Abstract
Aims
The purpose of this study was to clarify how the morphological traits of Chamaecyparis obtusa (Sieb. & Zucc.) Endl. roots vary with soil acid buffering capacity (ABC), i.e., along a gradient in soil acidification. We used an order-based root classification system instead of a diameter-based root classification system, as the former relates better to root function.
Methods
We sampled 210 intact fine root systems up to the fourth order and measured the morphological traits of a total of 16,657 individual branch-order roots in three C. obtusa stands with high soil ABC and four stands with low soil ABC.
Results
We found significant differences in the morphological traits of the first- to fourth-order roots between the soil ABCs. In the low-ABC soils, the fine root systems consisted of more and thinner roots than in the high-ABC soils. The diameter of the second-order roots was positively correlated with the soil pH and the concentration of base cations, but negatively with soil aluminum.
Conclusion
Morphological traits of fine roots are sensitive indicators of soil acidification in C. obtusa forests.
Similar content being viewed by others
Abbreviations
- ABC:
-
Acid buffering capacity
- BC:
-
Base cation
- BS:
-
Base saturation
- Rb:
-
Branching ratio
- SRL:
-
Specific root length
References
Braun S, Cantaluppi L, Flückiger W (2005) Fine roots in stands of Fagus sylvatica and Picea abies along a gradient of soil acidification. Environ Pollut 137:574–579. https://doi.org/10.1016/j.envpol.2005.01.042
De Schrijver A, De Frenne P, Staelens J, Verstraeten G, Muys B, Vesterdal L, Wuyts K, van Nevel L, Schelfhout S, De Neve S, Verheyen K (2012) Tree species traits cause divergence in soil acidification during four decades of postagricultural forest development. Glob Chang Biol 18:1127–1140. https://doi.org/10.1111/j.1365-2486.2011.02572.x
Doi R, Tanikawa T, Miyatani K, Hirano Y (2017) Intraspecific variation in morphological traits of root branch orders in Chamaecyparis obtusa. Plant Soil 416:503–513. https://doi.org/10.1007/s11104-017-3230-0
Duan L, Yu Q, Zhang Q, Wang Z, Pan Y, Larssen T, Tang J, Mulder J (2016) Acid deposition in Asia: emissions, deposition, and ecosystem effects. Atmos Environ 146:55–69. https://doi.org/10.1016/j.atmosenv.2016.07.018
Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124. https://doi.org/10.1111/nph.13451
Forestry Agency of Japan (1997) Report for forest damage- monitoring project by acid deposition (1990–1994). Tokyo (in Japanese)
Godbold DL, Fritz HW, Jentschke G, Meesenburg H, Rademacher P (2003) Root turnover and root necromass accumulation of Norway spruce (Picea abies) are affected by soil acidity. Tree Physiol 23:915–921
Guo D, Mitchell RJ, Withington JM, Fan PP, Hendricks JJ (2008) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745. https://doi.org/10.1111/j.1365-2745.2008.01385.x
Hirano Y, Hijii N (1998) Effects of low pH and Al on root morphology of Japanese red cedar saplings. Environ Pollut 101:339–347. https://doi.org/10.1016/S0269-7491(98)00058-X
Hirano Y, Isomura A, Kaneko S (2003) Root morphology and nutritional status of Japanese red cedar saplings subjected to in situ levels of aluminum in forest soil solution. J For Res 8:209–214. https://doi.org/10.1007/s10310-003-0027-1
Hirano Y, Mizoguchi T, Brunner I (2007) Root parameters of forest trees as sensitive indicators of acidifying pollutants: a review of research of Japanese forest trees. J For Res 12:134–142. https://doi.org/10.1007/s10310-006-0263-2
Hirano Y, Tanikawa T, Makita N (2017) Biomass and morphology of fine roots in eight Cryptomeria japonica stands in soils with different acid-buffering capacities. For Ecol Manag 384:122–131. https://doi.org/10.1016/j.foreco.2016.10.043
Hishi T, Tateno R, Takeda H (2006) Anatomical characteristics of individual roots within the fine-root architecture of Chamaecyparis obtusa (Sieb. & Zucc.) in organic and mineral soil layers. Ecol Res 21:754–758. https://doi.org/10.1007/s11284-006-0184-8
