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Tree stem methane emissions from subtropical lowland forest (Melaleuca quinquenervia) regulated by local and seasonal hydrology

Abstract

Tree stem mediated methane emissions represent a potentially important yet poorly constrained source of atmospheric methane. Here we present the first ever quantification of tree stem methane emissions from Melaleuca quinquenervia, a widespread iconic Australian lowland tree and globally invasive species. Under two distinct hydrological conditions (wet and dry) we captured 431 tree stem flux measurements encompassing six different vertical stem heights along a 50 m topo-gradient transect, separated into three distinct hydrological zones (upper, transitional and lower). The tree stem methane fluxes closely reflected local topography/hydrology and ranged from − 30.0 to 123,227 µmol m−2 day−1, with the maximum values amongst the highest values reported to date. The highest methane emissions were observed during wet conditions, within the inundated lower zone and from near the tree stem bases and water table. The average methane flux per tree (scaled to 1 m of stem) for the transitional and lower zones was 52-fold and 46-fold higher during wet conditions compared to dry, whereas the upper zone emissions changed little between seasons. Adjacent soil fluxes followed similar trends along the hydrology gradient with the upper zone tree stem emissions offsetting the adjacent soil methane sink capacity. A clear trend of sharply decreasing methane emissions with stem-height suggests a soil methane origin. A 45-h time-series of two trees within the lower zone revealed three to fourfold diel variability, with elevated morning-time fluxes. Overall, the study revealed that seasonal hydrological conditions and topo-gradient substantially regulated the methane emissions from M. quinquenervia and that this previously overlooked pathway should be accounted for within wetland methane budgets, especially during inundated conditions.

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Data availability

All data is available as supplementary materials and online repositories.

References

  1. Aben RCH, Barros N, van Donk E, Frenken T, Hilt S, Kazanjian G, Kosten S (2017) Cross continental increase in methane ebullition under climate change. Nat Commun 8(1):1682. https://doi.org/10.1038/s41467-017-01535-y

    Article  Google Scholar 

  2. Armstrong J, Armstrong W (1991) A convective through-flow of gases in Phragmites australis (Cav.) Trin. ex Steud. Aquat Bot 39(1–2):75–88

    Article  Google Scholar 

  3. Bamber RK (1962) The anatomy of the barks of Leptospermoideae. Aust J Bot 10(1):25–54

    Article  Google Scholar 

  4. Barba J, Bradford MA, Brewer PE, Bruhn D, Covey K, van Haren J, Pihlatie M (2019a) Methane emissions from tree stems: a new frontier in the global carbon cycle. New Phytol 222(1):18–28

    Article  Google Scholar 

  5. Barba J, Poyatos R, Vargas R (2019b) Automated measurements of greenhouse gases fluxes from tree stems and soils: magnitudes, patterns and drivers. Sci Rep 9(1):4005. https://doi.org/10.1038/s41598-019-39663-8

    Article  Google Scholar 

  6. Boon PI, Sorrell BK (1995) Methane fluxes from an Australian floodplain wetland: the importance of emergent macrophytes. J N Am Benthol Soc 14(4):582–598

    Article  Google Scholar 

  7. Borken W, Davidson EA, Savage K, Sundquist ET, Steudler P (2006) Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil. Soil Biol Biochem 38(6):1388–1395

    Article  Google Scholar 

  8. Brown DR, Johnston SG, Santos IR, Holloway CJ, Sanders CJ (2019) Significant organic carbon accumulation in two coastal acid sulfate soil wetlands. Geophys Res Lett. https://doi.org/10.1029/2019gl082076

    Article  Google Scholar 

  9. Burdige D (2012) Estuarine and coastal sediments–coupled biogeochemical cycling. Treatise Estuar Coast Sci 5:279–316

    Google Scholar 

  10. Bureau of Meteorology (2019) Daily weather observations for Taree Airport. http://www.bom.gov.au/climate/dwo/IDCJDW2129.latest.shtml. Accessed 2 March 2019 

  11. Bushong F (1907) Composition of gas from cottonwood trees. Trans Kansas Acad Sci 21:53–53

    Article  Google Scholar 

  12. CABI (2019) Datasheet on Melaleuca quinquenervia (paperbark tree).https://www.cabi.org/isc/datasheet/34348. Accessed 9 Sept 2019

  13. 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(1–3):1–24. https://doi.org/10.1007/s10533-014-9974-1

    Article  Google Scholar 

  14. Chanton JP (2005) The effect of gas transport on the isotope signature of methane in wetlands. Org Geochem 36(5):753–768. https://doi.org/10.1016/j.orggeochem.2004.10.007

