Functional variability in specific root respiration translates to autotrophic differences in soil respiration in a temperate deciduous forest

J. Aaron Hogan; Jessy L. Labbé; Alyssa A. Carrell; Jennifer Franklin; Kevin P. Hoyt; Oscar J. Valverde-Barrantes; Christopher Baraloto; Jeffrey M. Warren

doi:10.1016/j.geoderma.2023.116414

Functional variability in specific root respiration translates to autotrophic differences in soil respiration in a temperate deciduous forest

J. Aaron Hogan
, Jessy L. Labbé
, Alyssa A. Carrell
, Jennifer Franklin
, Kevin P. Hoyt
, Oscar J. Valverde-Barrantes
, Christopher Baraloto
, Jeffrey M. Warren

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

CO₂ release from forest soils (R_s) is a prominent flux in the global carbon cycle. R_s is derived from roots (autotrophic respiration, R_a) and microbial (heterotrophic) respiration and is highly dynamic, as it depends on edaphic and environmental conditions as well as root functional traits and microbial community composition. It is unclear how root functional traits affect root and microbial respiration rates; however, their consideration may help parse out the relative contributions of root and microbial respiration to R_s. At a temperate forest site, root systems of 3–4 functional root orders and their surrounding surface soil were carefully excavated and placed into custom trays designed to repeatedly measure R_s in situ on eight temperate tree species that varied in their root functional strategies and mycorrhizal affinity. R_s was measured bi-weekly to monthly for nearly one year using a custom chamber attached to a gas exchange system. R_s varied over time, ranging from 0.3 to 12 µmol m⁻² s⁻¹. Comparable root systems of the same species were excised from the soil and specific root respiration rates (R_r) were measured. R_r ranged from 2.5 to 9.0 nmol g⁻¹ s⁻¹ and was negatively correlated with root tissue density and positively related to root tissue nitrogen concentration. Using R_r to estimate R_a, we estimate that R_a accounts for <10%, on average 2–3%, of R_s for individual root systems (averaging 1.2 g dry biomass) housed in surrounding soil (average 1.3 kg dry mass) in situ; thus, R_a was roughly 20 times greater than R_h per unit mass. The contribution of R_a peaked in the fall and coincided with leaf senescence of the forest canopy. A soil-sterilizing experimental treatment designed to help isolate R_a in situ reduced bacterial biomass and shifted fungal community composition, but there was no reduction in R_s of the in-situ root-soil tray systems. The relative R_a to R_s ratio increased with root functional strategies characterized by greater specific root length and tip abundance, but also to greater root tissue density. The ratio of R_a to R_s also increased with warmer soil temperatures and decreased slightly with increasing soil moisture. We discuss how incorporating root functional traits as modulators of the autotrophic contribution to R_s could be considered when modeling total soil CO₂ efflux from forests.

Original language	English
Article number	116414
Journal	Geoderma
Volume	432
DOIs	https://doi.org/10.1016/j.geoderma.2023.116414
State	Published - Apr 2023

Funding

This work was completed in collaboration with the Forest Resources AgResearch and Education Center at the University of Tennessee. We thank Mindy Clark, Zach Ziegler, Jacob Wyre, Joe Gebhart and Yvonne Hitchcock for their help in the field. We are very grateful to Jana Philips, Joanne Childs, and Deanne Brice at the Division of Environmental Science at Oak Ridge National Laboratory for their help with the soil chloroform extractions and leaf nutrient analyses. We thank Sara Wilson at the Blue Carbon Lab at Florida International University for help with root tissue nutrient analyses. We also thank Cici Hall from Li-COR Inc. for her help with troubleshooting many questions and providing expertise on gas exchange measurements. Research sponsored by the U. S. Department of Energy (DOE), by the DOE Office of Science, Office of Biological and Environmental Research, and by Office of Science, Office of Workforce Development for Teachers and Scientists, Office of Science Graduate Student Research (SCGSR) program. The SCGSR program is administered by the Oak Ridge Institute for Science and Education (ORISE) for the DOE. ORISE is managed by ORAU under contract number DE-AC05-06OR23100 . Oak Ridge National Laboratory (ORNL) is managed by UT-Battelle, LLC, for the DOE under contract DE-AC05-00OR22725 . This work was completed in collaboration with the Forest Resources AgResearch and Education Center at the University of Tennessee. We thank Mindy Clark, Zach Ziegler, Jacob Wyre, Joe Gebhart and Yvonne Hitchcock for their help in the field. We are very grateful to Jana Philips, Joanne Childs, and Deanne Brice at the Division of Environmental Science at Oak Ridge National Laboratory for their help with the soil chloroform extractions and leaf nutrient analyses. We thank Sara Wilson at the Blue Carbon Lab at Florida International University for help with root tissue nutrient analyses. We also thank Cici Hall from Li-COR Inc. for her help with troubleshooting many questions and providing expertise on gas exchange measurements. Research sponsored by the U. S. Department of Energy (DOE), by the DOE Office of Science, Office of Biological and Environmental Research, and by Office of Science, Office of Workforce Development for Teachers and Scientists, Office of Science Graduate Student Research (SCGSR) program. The SCGSR program is administered by the Oak Ridge Institute for Science and Education (ORISE) for the DOE. ORISE is managed by ORAU under contract number DE-AC05-06OR23100. Oak Ridge National Laboratory (ORNL) is managed by UT-Battelle, LLC, for the DOE under contract DE-AC05-00OR22725.

