Abstract
Extreme winter temperatures govern the northern range limit of black mangroves (Avicennia germinans) in southeastern North America. There is a pressing need for studies that advance our understanding of how extreme cold temperature events affect mangroves near their range limits. However, such events are infrequent and challenging to study at regional scales. Here, we compared the damage to mangroves from extreme freeze events in 2018 and 2021, using local data from sites in USA (Florida, Louisiana, and Texas) and northeastern Mexico (Tamaulipas). In 2018, mangrove damage was concentrated in Louisiana and the upper Texas coast, where minimum temperatures ranged from -4 °C to -7 °C. In 2021, damage from a more severe freeze event was concentrated along the central to northern coasts of Texas, where minimum temperatures ranged from -4 °C to -10 °C. We used regional temperature and vegetation data from these events to quantify temperature thresholds for A. germinans leaf damage. Our results indicate that A. germinans leaf damage is likely to occur when temperatures are between -4 °C and -6 °C. These findings help refine temperature thresholds for A. germinans leaf damage and advance understanding of the effects of extreme freeze events on mangrove range expansion. This information is valuable for anticipating future range dynamics in a warming world.
References
Armitage, A.R., W.E. Highfield, S.D. Brody, and P. Louchouarn. 2015. The contribution of mangrove expansion to salt marsh loss on the Texas Gulf Coast. PLoS ONE 10: e0125404.
Attaway, J.A. 1997. A history of Florida citrus freezes. Lake Alfred, Florida, USA: Florida Science Source.
Bardou, R., M.J. Osland, S. Scyphers, C. Shepard, K.E. Aerni, J.B. Alemu, R. Crimian, R.H. Day, N.M. Enwright, L.C. Feher, S.L. Gibbs, K.O. O’Donnel, S.H. Swinea, K. Thorne, S. Truskey, A.R. Armitage, R. Baker, J.L. Breithaupt, K.C. Cavanaugh, J. Cebrian, K. Cummins, D.J. Devlin, J. Doty, K.H. Dunton, W.L. Ellis, I.C. Feller, C.A. Gabler, Y. Kang, D.A. Kaplan, J.P. Kennedy, K.W. Krauss, M.M. Lamont, K.B. Liu, M. Martinez, A.M. Matheny, G.M. McClenachan, K.L. McKee, I.A. Mendelssohn, T.C. Michot, C.M. Miller, J.A. Moon, R.P. Moyer, J. Nelson, R. O’Conner, J.W. Pahl, J.L. Pitchford, C.E. Proffitt, T. Quirk, K.R. Radabaugh, W.A. Sheffel, D.L. Smee, C.M. Snyder, E. Sparks, K.M. Swanson, W.C. Vervaeke, C.A. Weaver, J. Willis, E.S. Yando, Q. Yao, and A.R. Hughes. 2023. Rapidly changing range limits in a warming world: Critical data limitations and knowledge gaps for advancing understanding of mangrove range dynamics. Estuaries and Coasts 46: 1123–1140.
Cavanaugh, K.C., E.M. Dangremond, C.L. Doughty, A.P. Williams, J.D. Parker, M.A. Hayes, W. Rodriguez, and I.C. Feller. 2019. Climate-driven regime shifts in a mangrove–salt marsh ecotone over the past 250 years. Proceedings of the National Academy of Sciences 116: 21602–21608.
Cavanaugh, K.C., J.D. Parker, S.C. Cook-Patton, I.C. Feller, A.P. Williams, and J.R. Kellner. 2015. Integrating physiological threshold experiments with climate modeling to project mangrove species’ range expansion. Global Change Biology 21: 1928–1938.
Cavanaugh, K.C., J.R. Kellner, A.J. Forde, D.S. Gruner, J.D. Parker, W. Rodriguez, and 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 111: 723–727.
Cavanaugh, K.C., M.J. Osland, R. Bardou, G. Hinijosa-Arango, J.M. López-Vivas, J.D. Parker, and A.S. Rovai. 2018. Sensitivity of mangrove range limits to climate variability. Global Ecology and Biogeography 27: 925–935.
Coldren, G.A., and C.E. Proffitt. 2017. Mangrove seedling freeze tolerance depends on salt marsh presence, species, salinity, and age. Hydrobiologia 803: 159–171.
Cook-Patton, S.C., M. Lehmann, and J.D. Parker. 2015. Convergence of three mangrove species towards freeze-tolerant phenotypes at an expanding range edge. Functional Ecology 29: 1332–1340.
