Skip to main content

Advertisement

Log in

Microclimate Influences Mangrove Freeze Damage: Implications for Range Expansion in Response to Changing Macroclimate

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

In response to warming winter air temperatures, freeze-sensitive mangrove forests are expected to expand at the expense of freeze-tolerant salt marshes. To better anticipate and prepare for mangrove range expansion, there is a need to advance understanding of the modulating role of microclimate. Here, we synthesized hypotheses regarding the effects of microclimatic variation on temperature gradients and mangrove freeze damage. Temperature data from the literature and from temperature loggers were used to quantify ecologically relevant temperature gradients. Then, literature-derived mangrove freeze damage data were used to quantify the ecological effects of these temperature gradients. Six microclimatic factors are described that produce air temperature gradients that modulate mangrove responses to winter temperature extremes: (1) distance from the ocean; (2) distance from wind buffers; (3) mangrove canopy cover; (4) height above the soil surface; (5) local slope concavity; and (6) tidal inundation. Variation in these factors produces local temperature differences that range from 2 to 14 °C, with concomitant effects on horizontal and vertical patterns of biological damage from freezing. Collectively, our results elucidate the influence of microclimate on spatial patterns of biological damage and mortality due to winter temperature extremes. As mangrove ranges expand in response to climate change, we anticipate that microclimatic variation will produce adverse environments where mangrove expansion is prohibited as well as expansion hot spots where mangroves are protected. Subsequent expansion into newly available habitat will occur from protection zones, and microclimatic gradients may even produce positive feedback cycles that ultimately accelerate the rate of range expansion in response to warming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ackerly, D.D., S.R. Loarie, W.K. Cornwell, S.B. Weiss, H. Hamilton, R. Branciforte, and N.J.B. Kraft. 2010. The geography of climate change: Implications for conservation biogeography. Diversity and Distributions 16 (3): 476–487.

    Article  Google Scholar 

  • Boon, P.I. 2017. Are mangroves in Victoria (south-eastern Australia) already responding to climate change? Marine and Freshwater Research 68 (12): 2366. https://doi.org/10.1071/MF17015.

    Article  Google Scholar 

  • Boucek, R.E., E.E. Gaiser, H. Liu, and J.S. Rehage. 2016. A review of subtropical community resistance and resilience to extreme cold spells. Ecosphere 7: Article e01455.

    Article  Google Scholar 

  • Boucek, R.E., M.R. Heithaus, R. Santos, P. Stevens, and J.S. Rehage. 2017. Can animal habitat use patterns influence their vulnerability to extreme climate events? An estuarine sportfish case study. Global Change Biology 23 (10): 4045–4057.

    Article  Google Scholar 

  • Box, E.O., D.W. Crumpacker, and E.D. Hardin. 1993. A climatic model for location of plant species in Florida, USA. Journal of Biogeography 20 (6): 629–644.

    Article  Google Scholar 

  • 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 (2): 723–727.

    Article  CAS  Google Scholar 

  • 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 (5): 1928–1938.

    Article  Google Scholar 

  • 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 (8): 925–935.

    Article  Google Scholar 

  • Chen, L., W. Wang, Q.Q. Li, Y. Zhang, S. Yang, M.J. Osland, J. Huang, and C. Peng. 2017. Mangrove species’ responses to winter air temperature extremes in China. Ecosphere 8: Article e01865.

    Article  Google Scholar 

  • Coldren, G.A., and C.E. Proffitt. 2017. Mangrove seedling freeze tolerance depends on salt marsh presence, species, salinity, and age. Hydrobiologia 803 (1): 159–171.

    Article  CAS  Google Scholar 

  • 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 (10): 1332–1340.

    Article  Google Scholar 

  • Daly, C., E.H. Helmer, and M. Quiñones. 2003. Mapping the climate of Puerto Rico, Vieques and Culebra. International Journal of Climatology 23 (11): 1359–1381.

    Article  Google Scholar 

  • Daly, C., M. Halbleib, J.I. Smith, W.P. Gibson, M.K. Doggett, G.H. Taylor, J. Curtis, and P.P. Pasteris. 2008. Physiographically sensitive mapping of climatological temperature and precipitation across the conterminous United States. International Journal of Climatology 28 (15): 2031–2064.

