Remarkable Similarity in Timing of Absorptive Fine-Root Production Across 11 Diverse Temperate Tree Species in a Common Garden

Jennifer M. Withington; Marc Goebel; Bartosz Bułaj; Jacek Oleksyn; Peter B. Reich; David M. Eissenstat

doi:10.3389/fpls.2020.623722

Remarkable Similarity in Timing of Absorptive Fine-Root Production Across 11 Diverse Temperate Tree Species in a Common Garden

Jennifer M. Withington, Marc Goebel, Bartosz Bułaj, Jacek Oleksyn, Peter B. Reich, David M. Eissenstat

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Abstract

Long-term minirhizotron observations of absorptive fine roots provide insights into seasonal patterns of belowground root production and carbon dynamics. Our objective was to compare root dynamics over time across mature individuals of 11 temperate trees species: five evergreen and six deciduous. We analyzed the timing and growth on 1st-and 2nd-order roots in minirhizotron images down to a vertical depth of 35 cm, as well as monthly and total annual length production. Production patterns were related to total annual precipitation of the actual and previous year of root production over 6 years. The main or largest peak of annual fine-root production occurred between June and September for almost all species and years. In most years, when peaks occurred, the timing of peak root production was synchronized across all species. A linear mixed model revealed significant differences in monthly fine-root length production across species in certain years (species x year, P < 0.0001), which was strongly influenced by three tree species. Total annual root production was much higher in 2000–2002, when there was above-average rainfall in the previous year, compared with production in 2005–2007, which followed years of lower-than-average rainfall (2003–2006). Compared to the wetter period all species experienced a decline of at least 75% in annual production in the drier years. Total annual root length production was more strongly associated with previous year’s (P < 0.001) compared with the actual year’s precipitation (P = 0.003). Remarkably similar timing of monthly absorptive fine-root growth can occur across multiple species of diverse phylogeny and leaf habit in a given year, suggesting a strong influence of extrinsic factors on absorptive fine-root growth. The influence of previous year precipitation on annual absorptive fine-root growth underscores the importance of legacy effects in biological responses and suggests that a growth response of temperate trees to extreme precipitation or drought events can be exacerbated across years.

Original language	English (US)
Article number	623722
Journal	Frontiers in Plant Science
Volume	11
DOIs	https://doi.org/10.3389/fpls.2020.623722
State	Published - Jan 28 2021

Bibliographical note

Funding Information:
We thank Jakub Olesiński for his invaluable help organizing activities in Poland and the countless hours he worked collecting minirhizotron images. We appreciate the diligent efforts of undergraduate research assistants Mariellen Withers and Shariful R. Alam for spending hundreds of hours processing tens of thousands of images that generated these data. We extend a large thank you to the Forestry Personnel of the Siemianice Experimental Forest for collecting the temperature and precipitation data and Francoise Vermeylen of the Cornell Statistical Consulting Unit for providing valuable assistance with statistical analysis. We thank Marie Zwetsloot for her support creating the figure of the environmental conditions after the description of Walter and Lieth (1960). Funding. This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women’s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE.

Funding Information:
This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women’s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE.

Publisher Copyright:
© Copyright © 2021 Withington, Goebel, Bułaj, Oleksyn, Reich and Eissenstat.

Keywords

absorptive fine roots
deciduous
evergreen
precipitation
root phenology
root production
seasonal belowground dynamics
temperate tree species

