Drivers of greenhouse gas emissions from standing dead trees in ghost forests

Abstract

Coastal freshwater forested wetlands are rapidly transitioning from forest to marsh, leaving behind many standing dead trees (snags) in areas often called ‘ghost forests’. Snags can act as conduits for soil produced greenhouse gases (GHG) and can also be sources as they decompose. Thus, snags have the potential to contribute GHGs to the atmosphere, but emissions are not well understood. We assessed GHG emissions (carbon dioxide—CO2, methane—CH4, and nitrous oxide—N2O) from snags and soils in five ghost forests along a salinity gradient on the coast of North Carolina, USA. Mean (± SE) soil GHG fluxes (416 ± 44 mg CO2 m−2 h−1, 5.9 ± 1.9 mg CH4 m−2 h−1, and 0.1 ± 0.06 mg N2O m−2 h−1) were ~ 4 times greater than mean snag GHGs (116 ± 15 mg CO2 m−2 h−1, 0.3 ± 0.09 mg CH4 m−2 h−1, and 0.04 ± 0.009 mg N2O m−2 h−1). Hydrological conditions and salinity influenced soil GHG fluxes between the two field campaigns, but snags were less predictable and more variable. Snag and soil CO2/N2O fluxes were influenced by similar environmental parameters. The drivers for soil and snag CH4 however, were often not the same and at times oppositely correlated. Our results illustrate the need to further research into the drivers and importance of GHG emissions from snags, and the need to include tree stems into ecosystem GHG research.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author at request.

Code availability

The code used to process and analyzed data are available from the corresponding author at request.

References

  1. Ardón M, Morse JL, Colman BP, Bernhardt ES (2013) Drought-induced saltwater incursion leads to increased wetland nitrogen export. Glob Change Biol 19:2976–2985. https://doi.org/10.1111/gcb.12287

    Article  Google Scholar 

  2. Ardón M, Helton AM, Bernhardt ES (2018) Salinity effects on greenhouse gas emissions from wetland soils are contingent upon hydrologic setting: a microcosm experiment. Biogeochemistry 140:217–232. https://doi.org/10.1007/s10533-018-0486-2

    Article  Google Scholar 

  3. Barba J, Poyatos R, Vargas R (2019) Automated measurements of greenhouse gases fluxes from tree stems and soils: magnitudes, patterns and drivers. Sci Rep Nat Publ Group Lond 9:1–13. https://doi.org/10.1038/s41598-019-39663-8

    Article  Google Scholar 

  4. Carmichael MJ, Bernhardt ES, Bräuer SL, Smith WK (2014) The role of vegetation in methane flux to the atmosphere: should vegetation be included as a distinct category in the global methane budget? Biogeochemistry 119:1–24. https://doi.org/10.1007/s10533-014-9974-1

    Article  Google Scholar 

  5. Carmichael MJ, Helton AM, White JC, Smith WK (2017) Standing dead trees are a conduit for the atmospheric flux of CH4 and CO2 from wetlands. Wetlands. https://doi.org/10.1007/s13157-017-0963-8

    Article  Google Scholar 

  6. Chapin SF, Matson PA (2011) Principles of terrestrial ecosystem ecology. Springer, New York

    Book  Google Scholar 

  7. Corbett DR, Vance D, Letrick E et al (2007) Decadal-scale sediment dynamics and environmental change in the albemarle estuarine system, North Carolina. Estuar Coast Shelf Sci 71:717–729. https://doi.org/10.1016/j.ecss.2006.09.024

    Article  Google Scholar 

  8. Covey KR, Megonigal JP (2019) Methane production and emissions in trees and forests. New Phytol 222:35–51. https://doi.org/10.1111/nph.15624

    Article  Google Scholar 

  9. Covey KR, Wood SA, Warren RJ et al (2012) Elevated methane concentrations in trees of an upland forest. Geophys Res Lett 39:L15705. https://doi.org/10.1029/2012GL052361

    Article  Google Scholar 

  10. Gauci V, Gowing DJG, Hornibrook ERC et al (2010) Woody stem methane emission in mature wetland alder trees. Atmos Environ 44:2157–2160. https://doi.org/10.1016/j.atmosenv.2010.02.034

