Abstract
Viewing plant species by their mycorrhizal type has explained a range of ecosystem processes. However, mycorrhizal type is confounded with plant phylogeny and the environments in which mycorrhizal partners occur. To circumvent these confounding effects, “dual-mycorrhizal” plant species may be potential models for testing the influence of mycorrhizal type on stand biogeochemistry. To assess their use as models, duality in mycorrhizas within a single host species must be confirmed and factors underlying their variation understood. We surveyed roots, soils, and leaves of mature aspen (Populus tremuloides) across 27 stands in western Canada spanning two biomes: boreal forest and parklands. Aspen roots were mostly ectomycorrhizal with sporadic and rare occurrences of arbuscular mycorrhizas. We further tested whether a climate moisture index predicted abundance of ectomycorrhizal roots (number of ectomycorrhizal root tips m−1 root length) surveyed at two depths (0–20 cm and 20–40 cm) and found that ectomycorrhizal root abundance in subsoils (20–40 cm) was positively related to the index. We subsequently examined the relationships between ectomycorrhizal root abundance, leaf traits, and slow and fast pools of soil organic carbon and nitrogen. The ratio of leaf lignin:N, but not its components, increased along with ectomycorrhizal root abundance in subsoils. Soil carbon and nitrogen pools were independent of ectomycorrhizal root abundance. Our results suggest that (1) categorizing aspen as dual-mycorrhizal may overstate the functional importance of arbuscular mycorrhizas in this species and life stage, (2) water availability influences ectomycorrhizal root abundance, and (3) ectomycorrhizal root abundance coincides with leaf quality.
Similar content being viewed by others
Data Availability
The datasets analyzed during the current study are available in the University of Alberta Dataverse repository, https://doi.org/10.7939/DVN/QYOHZH
References
Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. Assessment methods for soil carbon. CRC Press, Boca Raton, FL, pp 159–196
Averill C, Bhatnagar JM, Dietze MC, Pearse WD, Kivlin SN (2019) Global imprint of mycorrhizal fungi on whole-plant nutrient economics. Proc Natl Acad Sci USA 116:23163–23168. https://doi.org/10.1073/pnas.1906655116
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Sci 355:181–184. https://doi.org/10.1126/science.aai8212
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
Brundrett MC, Tedersoo L (2020) Resolving the mycorrhizal status of important northern hemisphere trees. Plant Soil. https://doi.org/10.1007/s11104-020-04627-9
Brzostek ER, Dragoni D, Brown ZA, Phillips RP (2015) Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytol 206:1274–1282. https://doi.org/10.1111/nph.13303
Cheeke TE, Phillips RP, Brzostek ER, Rosling A, Bever JD, Fransson P (2017) Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol 214:432–442. https://doi.org/10.1111/nph.14343
Clark AL, St Clair SB (2011) Mycorrhizas and secondary succession in aspen-conifer forests: Light limitation differentially affects a dominant early and late successional species. For Ecol Manage 262:203–207. https://doi.org/10.1016/j.foreco.2011.03.024
Coleman MD, Dickson RE, Isebrands JG (2000) Contrasting fine-root production, survival and soil CO2 efflux in pine and poplar plantations. Plant Soil 225:129–139. https://doi.org/10.1023/a:1026564228951
Cornelissen J, Aerts R, Cerabolini B, Werger M, van der Heijden M (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecol 129:611–619. https://doi.org/10.1007/s004420100752
Cortini F, Comeau PG, Strimbu VC, Hogg EH, Bokalo M, Huang SM (2017) Survival functions for boreal tree species in northwestern North America. For Ecol Manage 402:177–185. https://doi.org/10.1016/j.foreco.2017.06.036
Craig ME, Turner BL, Liang C, Clay K, Johnson DJ, Phillips RP (2018) Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Glob Change Biol 24:3317–3330. https://doi.org/10.1111/gcb.14132
Del Valle I et al. (2020) Soil organic matter attenuates the efficacy of flavonoid-based plant-microbe communication. Science Advances 6:eaax8254 https://doi.org/10.1126/sciadv.aax8254
Dickie IA, Koide RT, Fayish AC (2001) Vesicular-arbuscular mycorrhizal infection of Quercus rubra seedlings. New Phytol 151:257–264. https://doi.org/10.1046/j.1469-8137.2001.00148.x
Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535. https://doi.org/10.1046/j.1469-8137.2002.00535.x
Forstmeier W, Wagenmakers E-J, Parker TH (2017) Detecting and avoiding likely false-positive findings—a practical guide. Biol Rev 92:1941–1968. https://doi.org/10.1111/brv.12315