Jia S, Wang Z, Li X, Zhang X, Mclaughlin NB (2011) Effect of nitrogen fertilizer, root branch order and temperature on respiration and tissue N concentration of fine roots in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 31:718–726. https://doi.org/10.1093/treephys/tpr057
Jia S, McLaughlin NB, Gu J, Li X, Wang Z (2013) Relationships between root respiration rate and root morphology, chemistry and anatomy in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 33:579–589. https://doi.org/10.1093/treephys/tpt040
Kong D, Ma C, Zhang Q, Li L, Chen X, Zeng H, Guo D (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872. https://doi.org/10.1111/nph.12842
Liu X, Duan L, Mo J, Du E, Shen J, Lu X, Zhang Y, Zhou X, He C, Zhang F (2011) Nitrogen deposition and its ecological impact in China: an overview. Environ Pollut 159:2251–2264
Makita N, Hirano Y, Dannoura M, Kominami Y, Mizoguchi T, Ishii H, Kanazawa Y (2009) Fine root morphological traits determine variation in root respiration of Quercus serrata. Tree Physiol 29:579–585. https://doi.org/10.1093/treephys/tpn050
Makita N, Hirano Y, Mizoguchi T, Kominami Y, Dannoura M, Ishii H, Finér L, Kanazawa Y (2011) Very fine roots respond to soil depth: biomass allocation, morphology, and physiology in a broad-leaved temperate forest. Ecol Res 26:95–104. https://doi.org/10.1007/s11284-010-0764-5
Makita N, Kosugi Y, Dannoura M, Takanashi S, Niiyama K, Kassim AR, Nik AR (2012) Patterns of root respiration rates and morphological traits in 13 tree species in a tropical forest. Tree Physiol 32:303–312. https://doi.org/10.1093/treephys/tps008
Makita N, Hirano Y, Sugimoto T, Tanikawa T, Ishii H (2015) Intraspecific variation in fine root respiration and morphology in response to in situ soil nitrogen fertility in a 100-year-old Chamaecyparis obtusa forest. Oecologia 179:959–967. https://doi.org/10.1007/s00442-015-3413-4
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363
Meng C, Tian D, Zeng H, Li C, Yi C, Niu S (2019) Global soil acidification impacts on belowground processes. Environ Res Lett 14:074003. https://doi.org/10.1088/1748-9326/ab239c
Miyatani K, Mizusawa Y, Okada K, Tanikawa T, Makita N, Hirano Y (2016) Fine root traits in Chamaecyparis obtusa forest soils with different acid buffering capacities. Trees Struct Funct 30:415–429. https://doi.org/10.1007/s00468-015-1291-3
Miyatani K, Tanikawa T, Makita N, Hirano Y (2018) Relationships between specific root length and respiration rate of fine roots across stands and seasons in Chamaecyparis obtusa. Plant Soil 423:215–227. https://doi.org/10.1007/s11104-017-3499-z
Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442. https://doi.org/10.1080/11263500701626069
Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309. https://doi.org/10.1890/0012-9615(2002)072[0293:FRAONN]2.0.CO;2
Singh S, Tripathi DK, Sharma S, Dubey NK, Chauhan DK, Vaculik M (2017) Toxicity of aluminum on various levels of plant cells and organism: a review. Environ Exp Bot 137:177-193. https://doi.org/10.1016/j.envexpbot.2017.01.005
Takahashi M, Sakata T, Ishizuka K (2001) Chemical characteristics and acid buffering capacity of surface soils in Japanese forests. Water Air Soil Pollut 130:727–732
Tanikawa T, Sobue A, Hirano Y (2014) Acidification processes in soils with different acid buffering capacity in Cryptomeria japonica and Chamaecyparis obtusa forests over two decades. For Ecol Manag 334:284–292. https://doi.org/10.1016/j.foreco.2014.08.036
Tanikawa T, Ito Y, Fukushima S, Yamashita M, Sugiyama A, Mizoguchi T, Okamoto T, Hirano Y (2017) Calcium is cycled tightly in Cryptomeria japonica stands on soils with low acid buffering capacity. For Ecol Manag 399:64–73. https://doi.org/10.1016/j.foreco.2017.04.022
Tanikawa T, Fujii S, Sun L, Hirano Y, Matsuda Y, Miyatani K, Doi R, Mizoguchi T, Maie N (2018) Leachate from fine root litter is more acidic than leaf litter leachate: a 2.5-year laboratory incubation. Sci Total Environ 645:179–191. https://doi.org/10.1016/j.scitotenv.2018.07.038