    Article  Google Scholar 

  11. Helton A, Bernhardt E, Fedders A (2014) Biogeochemical regime shifts in coastal landscapes: the contrasting effects of saltwater incursion and agricultural pollution on greenhouse gas emissions from a freshwater wetland. Biogeochemistry 120:133–147. https://doi.org/10.1007/s10533-014-9986-x

    Article  Google Scholar 

  12. Helton AM, Ardón M, Bernhardt ES (2019) Hydrologic context alters greenhouse gas feedbacks of coastal wetland salinization. Ecosystems 22:1108–1125. https://doi.org/10.1007/s10021-018-0325-2

    Article  Google Scholar 

  13. Hornibrook ERC, Longstaffe FJ, Fyfe WS (1997) Spatial distribution of microbial methane production pathways in temperate zone wetland soils: Stable carbon and hydrogen isotope evidence. Geochim Cosmochim Acta 61:745–753. https://doi.org/10.1016/S0016-7037(96)00368-7

    Article  Google Scholar 

  14. Huntington JL, Hegewisch KC, Daudert B et al (2017) Climate engine: cloud computing and visualization of climate and remote sensing data for advanced natural resource monitoring and process understanding. Bull Am Meteorol Soc 98:2397–2410. https://doi.org/10.1175/BAMS-D-15-00324.1

    Article  Google Scholar 

  15. Hutchinson GL, Mosier AR (1981) Improved soil cover method for field measurement of nitrous oxide fluxes. Soil Sci Soc Am J 45:311–316. https://doi.org/10.2136/sssaj1981.03615995004500020017x

    Article  Google Scholar 

  16. Jeffrey LC, Reithmaier G, Sippo JZ et al (2019) Are methane emissions from mangrove stems a cryptic carbon loss pathway? Insights from a catastrophic forest mortality. New Phytol 224:146–154. https://doi.org/10.1111/nph.15995

    Article  Google Scholar 

  17. Jeffrey LC, Maher DT, Tait DR et al (2021) Isotopic evidence for axial tree stem methane oxidation within subtropical lowland forests. New Phytol. https://doi.org/10.1111/nph.17343

    Article  Google Scholar 

  18. Kirwan ML, Gedan KB (2019) Sea-level driven land conversion and the formation of ghost forests. Nat Clim Change 9:450–457. https://doi.org/10.1038/s41558-019-0488-7

    Article  Google Scholar 

  19. Kirwan ML, Megonigal JP (2013) Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53–60. https://doi.org/10.1038/nature12856

    Article  Google Scholar 

  20. Kohl L, Koskinen M, Rissanen K et al (2019) Technical note: interferences of volatile organic compounds (VOCs) on methane concentration measurements. Biogeosciences 16:3319–3332. https://doi.org/10.5194/bg-16-3319-2019

    Article  Google Scholar 

  21. Kopp RE, Hay CC, Little CM, Mitrovica JX (2015) Geographic variability of sea-level change. Curr Clim Change Rep 1:192–204. https://doi.org/10.1007/s40641-015-0015-5

    Article  Google Scholar 

  22. Krauss KW, Duberstein JA, Doyle TW et al (2009) Site condition, structure, and growth of baldcypress along tidal/non-tidal salinity gradients. Wetlands 29:505–519. https://doi.org/10.1672/08-77.1

    Article  Google Scholar 

  23. Krauss KW, Noe GB, Duberstein JA et al (2018) The role of the upper tidal estuary in wetland blue carbon storage and flux. Glob Biogeochem Cycles. https://doi.org/10.1029/2018GB005897

    Article  Google Scholar 

  24. Machacova K, Papen H, Kreuzwieser J, Rennenberg H (2013) Inundation strongly stimulates nitrous oxide emissions from stems of the upland tree fagus sylvatica and the riparian tree Alnus glutinosa. Plant Soil 364:287–301. https://doi.org/10.1007/s11104-012-1359-4

    Article  Google Scholar 

  25. Machacova K, Bäck J, Vanhatalo A et al (2016) Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci Rep Nat Publ Group Lond. https://doi.org/10.1038/srep23410

    Article  Google Scholar 

  26. Machacova K, Vainio E, Urban O, Pihlatie M (2019) Seasonal dynamics of stem N2O exchange follow the physiological activity of boreal trees. Nat Commun. https://doi.org/10.1038/s41467-019-12976-y