    Article  Google Scholar 

  15. Chanton JP, Martens CS, Kelley CA, Crill PM, Showers WJ (1992) Methane transport mechanisms and isotopic fractionation in emergent macrophytes of an Alaskan tundra lake. J Geophys Res 97(D15):16681–16688

    Article  Google Scholar 

  16. Chanton JP, Arkebauer TJ, Harden HS, Verma SB (2002) Diel variation in lacunal CH4 and CO2 concentration and δ13C in Phragmites australis. Biogeochemistry 59(3):287–301

    Article  Google Scholar 

  17. Covey KR, Megonigal JP (2019) Methane production and emissions in trees and forests. New Phytol 222(1):35–51. https://doi.org/10.1111/nph.15624

    Article  Google Scholar 

  18. Covey KR, Wood SA, Warren RJ, Lee X, Bradford MA (2012) Elevated methane concentrations in trees of an upland forest. Geophys Res Lett 39(15):L15705. https://doi.org/10.1029/2012gl052361

    Article  Google Scholar 

  19. Davidson TA, Audet J, Jeppesen E, Landkildehus F, Lauridsen TL, Søndergaard M, Syväranta J (2018) Synergy between nutrients and warming enhances methane ebullition from experimental lakes. Nat Clim Change 8(2):156–160

    Article  Google Scholar 

  20. Dean JF, Middelburg JJ, Röckmann T, Aerts R, Blauw LG, Egger M, Dolman AJ (2018) Methane feedbacks to the global climate system in a warmer world. Rev Geophys. https://doi.org/10.1002/2017rg000559

    Article  Google Scholar 

  21. Etminan M, Myhre G, Highwood E, Shine K (2016) Radiative forcing of carbon dioxide, methane, and nitrous oxide: a significant revision of the methane radiative forcing. Geophys Res Lett 43(24):12614–612623

    Article  Google Scholar 

  22. Fuss R (2019) Gasfluxes: greenhouse gas flux calculation from chamber measurements. R package version 0.4-3. https://CRAN.R-project.org/package=gasfluxes

  23. Gauci V, Gowing DJ, Hornibrook ER, Davis JM, Dise NB (2010) Woody stem methane emission in mature wetland alder trees. Atmos Environ 44(17):2157–2160

    Article  Google Scholar 

  24. Jeffrey LC, Maher DT, Johnston SG, Kelaher BP, Steven A, Tait DR (2019a) Wetland methane emissions dominated by plant-mediated fluxes: contrasting emissions pathways and seasons within a shallow freshwater subtropical wetland. Limnol Oceanogr. https://doi.org/10.1002/lno.11158

    Article  Google Scholar 

  25. Jeffrey LC, Maher DT, Johnston SG, Maguire K, Steven ADL, Tait DR (2019b) Rhizosphere to the atmosphere: contrasting methane pathways, fluxes, and geochemical drivers across the terrestrial–aquatic wetland boundary. Biogeosciences 16(8):1799–1815. https://doi.org/10.5194/bg-16-1799-2019

    Article  Google Scholar 

  26. Jeffrey LC, Reithmaier G, Sippo JZ, Johnston SG, Tait DR, Harada Y, Maher DT (2019c) Are methane emissions from mangrove stems a cryptic carbon loss pathway? Insights from a catastrophic forest mortality. New Phytol 224(1):146–154. https://doi.org/10.1111/nph.15995

    Article  Google Scholar 

  27. Jeffrey LC, Maher DT, Tait DR, Johnston SG (2020) A small nimble in situ fine-scale flux method for measuring tree stem greenhouse gas emissions and processes (S.N.I.F.F). Ecosystems. https://doi.org/10.1007/s10021-020-00496-6

    Article  Google Scholar 

  28. Johnston SG, Slavich PG, Hirst P (2003) Alteration of groundwater and sediment geochemistry in a sulfidic backswamp due to Melaleuca quinquenervia encroachment. Soil Res 41(7):1343–1367. https://doi.org/10.1071/sr03027

    Article  Google Scholar 

  29. Kim J, Verma S, Billesbach D, Clement R (1998) Diel variation in methane emission from a midlatitude prairie wetland: significance of convective throughflow in Phragmites australis. J Geophys Res 103(D21):28029–28039

    Article  Google Scholar 

  30. Laroche FB (1999) Melaleuca management plan. Miami, Florida exotic Pest Plant Council

    Google Scholar 

  31. Lenhart K, Bunge M, Ratering S, Neu TR, Schüttmann I, Greule M, Keppler F (2012) Evidence for methane production by saprotrophic fungi. Nat Commun 3:1046. https://doi.org/10.1038/ncomms2049

