Understory effects on overstory trees: A review

doi:10.13287/j.1001-9332.201603.033

Abstract

Abstract: Plant-plant interactions play a key role in regulating the composition and structure of communities and ecosystems. Studies of plant-plant interactions in forest ecosystems have traditionally concentrated on either tree-tree interactions or overstory species’ impacts on understory plants. The possible effects of understory species on overstory trees have received less attention. We summarized the effects of understory species on soil physiological properties, soil fauna activities, leaf litter decomposition, and ecophysiology and growth of the overstory species. Then the effects of distur-bance on understory-overstory interactions were discussed. Finally, an ecophysiology-based concept model of understory effects on overstory trees was proposed. Understory removal experiments showed that the study area, overstory species age, soil fertility and understory species could significantly affect the understory-overstory interactions.

DU Zhong, CAI Xiao-hu, BAO Wei-kai, CHEN Huai, PAN Hong-li. Understory effects on overstory trees: A review[J]. Chinese Journal of Applied Ecology, 2016, 27(3): 963-972.

References

[1] Kelty MJ. The role of species mixtures in plantation fore-stry. Forest Ecology and Management, 2000, 233: 195-204
[2] Brooker RW. Plant-plant interactions and environmental change. New Phytologist, 2006, 171: 271-284
[3] Maestre FT, Valladares F, Reynolds JF. Is the change of plant-plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments. Journal of Ecology, 2005, 93: 748-757
[4] Walters MB, Reich PB. Growth of Acer saccharum seedlings in deeply shaded understories of northern Wisconsin: Effects of nitrogen and water availability. Canadian Journal of Forest Research, 1997, 27: 237-247
[5] Lhotka JM, Loewenstein EF. Influence of canopy structure on the survival and growth of underplanted seedlings. New Forests, 2008, 35: 89-104
[6] Parker WC, Dey DC. Influence of overstory density on ecophysiology of red oak (Quercus rubra) and sugar maple (Acer saccharum) seedlings in central Ontario shelter woods. Tree Physiology, 2008, 28: 797-804
[7] Uliassi DD, Ruess RW. Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology, 2002, 83: 88-103
[8] Rodriguez-Calcerrada J, Regneri SM, Pardos JA, et al. Influence of overstory density on understory light, soil moisture, and survival of two underplanted oak species in a Mediterranean montane Scots pine forest. Investigacion Agraria: Sistemas Y Recursos Forestales, 2008, 17: 31-38
[9] Li MH, Du Z, Pan HL, et al. Effects of neighboring woody plants on target trees with emphasis on effects of understorey shrubs on overstorey physiology in forest communities: A mini-review. Community Ecology, 2012, 13: 117-128
[10] Wan SZ, Zhang CL, Chen YQ, et al. The understory fern Dicranopteris dichotoma facilitates the overstory Eucalyptus trees in subtropical plantations. Ecosphere, 2014, 5: 1-12
[11] Kobayashi T, Shimano K, Muraoka H. Effects of light availability on the carbon gain of beech (Fagus crenata) seedlings with reference to the density of dwarf bamboo (Sasa kurilensis) in an understory of Japan Sea type beech forest. Plant Species Biology, 2004, 19: 33-46
[12] Nilsson MC, Wardle DA. Understory vegetation as a forest ecosystem driver: Evidence from the northern Swedish boreal forest. Frontiers in Ecology and the Environment, 2005, 3: 421-428
[13] Gilliam FS. The ecological significance of the herbaceous layer in temperate forest ecosystems. BioScience, 2007, 57: 845-858
[14] Elliott KJ, Vose JM, Knoepp JD, et al. Functional role of the herbaceous layer in eastern deciduous forest ecosystems. Ecosystems, 2015, 18: 221-236
[15] Ito A, Saigusa N, Murayama S, et al. Modeling of gross and net carbon dioxide exchange over a cool-temperate deciduous broad-leaved forest in Japan: Analysis of seasonal and interannual change. Agricultural and Forest Meteorology, 2005, 134: 122-134
[16] Harden JW, O’Neill KP, Trumbore SE, et al. Moss and soil contributions to the annual net carbon flux of a maturing boreal forest. Journal of Geophysical Research, 1997, 102: 28805-28816
[17] Turetsky MR. The role of bryophytes in carbon and nitrogen cycling. The Bryologist, 2003, 106: 395-409
[18] Kolari P, Pumpanen J, Kulmala L, et al. Forest floor vegetation plays an important role in photosynthetic production of boreal forests. Forest Ecology and Management, 2006, 221: 241-248
[19] Wu JP, Liu ZF, Wang XL, et al. Effects of understory removal and tree girdling on soil microbial community composition and litter decomposition in two eucalyptus plantations in south China. Functional Ecology, 2011, 25: 921-931
[20] Gonzalez M, Augusto L, Gallet-Budynek A, et al. Contribution of understory species to total ecosystem aboveground and belowground biomass in temperate Pinus pinaster Ait. forests. Forest Ecology and Management, 2013, 289: 38-47