    Article  Google Scholar 

  • Daly, C., M.P. Widrlechner, M.D. Halbleib, J.I. Smith, and W.P. Gibson. 2012. Development of a new USDA plant hardiness zone map for the United States. Journal of Applied Meteorology and Climatology 51 (2): 242–264.

    Article  Google Scholar 

  • Davis, J.H. 1940. The ecology and geologic role of mangroves in Florida. Carnegie Institute of Washington Publications. Papers from Tortugas Laboratory 32: 303–412.

    Google Scholar 

  • de Lange, W.P., and P.J. De Lange. 1994. An appraisal of factors controlling the latitudinal distribution of mangrove (Avicennia marina var. resinifera) in New Zealand. Journal of Coastal Research 10: 539–548.

    Google Scholar 

  • Devaney, J.L., M. Lehmann, I.C. Feller, and J.D. Parker. 2017. Mangrove microclimates alter seedling dynamics at the range edge. Ecology 98 (10): 2513–2520.

    Article  Google Scholar 

  • D'Odorico, P., Y. He, S. Collins, S.F.J. De Wekker, V. Engel, and J.D. Fuentes. 2013. Vegetation–microclimate feedbacks in woodland–grassland ecotones. Global Ecology and Biogeography 22 (4): 364–379.

    Article  Google Scholar 

  • 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: article e01956.

    Article  Google Scholar 

  • Fridley, J.D. 2009. Downscaling climate over complex terrain: High finescale (< 1000 m) spatial variation of near-ground temperatures in a montane forested landscape (Great Smoky Mountains). Journal of Applied Meteorology and Climatology 48 (5): 1033–1049.

    Article  Google Scholar 

  • 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 (2): 142–147.

    Article  Google Scholar 

  • Geiger, R., R.H. Aron, and P. Todhunter. 2012. The climate near the ground. Cambridge: Harvard University Press.

    Google Scholar 

  • Greller, A.M. 1980. Correlation of some climate statistics with distribution of broadleaved forest zones in Florida, USA. Bulletin of the Torrey Botanical Club 107 (2): 189–219.

    Article  Google Scholar 

  • Guo, H., C. Weaver, S.P. Charles, A. Whitt, S. Dastidar, P. D'Odorico, J.D. Fuentes, J.S. Kominoski, A.R. Armitage, and S.C. Pennings. 2017. Coastal regime shifts: Rapid responses of coastal wetlands to changes in mangrove cover. Ecology 98 (3): 762–772.

    Article  Google Scholar 

  • Hannah, L., L. Flint, A.D. Syphard, M.A. Moritz, L.B. Buckley, and I.M. McCullough. 2014. Fine-grain modeling of species’ response to climate change: Holdouts, stepping-stones, and microrefugia. Trends in Ecology & Evolution 29 (7): 390–397.

    Article  Google Scholar 

  • Holdridge, L.R. 1967. Life zone ecology. San Jose: Tropical Science Center.

    Google Scholar 

  • Jiang, J., D.L. DeAngelis, S.-Y. Teh, K.W. Krauss, H. Wang, H. Li, T.J. Smith, and H.-L. Koh. 2016. Defining the next generation modeling of coastal ecotone dynamics in response to global change. Ecological Modelling 326: 168–176.

    Article  Google Scholar 

  • Krauss, K.W., C.E. Lovelock, K.L. McKee, L. López-Hoffman, S.M.L. Ewe, and W.P. Sousa. 2008. Environmental drivers in mangrove establishment and early development: A review. Aquatic Botany 89 (2): 105–127.

    Article  Google Scholar 

  • Langston, A.K., D.A. Kaplan, and C. Angelini. 2017. Predation restricts black mangrove (Avicennia germinans) colonization at its northern range limit along Florida’s Gulf Coast. Hydrobiologia 803 (1): 317–331.

    Article  Google Scholar 

  • Liu, K., L. Liu, H. Liu, X. Li, and S. Wang. 2014. Exploring the effects of biophysical parameters on the spatial pattern of rare cold damage to mangrove forests. Remote Sensing of Environment 150: 20–33.

    Article  Google Scholar 

  • 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: Springer.