Keywords

Belowground physiology
Root functional traits
Soil fungi and bacteria
Soil microbial nitrogen
Temperate forest
ZeroTol

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10.1016/j.geoderma.2023.116414

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title = "Functional variability in specific root respiration translates to autotrophic differences in soil respiration in a temperate deciduous forest",

abstract = "CO2 release from forest soils (Rs) is a prominent flux in the global carbon cycle. Rs is derived from roots (autotrophic respiration, Ra) and microbial (heterotrophic) respiration and is highly dynamic, as it depends on edaphic and environmental conditions as well as root functional traits and microbial community composition. It is unclear how root functional traits affect root and microbial respiration rates; however, their consideration may help parse out the relative contributions of root and microbial respiration to Rs. At a temperate forest site, root systems of 3–4 functional root orders and their surrounding surface soil were carefully excavated and placed into custom trays designed to repeatedly measure Rs in situ on eight temperate tree species that varied in their root functional strategies and mycorrhizal affinity. Rs was measured bi-weekly to monthly for nearly one year using a custom chamber attached to a gas exchange system. Rs varied over time, ranging from 0.3 to 12 µmol m−2 s−1. Comparable root systems of the same species were excised from the soil and specific root respiration rates (Rr) were measured. Rr ranged from 2.5 to 9.0 nmol g−1 s−1 and was negatively correlated with root tissue density and positively related to root tissue nitrogen concentration. Using Rr to estimate Ra, we estimate that Ra accounts for <10\%, on average 2–3\%, of Rs for individual root systems (averaging 1.2 g dry biomass) housed in surrounding soil (average 1.3 kg dry mass) in situ; thus, Ra was roughly 20 times greater than Rh per unit mass. The contribution of Ra peaked in the fall and coincided with leaf senescence of the forest canopy. A soil-sterilizing experimental treatment designed to help isolate Ra in situ reduced bacterial biomass and shifted fungal community composition, but there was no reduction in Rs of the in-situ root-soil tray systems. The relative Ra to Rs ratio increased with root functional strategies characterized by greater specific root length and tip abundance, but also to greater root tissue density. The ratio of Ra to Rs also increased with warmer soil temperatures and decreased slightly with increasing soil moisture. We discuss how incorporating root functional traits as modulators of the autotrophic contribution to Rs could be considered when modeling total soil CO2 efflux from forests.",

keywords = "Belowground physiology, Root functional traits, Soil fungi and bacteria, Soil microbial nitrogen, Temperate forest, ZeroTol",

author = "\{Aaron Hogan\}, J. and Labb{\'e}, \{Jessy L.\} and Carrell, \{Alyssa A.\} and Jennifer Franklin and Hoyt, \{Kevin P.\} and Valverde-Barrantes, \{Oscar J.\} and Christopher Baraloto and Warren, \{Jeffrey M.\}",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = apr,

doi = "10.1016/j.geoderma.2023.116414",

language = "English",

volume = "432",

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T1 - Functional variability in specific root respiration translates to autotrophic differences in soil respiration in a temperate deciduous forest

AU - Aaron Hogan, J.

AU - Labbé, Jessy L.

AU - Carrell, Alyssa A.

AU - Franklin, Jennifer

AU - Hoyt, Kevin P.

AU - Valverde-Barrantes, Oscar J.

AU - Baraloto, Christopher

AU - Warren, Jeffrey M.

