Abstract
Background and aims
Studies on the aboveground growth and traits of plants suggest that plants exhibit faster growth with greater plasticity in leaf traits to adapt to changing environments. However, our knowledge of belowground growth and trait responses and associated root foraging strategies, under competition remains limited.
Methods
Using an understory species-addition experiment, we investigated the responses of function-based root (absorptive fine roots [AFRs] vs. transport fine roots [TFRs]) growth, mycorrhizal association, and order-based root traits (morphological, architectural, and chemical traits) of Pinus massoniana (native species) and Pinus elliottii (exotic species), which are the dominant coniferous tree species in subtropical China.
Results
Higher understory-species diversity increased the biomass of AFRs, but not TFRs and total fine roots (AFRs plus TFRs) of both species. Higher diversity increased the biomass ratio of the AFRs and TFRs of P. elliottii, indicating a tradeoff in plant carbon investment between the two functional root modules for P. elliottii. Higher diversity increased the total root length of P. massoniana, but did not affect that of P. elliottii. Increased species diversity decreased the ectomycorrhizal colonization rate of P. massoniana, but increased that of P. elliottii. Increased species diversity altered the branching-related traits (increased branching ratio and intensity), but did not affect the morphological (diameter, specific root length, and root tissue density) or chemical traits across the root orders of either species.
Conclusions
Our findings indicate that P. elliottii employed dual root foraging strategies (growth and mycorrhizal strategies) and had a cost-benefit tradeoff between AFR and TFR construction. In comparison, P. massoniana only accelerated root growth under competition. These results facilitate a better understanding of the root foraging strategies of plants and the rapid adaptation of exotic species in novel environments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ashbacher AC, Cleland EE (2015) Native and exotic plant species show differential growth but similar functional trait responses to experimental rainfall. Ecosphere 6:1–14. https://doi.org/10.1890/es15-00059.1
Bauhus J, Khanna PK, Menden N (2000) Aboveground and belowground interactions in mixed plantations of Eucalyptus globulus and Acacia mearnsii. Can J For Res 30:1886–1894. https://doi.org/10.1139/cjfr-30-12-1886
Brassard BW, Chen H, Bergeron Y, Paré D (2011) Differences in fine root productivity between mixed- and single-species stands. Funct Ecol 25:238–246. https://doi.org/10.1111/j.1365-2435.2010.01769.x
Brassard BW, Chen HYH, Cavard X, Laganière J, Reich PB, Bergeron Y, Paré D, Yuan Z, Chen H (2013) Tree species diversity increases fine root productivity through increased soil volume filling. J Ecol 101:210–219. https://doi.org/10.1111/1365-2745.12023
Cahill JF, McNickle GG (2011) The behavioral ecology of nutrient foraging by plants. Annu Rev Ecol Evol S 42:289–311. https://doi.org/10.1146/annurev-ecolsys-102710-145006
Cahill JF, Mcnickle GG, Haag JJ, Lamb EG, Nyanumba SM, Clair CCS (2010) Plants integrate information about nutrients and neighbors. Science 328:1657. https://doi.org/10.1126/science.1189736
Chen WL, Koide RT, Eissenstat DM, Field K (2018) Nutrient foraging by mycorrhizas: from species functional traits to ecosystem processes. Funct Ecol 32:858–869. https://doi.org/10.1111/1365-2435.13041
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
Dobrowolska D (2008) Effect of stand density on oak regeneration in flood plain forests in lower Silesia, Poland. Forestry 81:511–523. https://doi.org/10.1093/forestry/cpn025
Domisch T, Finér L, Dawud SM, Vesterdal L, Raulund-Rasmussen K (2015) Does species richness affect fine root biomass and production in young forest plantations? Oecologia 177:581–594. https://doi.org/10.1007/s00442-014-3107-3
Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60. https://doi.org/10.1016/s0065-2504(08)60005-7