    Article  Google Scholar 

  32. Machacova K, Back J, Vanhatalo A, Halmeenmaki E, Kolari P, Mammarella I, Pihlatie M (2016) Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci Rep 6:23410. https://doi.org/10.1038/srep23410

    Article  Google Scholar 

  33. Maier M, Machacova K, Lang F, Svobodova K, Urban O (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(1):31–35

    Article  Google Scholar 

  34. Matthews E, Fung I (1987) Methane emission from natural wetlands: global distribution, area, and environmental characteristics of sources. Glob Biogeochem Cycles 1(1):61–86

    Article  Google Scholar 

  35. McJannet D (2008) Water table and transpiration dynamics in a seasonally inundated Melaleuca quinquenervia forest, north Queensland, Australia. Hydrol Process 22(16):3079–3090

    Article  Google Scholar 

  36. McNicol G, Sturtevant CS, Knox SH, Dronova I, Baldocchi DD, Silver WL (2017) Effects of seasonality, transport pathway, and spatial structure on greenhouse gas fluxes in a restored wetland. Glob Change Biol 23(7):2768–2782

    Article  Google Scholar 

  37. Megonigal JP, Guenther AB (2008) Methane emissions from upland forest soils and vegetation. Tree Physiol 28(4):491–498

    Article  Google Scholar 

  38. Megonigal JP, Brewer PE, Knee KL (2019) 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 

  39. Nauer PA, Hutley LB, Arndt SK (2018) Termite mounds mitigate half of termite methane emissions. Proc Natl Acad Sci 115(52):13306–13311

    Article  Google Scholar 

  40. Nisbet E, Manning M, Dlugokencky E, Fisher R, Lowry D, Michel S, Bousquet P (2019) Very strong atmospheric methane growth in the 4 years 2014–2017: implications for the Paris Agreement. Glob Biogeochem Cycles 33(3):318–342

    Article  Google Scholar 

  41. Pangala SR, Moore S, Hornibrook ER, Gauci V (2013) Trees are major conduits for methane egress from tropical forested wetlands. New Phytol 197(2):524–531

    Article  Google Scholar 

  42. Pangala SR, Gowing DJ, Hornibrook ER, Gauci V (2014) Controls on methane emissions from Alnus glutinosa saplings. New Phytol 201(3):887–896. https://doi.org/10.1111/nph.12561

    Article  Google Scholar 

  43. Pangala SR, Hornibrook ER, Gowing DJ, Gauci V (2015) The contribution of trees to ecosystem methane emissions in a temperate forested wetland. Glob Change Biol 21(7):2642–2654

    Article  Google Scholar 

  44. Pangala SR, Enrich-Prast A, Basso LS, Peixoto RB, Bastviken D, Hornibrook ER, Sakuragui CM (2017) Large emissions from floodplain trees close the Amazon methane budget. Nature 552(7684):230

    Article  Google Scholar 

  45. Pitz S, Megonigal JP (2017) Temperate forest methane sink diminished by tree emissions. New Phytol 214(4):1432–1439

    Article  Google Scholar 

  46. Pitz SL, Megonigal JP, Chang C-H, Szlavecz K (2018) Methane fluxes from tree stems and soils along a habitat gradient. Biogeochemistry 137(3):307–320

    Article  Google Scholar 

  47. Plain C, Ndiaye FK, Bonnaud P, Ranger J, Epron D (2019) Impact of vegetation on the methane budget of a temperate forest. New Phytol 221(3):1447–1456

    Article  Google Scholar 

  48. Rusch H, Rennenberg H (1998) Black alder (Alnus glutinosa (L.) Gaertn.) trees mediate methane and nitrous oxide emission from the soil to the atmosphere. Plant Soil 201(1):1–7

    Article  Google Scholar 

  49. Saunois M, Stavert AR, Poulter B, Bousquet P, Canadell JG, Jackson RB, Zhuang Q (2019) The global methane budget 2000–2017. Earth Syst Sci Data Discuss. https://doi.org/10.5194/essd-2019-128

    Article  Google Scholar 

  50. Schutz H (1991) Role of plants in regulating the methane flux to the atmosphere. Trace Gas Emiss Plants. https://doi.org/10.1016/C2009-0-02643-9

    Article  Google Scholar 

  51. Sjögersten S, Siegenthaler A, Lopez OR, Aplin P, Turner B, Gauci V (2019) Methane emissions from tree stems in neotropical peatlands. New Phytol 225(2):769–781

    Article  Google Scholar 

  52. Sorz J, Hietz P (2006) Gas diffusion through wood: implications for oxygen supply. Trees 20:34–41

    Article  Google Scholar 

  53. Steppe K, Sterck F, Deslaurier A (2015) Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends Plant Sci 20::1360–1385