    Article  Google Scholar 

  27. Machacova K, Borak L, Agyei T et al (2021) Trees as net sinks for methane (CH4) and nitrous oxide (N2O) in the lowland tropical rain forest on volcanic Réunion Island. New Phytol 229:1983–1994. https://doi.org/10.1111/nph.17002

    Article  Google Scholar 

  28. Maier M, Machacova K, Lang F et al (2018) Combining soil and tree-stem flux measurements and soil gas profiles to understand CH4 pathways in fagus sylvatica forests. J Plant Nutr Soil Sci 181:31–35. https://doi.org/10.1002/jpln.201600405

    Article  Google Scholar 

  29. Manda AK, Giuliano AS, Allen TR (2014) Influence of artificial channels on the source and extent of saline water intrusion in the wind tide dominated wetlands of the southern Albemarle estuarine system (USA). Environ Earth Sci 71:4409–4419. https://doi.org/10.1007/s12665-013-2834-9

    Article  Google Scholar 

  30. Megonigal JP, Brewer PE, Knee KL (2020) Radon as a natural tracer of gas transport through trees. New Phytol 225:1470–1475. https://doi.org/10.1111/nph.16292

    Article  Google Scholar 

  31. Minick KJ, Mitra B, Li X et al (2019) Water table drawdown alters soil and microbial carbon pool size and isotope composition in coastal freshwater forested wetlands. Front For Glob Change. https://doi.org/10.3389/ffgc.2019.00007

    Article  Google Scholar 

  32. Moldaschl E, Kitzler B, Machacova K et al (2021) Stem CH4 and N2O fluxes of fraxinus excelsior and populus alba trees along a flooding gradient. Plant Soil. https://doi.org/10.1007/s11104-020-04818-4

    Article  Google Scholar 

  33. Moorhead KK, Brinson MM (1995) Response of wetlands to rising sea level in the lower coastal plain of North Carolina. Ecol Appl 5:261–271. https://doi.org/10.2307/1942068

    Article  Google Scholar 

  34. Morse JL, Ardón M, Bernhardt ES (2012) Using environmental variables and soil processes to forecast denitrification potential and nitrous oxide fluxes in coastal plain wetlands across different land uses. J Geophys Res Biogeosci. https://doi.org/10.1029/2011JG001923

    Article  Google Scholar 

  35. Neubauer SC (2013) Ecosystem responses of a tidal freshwater marsh experiencing saltwater intrusion and altered hydrology. Estuaries Coasts 36:491–507. https://doi.org/10.1007/s12237-011-9455-x

    Article  Google Scholar 

  36. Neubauer SC, Megonigal JP (2015) Moving beyond global warming potentials to quantify the climatic role of ecosystems. Ecosystems 18:1000–1013. https://doi.org/10.1007/s10021-015-9879-4

    Article  Google Scholar 

  37. Pangala SR, Moore S, Hornibrook ERC, Gauci V (2013) Trees are major conduits for methane egress from tropical forested wetlands. New Phytol 197:524–531. https://doi.org/10.1111/nph.12031

    Article  Google Scholar 

  38. Pangala SR, J. GD, Hornibrook ERC, et al (2015) The contribution of trees to ecosystem methane emissions in a temperate forested wetland. Glob Change Biol 21:2642–2654. https://doi.org/10.1111/gcb.12891

    Article  Google Scholar 

  39. Pangala SR, Enrich-Prast A, Basso LS et al (2017) Large emissions from floodplain trees close the Amazon methane budget. Nature 552:230–234. https://doi.org/10.1038/nature24639

    Article  Google Scholar 

  40. Pedersen AR, Petersen SO, Schelde K (2010) A comprehensive approach to soil-atmosphere trace-gas flux estimation with static chambers. Eur J Soil Sci 61:888–902. https://doi.org/10.1111/j.1365-2389.2010.01291.x

    Article  Google Scholar 

  41. Pitz S, Megonigal PJ (2017) Temperate forest methane sink diminished by tree emissions. New Phytol 214:1432–1439. https://doi.org/10.1111/nph.14559

    Article  Google Scholar 

  42. Pitz SL, Megonigal JP, Chang C-H, Szlavecz K (2018) Methane fluxes from tree stems and soils along a habitat gradient. Biogeochemistry 137:307–320. https://doi.org/10.1007/s10533-017-0400-3