PY - 2023/4

Y1 - 2023/4

N2 - CO2 release from forest soils (Rs) is a prominent flux in the global carbon cycle. Rs is derived from roots (autotrophic respiration, Ra) and microbial (heterotrophic) respiration and is highly dynamic, as it depends on edaphic and environmental conditions as well as root functional traits and microbial community composition. It is unclear how root functional traits affect root and microbial respiration rates; however, their consideration may help parse out the relative contributions of root and microbial respiration to Rs. At a temperate forest site, root systems of 3–4 functional root orders and their surrounding surface soil were carefully excavated and placed into custom trays designed to repeatedly measure Rs in situ on eight temperate tree species that varied in their root functional strategies and mycorrhizal affinity. Rs was measured bi-weekly to monthly for nearly one year using a custom chamber attached to a gas exchange system. Rs varied over time, ranging from 0.3 to 12 µmol m−2 s−1. Comparable root systems of the same species were excised from the soil and specific root respiration rates (Rr) were measured. Rr ranged from 2.5 to 9.0 nmol g−1 s−1 and was negatively correlated with root tissue density and positively related to root tissue nitrogen concentration. Using Rr to estimate Ra, we estimate that Ra accounts for <10%, on average 2–3%, of Rs for individual root systems (averaging 1.2 g dry biomass) housed in surrounding soil (average 1.3 kg dry mass) in situ; thus, Ra was roughly 20 times greater than Rh per unit mass. The contribution of Ra peaked in the fall and coincided with leaf senescence of the forest canopy. A soil-sterilizing experimental treatment designed to help isolate Ra in situ reduced bacterial biomass and shifted fungal community composition, but there was no reduction in Rs of the in-situ root-soil tray systems. The relative Ra to Rs ratio increased with root functional strategies characterized by greater specific root length and tip abundance, but also to greater root tissue density. The ratio of Ra to Rs also increased with warmer soil temperatures and decreased slightly with increasing soil moisture. We discuss how incorporating root functional traits as modulators of the autotrophic contribution to Rs could be considered when modeling total soil CO2 efflux from forests.

AB - CO2 release from forest soils (Rs) is a prominent flux in the global carbon cycle. Rs is derived from roots (autotrophic respiration, Ra) and microbial (heterotrophic) respiration and is highly dynamic, as it depends on edaphic and environmental conditions as well as root functional traits and microbial community composition. It is unclear how root functional traits affect root and microbial respiration rates; however, their consideration may help parse out the relative contributions of root and microbial respiration to Rs. At a temperate forest site, root systems of 3–4 functional root orders and their surrounding surface soil were carefully excavated and placed into custom trays designed to repeatedly measure Rs in situ on eight temperate tree species that varied in their root functional strategies and mycorrhizal affinity. Rs was measured bi-weekly to monthly for nearly one year using a custom chamber attached to a gas exchange system. Rs varied over time, ranging from 0.3 to 12 µmol m−2 s−1. Comparable root systems of the same species were excised from the soil and specific root respiration rates (Rr) were measured. Rr ranged from 2.5 to 9.0 nmol g−1 s−1 and was negatively correlated with root tissue density and positively related to root tissue nitrogen concentration. Using Rr to estimate Ra, we estimate that Ra accounts for <10%, on average 2–3%, of Rs for individual root systems (averaging 1.2 g dry biomass) housed in surrounding soil (average 1.3 kg dry mass) in situ; thus, Ra was roughly 20 times greater than Rh per unit mass. The contribution of Ra peaked in the fall and coincided with leaf senescence of the forest canopy. A soil-sterilizing experimental treatment designed to help isolate Ra in situ reduced bacterial biomass and shifted fungal community composition, but there was no reduction in Rs of the in-situ root-soil tray systems. The relative Ra to Rs ratio increased with root functional strategies characterized by greater specific root length and tip abundance, but also to greater root tissue density. The ratio of Ra to Rs also increased with warmer soil temperatures and decreased slightly with increasing soil moisture. We discuss how incorporating root functional traits as modulators of the autotrophic contribution to Rs could be considered when modeling total soil CO2 efflux from forests.

KW - Belowground physiology

KW - Root functional traits

KW - Soil fungi and bacteria

KW - Soil microbial nitrogen

KW - Temperate forest

KW - ZeroTol

UR - https://www.scopus.com/pages/publications/85149804280

U2 - 10.1016/j.geoderma.2023.116414

DO - 10.1016/j.geoderma.2023.116414

M3 - Article

AN - SCOPUS:85149804280

SN - 0016-7061

VL - 432

JO - Geoderma

JF - Geoderma

M1 - 116414

ER -

Functional variability in specific root respiration translates to autotrophic differences in soil respiration in a temperate deciduous forest

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