Odum Graduate Fellowship. CA acknowledges funding from National Science Foundation Department of Environmental Biology (Award 1546638).

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Correspondence to David A. Kaplan.

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Guest editors: K. W. Krauss, I. C. Feller, D. A. Friess, R. R. Lewis III / Causes and Consequences of Mangrove Ecosystem Responses to an Ever-Changing Climate

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Langston, A.K., Kaplan, D.A. & Angelini, C. Predation restricts black mangrove (Avicennia germinans) colonization at its northern range limit along Florida’s Gulf Coast. Hydrobiologia 803, 317–331 (2017) doi:10.1007/s10750-017-3197-0

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  • Bottom-up
  • Community reassembly
  • Herbivory
  • Predation
  • Sea level rise
  • Sesarma reticulatum
  • Top-down