    Article  Google Scholar 

  54. Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Bex V, Midgley PM (2013) Climate change 2013: the physical science basis. In: Contribution of working Group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK

  55. Terazawa K, Ishizuka S, Sakata T, Yamada K, Takahashi M (2007) Methane emissions from stems of Fraxinus mandshurica var. japonica trees in a floodplain forest. Soil Biol Biochem 39(10):2689–2692

    Article  Google Scholar 

  56. Terazawa K, Yamada K, Ohno Y, Sakata T, Ishizuka S (2015) Spatial and temporal variability in methane emissions from tree stems of Fraxinus mandshurica in a cool-temperate floodplain forest. Biogeochemistry 123(3):349–362

    Article  Google Scholar 

  57. Teskey RO, Saveyn A, Steppe K, McGuire MA (2008) Origin, fate and significance of CO2 in tree stems. New Phytol 177:7–32

    Google Scholar 

  58. Van Der Nat F-FW, Middelburg JJ, Van Meteren D, Wielemakers A (1998) Diel methane emission patterns from Scirpus lacustris and Phragmites australis. Biogeochemistry 41(1):1–22

    Article  Google Scholar 

  59. Waldo NB, Hunt BK, Fadely EC, Moran JJ, Neumann RB (2019) Plant root exudates increase methane emissions through direct and indirect pathways. Biogeochemistry 145(1–2):213–234. https://doi.org/10.1007/s10533-019-00600-6

    Article  Google Scholar 

  60. Wang ZP, Gu Q, Deng FD, Huang JH, Megonigal JP, Yu Q, Han XG (2016) Methane emissions from the trunks of living trees on upland soils. New Phytol 211(2):429–439. https://doi.org/10.1111/nph.13909

    Article  Google Scholar 

  61. Wang ZP, Han SJ, Li HL, Deng FD, Zheng YH, Liu HF, Han XG (2017) Methane production explained largely by water content in the heartwood of living trees in upland forests. J Geophys Res 122(10):2479–2489

    Article  Google Scholar 

  62. Warner DL, Villarreal S, McWilliams K, Inamdar S, Vargas R (2017) Carbon dioxide and methane fluxes from tree stems, coarse woody debris, and soils in an upland temperate forest. Ecosystems 20(6):1205–1216

    Article  Google Scholar 

  63. Wassmann R, Alberto MC, Tirol-Padre A, Hoang NT, Romasanta R, Centeno CA, Sander BO (2018) Increasing sensitivity of methane emission measurements in rice through deployment of ‘closed chambers’ at nighttime. PLoS ONE 13(2):e0191352

    Article  Google Scholar 

  64. Welch B, Gauci V, Sayer EJ (2018) 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(1):361–372. https://doi.org/10.1111/gcb.14498

    Article  Google Scholar 

  65. Yip DZ, Veach AM, Yang ZK, Cregger MA, Schadt CW (2018) Methanogenic Archaea dominate mature heartwood habitats of Eastern Cottonwood (Populus deltoides). New Phytol 222(1):115–121

    Article  Google Scholar 

  66. Zeikus J, Ward J (1974) Methane formation in living trees: a microbial origin. Science 184(4142):1181–1183

    Article  Google Scholar 

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Acknowledgements

We thank Bob McDonnell and Mid-Coast Council for fieldwork assistance and Roz Hagan for laboratory assistance.

Funding

This work was funded by the ARC (LP160100061 and DP180101285). LJ and DT acknowledge support from the Australian Research Council that partially funds their salaries (LP160100061 and DE180100535 respectively).

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SJ and LJ conceived the study. SJ, DT, SE and LJ conducted the fieldwork. SJ, DM, DT assisted LJ with analysis and interpretation. LJ wrote the first draft with assistance from SJ. All authors contributed to and approved the final manuscript. We thank one anonymous referee and Pat Megonigal, for their constructive review comments and suggestions which helped to strengthen the manuscript and thank the associate editor Jan Mulder for coordinating the review process.

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Correspondence to Luke C. Jeffrey.

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Jeffrey, L.C., Maher, D.T., Tait, D.R. et al. Tree stem methane emissions from subtropical lowland forest (Melaleuca quinquenervia) regulated by local and seasonal hydrology. Biogeochemistry 151, 273–290 (2020). https://doi.org/10.1007/s10533-020-00726-y

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Keywords

  • Carbon cycle
  • Climate change
  • Flooded forest
  • Greenhouse gasses
  • Paperbark wetland
  • Plant-mediated emissions
  • Sediment diffusion
  • Tree stem methane fluxes