Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest.
arbuscular mycorrhiza
ectomycorrhiza
functional traits
nutrient cycling
plant-soil feedback
soil fertility
tropical forests
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
22
10
2019
accepted:
11
05
2020
pubmed:
22
5
2020
medline:
15
5
2021
entrez:
22
5
2020
Statut:
ppublish
Résumé
Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant-soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF-hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF-hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF-hosting species had slower leaf economics than AMF-hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale-dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
253-268Informations de copyright
© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.
Références
Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1-67.
Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
Ashton, PS. 2005. Lambir's forest: the world's most diverse known tree assemblage? In: Roubik, D, Sakai, S, Hamid, AA, eds. Pollination ecology and the rain forest: Sarawak studies. New York, NY, USA: Springer, 191-216.
Ashton PS, Hall P. 1992. Comparisons of structure among mixed dipterocarp forests of north-western Borneo. Journal of Ecology 80: 459-481.
Auge RM, Stodola AJW, Brown MS, Bethlenfalvay GJ. 1992. Stomatal response of mycorrhizal cowpea and soybean to short-term osmotic stress. New Phytologist 120: 117-125.
Augusto L, Achat DL, Jonard M, Vidal D, Ringeval B. 2017. Soil parent material-a major driver of plant nutrient limitations in terrestrial ecosystems. Global Change Biology 23: 3808-3824.
Averill C, Bhatnagar JM, Dietze MC, Pearse WD, Kivlin SN. 2019. Global imprint of mycorrhizal fungi on whole-plant nutrient economics. Proceedings of the National Academy of Sciences, USA 116: 23163.
Baillie IC, Ashton PS, Chin SP, Davies SJ, Palmiotto PA, Russo SE, Tan S. 2006. Spatial associations of humus, nutrients, and soils in mixed dipterocarp forest at Lambir, Sarawak, Malaysian Borneo. Journal of Tropical Ecology 22: 543-553.
Baillie IC, Ashton PS, Court MN, Anderson JAR, Fitzpatrick EA, Tinsley J. 1987. Site characteristics and the distribution of tree species in mixed dipterocarp forest on Tertiary sediments in Central Sarawak, Malaysia. Journal of Tropical Ecology 3: 201-220.
Baltzer JL, Thomas SC, Nilus R, Burslem DFRP. 2005. Edaphic specialization in tropical trees: physiological correlates and responses to reciprocal transplantation. Ecology 86: 3063-3077.
Bates D, Mächler M, Bolker BM, Walker SC. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1-48.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57: 289-300.
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, Rillig MC, Stock WD, Tibbett M, Zobel M. 2010. Rooting theories of plant community ecology in microbial interactions. Trends in Ecology & Evolution 25: 468-478.
Bever JD, Westover KM, Antonovics J. 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology 85: 561-573.
Blum JD, Klaue A, Nezat CA, Driscoll CT, Johnson CE, Siccama TG, Eagar C, Fahey TJ, Likens GE. 2002. Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417: 729-731.
Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson Å, Lindahl BD. 2014. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist 203: 245-256.
Brearley F. 2012. Ectomycorrhizal associations of the Dipterocarpaceae. Biotropica 44: 637-648.
Brearley FQ, Press MC, Scholes JD. 2003. Nutrients obtained from leaf litter can improve the growth of dipterocarp seedlings. New Phytologist 160: 101-110.
Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320: 37-77.
Brundrett MC, Tedersoo L. 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220: 1108-1115.
Brzostek ER, Fisher JB, Phillips RP. 2014. Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation. Journal of Geophysical Research: Biogeosciences 119: 1684-1697.
Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO. 1999. Changing sources of nutrients during four million years of ecosystem development. Nature 397: 491-497.
Chapin FS, Autumn K, Pugnaire F. 1993. Evolution of suites of traits in response to environmental stress. American Naturalist 142: S78-S92.
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 Phytologist 214: 432-442.
Clark DA, Clark DB. 1992. Life history diversity of canopy and emergent trees in a neotropical rain forest. Ecological Monographs 62: 315-344.