Dangremond, E.M., and I.C. Feller. 2016. Precocious reproduction increases at the leading edge of a mangrove range expansion. Ecology and Evolution 6: 5087–5092.
Dangremond, E.M., L.T. Simpson, T.Z. Osborne, and I.C. Feller. 2020. Nitrogen enrichment accelerates mangrove range expansion in the temperate–tropical ecotone. Ecosystems 23: 703–714.
Devaney, J.L., M. Lehmann, I.C. Feller, and J.D. Parker. 2017. Mangrove microclimates alter seedling dynamics at the range edge. Ecology 98: 2513–2520.
Everitt, J.H., F.W. Judd, D.E. Escobar, and M.R. Davis. 1996. Integration of remote sensing and spatial information technologies for map** black mangrove on the Texas gulf coast. Journal of Coastal Research 12: 64–69.
Feller, I.C., U. Berger, S.K. Chapman, E.M. Dangremond, N.G. Dix, J.A. Langley, C.E. Lovelock, T.Z. Osborne, A.C. Shor, and L.T. Simpson. 2023. Nitrogen addition increases freeze resistance in black mangrove (Avicennia germinans) shrubs in a temperate-tropical ecotone. Ecosystems 26: 800–814.
Gabler, C.A., M.J. Osland, J.B. Grace, C.L. Stagg, R.H. Day, S.B. Hartley, N.M. Enwright, A.S. From, M.L. McCoy, and J.L. McLeod. 2017. Macroclimatic change expected to transform coastal wetland ecosystems this century. Nature Climate Change 7: 142–147.
Hayes, M.A., A.C. Shor, A. Jesse, C. Miller, J.P. Kennedy, and I. Feller. 2020. The role of glycine betaine in range expansions; protecting mangroves against extreme freeze events. Journal of Ecology 108: 61–69.
Hesterberg, S.G., K. Jackson, and S.S. Bell. 2022. Climate drives coupled regime shifts across subtropical estuarine ecosystems. Proceedings of the National Academy of Sciences 119: e2121654119.
Hoffman, S.E., D.J. Devlin, and C.E. Proffitt. 2022. Maternal nutrient history enhances black mangrove (Avicennia germinans) seedling growth after propagules experience a hard freeze. Estuaries and Coasts 45: 2534–2542.
Kaalstad, S., D.J. Devlin, C.E. Proffitt, M.J. Osland, K.M. Swanson, D.A. Kaplan, R.H. Day, L.C. Feher, N.G.F. Reever, K.H. Dunton, A.P. Stetter, A.F. Cabo, A.S. From, J. Cebrian, C.J. Miller, K.L. Cummins, A.R. Armitage, C.R. Sanspree, E.A. Flores, A.R. Hughes, C. Zamora-Tovar, C.M. Snyder, J.E. Thompson, and G.H. Anderson. 2023. 2021 Gulf of Mexico mangrove freeze damage data. U.S. Geological Survey data release. https://doi.org/10.5066/P97GF4NP.
Kennedy, J.P., R.F. Preziosi, J.K. Rowntree, and I.C. Feller. 2020. Is the central-marginal hypothesis a general rule? Evidence from three distributions of an expanding mangrove species, Avicennia germinans (L.) L. Molecular Ecology 29: 704–719.
Kennedy, J.P., G.N. Johnson, R.F. Preziosi, and J.K. Rowntree. 2022. Genetically based adaptive trait shifts at an expanding mangrove range margin. Hydrobiologia 849: 1777–1794.
Langston, A.K., and D.A. Kaplan. 2020. Modelling the effects of climate, predation, and dispersal on the poleward range expansion of black mangrove (Avicennia germinans). Ecological Modelling 434: 109245.
Lovelock, C.E., K.W. Krauss, M.J. Osland, R. Reef, and M.C. Ball. 2016. The physiology of mangrove trees with changing climate. In Tropical tree physiology: Adaptations and responses in a changing environment, ed. G. Goldstein and L.S. Santiago, 149–179. New York, New York, USA: Springer.
Macy, A., M.J. Osland, J.A. Cherry, and J. Cebrian. 2021. Effects of chronic and acute stressors on transplanted black mangrove (Avicennia germinans) seedlings along an eroding Louisiana shoreline. Restoration Ecology 29: e13373.