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10.3389/fpls.2020.623722

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title = "Remarkable Similarity in Timing of Absorptive Fine-Root Production Across 11 Diverse Temperate Tree Species in a Common Garden",

abstract = "Long-term minirhizotron observations of absorptive fine roots provide insights into seasonal patterns of belowground root production and carbon dynamics. Our objective was to compare root dynamics over time across mature individuals of 11 temperate trees species: five evergreen and six deciduous. We analyzed the timing and growth on 1st-and 2nd-order roots in minirhizotron images down to a vertical depth of 35 cm, as well as monthly and total annual length production. Production patterns were related to total annual precipitation of the actual and previous year of root production over 6 years. The main or largest peak of annual fine-root production occurred between June and September for almost all species and years. In most years, when peaks occurred, the timing of peak root production was synchronized across all species. A linear mixed model revealed significant differences in monthly fine-root length production across species in certain years (species x year, P < 0.0001), which was strongly influenced by three tree species. Total annual root production was much higher in 2000–2002, when there was above-average rainfall in the previous year, compared with production in 2005–2007, which followed years of lower-than-average rainfall (2003–2006). Compared to the wetter period all species experienced a decline of at least 75% in annual production in the drier years. Total annual root length production was more strongly associated with previous year{\textquoteright}s (P < 0.001) compared with the actual year{\textquoteright}s precipitation (P = 0.003). Remarkably similar timing of monthly absorptive fine-root growth can occur across multiple species of diverse phylogeny and leaf habit in a given year, suggesting a strong influence of extrinsic factors on absorptive fine-root growth. The influence of previous year precipitation on annual absorptive fine-root growth underscores the importance of legacy effects in biological responses and suggests that a growth response of temperate trees to extreme precipitation or drought events can be exacerbated across years.",

keywords = "absorptive fine roots, deciduous, evergreen, precipitation, root phenology, root production, seasonal belowground dynamics, temperate tree species",

author = "Withington, {Jennifer M.} and Marc Goebel and Bartosz Bu{\l}aj and Jacek Oleksyn and Reich, {Peter B.} and Eissenstat, {David M.}",

note = "Funding Information: We thank Jakub Olesi{\'n}ski for his invaluable help organizing activities in Poland and the countless hours he worked collecting minirhizotron images. We appreciate the diligent efforts of undergraduate research assistants Mariellen Withers and Shariful R. Alam for spending hundreds of hours processing tens of thousands of images that generated these data. We extend a large thank you to the Forestry Personnel of the Siemianice Experimental Forest for collecting the temperature and precipitation data and Francoise Vermeylen of the Cornell Statistical Consulting Unit for providing valuable assistance with statistical analysis. We thank Marie Zwetsloot for her support creating the figure of the environmental conditions after the description of Walter and Lieth (1960). Funding. This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women{\textquoteright}s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE. Funding Information: This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women{\textquoteright}s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE. Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2021 Withington, Goebel, Bu{\l}aj, Oleksyn, Reich and Eissenstat.",

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doi = "10.3389/fpls.2020.623722",

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AU - Goebel, Marc

AU - Bułaj, Bartosz

AU - Oleksyn, Jacek

AU - Reich, Peter B.

AU - Eissenstat, David M.

N1 - Funding Information: We thank Jakub Olesiński for his invaluable help organizing activities in Poland and the countless hours he worked collecting minirhizotron images. We appreciate the diligent efforts of undergraduate research assistants Mariellen Withers and Shariful R. Alam for spending hundreds of hours processing tens of thousands of images that generated these data. We extend a large thank you to the Forestry Personnel of the Siemianice Experimental Forest for collecting the temperature and precipitation data and Francoise Vermeylen of the Cornell Statistical Consulting Unit for providing valuable assistance with statistical analysis. We thank Marie Zwetsloot for her support creating the figure of the environmental conditions after the description of Walter and Lieth (1960). Funding. This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women’s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE. Funding Information: This research was supported by the NSF Root Biology Training Grant (NSF DBI 9602255), a William J. Fulbright Foundation Fellowship in Poland, and scholarships from the Women’s Welsh Clubs of America to JW. This work was supported by the Department of Horticulture, Ecology IGDP, and the College of Agriculture Science at Penn State University to MG. It was also supported by an Eastern European International Supplement to an NSF grant (IBN 9596050) and partially supported by the US Department of Agriculture National Institute of Food and Agriculture Federal Appropriations Program under Project (PEN 04591) and Accession Number (1006803). NSF also contributed to the work through the following grants to Penn State (DEB 01298944) and to the University of Minnesota (DEB 0090069 and DEB 0128958). The USDA National Institute of Food and Agriculture and Hatch Appropriations also contributed this research under Project (PEN04744) and Accession (1023222) to DE. Publisher Copyright: © Copyright © 2021 Withington, Goebel, Bułaj, Oleksyn, Reich and Eissenstat.