Tawa Y, Takeda H (2015) Which is the best indicator for distinguishing between fine roots with primary and secondary development in Cryptomeria japonica D. Don: diameter, branching order, or protoxylem groups? Plant Roots 9:79–84. https://doi.org/10.3117/plantroot.9.79
Vanguelova EI, Hirano Y, Eldhuset TD, Sas-Paszt L, Bakker MR, Püttsepp Ü, Brunner I, Lõhmus K, Godbold D (2007) Tree fine root Ca/Al molar ratio - Indicator of Al and acidity stress. Plant Biosyst 141:460–480. https://doi.org/10.1080/11263500701626192
Wada R, Tanikawa T, Doi R, Hirano Y (2019) Variation in the morphology of fine roots in Cryptomeria japonica determined by branch order-based classification. Plant Soil:139–151. https://doi.org/10.1007/s11104-019-04264-x
Wang Z, Guo D, Wang X, Gu J, Mei L (2006) Fine root architecture, morphology, and biomass of different branch orders of two Chinese temperate tree species. Plant Soil 288:155–171. https://doi.org/10.1007/s11104-006-9101-8
Wang G, Fahey TJ, Xue S, Liu F (2013) Root morphology and and architecture respond to N addition in Pinus tabuliformis, West China. Oecologia 171:583–390. https://doi.org/10.1007/s00442-012-2441-6
Yan G, Zhou M, Wang M, Han S, Liu G, Zhang X, Sun W, Huang B, Wang H, Xing Y, Wang Q (2019) Nitrogen deposition and decreased precipitation altered nutrient foraging strategies of three temperate trees by affecting root and mycorrhizal traits. Catena 181:104094. https://doi.org/10.1016/j.catena.2019.104094
Zadworny M, McCormack ML, Rawlik K, Jagodziński AM (2015) Seasonal variation in chemistry, but not morphology, in roots of Quercus robur growing in different soil types. Tree Physiol 35:644–652. https://doi.org/10.1093/treephys/tpv018
Zadworny M, McCormack ML, Mucha J, Reich P, Oleksyn J (2016) Scots pine fine roots adjust along a 2000-km latitudinal climatic gradient. New Phytol 212:389–399. https://doi.org/10.1111/nph.14048
Zadworny M, McCormack ML, Żytkowiak R, Karolewski P, Mucha J, Oleksyn J (2017) Patterns of structural and defense investments in fine roots of scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe. Glob Chang Biol 23:1218–1231. https://doi.org/10.1111/gcb.13514
Acknowledgements
We are grateful to the editor and two anonymous reviewers for giving constructive comments and fruitful suggestions on our earlier version of the manuscript. We thank M. Ohashi (University of Hyogo) for reading the first draft of the manuscript and providing invaluable comments. We thank M. Takano, Y. Yamaguchi, and T. Miyasaka (Nagoya University) for their valuable suggestions. We thank K. Miyatani (Nagoya University), T. Okamoto, T. Mizoguchi (Forestry and Forest Product Research Institute) for their assistance and guidance with the field work and laboratory analyses. We thank H. Fukumoto (Mie Prefectural Forestry Research Center), Y. Kodaka (Inabe Hokusei agency), S. Suzuki (Okazaki municipal office), T. Kadoya (Aichi Prefectural Forestry Institute), T. Hakamata (Shizuoka Prefectural Research Institute of Agriculture and Forestry), S. Ishihara (Numazu municipal office), H. Watanabe, Y. Motegi (Gifu Prefectural Research Institute for Forests), and the Tenryuu District Forest Office for permission to use the forest health-monitoring survey sites of the Forest Agency of Japan. This study was partly supported by JSPS KAKENHI Grant Number 15H04519, 18J23364, 19H03011.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Boris Rewald.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 21 kb)
Rights and permissions
About this article
Cite this article
Doi, R., Tanikawa, T., Wada, R. et al. Morphological traits of Chamaecyparis obtusa fine roots are sensitive to soil acid buffering capacity. Plant Soil 452, 73–85 (2020). https://doi.org/10.1007/s11104-020-04561-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04561-w