Origin of volatile organic compound emissions from subarctic tundra under global warming

Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. Howe...

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Bibliographic Details
Published inGlobal change biology Vol. 26; no. 3; pp. 1908 - 1925
Main Authors Ghirardo, Andrea, Lindstein, Frida, Koch, Kerstin, Buegger, Franz, Schloter, Michael, Albert, Andreas, Michelsen, Anders, Winkler, J. Barbro, Schnitzler, Jörg‐Peter, Rinnan, Riikka
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.03.2020
John Wiley and Sons Inc
Subjects
13CO2
Arctic
Arctic region
Arctic Regions
Atmosphere
Atmospheric chemistry
Atmospheric models
Betula
biochemical mechanisms
Biosynthesis
carbon
Carbon dioxide
carbon sequestration
Chemical composition
Climate
Climate change
Computer simulation
Current data
de novo biosynthesis
Ecosystem
Ecosystems
Emissions
Environment models
Global climate
Global Warming
Heat exchange
Hydrocarbons
Isomers
monoterpenoids
net ecosystem exchange
Organic compounds
plant communities
Plant species
prediction
Primary
Primary s
Salix
sesquiterpenoids
Shrubs
Soil
Soils
Species composition
species diversity
stable isotopes
subarctic heath
summer
Taiga & tundra
Temperature
Temperature dependence
terpene
Terpenes
Terrestrial ecosystems
Tundra
Vegetation
VOCs
Volatile compounds
volatile organic compound
Volatile Organic Compounds
Volatiles
Willow
Arctic Regions
Arctic region
tundra
de novo biosynthesis
global warming
net ecosystem exchange
terpene
subarctic heath
Arctic
volatile organic compound
13CO2
climate change
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Abstract Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13CO2‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% (Salix) and 60%–68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% (Salix) and 87%–95% (Betula). Analyses of above‐ and belowground 12/13C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems. We studied the origin of biogenic volatile organic compounds (VOCs) and carbon (C) allocation under global warming in subarctic heath tundra ecosystem using isotope labeling of 13CO2. Our results show the importance of de novo monoterpene biosynthesis and the impact of warming in vegetation communities characterized by Salix spp. (willows) or Betula spp. (birch). Warming increased overall VOC emissions and altered the composition of the volatile blend toward more reactive compounds. Analyses of above‐ and belowground 12/13C suggest shifts of C allocation and negative effects of warming on C sequestration in these delicate tundra ecosystems.
AbstractList Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO 2 ‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula . The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% ( Salix ) and 60%–68% ( Betula ) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% ( Salix ) and 87%–95% ( Betula ). Analyses of above‐ and belowground 12/13 C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO 2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature-dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO2 -labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil-plant-atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%-44% (Salix) and 60%-68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%-58% (Salix) and 87%-95% (Betula). Analyses of above- and belowground 12/13 C showed shifts of C allocation in the plant-soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature-dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO2 -labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil-plant-atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%-44% (Salix) and 60%-68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%-58% (Salix) and 87%-95% (Betula). Analyses of above- and belowground 12/13 C showed shifts of C allocation in the plant-soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13CO2‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% (Salix) and 60%–68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% (Salix) and 87%–95% (Betula). Analyses of above‐ and belowground 12/13C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO 2 ‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula . The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% ( Salix ) and 60%–68% ( Betula ) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% ( Salix ) and 87%–95% ( Betula ). Analyses of above‐ and belowground 12/13 C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO 2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems. We studied the origin of biogenic volatile organic compounds (VOCs) and carbon (C) allocation under global warming in subarctic heath tundra ecosystem using isotope labeling of 13 CO 2 . Our results show the importance of de novo monoterpene biosynthesis and the impact of warming in vegetation communities characterized by Salix spp. (willows) or Betula spp. (birch). Warming increased overall VOC emissions and altered the composition of the volatile blend toward more reactive compounds. Analyses of above‐ and belowground 12/13 C suggest shifts of C allocation and negative effects of warming on C sequestration in these delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature-dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using CO -labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil-plant-atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%-44% (Salix) and 60%-68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%-58% (Salix) and 87%-95% (Betula). Analyses of above- and belowground C showed shifts of C allocation in the plant-soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using ¹³CO₂‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The ¹³C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% (Salix) and 60%–68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% (Salix) and 87%–95% (Betula). Analyses of above‐ and belowground ¹²/¹³C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO₂ and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.
Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13CO2‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% (Salix) and 60%–68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% (Salix) and 87%–95% (Betula). Analyses of above‐ and belowground 12/13C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems. We studied the origin of biogenic volatile organic compounds (VOCs) and carbon (C) allocation under global warming in subarctic heath tundra ecosystem using isotope labeling of 13CO2. Our results show the importance of de novo monoterpene biosynthesis and the impact of warming in vegetation communities characterized by Salix spp. (willows) or Betula spp. (birch). Warming increased overall VOC emissions and altered the composition of the volatile blend toward more reactive compounds. Analyses of above‐ and belowground 12/13C suggest shifts of C allocation and negative effects of warming on C sequestration in these delicate tundra ecosystems.