Condit R. 1998. tropical forest census plots: methods and results from Barro Colorado Island, Panama and a comparison with other plots. Berlin, Germany: Springer.
Coomes DA, Georges K, Charles DC, Elaine W. 2009. A greater range of shade-tolerance niches in nutrient-rich forests: an explanation for positive richness-productivity relationships? Journal of Ecology 97: 705-717.
Cornelissen J, Aerts R, Cerabolini B, Werger M, van der Heijden M. 2001. Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129: 611-619.
Cornelissen JHC, Quested HM, Gwynn-Jones D, Van Logtestijn RSP, De Beus MAH, Kondratchuk A, Callaghan TV, Aerts R. 2004. Leaf digestibility and litter decomposability are related in a wide range of subarctic plant species and types. Functional Ecology 18: 779-786.
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N et al. 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters 11: 1065-1071.
Corrales A, Henkel TW, Smith ME. 2018. Ectomycorrhizal associations in the tropics - biogeography, diversity patterns and ecosystem roles. New Phytologist 220: 1076-1091.
Corrales A, Mangan SA, Turner BL, Dalling JW. 2016. An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecology Letters 19: 383-392.
Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A et al. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytologist 183: 980-992.
Davies SJ, Becker P. 1996. Floristic composition and stand structure of mixed dipterocarp and heath forests in Brunei Darussalam. Journal of Tropical Forest Science 8: 542-569.
Davies SJ, Palmiotto PA, Ashton PS, Lee HS, Lafrankie JV. 1998. Comparative ecology of 11 sympatric species of Macaranga in Borneo: Tree distribution in relation to horizontal and vertical resource heterogeneity. Journal of Ecology 86: 662-673.
Davies SJ, Tan S, LaFrankie JV, Potts MD. 2005. Soil-related floristic variation in the hyperdiverse dipterocarp forest in Lambir Hills, Sarawak. In: Roubik DW, Sakai S, Hamid A, eds. Pollination Ecology and Rain Forest Diversity, Sarawak Studies. New York, NY, USA: Springer-Verlag, 22-34.
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP. 2002. Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33: 507-559.
DeForest JL, Snell RS. 2020. Tree growth response to shifting soil nutrient economy depends on mycorrhizal associations. New Phytologist 225: 2557-2566.
Dent DH, Bagchi R, Robinson D, Majalap-Lee N, Burslem D. 2006. Nutrient fluxes via litterfall and leaf litter decomposition vary across a gradient of soil nutrient supply in a lowland tropical rain forest. Plant and Soil 288: 197-215.
Ehleringer JR, Hall AE, Farquhar GD. 1993. Stable isotopes and plant carbon/water relations. San Diego, CA, USA: Academic Press.
Fernandez CW, Kennedy PG. 2016. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytologist 209: 1382-1394.
Fine PVA, Kembel SW. 2011. Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34: 552-565.
Freschet GT, Aerts R, Cornelissen JHC. 2012. A plant economics spectrum of litter decomposability: Afterlife effects of the plant economics spectrum. Functional Ecology 26: 56-65.
Fukami T, Nakajima M, Fortunel C, Fine PVA, Baraloto C, Russo SE, Peay KG. 2017. Geographical variation in community divergence: Insights from tropical forest monodominance by ectomycorrhizal trees. American Naturalist 190(S1): S105-S122.
Gadgil RL, Gadgil PD. 1971. Mycorrhiza and litter decomposition. Nature 233: 133.
Grime JP, Cornelissen JHC, Thompson K, Hodgson JG. 1996. Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77: 489-494.
Güsewell S. 2004. N : P ratios in terrestrial plants: variation and functional significance. New Phytologist 164: 243-266.
Hobbie EA. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87: 563-569.
Hobbie EA, Agerer R. 2010. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil 327: 71-83.
Hobbie EA, Colpaert JV. 2003. Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytologist 157: 115-126.
Hobbie EA, Hobbie JE. 2008. Natural abundance of 15N in nitrogen-limited forests and Tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11: 815-830.
Hobbie SE. 1992. Effects of plant species on nutrient cycling. Trends in Ecology & Evolution 7: 336-339.