Madrid, E.N., A.R. Armitage, and J. López-Portillo. 2014. Avicennia germinans (black mangrove) vessel architecture is linked to chilling and salinity tolerance in the Gulf of Mexico. Frontiers in Plant Science 5: 503.
Martinez, M., M.J. Osland, J.B. Grace, N.M. Enwright, C.L. Stagg, S. Kaalstad, G.H. Anderson, A.R. Armitage, J. Cebrian, K.L. Cummins, R.H. Day, D.J. Devlin, K.H. Dunton, L.C. Feher, A. Fierro-Cabo, E.A. Flores, A.S. From, R.A. Hughes, D.A. Kaplan, A.K. Langston, B. Martinez, C. Miller, C.E. Proffitt, N.G.F. Reaver, C.R. Sanspree, C.M. Snyder, A.P. Stetter, K. Swanson, J.E. Thompson, and C. Zamora-Tovar. 2023. Integrating remote sensing with ground-based observations to quantify the effects of an extreme freeze event on black mangroves (Avicennia germinans) at the landscape scale. Ecosystems. https://doi.org/10.1007/s10021-023-00871-z.
McClenachan, G., M. Witt, and L.J. Walters. 2021. Replacement of oyster reefs by mangroves: Unexpected climate-driven ecosystem shifts. Global Change Biology 27: 1226–1238.
McKee, K.L., and W.C. Vervaeke. 2018. Will fluctuations in salt marsh-mangrove dominance alter vulnerability of a subtropical wetland to sea-level rise? Global Change Biology 24: 1224–1238.
Montagna, P.A., J. Brenner, J.C. Gibeaut, and S. Morehead. 2011. Coastal impacts. In The Impact of Global Warming on Texas, 2nd ed., ed. J. Schmandt, G.R. North, and J. Clarkson, 96–123. Austin, Texas, USA: University of Texas Press.
Osland, M.J., and L.C. Feher. 2020. Winter climate change and the poleward range expansion of a tropical invasive tree (Brazilian pepper - Schinus terebinthifolius). Global Change Biology 26: 607–615.
Osland, M.J., A.M. Hartmann, R.H. Day, M.H. Ross, C.T. Hall, L.C. Feher, and W.C. Vervaeke. 2019b. Microclimate influences mangrove freeze damage: Implications for range expansion in response to changing macroclimate. Estuaries and Coasts 42: 1084–1096.
Osland, M.J., B. Chivoiu, L.C. Feher, L.L. Dale, D. Lieurance, W.M. Daniel, and J.E. Spencer. 2023. Plant migration and winter climate change: Range expansion of tropical invasive plants in response to warming winters. Biological Invasions 25: 2813–2830.
Osland, M.J., J.B. Grace, G.R. Guntenspergen, K.M. Thorne, J.A. Carr, and L.C. Feher. 2019a. Climatic controls on the distribution of foundation plant species in coastal wetlands of the conterminous United States: Knowledge gaps and emerging research needs. Estuaries and Coasts 42: 1991–2003.
Osland, M.J., N. Enwright, R.H. Day, and 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.
Osland, M.J., P.W. Stevens, M.M. Lamont, R.C. Brusca, K.M. Hart, J.H. Waddle, C.A. Langtimm, C.M. Williams, B.D. Keim, and A.J. Terando. 2021. Tropicalization of temperate ecosystems in North America: The northward range expansion of tropical organisms in response to warming winter temperatures. Global Change Biology 27: 3009–3034.
Osland, M.J., R.H. Day, and T.C. Michot. 2020a. Frequency of extreme freeze events controls the distribution and structure of black mangroves (Avicennia germinans) near their northern range limit in coastal Louisiana. Diversity and Distributions 26: 1366–1382.
Osland, M.J., R.H. Day, A.S. From, M.L. McCoy, J.L. McLeod, and J.J. Kelleway. 2015. Life stage influences the resistance and resilience of black mangrove forests to winter climate extremes. Ecosphere 6: 160.
Osland, M.J., R.H. Day, C.T. Hall, M.D. Brumfield, J.L. Dugas, and W.R. Jones. 2017. Mangrove expansion and contraction at a poleward range limit: Climate extremes and land-ocean temperature gradients. Ecology 98: 125–137.