    Article  Google Scholar 

  43. Plain C, Ndiaye F-K, Bonnaud P et al (2019) Impact of vegetation on the methane budget of a temperate forest. New Phytol 221:1447–1456. https://doi.org/10.1111/nph.15452

    Article  Google Scholar 

  44. Poffenbarger HJ, Needelman BA, Megonigal JP (2011) Salinity influence on methane emissions from tidal marshes. Wetlands 31:831–842. https://doi.org/10.1007/s13157-011-0197-0

    Article  Google Scholar 

  45. Pohlert T (2014) The pairwise multiple comparison of mean ranks Package (PMCMR). R Package 27(2019):9

    Google Scholar 

  46. Poulter B, Christensen NL, Halpin PN (2006) Carbon emissions from a temperate peat fire and its relevance to interannual variability of trace atmospheric greenhouse gases. J Geophys Res Atmos. https://doi.org/10.1029/2005JD006455

    Article  Google Scholar 

  47. Prendergast-Miller MT, Baggs EM, Johnson D (2011) Nitrous oxide production by the ectomycorrhizal fungi paxillus involutus and tylospora fibrillosa. FEMS Microbiol Lett 316:31–35. https://doi.org/10.1111/j.1574-6968.2010.02187.x

    Article  Google Scholar 

  48. Pulliam WM (1992) Methane emissions from cypress knees in a southeastern floodplain swamp. Oecologia 91:126–128. https://doi.org/10.1007/BF00317250

    Article  Google Scholar 

  49. R Core Team (2020) R: a language and environment for statistical computing. Version 3.5.1. Vienna, Austria. http://www.R-project.org/

  50. Reddy KR, DeLaune RD (2008) Biogeochemistry of wetlands science and applications. CRC Press, Boca Raton

    Book  Google Scholar 

  51. Riggs SR, Cleary WJ, Snyder SW (1995) Influence of inherited geologic framework on barrier shoreface morphology and dynamics. Mar Geol 126:213–234. https://doi.org/10.1016/0025-3227(95)00079-E

    Article  Google Scholar 

  52. Siegenthaler A, Welch B, Pangala SR et al (2016) Semi-rigid chambers for methane gas flux measurements on tree stems. Biogeosciences 13:1197–1207

    Article  Google Scholar 

  53. Sjögersten S, Siegenthaler A, Lopez OR et al (2019) Methane emissions from tree stems in neotropical peatlands. New Phytol. https://doi.org/10.1111/nph.16178

    Article  Google Scholar 

  54. Smart LS, Taillie PJ, Poulter B et al (2020) Aboveground carbon loss associated with the spread of ghost forests as sea levels rise. Environ Res Lett 15:104028. https://doi.org/10.1088/1748-9326/aba136

    Article  Google Scholar 

  55. Sweet WV, Dusek G, Obeysekera J, Marra JJ (2018) Patterns and projections of high tide flooding along the U.S. coastline using a common impact threshold. NOAA, Washington, DC

    Google Scholar 

  56. Taillie PJ, Moorman CE, Poulter B et al (2019) Decadal-scale vegetation change driven by salinity at leading edge of rising sea level. Ecosystems 22:1918–1930. https://doi.org/10.1007/s10021-019-00382-w

    Article  Google Scholar 

  57. Terazawa K, Ishizuka S, Sakata T et al (2007) Methane emissions from stems of Fraxinus mandshurica var. japonica trees in a floodplain forest. Soil Biol Biochem 39:2689–2692. https://doi.org/10.1016/j.soilbio.2007.05.013

    Article  Google Scholar 

  58. Terazawa K, Yamada K, Ohno Y et al (2015) Spatial and temporal variability in methane emissions from tree stems of Fraxinus mandshurica in a cool-temperate floodplain forest. Biogeochem 123:349–362. https://doi.org/10.1007/s10533-015-0070-y

    Article  Google Scholar 

  59. Ury EA, Yang X, Wright JP, Bernhardt ES (2021) Rapid deforestation of a coastal landscape driven by sea level rise and extreme events. Ecol Appl n/a:e2339. https://doi.org/10.1002/eap.2339