    Chapter  Google Scholar 

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

    Google Scholar 

  • Maclean, I., J.J. Hopkins, J. Bennie, C.R. Lawson, and R.J. Wilson. 2015. Microclimates buffer the responses of plant communities to climate change. Global Ecology and Biogeography 24 (11): 1340–1350.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Markley, J.L., C. McMillan, and G.A. Thompson Jr. 1982. Latitidinal differentiation in response to chilling temperatures among populations of three mangroves, Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle, from the western tropical Atlantic and Pacific Panama. Canadian Journal of Botany 60 (12): 2704–2715.

    Article  CAS  Google Scholar 

  • Matich, P., and M.R. Heithaus. 2012. Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas. Marine Ecology Progress Series 447: 165–178.

    Article  Google Scholar 

  • McAfee, D., W.A. O'connor, and M.J. Bishop. 2017. Fast-growing oysters show reduced capacity to provide a thermal refuge to intertidal biodiversity at high temperatures. Journal of Animal Ecology 86 (6): 1352–1362.

    Article  Google Scholar 

  • McLaughlin, B.C., D.D. Ackerly, P.Z. Klos, J. Natali, T.E. Dawson, and S.E. Thompson. 2017. Hydrologic refugia, plants, and climate change. Global Change Biology 23 (8): 2941–2961.

    Article  Google Scholar 

  • Olmsted, I., H. Dunevitz, and W.J. Platt. 1993. Effects of freezes on tropical trees in Everglades National Park Florida, USA. Tropical Ecology 34: 17–34.

    Google Scholar 

  • 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: Article 160.

    Article  Google Scholar 

  • Osland, M.J., R.H. Day, C.T. Hall, M.D. Brumfield, J.L. Dugas, and W.R. Jones. 2017a. Mangrove expansion and contraction at a poleward range limit: Climate extremes and land-ocean temperature gradients. Ecology 98 (1): 125–137.

    Article  Google Scholar 

  • Osland, M.J., L.C. Feher, K.T. Griffith, K.C. Cavanaugh, N.M. Enwright, R.H. Day, C.L. Stagg, K.W. Krauss, R.J. Howard, J.B. Grace, and K. Rogers. 2017b. Climatic controls on the global distribution, abundance, and species richness of mangrove forests. Ecological Monographs 87 (2): 341–359.

    Article  Google Scholar 

  • Osland, M.J., A.M. Hartmann, R.H. Day, C.T. Hall, and L.C. Feher. 2019. Microclimate influences mangrove freeze damage: Implications for range expansion in response to changing macroclimate: U.S. Geological Survey data release. https://doi.org/10.5066/P9YWSV4O.

    Book  Google Scholar 

  • 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 (4): 824–830.

    Article  Google Scholar 

  • Pickens, C.N., T.M. Sloey, and M.W. Hester. 2018. Influence of salt marsh canopy on black mangrove (Avicennia germinans) survival and establishment at its northern latitudinal limit. Hydrobiologia: 1–14. https://doi.org/10.1007/s10750-018-3730-9.

  • Potter, K.A., H. Arthur Woods, and S. Pincebourde. 2013. Microclimatic challenges in global change biology. Global Change Biology 19 (10): 2932–2939.

    Article  Google Scholar 

  • Quisthoudt, K., N. Schmitz, C.F. Randin, F. Dahdouh-Guebas, E.M.R. Robert, and N. Koedam. 2012. Temperature variation among mangrove latitudinal range limits worldwide. Trees 26 (6): 1919–1931.

    Article  Google Scholar 

  • Rehage, J., J. Blanchard, R. Boucek, J. Lorenz, and M. Robinson. 2016. Knocking back invasions: Variable resistance and resilience to multiple cold spells in native vs. nonnative fishes. Ecosphere 7: Article e01268.

    Article  Google Scholar 

  • 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 (7): 1817–1832.

    Article  Google Scholar 

  • Saintilan, N., N.C. Wilson, K. Rogers, A. Rajkaran, and K.W. Krauss. 2014. Mangrove expansion and salt marsh decline at mangrove poleward limits. Global Change Biology 20 (1): 147–157.