Felten SV, Schmid B (2008) Complementarity among species in horizontal versus vertical rooting space. J Plant Ecol 1:33–41. https://doi.org/10.1093/jpe/rtm006
Fort F, Cruz P, Jouany C, Field K (2014) Hierarchy of root functional trait values and plasticity drive early-stage competition for water and phosphorus among grasses. Funct Ecol 28:1030–1040. https://doi.org/10.1111/1365-2435.12217
Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457. https://doi.org/10.1007/s00442-004-1596-1
Hector A (2006) Overyielding and stable species coexistence. New Phytol 172:1–3. https://doi.org/10.1111/j.1469-8137.2006.01865.x
Hishi T, Tateno R, Fukushima K, Fujimaki R, Itoh M, Tokuchi N, Näsholm T (2016) Changes in the anatomy, morphology and mycorrhizal infection of fine root systems of Cryptomeria japonica in relation to stand ageing. Tree Physiol 37. https://doi.org/10.1093/treephys/tpw076
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Holzapfel C, Alpert P (2003) Root cooperation in a clonal plant: connected strawberries segregate roots. Oecologia 134:72–77. https://doi.org/10.1007/s00442-002-1062-x
Jacob A, Hertel D, Leuschner C (2013) On the significance of belowground overyielding in temperate mixed forests: separating species identity and species diversity effects. Oikos 122:463–473. https://doi.org/10.1111/j.1600-0706.2012.20476.x
Kong DL, Ma CE, Zhang Q, Li L, Chen XY, Zeng H, Guo DL (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872. https://doi.org/10.1111/nph.12842
Kou L, Guo DL, Yang H, Gao WL, Li SG (2015) Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant Soil 391:207–218. https://doi.org/10.1007/s11104-015-2420-x
Kou L, Jiang L, Fu XL, Dai XW, Wang HM, Li SG (2018) Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations. New Phytol 218:1450–1461. https://doi.org/10.1111/nph.15066
Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and fnction in the soil. Ecology 83:3152–3166. https://doi.org/10.2307/3071850
Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol 176:635–643. https://doi.org/10.1111/j.1469-8137.2007.02189.x
Liu C, Xiang WH, Lei PF, Deng XW, Tian DL, Fang X, Peng CH (2013) Standing fine root mass and production in four Chinese subtropical forests along a succession and species diversity gradient. Plant Soil 376:445–459. https://doi.org/10.1007/s11104-013-1998-0
Liu BT, Li HB, Zhu B, Koide RT, Eissenstat DM, Guo DL (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136. https://doi.org/10.1111/nph.13434
Lõhmus K, Truu M, Truu J, Ostonen I, Kaar E, Vares A, Uri V, Alama S, Kanal A (2006) Functional diversity of culturable bacterial communities in the rhizosphere in relation to fine-root and soil parameters in alder stands on forest, abandoned agricultural, and oil-shale mining areas. Plant Soil 283:1–10. https://doi.org/10.1007/s11104-005-2509-8
Ma ZL, Chen HYH (2016) Effects of species diversity on fine root productivity increase with stand development and associated mechanisms in a boreal forest. J Ecol 105:237–245. https://doi.org/10.1111/1365-2745.12667
Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97. https://doi.org/10.1038/nature26163
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-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
Meinen C, Hertel D, Leuschner C (2009) Root growth and recovery in temperate broad-leaved forest stands differing in tree species diversity. Ecosystems 12:1103–1116. https://doi.org/10.1007/s10021-009-9271-3
Mohammad B, Peay KG, Leho T (2015) Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytol 205:1454–1463. https://doi.org/10.1111/nph.13206
Mordechai G, S BJ, O'Brien EE, Maina GM, Zvika A (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669. https://doi.org/10.1046/j.0022-0477.2001.00609.x
Noguchi K, Nagakura J, Konôpka B, Sakata T, Kaneko S, Takahashi M (2013) Fine-root dynamics in sugi (Cryptomeria japonica) under manipulated soil nitrogen conditions. Plant Soil 364:159–169. https://doi.org/10.1007/s11104-012-1354-9