Hobbie SE. 2015. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends in Ecology & Evolution 30: 357-363.
Hodge A. 2001. Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151: 725-734.
Hogberg P. 1997. Tansley Review No. 95. 15N natural abundance in soil-plant systems. New Phytologist 137: 179-203.
Horner JD, Gosz JR, Cates RG. 1988. The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. American Naturalist 132: 869-883.
Houlton BZ, Sigman DM, Schuur EAG, Hedin LO. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proceedings of the National Academy of Sciences, USA 104: 8902-8906.
Jenny H. 1980. The soil resource: origin and behavior. New York, NY, USA: Springer-Verlag.
Jucker T, Bongalov B, Burslem DFRP, Nilus R, Dalponte M, Lewis SL, Phillips OL, Qie L, Coomes DA. 2018. Topography shapes the structure, composition and function of tropical forest landscapes. Ecology Letters 21: 989-1000.
Katabuchi M, Kurokawa H, Davies SJ, Tan S, Nakashizuka T. 2012. Soil resource availability shapes community trait structure in a species-rich dipterocarp forest. Journal of Ecology 100: 643-651.
Keller AB, Phillips RP. 2019. Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytologist 222: 556-564.
Kobe RK, Lepczyk CA, Iyer M. 2005. Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86: 2780-2792.
Kochsiek A, Tan S, Russo SE. 2013. Fine root dynamics in relation to nutrients in oligotrophic Bornean rain forest soils. Plant Ecology 214: 869-882.
Koele N, Dickie IA, Blum JD, Gleason JD, de Graaf L. 2014. Ecological significance of mineral weathering in ectomycorrhizal and arbuscular mycorrhizal ecosystems from a field-based comparison. Soil Biology and Biochemistry 69: 63-70.
Koele N, Dickie IA, Oleksyn J, Richardson SJ, Reich PB. 2012. No globally consistent effect of ectomycorrhizal status on foliar traits. New Phytologist 196: 845-852.
Kurokawa H, Nakashizuka T. 2008. Leaf herbivory and decomposability in a Malaysian tropical rain forest. Ecology 89: 2645-2656.
Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N. 2001. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends in Ecology & Evolution 16: 248-254.
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany 82: 1016-1045.
Lee HS, Ashton PS, Yamakura T, Tan S, Davies SJ, Itoh A, Chai EOK, Ohkubo T, LaFrankie JV. 2002a. The 52-ha forest research plot at Lambir Hills National Park, Sarawak, Malaysia: tree distribution maps, diameter tables, and species documentation. Kuching, Sarawak, Malaysia: Sarawak Forest Department, Center for Tropical Forest Science - Arnold Arboretum Asia Program, & Smithsonian Tropical Research Institute.
Lee HS, Davies SJ, LaFrankie JV, Tan S, Yamakura T, Itoh A, Ohkubo T, Ashton PS. 2002b. Floristic and structural diversity of mixed dipterocarp forest in Lambir Hills National Park, Sarawak, Malaysia. Journal of Tropical Forest Science 14: 379-400.
Lehto T, Zwiazek JJ. 2011. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21: 71-90.
Lin G, Guo D, Li L, Ma C, Zeng D-H. 2018. Contrasting effects of ectomycorrhizal and arbuscular mycorrhizal tropical tree species on soil nitrogen cycling: the potential mechanisms and corresponding adaptive strategies. Oikos 127: 518-530.
Lindahl BD, Tunlid A. 2015. Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. New Phytologist 205: 1443-1447.
Liu X, Burslem DFRP, Taylor JD, Taylor AFS, Khoo E, Majalap-Lee N, Helgason T, Johnson D. 2018. Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests. Ecology Letters 21: 713-723.
Liu X, Swenson NG, Wright SJ, Zhang L, Song K, Du Y, Zhang J, Mi X, Ren H, Ma K. 2012. Covariation in plant functional traits and soil fertility within two species-rich forests. PLoS ONE 7: e34767.
Lu M, Hedin LO. 2019. Global plant-symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling. Nature Ecology & Evolution 3: 239-250.
Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. 1999. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry 46: 45-65.
Mayor J, Bahram M, Henkel T, Buegger F, Pritsch K, Tedersoo L. 2015. Ectomycorrhizal impacts on plant nitrogen nutrition: emerging isotopic patterns, latitudinal variation and hidden mechanisms. Ecology Letters 18: 96-107.
McGuire KL. 2007. Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88: 567-574.
Michelsen A, Quarmby C, Sleep D, Jonasson S. 1998. Vascular plant 15N natural abundance in heath and forest tundra ecosystems Is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115: 406-418.
Northup RR, Dahlgren RA, McColl JG. 1998. Polyphenols as regulators of plant-litter-soil interactions in northern California's pygmy forest: a positive feedback? Biogeochemistry 42: 189-220.
Northup RR, Yu Z, Dahlgren RA, Vogt KA. 1995. Polyphenol control of nitrogen release from pine litter. Nature 377: 227-229.
Oksanen F, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Peter Solymos Met al. 2019. vegan: community ecology package. [WWW document] URL https://CRAN.R-project.org/package=vegan [accessed June 2019].
Ordoñez JC, van Bodegom PM, Witte J-PM, Bartholomeus RP, van Dobben HF, Aerts R. 2010. Leaf habit and woodiness regulate different leaf economy traits at a given nutrient supply. Ecology 91: 3218-3228.
Peay KG. 2016. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annual Review of Ecology, Evolution, and Systematics 47: 143-164.
Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD. 2009. Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytologist 185: 529-542.
Pellitier PT, Zak DR. 2018. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytologist 217: 68-73.
Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE et al. 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.
Phillips RP, Brzostek E, Midgley MG. 2013. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytologist 199: 41-51.
Pigliucci M. 2003. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecology Letters 6: 265-272.
Poorter L. 2009. Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytologist 181: 890-900.
Potts MD, Ashton PS, Kaufman LS, Plotkin JB. 2002. Habitat patterns in tropical rain forests: a comparison of 105 plots in northwest Borneo. Ecology 83: 2782-2797.
Proctor J. 1999. Heath forests and acid soils. Botanical Journal of Scotland 51: 1-14.
Quirk J, Andrews MY, Leake JR, Banwart SA, Beerling DJ. 2014. Ectomycorrhizal fungi and past high CO2 atmospheres enhance mineral weathering through increased below-ground carbon-energy fluxes. Biology Letters 10: 20140375.
R Core Development Team. 2017. A language and environment for statistical computing, v.3.4.0. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/ [accessed June, 2017].
Read DJ. 1991. Mycorrhizas in ecosystems. Experientia 47: 376-391.
Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157: 475-492.
Reich PB. 2014. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102: 275-301.
Rillig MC. 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7: 740-754.
Rineau F, Roth D, Shah F, Smits M, Johansson T, Canbäck B, Olsen PB, Persson P, Grell MN, Lindquist E et al. 2012. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry: Organic matter degradation by ectomycorrhizal fungi. Environmental Microbiology 14: 1477-1487.
Robinson D. 2001. δ15N as an integrator of the nitrogen cycle. Trends in Ecology & Evolution 16: 153-162.
Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP. 2016. Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytologist 209: 1184-1195.
Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ. 2010. Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest. American Journal of Botany 97: 1109-1120.
Russo SE, Davies SJ, King DA, Tan S. 2005. Soil-related performance variation and distributions of tree species in a Bornean rain forest. Journal of Ecology 93: 879-889.
Russo SE, Kitajima K. 2016. The ecophysiology of leaf lifespan in tropical forests: adaptive and plastic responses to environmental heterogeneity. In: Goldstein G, Santiago LS, eds. Tropical Tree Physiology. Basel, Switzerland: Springer International, 357-383.
Russo SE, Kochsiek A, Olney J, Thompson L, Miller AE, Tan S. 2013. Nitrogen uptake strategies of edaphically specialized Bornean tree species. Plant Ecology 214: 1405-1416.