Osland, M.J., R.H. Day, C.T. Hall, L.C. Feher, A.R. Armitage, J. Cebrian, K.H. Dunton, A.R. Hughes, D.A. Kaplan, A.K. Langston, A. Macy, C.A. Weaver, G.H. Anderson, K. Cummins, I.C. Feller, and C.M. Snyder. 2020b. Temperature thresholds for black mangrove (Avicennia germinans) freeze damage, mortality, and recovery in North America: Refining tip** points for range expansion in a warming climate. Journal of Ecology 108: 654–665.
Pickens, C.N., and M.W. Hester. 2011. Temperature tolerance of early life history stages of black mangrove Avicennia germinans: Implications for range expansion. Estuaries and Coasts 34: 824–830.
R Core Team. 2021. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rogers, J.C., and R.V. Rohli. 1991. Florida citrus freezes and polar anticyclones in the Great Plains. Journal of Climate 4: 1103–1113.
Ross, M.S., P.L. Ruiz, J.P. Sah, and E.J. Hanan. 2009. Chilling damage in a changing climate in coastal landscapes of the subtropical zone: A case study from south Florida. Global Change Biology 15: 1817–1832.
Sherrod, C.L., and C. McMillan. 1981. Black mangrove, Avicennia germinans, in Texas: Past and present distribution. Contributions in Marine Science 24: 115–131.
Sherrod, C.L., and C. McMillan. 1985. The distributional history and ecology of mangrove vegetation along the northern Gulf of Mexico coastal region. Contributions in Marine Science 28: 129–140.
Simpson, L., T. Osborne, L. Duckett, and I. Feller. 2017. Carbon storages along a climate induced coastal wetland gradient. Wetlands 37: 1023–1035.
Snyder, C.M., L.C. Feher, M.J. Osland, C.M. Miller, A.R. Hughes, and K.L. Cummins. 2021. The distribution and structure of mangroves (Avicennia germinans and Rhizophora mangle) near a rapidly changing range limit in the northeastern Gulf of Mexico. Estuaries and Coasts 45: 181–195.
Stout, J. 1984. The ecology of irregularly flooded salt marhses of the northeastern Gulf of Mexico: a community profile. Washington, D.C., USA: U.S. Fish and Wildlife Service Biological Report 85 (7.1).
Vergés, A., P.D. Steinberg, M.E. Hay, A.G.B. Poore, A.H. Campbell, E. Ballesteros, K.L. Heck, D.J. Booth, M.A. Coleman, D.A. Feary, W. Figueira, T. Langlois, E.M. Marzinelli, T. Mizerek, P.J. Mumby, Y. Nakamura, M. Roughan, E. van Sebille, A. Sen Gupta, D.A. Smale, F. Tomas, T. Wernberg, and S.K. Wilson. 2014. The tropicalization of temperate marine ecosystems: Climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society b: Biological Sciences 281: 20140846.
Weaver, C.A., and A.R. Armitage. 2018. Nutrient enrichment shifts mangrove height distribution: Implications for coastal woody encroachment. PloS One 13: e0193617.
Yando, E.S., M.J. Osland, J.M. Willis, R.H. Day, K.W. Krauss, and M.W. Hester. 2016. Salt marsh-mangrove ecotones: Using structural gradients to investigate the effects of woody plant encroachment on plant-soil interactions and ecosystem carbon pools. Journal of Ecology 104: 1020–1031.
Yando, E.S., M.J. Osland, and M.W. Hester. 2018. Microspatial ecotone dynamics at a shifting range limit: Plant-soil variation across salt marsh-mangrove interfaces. Oecologia 187: 319–331.
Acknowledgements
We thank the many individuals that generously contributed leaf damage data following the 2018 and 2021 freeze events. MJO, LCF, RHD, GHA, and ASF were supported by the U.S. Geological Survey (USGS) Southeast Climate Adaptation Science Center, the USGS Climate R&D Program and/or the USGS Greater Everglades Priority Ecosystem Science Program. ARH and MJO were supported by a National Academy of Sciences, Engineering, and Medicine Gulf Research Program Healthy Ecosystems Grant. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
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Kaalstad, S., Osland, M.J., Devlin, D.J. et al. Temperature Thresholds for Leaf Damage from Two Extreme Freeze Events (2018 and 2021) Near the Northern Range Limit of Black Mangroves (Avicennia germinans) in Southeastern North America. Estuaries and Coasts 47, 292–300 (2024). https://doi.org/10.1007/s12237-023-01279-7
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DOI: https://doi.org/10.1007/s12237-023-01279-7