Ectomycorrhizal (EcM) tree species often become more dominant than arbuscular mycorrhizal (AM) tree species in temperate forests, but they generally coexist. Theory predicts that ecological feedback mediated by aboveground herbivory and/or belowground microbes could explain these dominance/coexistence patterns. An experimental test of how aboveground/belowground organisms associated with AM/EcM trees mediate ecological feedbacks has been lacking at the community-level. By establishing AM and EcM tree sapling assemblages in mesocosms and then introducing seedlings of each type in a reciprocal planting experiment, we compared seedling performance under varying sapling species (conspecifics, heterospecifics within the same and different mycorrhizal types), using traits that reflect either aboveground herbivory-mediated feedback or belowground fungal-mediated feedback or both. When examining seedling traits that reflect aboveground herbivory-mediated feedbacks (i.e., foliar damage), AM plants tended to experience less foliar damage and EcM plants more damage under conspecific versus heterospecific saplings within the same mycorrhizal types, and aboveground herbivory-mediated feedback was species-specific rather than mycorrhizal type–specific. Conversely, when examining traits that reflect belowground fungal-mediated feedbacks, both AM and EcM plant species often exhibited mycorrhizal type-specific feedbacks (e.g., greater aboveground biomass under the same versus different mycorrhizal-type saplings) rather than species-specific feedbacks. Furthermore, tree species affected by herbivory-mediated feedback were less affected by belowground feedback, indicating that the relative importance of the feedbacks varied among plant species. Analysis of plant-associated organisms verified that the feedback outcomes corresponded with species accumulation of belowground fungi (but not of aboveground herbivores). Thus, aboveground herbivores drive stronger plant species-specific feedback than belowground fungi to regulate temperate tree diversity.
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Arthropod data and its taxonomic information are provided as Online Resource Data 1. Fungal ITS sequences have been deposited under accession numbers BioProject PRJDB5467 and DDBJ DRA005499. The fungal community data is available as Appendix Data 2 of a previous publication (Kadowaki et al. 2018).
Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatRef. https://doi.org/10.1002/9781118445112.stat07841
Babikova Z, Gilbert L, Bruce TJA, Birkett M, Woodcock C, Pickett JA, Johnson D (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843
Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis VE, Freckleton RF, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88
Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Baxendale C, Orwin KH, Poly F, Pommier T, Bardgett RD (2014) Are plant–soil feedback responses explained by plant traits? New Phytol 204:408–423
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478
Booth MG (2004) Mycorrhizal networks mediate overstorey–understorey competition in a temperate forest. Ecol Lett 7:538–546
Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodomicance in a neotropical forest. Ecol Lett 19:383–392
Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–162
Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255
Gorzelek MA, Asay AK, Pickles BJ, Simard SW (2015) Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7:plv050
Guyot V, Jactel H, Imbaud B, Burnel L, Castagnerol B, Heinz W, Deconchat M, Vialatte (2018) Tree diversity drives associational resistance to herbivory at both forest edge and interior. Ecol Evol 9:9040–9051
Heinze J, Simons BK, Seibold S, Wacker A, Weithoff G, Gossner MM, Prati D, Bezemer TM, Joshi J (2019) The relative importance if plant–soil feedbacks for plans-species performance increases with decreasing intensity of herbivory. Oecologia 190:651–664
Hendriks M, Ravenek JM, Smit-Tiekstra AE, van Paauw JW, de Cluwe H, van der Putten WH (2015) Spatial heterogeneity of plant–soil feedback affects root interactions and interspecific competition. New Phytol 207:830–840
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Kadowaki K, Yamamoto S, Sato H, Tanabe AS, Hidaka A, Toju H (2018) Mycorrhizal fungi mediate the direction and strength of plant–soil feedback differently. Commun Biol 1:196
Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman T (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 72:147−162
Kong HG, Song GC, Ryu CM (2019) Inheritance of seed and rhizosphere microbial communities through plant–soil feedback and soil memory. Environ Microbiol Rep 11:479–486
Kos M, Bukovinszky T, Mulder PPJ, Bezemer TM (2015) Disentangling above- and belowground neighbor effects on the growth, chemistry, and arthropod community on a focal plant. Ecology 96:164–175
Liang M, Liu X, Etienne RS, Huang F, Wang Y, Yu S (2015) Arbuscular mycorrhizal fungi counteract the Janzen–Connell effect of soil pathogens. Ecology 96:562–574
Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755
Oksanen JF, Blanchet G, Kindt R, Legendre PR, Minchin RB, O'Hara GL, Solymos SP, Henry M, Stevens H, Wagner H (2019) vegan. R package version 2.4-5.
Pendergast T IV, Burke HDJ, Carson WP (2013) Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytol 197:1300–1310
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 99:41–51
Plath M, Dorn S, Riedel J, Barrios H, Mody K (2012) Associational resistance and associational susceptibility: specialist herbivores show contrasting responses to tree stand diversification. Oecologia 169:477–487
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391
Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL (2014) Soil microbes drive the classic diversity-productivity pattern. Ecology 92:296–303
Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165
Smith-Ramesh LM, Reynolds HL (2017) The next frontier of plant–soil feedback research: unraveling context dependence across biotic and abiotic gradients. J Veg Sci 28:484–494
Tedersoo L, Bahram M (2019) Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol Rev 94:1857–1880
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367:eaba1223
Toju H, Guimares PR, Olsen JM, Thompson JN (2014) Assembly of complex plant–fungus networks. Nat Comm 5:5273
Toju H, Guimares PR, Olsen JM, Thompson JN (2015) Below-ground plant–fungus network topology is not congruent with above-ground plant–animal network topology. Sci Adv 1:e1500291
Toju H, Tanabe AS, Sato H (2018) Network hubs in root-associated fungal metacommunities. Microbiome 6:116
van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276
Wolda H (1981) Similarity indices, sample size and diversity. Oecologia 50:296–302
Wubs ERJ, Bezemer TM (2017) Plant community evenness responds to spatial plant–soil feedback heterogeneity primarily through the diversity of soil conditioning. Funct Ecol 32:509–521
This work was supported by Next Generation World-Leading Researchers of Cabinet Office, the Japanese Government (GS014), KAKENHI (26711026), JST PRESTO (JPMJPR16Q6) and Human Frontier Science Program (RGP0029/2019) to HT and JSPS Research Fellowship (13J02732) to KK. We thank Kyoto University Botanical Garden for supporting this work, and Hiroyuki Yoshitomi and Naoki Koike for taxonomic assistance. Tomoko Kadowaki and many students assisted with this experiment, and their help has been invaluable. Corné Pieterse and three anonymous reviewers provided comments that improved the manuscript greatly.
Conflict of interest
The authors declare no conflict of interest.
Communicated by Corné Pieterse.
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Kadowaki, K., Yamamoto, S., Sato, H. et al. Aboveground herbivores drive stronger plant species-specific feedback than belowground fungi to regulate tree community assembly. Oecologia (2021). https://doi.org/10.1007/s00442-021-04868-0
- Mycorrhizal fungi
- Mycorrhizal type