PY - 2021/1/28

Y1 - 2021/1/28

N2 - Long-term minirhizotron observations of absorptive fine roots provide insights into seasonal patterns of belowground root production and carbon dynamics. Our objective was to compare root dynamics over time across mature individuals of 11 temperate trees species: five evergreen and six deciduous. We analyzed the timing and growth on 1st-and 2nd-order roots in minirhizotron images down to a vertical depth of 35 cm, as well as monthly and total annual length production. Production patterns were related to total annual precipitation of the actual and previous year of root production over 6 years. The main or largest peak of annual fine-root production occurred between June and September for almost all species and years. In most years, when peaks occurred, the timing of peak root production was synchronized across all species. A linear mixed model revealed significant differences in monthly fine-root length production across species in certain years (species x year, P < 0.0001), which was strongly influenced by three tree species. Total annual root production was much higher in 2000–2002, when there was above-average rainfall in the previous year, compared with production in 2005–2007, which followed years of lower-than-average rainfall (2003–2006). Compared to the wetter period all species experienced a decline of at least 75% in annual production in the drier years. Total annual root length production was more strongly associated with previous year’s (P < 0.001) compared with the actual year’s precipitation (P = 0.003). Remarkably similar timing of monthly absorptive fine-root growth can occur across multiple species of diverse phylogeny and leaf habit in a given year, suggesting a strong influence of extrinsic factors on absorptive fine-root growth. The influence of previous year precipitation on annual absorptive fine-root growth underscores the importance of legacy effects in biological responses and suggests that a growth response of temperate trees to extreme precipitation or drought events can be exacerbated across years.

AB - Long-term minirhizotron observations of absorptive fine roots provide insights into seasonal patterns of belowground root production and carbon dynamics. Our objective was to compare root dynamics over time across mature individuals of 11 temperate trees species: five evergreen and six deciduous. We analyzed the timing and growth on 1st-and 2nd-order roots in minirhizotron images down to a vertical depth of 35 cm, as well as monthly and total annual length production. Production patterns were related to total annual precipitation of the actual and previous year of root production over 6 years. The main or largest peak of annual fine-root production occurred between June and September for almost all species and years. In most years, when peaks occurred, the timing of peak root production was synchronized across all species. A linear mixed model revealed significant differences in monthly fine-root length production across species in certain years (species x year, P < 0.0001), which was strongly influenced by three tree species. Total annual root production was much higher in 2000–2002, when there was above-average rainfall in the previous year, compared with production in 2005–2007, which followed years of lower-than-average rainfall (2003–2006). Compared to the wetter period all species experienced a decline of at least 75% in annual production in the drier years. Total annual root length production was more strongly associated with previous year’s (P < 0.001) compared with the actual year’s precipitation (P = 0.003). Remarkably similar timing of monthly absorptive fine-root growth can occur across multiple species of diverse phylogeny and leaf habit in a given year, suggesting a strong influence of extrinsic factors on absorptive fine-root growth. The influence of previous year precipitation on annual absorptive fine-root growth underscores the importance of legacy effects in biological responses and suggests that a growth response of temperate trees to extreme precipitation or drought events can be exacerbated across years.

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KW - deciduous

KW - evergreen

KW - precipitation

KW - root phenology

KW - root production

KW - seasonal belowground dynamics

KW - temperate tree species

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Remarkable Similarity in Timing of Absorptive Fine-Root Production Across 11 Diverse Temperate Tree Species in a Common Garden

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