    Article  Google Scholar 

  60. Wang Z-P, Gu Q, Deng F-D et al (2016) Methane emissions from the trunks of living trees on upland soils. New Phytol 211:429–439. https://doi.org/10.1111/nph.13909

    Article  Google Scholar 

  61. Wang Z-P, Han S-J, Li H-L et al (2017) Methane production explained largely by water content in the heartwood of living trees in upland forests. J Geophys Res Biogeosci 122:2479–2489. https://doi.org/10.1002/2017JG003991

    Article  Google Scholar 

  62. Warner DL, Villarreal S, McWilliams K et al (2017) Carbon dioxide and methane fluxes from tree stems, coarse woody debris, and soils in an upland temperate forest. Ecosystems 20:1205–1216. https://doi.org/10.1007/s10021-016-0106-8

    Article  Google Scholar 

  63. Welch B, Gauci V, Sayer EJ (2019) Tree stem bases are sources of CH4 and N2O in a tropical forest on upland soil during the dry to wet season transition. Glob Change Biol 25:361–372. https://doi.org/10.1111/gcb.14498

    Article  Google Scholar 

  64. Weston NB, Vile MA, Neubauer SC, Velinsky DJ (2011) Accelerated microbial organic matter mineralization following salt-water intrusion into tidal freshwater marsh soils. Biogeochemistry 102:135–151. https://doi.org/10.1007/s10533-010-9427-4

    Article  Google Scholar 

  65. Wilson BJ, Servais S, Charles SP et al (2018) Declines in plant productivity drive carbon loss from brackish coastal wetland mesocosms exposed to saltwater intrusion. Estuaries Coasts. https://doi.org/10.1007/s12237-018-0438-z

    Article  Google Scholar 

  66. Winton RS, Richardson CJ (2016) A cost-effective method for reducing soil disturbance-induced errors in static chamber measurement of wetland methane emissions. Wetl Ecol Manag 24:419–425. https://doi.org/10.1007/s11273-015-9468-5

    Article  Google Scholar 

  67. Winton RS, Richardson CJ (2017) Top-down control of methane emission and nitrogen cycling by waterfowl. Ecology 98:265–277. https://doi.org/10.1002/ecy.1640

    Article  Google Scholar 

  68. Winton RS, Moorman M, Richardson CJ (2016) Waterfowl impoundments as sources of nitrogen pollution. Water Air Soil Pollut 227:390. https://doi.org/10.1007/s11270-016-3082-x

    Article  Google Scholar 

  69. Wobbrock JO, Findlater L, Gergle D, Higgins JJ (2011) The aligned rank transform for nonparametric factorial analyses using only anova procedures. In: Proceedings of the 2011 Annual Conference on Human Factors in Computing Systems—CHI ’11. ACM Press, Vancouver, BC, Canada, p 143

  70. Zhang L, Shao H, Wang B et al (2019) Effects of nitrogen and phosphorus on the production of carbon dioxide and nitrous oxide in salt-affected soils under different vegetation communities. Atmos Environ 204:78–88. https://doi.org/10.1016/j.atmosenv.2019.02.024

    Article  Google Scholar 

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Acknowledgements

We thank Destinee Parson, Colin Dail, Cam Phipps, Margaret Maynardie, Kelsey Morton, and Steve Anderson for field and lab assistance. We are also thankful for the Ardón lab, Dr. Jodi Forrester, and Dr. Mary Jane Carmichael for feedback on this manuscript. This work was funded by National Science Foundation (DEB1713592) as well as North Carolina Sea Grant/SpaceGrant Fellowship (2019).

Funding

This work was funded by National Science Foundation (DEB1713592) as well as North Carolina Sea Grant/SpaceGrant Fellowship (2019).

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All authors conceived the study and research methods. Material preparation, data collection and data analysis were performed by MM. The first draft of the manuscript was written by MM with feedback and comments from MA. All authors reviewed, edited, and approved the manuscript to its final form.

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Correspondence to Melinda Martinez.

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Martinez, M., Ardón, M. Drivers of greenhouse gas emissions from standing dead trees in ghost forests. Biogeochemistry 154, 471–488 (2021). https://doi.org/10.1007/s10533-021-00797-5

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Keywords

  • Carbon dioxide (CO2)
  • Methane (CH4)
  • Nitrous oxide (N2O)
  • Freshwater
  • Wetlands
  • Ghost forests