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Nitrogen Addition Increases Freeze Resistance in Black Mangrove (Avicennia germinans) Shrubs in a Temperate-Tropical Ecotone

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Abstract

Low temperature stress is the primary factor determining the latitudinal limits of tropical plants. As the climate warms, tropical species are migrating poleward, displacing native species and modifying ecosystem structure and function. Changes are particularly evident along latitudinal gradients with the highest velocity of change occurring in wetlands. In coastal wetlands, saltmarshes dominate at latitudes above 30°, whereas mangroves occur mostly in the tropics because most species are intolerant of freezing temperatures, but others, like Avicennia germinans (black mangrove), do tolerate freezing temperatures. In response to a warmer climate and fewer killing freezes, mangroves are currently expanding into saltmarshes. However, the speed of the transition from saltmarsh to mangrove can also be modified by extreme events and nutrient subsidies. In a fertilization experiment along the Atlantic coast of North America, we found that nitrogen addition altered plant traits in Avicennia, which increased their resistance to freezing temperatures. This trait shift resulted in negligible freeze effects during a January 2018 extreme freeze event compared to unfertilized plants, which lost more than 80% of the leaves and more than 40% of the wood in their canopies. The freeze-killed litter from unfertilized plants provided a nutrient pulse that influenced recovery, growth and mangrove cover for three years following the freeze. Nutrient enrichment and recovery from the freeze effects led to increased growth and structural complexity of the mangrove canopy, which further enhanced freeze tolerance, shrub growth form and the ability of Avicennia to displace the saltmarsh in the temperate–tropical ecotone.

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All data available at Smithsonian Figshare https://doi.org/10.25573/serc.21206261.v1.

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Acknowledgements

Funding provided by NSF (Macrosystems Biology 1065821, DEB 1655659, Postdoctoral Fellowship in Biology 1308565) and NASA (Climate and Biological Response Program NNX11AO94G). The Guana Tolomato Matanzas NERR provided research permits; the GTMNERR staff aided with field logistics and project support.

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Author notes

  1. ICF conceived the study, established the fertilization experiment, performed research, drafted the paper and acquired funding. SKC, EMD, JAL, CEL, LTS, NGD and TZO performed research, collected data and contributed to writing the paper. SKC and EMD acquired funding. EMD analyzed all the data. ACS developed the method for glycine betaine analysis and contributed to writing the paper.

Authors and Affiliations

  1. Smithsonian Environmental Research Center, Smithsonian Institution, 647 Contees Wharf Road, Edgewater, Maryland, 21037, USA

    Ilka C. Feller

  2. Department 8 Service Center Studies 01062, Dresden Technische Universität, Hauptgebäude (Altbau), 1. Floor, Room 23; Pienner Straße 8, Postfach 1117, Tharandt, 01737, Germany

    Uta Berger

  3. Department of Biology, Villanova University, Villanova, Pennsylvania, 19085, USA

    Samantha K. Chapman & J. Adam Langley

  4. Department of Biological, Physical and Health Sciences, Roosevelt University, 430 S. Michigan Ave., Chicago, Illinois, 60605, USA

    Emily M. Dangremond

  5. Guana Tolomato Matanzas National Estuarine Research Reserve, 505 Guana River Rd., Ponte Vedra, Florida, 32082, USA

    Nicole G. Dix

  6. School of Biological Sciences, Goddard Building, The University of Queensland, Brisbane, Queensland, 4072, Australia

    Catherine E. Lovelock

  7. Whitney Laboratory, University of Florida, 9505 Ocean Shore Blvd, St. Augustine, Gainesville, Florida, 32080, USA

    Todd Z. Osborne

  8. Department of Biology, St. Leo University, 33701 State Rd. 52, St Leo, Florida, 33574, USA

    Audrey C. Shor

  9. Florida Oceanographic Society, 890 Northeast Ocean Blvd, Stuart, Florida, 34996, USA

    Loraé T. Simpson

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  1. Ilka C. Feller
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  2. Uta Berger
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Feller, I.C., Berger, U., Chapman, S.K. et al. Nitrogen Addition Increases Freeze Resistance in Black Mangrove (Avicennia germinans) Shrubs in a Temperate-Tropical Ecotone. Ecosystems 26, 800–814 (2023). https://doi.org/10.1007/s10021-022-00796-z

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