Russo SE, Legge R, Weber KA, Brodie EL, Goldfarb KC, Benson AK, Tan S. 2012. Bacterial community structure of contrasting soils underlying Bornean rain forests: Inferences from microarray and next-generation sequencing methods. Soil Biology and Biochemistry 55: 48-59.
See CR, Luke McCormack M, Hobbie SE, Flores-Moreno H, Silver WL, Kennedy PG. 2019. Global patterns in fine root decomposition: climate, chemistry, mycorrhizal association and woodiness. Ecology Letters 22: 946-953.
Segnitz RM, Russo SE, Davies SJ, Peay KG. 2020. Ectomycorrhizal fungi drive positive phylogenetic plant-soil feedbacks in a regionally dominant tropical plant family. Ecology doi: 10.1002/ecy.3083.
Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau F, Canbäck B, Floudas D, Carleer R, Lackner G et al. 2016. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytologist 209: 1705-1719.
Smith SE, Read D. 2008. Mycorrhizal symbiosis. London, UK: Academic Press.
Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227-250.
Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA, Reich PB, Nabuurs GJ, de-Miguel S, Zhou M, Picard N et al. 2019. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569: 404-408.
Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG. 2013. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biology and Biochemistry 57: 282-291.
Tan S, Yamakura T, Tani M, Palmiotto P, Mamit JD, Pin CS, Davies S, Ashton P, Baillie I. 2009. Review of soils on the 52-ha long term ecological research plot in mixed dipterocarp forest at Lambir, Sarawak, Malaysian Borneo. Tropics 18: 61-86.
Tedersoo L, Brundrett MC. 2017. Evolution of ectomycorrhizal symbiosis in plants. In: Tedersoo L, ed. Biogeography of mycorrhizal symbiosis. Cham, Switzerland: Springer International Publishing, 407-467.
Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E. 2017. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355: 173-176.
Tilman, D. 1982. Resource competition and community structure. Princeton, NJ, USA: Princeton University Press.
Torti SD, Coley PD, Kursar TA. 2001. Causes and consequences of monodominance in tropical lowland forests. The American Naturalist 157: 141-153.
Vitousek P. 2004. Nutrient cycling and limitation: Hawai'i as a model system. Princeton, NJ, USA: Princeton University Press.
Vitousek PM, Chadwick OA. 2013. Pedogenic thresholds and soil process domains in basalt-derived soils. Ecosystems 16: 1379-1395.
Walker TW, Syers JK. 1976. The fate of phosphorus during pedogenesis. Geoderma 15: 1-19.
Walters MB, Reich PB. 1996. Are shade tolerance, survival, and growth linked? Low light and nitrogen effects on hardwood seedlings. Ecology 77: 841-853.
Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.
Waring BG, Adams R, Branco S, Powers JS. 2016. Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytologist 209: 845-854.
Watson H. 1985. Lambir Hills National Park: Resource Inventory with Management Recomendations. Kuching, Sarawak, Malaysia: National Parks and Wildlife Office, Forest Department.
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
Wright IJ, Westoby M. 1999. Differences in seedling growth behaviour among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. Journal of Ecology 87: 85-97.
Wright IJ, Westoby M. 2003. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Functional Ecology 17: 10-19.
Wurzburger N, Brookshire ENJ, McCormack ML, Lankau RA. 2017. Mycorrhizal fungi as drivers and modulators of terrestrial ecosystem processes. New Phytologist 213: 996-999.
Yang X, Post WM. 2011. Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8: 2907-2916.
Zapala MA, Schork NJ. 2006. Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proceedings of the National Academy of Sciences, USA 103: 19430-19435.
Zhang H-Y, Lü X-T, Hartmann H, Keller A, Han X-G, Trumbore S, Phillips RP. 2018. Foliar nutrient resorption differs between arbuscular mycorrhizal and ectomycorrhizal trees at local and global scales. Global Ecology and Biogeography 27: 875-885.
Zhu K, McCormack ML, Lankau RA, Egan JF, Wurzburger N. 2018. Association of ectomycorrhizal trees with high carbon-to-nitrogen ratio soils across temperate forests is driven by smaller nitrogen not larger carbon stocks. Journal of Ecology 106: 524-535.