O’Brien EE, Brown JS (2008) Games roots play: effects of soil volume and nutrients. J Ecol 96:438–446. https://doi.org/10.1111/j.1365-2745.2008.01354.x
Ostonen I, Lãμhmus K, Helmisaari HS, Truu J, Meel S (2007) Fine root morphological adaptations in scots pine, Norway spruce and silver birch along a latitudinal gradient in boreal forests. Tree Physiol 27:1627–1634. https://doi.org/10.1093/treephys/27.11.1627
Ostonen I, Helmisaari H-S, Borken W, Tedersoo L, Kukumägi M, Bahram M, Lindroos A-J, Nöjd P, Uri V, Merilä P, Asi E, Lõhmus K (2011) Fine root foraging strategies in Norway spruce forests across a European climate gradient. Glob Chang Biol 17:3620–3632. https://doi.org/10.1111/j.1365-2486.2011.02501.x
Pollastrini M, Holland V, Brüggemann W, Koricheva J, Jussila I, Scherer-Lorenzen M, Berger S, Bussotti F (2014) Interactions and competition processes among tree species in young experimental mixed forests, assessed with chlorophyll fluorescence and leaf morphology. Plant Biol 16:323–331. https://doi.org/10.1111/plb.12068
Pollastrini M, Nogales AG, Benavides R, Bonal D, Finer L, Fotelli M, Gessler A, Grossiord C, Radoglou K, Strasser RJ, Bussotti F (2017) Tree diversity affects chlorophyll a fluorescence and other leaf traits of tree species in a boreal forest. Tree Physiol 37:199–208. https://doi.org/10.1093/treephys/tpw132
Potvin C, Dutilleul P (2009) Neighborhood effects and size-asymmetric competition in a tree plantation varying in diversity. Ecology 90:321–327. https://doi.org/10.1890/08-0353.1
Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine noeth american trees. Ecol Monogr 72:293–309. https://doi.org/10.2307/3100029
Salahuddin RB, Razaq M, Yang L, Ji L, Khan F, Zhang J (2018) Root order-based traits of Manchurian walnut & larch and their plasticity under interspecific competition. Sci Rep 8(9815):9815. https://doi.org/10.1038/s41598-018-27832-0
Schmid I (2002) The influence of soil type and interspecific competition on the fine root system of Norway spruce and European beech. Basic Appl Ecol 3:339–346. https://doi.org/10.1078/1439-1791-00116
Sorte CJB, Ibáñez I, Blumenthal DM, Molinari NA, Miller LP, Grosholz ED, Diez JM, D'Antonio CM, Olden JD, Jones SJ (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270. https://doi.org/10.1111/ele.12017
Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273. https://doi.org/10.1111/j.1469-8137.2007.02207.x
Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–187. https://doi.org/10.1046/j.1469-8137.1998.00176.x
Wang YD, Wang ZL, Wang HM, Guo CC, Bao WK (2012) Rainfall pulse primarily drives litterfall respiration and its contribution to soil respiration in a young exotic pine plantation in subtropical China. Can J For Res 42:657–666. https://doi.org/10.1139/x2012-017
Wang GL, Fahey TJ, Xue S, Liu F (2013) Root morphology and architecture respond to N addition in Pinus tabuliformis, West China. Oecologia 171:583–590. https://doi.org/10.1007/s00442-012-2441-6
Wen XF, Wang HM, Wang JL, Yu GR, Sun XM (2010) Ecosystem carbon exchanges of a subtropical evergreen coniferous plantation subjected to seasonal drought, 2003-2007. Biogeosciences 7:357–369. https://doi.org/10.5194/bg-7-357-2010
Xia MX, Guo DL, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188:1065–1074. https://doi.org/10.1111/j.1469-8137.2010.03423.x
Acknowledgements
This research is financially supported by the National Natural Science Foundation of China (No. 31730014; 31670635; 31700379). The authors acknowledge the contributions of the anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Thom W. Kuyper.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 3389 kb)
Rights and permissions
About this article
Cite this article
Yan, H., Kou, L., Wang, H. et al. Contrasting root foraging strategies of two subtropical coniferous forests under an increased diversity of understory species. Plant Soil 436, 427–438 (2019). https://doi.org/10.1007/s11104-019-03936-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-03936-y