    Article  Google Scholar 

  • Sherrod, C.L., and C. McMillan. 1981. Black mangrove, Avicennia germinans, in Texas: Past and present distribution. Contributions in Marine Science 24: 115–131.

    Google Scholar 

  • 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.

    Google Scholar 

  • Stevens, P.W., S.L. Fox, and C.L. Montague. 2006. The interplay between mangroves and saltmarshes at the transition between temperate and subtropical climate in Florida. Wetlands Ecology and Management 14 (5): 435–444.

    Article  Google Scholar 

  • Stevens, P.W., D.A. Blewett, R.E. Boucek, J.S. Rehage, B.L. Winner, J.M. Young, J.A. Whittington, and R. Paperno. 2016. Resilience of a tropical sport fish population to a severe cold event varies across five estuaries in southern Florida. Ecosphere 7: Article e01400.

    Article  Google Scholar 

  • Stuart, S.A., B. Choat, K.C. Martin, N.M. Holbrook, and M.C. Ball. 2007. The role of freezing in setting the latitudinal limits of mangrove forests. New Phytologist 173 (3): 576–583.

    Article  CAS  Google Scholar 

  • Suggitt, A.J., P.K. Gillingham, J.K. Hill, B. Huntley, W.E. Kunin, D.B. Roy, and C.D. Thomas. 2011. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120 (1): 1–8.

    Article  Google Scholar 

  • Turlure, C., J. Choutt, M. Baguette, and H. Van Dyck. 2010. Microclimatic buffering and resource-based habitat in a glacial relict butterfly: Significance for conservation under climate change. Global Change Biology 16: 1883–1893.

    Article  Google Scholar 

  • Wang, W., S. You, Y. Wang, L. Huang, and M. Wang. 2011. Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant and Soil 342 (1-2): 105–115.

    Article  CAS  Google Scholar 

  • Ward, R.D., D.A. Friess, R.H. Day, and R.A. MacKenzie. 2016. Impacts of climate change on mangrove ecosystems: A region by region overview. Ecosystem Health and Sustainability 2 (4): e01211.

    Article  Google Scholar 

  • Weaver, C.A., and A.R. Armitage. 2018. Nutrient enrichment shifts mangrove height distribution: Implications for coastal woody encroachment. PloS One 13: article e0193617.

    Article  CAS  Google Scholar 

  • West, R.C. 1977. Tidal salt-marsh and mangal formations of Middle and South America. In Ecosystems of the world. 1. Wet coastal ecosystems, ed. V.J. Chapman, 193–213. Amsterdam: Elsevier.

    Google Scholar 

  • Whittaker, R.H. 1970. Communities and ecosystems. New York: The McMillan Company.

    Google Scholar 

  • 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 (4): 1020–1031.

    Article  CAS  Google Scholar 

  • Zhang, K., B. Thapa, M. Ross, and D. Gann. 2016. Remote sensing of seasonal changes and disturbances in mangrove forest: A case study from South Florida. Ecosphere 7: Article e01366.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Don Cahoon and two anonymous reviewers for their comments on a previous version of this manuscript. This research was partially supported by the USGS Ecosystems Mission Area, USGS Land Change Science Program, and the USGS Greater Everglades Priority Ecosystems Science Program. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government. We thank the ConocoPhillips Company/Louisiana Land and Exploration Company LLC for permission to conduct research on their land.

Author information

Authors and Affiliations

Authors

Contributions

MJO conceived the study. AMH compiled the literature-derived data with guidance from MJO. CTH, LCF, MJO, and RHD collected the field-derived temperature data. AMH and MJO analyzed the data and developed the figures. MJO wrote the first manuscript draft. All authors contributed to subsequent manuscript drafts and gave final approval for publication. The field-derived temperature data are available via Osland et al. (2019).

Corresponding author

Correspondence to Michael J. Osland.

Additional information

Communicated by Dan Friess

Electronic Supplementary Material

ESM 1

(DOCX 330 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Osland, M.J., Hartmann, A.M., Day, R.H. et al. Microclimate Influences Mangrove Freeze Damage: Implications for Range Expansion in Response to Changing Macroclimate. Estuaries and Coasts 42, 1084–1096 (2019). https://doi.org/10.1007/s12237-019-00533-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-019-00533-1

Keywords

Navigation