Frey SD (2019) Mycorrhizal fungi as mediators of soil organic matter dynamics. Annu Rev Ecol Evol Syst 50(50):237–259. https://doi.org/10.1146/annurev-ecolsys-110617-062331
Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecol 149:158–164. https://doi.org/10.1007/s00442-006-0437-9
Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307. https://doi.org/10.1016/j.scitotenv.2007.11.013
Hasselquist NJ, Metcalfe DB, Inselsbacher E, Stangl Z, Oren R, Nasholm T, Hogberg P (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecol 97:1012–1022. https://doi.org/10.1890/15-1222.1
Hendrick RL, Pregitzer KS (1996) Temporal and depth-related patterns of fine root dynamics in northern hardwood forests. J Ecol 84:167–176. https://doi.org/10.2307/2261352
Hogg EH (1994) Climate and the southern limit of the western Canadian boreal forest. Can J For Res 24:1835–1845. https://doi.org/10.1139/x94-237
Hogg EH (1997) Temporal scaling of moisture and the forest-grassland boundary in western Canada. Agric For Meteorol 84:115–122
Hogg EH, Brandt JP, Kochtubajda B (2005) Factors affecting interannual variation in growth of western Canadian aspen forests during 1951–2000. Can J For Res 35:610–622. https://doi.org/10.1139/x04-211
Hogg EH, Brandt JP, Michaellian M (2008) Impacts of a regional drought on the productivity, dieback, and biomass of western Canadian aspen forests. Can J For Res 38:1373–1384. https://doi.org/10.1139/x08-001
Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436. https://doi.org/10.1890/1051-0761(2000)010[0423:tvdoso]2.0.co;2
Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a C-14-labeled hardwood forest. New Phytol 172:523–535. https://doi.org/10.1111/j.1469-8137.2006.01847.x
Krishnan P, Black TA, Grant NJ, Barr AG, Hogg ETH, Jassal RS, Morgenstern K (2006) Impact of changing soil moisture distribution on net ecosystem productivity of a boreal aspen forest during and following drought. Agric For Meteorol 139:208–223. https://doi.org/10.1016/j.agrformet.2006.07.002
Kumar A, Phillips RP, Scheibe A, Klink S, Pausch J (2020) Organic matter priming by invasive plants depends on dominant mycorrhizal association Soil Biol Biochem 140. https://doi.org/10.1016/j.soilbio.2019.107645
Kuyper TW, Koele N (2016) Mycorrhizal phosphorus economies: a field test of the MANE framework. New Phytol 209:894–895. https://doi.org/10.1111/nph.13783
Lang AK, Jevon, FV, Ayres MP, Matthes JH (2020). Higher soil respiration rate beneath arbuscular mycorrhizal trees in a northern hardwood forest is driven by associated soil properties. Ecosystems 23:1243–1253. https://doi.org/10.1007/s10021-019-00466-7
Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84:2302–2312. https://doi.org/10.1890/02-0282
Liang C, Read HW, Balser TC (2012) GC-based detection of aldononitrile acetate derivatized glucosamine and muramic acid for microbial residue determination in soil. JoVE:e3767 https://doi.org/10.3791/3767
Lin G, McCormack ML, Ma C, Guo D (2017) Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–1451. https://doi.org/10.1111/nph.14206
Lodge DJ (1989) The influence of soil-moisture and flooding on formation of VA-endomycorrhizae and ectomycorrhizae in Populus and Salix. Plant Soil 117:243–253. https://doi.org/10.1007/bf02220718
Lodge DJ, Wentworth TR (1990) Negative associations among VA-mycorrhizal fungi and some ectomycorrhizal fungi inhabiting the same root-system. Oikos 57:347–356. https://doi.org/10.2307/3565964
Lofgren LA, Uehling JK, Branco S, Bruns TD, Martin F, Kennedy PG (2019) Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Mol Ecol 28:721–730. https://doi.org/10.1111/mec.14995
Michaelian M, Hogg E, Hall R, Arsenault E (2011) Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob Change Biol 17:2084–2094. https://doi.org/10.1111/j.1365-2486.2010.02357.x
Moorhead DL, Reynolds JF (1993) Changing carbon-chemistry of buried creosote bush litter during decomposition in the northern Chihuahuan desert. Am Midl Nat 130:83–89. https://doi.org/10.2307/2426277
Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216. https://doi.org/10.1016/s0929-1393(01)00193-7
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221
Piotrowski JS, Morford SL, Rillig MC (2008) Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. Soil Biol Biochem 40:709–717. https://doi.org/10.1016/j.soilbio.2007.10.005
Rasband W (2016) ImageJ. U.S, National Institutes of Health, Bethesda, Maryland, U.S.
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391. https://doi.org/10.1007/bf01972080
Read DJ, Perez‐Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems–a journey towards relevance? New phytologist 1;157(3):475-92.
Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, Taylor AFS, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–783. https://doi.org/10.1046/j.1469-8137.2003.00829.x
Soudzilovskaia NA et al (2015a) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382. https://doi.org/10.1111/geb.12272
Soudzilovskaia NA et al (2020) FungalRoot: global online database of plant mycorrhizal associations. New Phytol 227:955–966. https://doi.org/10.1111/nph.16569
Soudzilovskaia et al (2019) Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nat Commun https://doi.org/10.1038/s41467-019-13019-2
Soudzilovskaia NA et al (2015b) Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling. New Phytol 208:280–293. https://doi.org/10.1111/nph.13447
Steidinger BS et al (2019) Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569:404–408. https://doi.org/10.1038/s41586-019-1128-0
Sun T, Hobbie SE, Berg B, Zhang H, Wang Q, Wang Z, Hättenschwiler S (2018) Contrasting dynamics and trait controls in first-order root compared with leaf litter decomposition. Proc Natl Acad Sci 115:10392–10397. https://doi.org/10.1073/pnas.1716595115
Talbot JM, Treseder KK (2012) Interactions among lignin, cellulose, and nitrogen drive litter chemistry-decay relationships. Ecology 93:345–354. https://doi.org/10.1890/11-0843.1
Tedersoo L, Bahram M (2019) Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol Rev. https://doi.org/10.1111/brv.12538
Terrer C, Vicca S, Hungate BA, Phillips RP, Prentice IC (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74. https://doi.org/10.1126/science.aaf4610
Teste FP, Jones MD, Dickie IA (2020) Dual-mycorrhizal plants: their ecology and relevance. New Phytol 225:1835–1851. https://doi.org/10.1111/nph.16190
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. https://doi.org/10.1111/j.1469-8137.2004.01159.x
Visser S, Maynard D, Danielson RM (1998) Response of ecto- and arbuscular mycorrhizal fungi to clear-cutting and the application of chipped aspen wood in a mixedwood site in Alberta, Canada. Appl Soil Ecol 7:257–269. https://doi.org/10.1016/s0929-1393(97)00060-7
Wallander H et al (2013) Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils - a review. Soil Biol Biochem 57:1034–1047. https://doi.org/10.1016/j.soilbio.2012.08.027
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants Mycorrhiza 16. https://doi.org/10.1007/s00572-005-0033-6
Weber A, Karst J, Gilbert B, Kimmins JP (2005) Thuja plicata exclusion in ectomycorrhiza-dominated forests: testing the role of inoculum potential of arbuscular mycorrhizal fungi. Oecol 143:148–156. https://doi.org/10.1007/s00442-004-1777-y
Weemstra M, Peay KG, Davies SJ, Mohamad M, Itoh A, Tan S, Russo SE (2020) Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest. New Phytol. https://doi.org/10.1111/nph.16672
Worrall JJ, Rehfeldt GE, Hamann A, Hogg EH, Marchetti SB, Michaelian M, Gray LK (2013) Recent declines of Populus tremuloides in North America linked to climate. For Ecol Manage 299:35–51. https://doi.org/10.1016/j.foreco.2012.12.033
Youngentob KN, Zdenek C, van Gorsel E (2016) A simple and effective method to collect leaves and seeds from tall trees. Methods Ecol Evol 7:1119–1123. https://doi.org/10.1111/2041-210x.12554
Zhang HY, Lu XT, Hartmann H, Keller A, Han XG, Trumbore S, Phillips RP (2018) Foliar nutrient resorption differs between arbuscular mycorrhizal and ectomycorrhizal trees at local and global scales. Glob Ecol Biogeogr 27:875–885. https://doi.org/10.1111/geb.12738
Acknowledgements
Brea Burton, Christine Simard, Jason Eerkes, and Nicholas Brown collected field samples with JK. JK also had help from Ariel Brown, Paul Metzler, and Serena Farrugia to pick roots from soils. NE’s lab and Pak Chow analyzed amino sugars. Amy Nixon, Kelly Karst, and Kelsey Krause provided free lodging during the field survey. Sincere thanks to the Peace River Conservation Officers for trapping a problem bear. Mike Michaelian and Ted Hogg from the Canadian Forest Service facilitated access to the field sites and gave feedback on the manuscript. Location, aspen basal area, and climate moisture index data provided by the Canadian Forest Service (Natural Resources Canada). Melanie Jones and Richard Phillips provided constructive feedback on the manuscript.
Funding
Natural Sciences and Engineering Research Council of Canada.
Author information
Authors and Affiliations
Contributions
JK conceived, designed, and performed the survey with input from JB. JK analyzed data with guidance from JB. JF, AS, JB, and AL processed samples. NE developed methods for quantifying amino sugars. JK wrote first draft of manuscript, and all authors contributed substantially to revisions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Karst, J., Franklin, J., Simeon, A. et al. Assessing the dual-mycorrhizal status of a widespread tree species as a model for studies on stand biogeochemistry. Mycorrhiza 31, 313–324 (2021). https://doi.org/10.1007/s00572-021-01029-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-021-01029-2