Author Schnitzler, Jörg‐Peter
Koch, Kerstin
Michelsen, Anders
Albert, Andreas
Winkler, J. Barbro
Buegger, Franz
Rinnan, Riikka
Schloter, Michael
Ghirardo, Andrea
Lindstein, Frida
AuthorAffiliation 1 Research Unit Environmental Simulation (EUS) Institute of Biochemical Plant Pathology Helmholtz Zentrum München Neuherberg Germany
2 Terrestrial Ecology Section Department of Biology University of Copenhagen Copenhagen Denmark
4 Research Unit for Comparative Microbiome Analysis (COMI) Helmholtz Zentrum München Neuherberg Germany
5 Center for Permafrost Department of Geoscience and Natural Resource Management University of Copenhagen Copenhagen Denmark
3 Institute of Biochemical Plant Pathology (BIOP) Helmholtz Zentrum München Neuherberg Germany
AuthorAffiliation_xml – name: 4 Research Unit for Comparative Microbiome Analysis (COMI) Helmholtz Zentrum München Neuherberg Germany
– name: 1 Research Unit Environmental Simulation (EUS) Institute of Biochemical Plant Pathology Helmholtz Zentrum München Neuherberg Germany
– name: 2 Terrestrial Ecology Section Department of Biology University of Copenhagen Copenhagen Denmark
– name: 5 Center for Permafrost Department of Geoscience and Natural Resource Management University of Copenhagen Copenhagen Denmark
– name: 3 Institute of Biochemical Plant Pathology (BIOP) Helmholtz Zentrum München Neuherberg Germany
Author_xml – sequence: 1
  givenname: Andrea
  orcidid: 0000-0003-1973-4007
  surname: Ghirardo
  fullname: Ghirardo, Andrea
  organization: Helmholtz Zentrum München
– sequence: 2
  givenname: Frida
  orcidid: 0000-0002-3981-5966
  surname: Lindstein
  fullname: Lindstein, Frida
  organization: University of Copenhagen
– sequence: 3
  givenname: Kerstin
  orcidid: 0000-0001-5834-8550
  surname: Koch
  fullname: Koch, Kerstin
  organization: Helmholtz Zentrum München
– sequence: 4
  givenname: Franz
  orcidid: 0000-0003-3526-4711
  surname: Buegger
  fullname: Buegger, Franz
  organization: Helmholtz Zentrum München
– sequence: 5
  givenname: Michael
  orcidid: 0000-0003-1671-1125
  surname: Schloter
  fullname: Schloter, Michael
  organization: Helmholtz Zentrum München
– sequence: 6
  givenname: Andreas
  orcidid: 0000-0002-0582-2674
  surname: Albert
  fullname: Albert, Andreas
  organization: Helmholtz Zentrum München
– sequence: 7
  givenname: Anders
  orcidid: 0000-0002-9541-8658
  surname: Michelsen
  fullname: Michelsen, Anders
  organization: University of Copenhagen
– sequence: 8
  givenname: J. Barbro
  orcidid: 0000-0002-7092-9742
  surname: Winkler
  fullname: Winkler, J. Barbro
  organization: Helmholtz Zentrum München
– sequence: 9
  givenname: Jörg‐Peter
  orcidid: 0000-0002-9825-867X
  surname: Schnitzler
  fullname: Schnitzler, Jörg‐Peter
  organization: Helmholtz Zentrum München
– sequence: 10
  givenname: Riikka
  orcidid: 0000-0001-7222-700X
  surname: Rinnan
  fullname: Rinnan, Riikka
  email: riikkar@bio.ku.dk
  organization: University of Copenhagen
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31957145$$D View this record in MEDLINE/PubMed
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Issue 3
Keywords tundra
de novo biosynthesis
global warming
net ecosystem exchange
terpene
subarctic heath
Arctic
volatile organic compound
13CO2
climate change
Language English
License Attribution
2020 The Authors. Global Change Biology published by John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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content type line 14
content type line 23
Andrea Ghirardo and Frida Lindstein contributed equally to this work.
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Snippet Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile...
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pubmed
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SourceType Open Access Repository
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Enrichment Source
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StartPage 1908
SubjectTerms 13CO2
Arctic
Arctic region
Arctic Regions
Atmosphere
Atmospheric chemistry
Atmospheric models
Betula
biochemical mechanisms
Biosynthesis
carbon
Carbon dioxide
carbon sequestration
Chemical composition
Climate
Climate change
Computer simulation
Current data
de novo biosynthesis
Ecosystem
Ecosystems
Emissions
Environment models
Global climate
Global Warming
Heat exchange
Hydrocarbons
Isomers
monoterpenoids
net ecosystem exchange
Organic compounds
plant communities
Plant species
prediction
Primary
Primary s
Salix
sesquiterpenoids
Shrubs
Soil
Soils
Species composition
species diversity
stable isotopes
subarctic heath
summer
Taiga & tundra
Temperature
Temperature dependence
terpene
Terpenes
Terrestrial ecosystems
Tundra
Vegetation
VOCs
Volatile compounds
volatile organic compound
Volatile Organic Compounds
Volatiles
Willow
Title Origin of volatile organic compound emissions from subarctic tundra under global warming
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fgcb.14935
https://www.ncbi.nlm.nih.gov/pubmed/31957145
https://www.proquest.com/docview/2371047927
https://www.proquest.com/docview/2342361066
https://www.proquest.com/docview/2400484154
https://pubmed.ncbi.nlm.nih.gov/PMC7078956
Volume 26
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