[21] Chapin FS III. Nitrogen and phosphorus nutrition and nutrient cycling by evergreen and deciduous understory shrubs in an Alaskan black spruce forest. Canadian Journal of Forest Research, 1983, 13: 773-781
[22] He Y-L (何艺玲), Fu M-Y (傅懋毅). Review of studies on understorey of plantations. Forest Research (林业科学研究), 2002, 15(6): 727-733 (in Chinese)
[23] Mo JM, Brown S, Peng SL, et al. Nitrogen availability in disturbed, rehabilitated and mature forests of tropical China. Forest Ecology and Management, 2003, 175: 573-583
[24] Camprodon J, Brotons L. Effects of undergrowth clearing on the bird communities of the Northwestern Mediterranean Coppice Holm oak forests. Forest Ecology and Management, 2006, 221: 72-82
[25] Zhang JW, Oliver WW, Busse MD. Growth and deve-lopment of ponderosa pine on sites of contrasting productivities: Relative importance of stand density and shrub competition effects. Canadian Journal of Forest Research, 2006, 36: 2426-2438
[26] Bardgett RD, Wardle DA. Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change. Oxford, UK: Oxford University Press, 2010
[27] Jäderlund A, Zackrisson O, Dahlberg A, et al. Interfe-rence of Vaccinium myrtillus on establishment, growth, and nutrition of Picea abies seedlings in a northern boreal site. Canadian Journal of Forest Research, 1997, 27: 2017-2025
[28] Steijlen I, Nilsson MC, Zackrisson O. Seed regeneration of Scots pine in boreal forest stands dominated by lichen and feather moss. Canadian Journal of Forest Research, 1995, 25: 713-723
[29] Zackrisson O, Nilsson MC, Jäderlund A, et al. Nutritional effects of seed fall during mast years in boreal fo-rest. Oikos, 1999, 84: 17-26
[30] Zackrisson O, Nilsson MC, Dahlberg A, et al. Interfe-rence mechanisms in conifer-Ericaceae-feathermoss communities. Oikos, 1997, 78: 209-220
[31] Odén PC, Brandtberg PO, Andersson R, et al. Isolation and characterization of a germination inhibitor from lea-ves of Empetrum hermaphroditum. Scandinavian Journal of Forest Research, 1992, 7: 497-502
[32] Nilsson MC, Zackrisson O, Sterner O, et al. Characterisation of the differential interference effects of two boreal dwarf shrub species. Oecologia, 2000, 123: 122-128
[33] Zackrisson O, Nilsson MC, Wardle DA. Key ecological function of charcoal from wildfire in the Boreal forest. Oikos, 1996, 77: 10-19
[34] DeLuca TH, Nilsson MC, Zackrisson O. Nitrogen mi-neralization and phenol accumulation along a fire chronosequence in northern Sweden. Oecologia, 2002, 133: 206-214
[35] Wardle DA, HÖrnberg G, Zackrisson O, et al. Long-term effects of wildfire on ecosystem properties across an island area gradient. Science, 2003, 300: 972-975
[36] Wallstedt A, Gallet C, Nilsson MC. Behaviour and recovery of the secondary metabolite Batatasin-III from boreal forest humus: Influence of temperature, humus type and microbial community. Biochemical Systematics and Ecology, 2005, 33: 385-407
[37] Mallik AU. Conifer regeneration problems in boreal and temperate forests with ericaceous understory: Role of disturbance, seedbed limitation, and keystone species change. Critical Reviews in Plant Sciences, 2003, 22: 341-366
[38] Thiffault N, Titus BD, Munson AD. Black spruce seedlings in a Kalmia-Vaccinium association: Microsite manipulation to explore interactions in the field. Canadian Journal of Forest Research, 2004, 34: 1657-1668
[39] Zang R-G (臧润国). Measurement and analysis on light and temperature regimes in different patch types of forest cycle in a tropical mountain rain forest, Hainan Island. Journal of Beijing Forestry University (北京林业大学学报), 2002, 24(5/6): 125-130 (in Chinese)
[40] Wu Y (吴彦), Liu Q (刘庆), He H (何海), et al. Effects of light and temperature on seed germination of Picea asperata and Betula albosinensis. Chinese Journal of Applied Ecology (应用生态学报), 2004, 15(10): 1703-1710 (in Chinese)
[41] Matsushima M, Chang SX. Effects of understory remo-val, N fertilization, and litter layer removal on soil N cycling in a 13-year-old white spruce plantation infested with Canada bluejoint grass. Plant and Soil, 2007, 292: 243-258
[42] Hogg EH, Lieffers VJ. The impact of Calamagrostis canadensis on soil thermal regimes after logging in nor-thern Alberta. Canadian Journal of Forest Research, 1991, 21: 387-394
[43] Wang FM, Zou B, Li HF, et al. The effect of understory removal on microclimate and soil properties in two subtropical lumber plantations. Journal of Forest Research, 2014, 19: 238-243
[44] Takahashi K, Uemura S, Suzuki JI, et al. Effects of understory dwarf bamboo on soil water and the growth of overstory trees in a dense secondary Betula ermanii fo-rest, northern Japan. Ecological Research, 2003, 18: 767-774
[45] Lambert JL, Gardner WR, Boyle JR. Hydrologic response of a young pine plantation to weed removal. Water Resources Research, 1971, 7: 1013-1019
[46] O’ren R, Waring RH, Stafford SG, et al. Twenty-four years of ponderosa pine growth in relation to canopy leaf area and understory competition. Forest Science, 1987, 33: 538-547
[47] Kelliher FM, Black TA. Estimating the effects of understory removal from a Douglas fir forest using a two-layer canopy evapotranspiration model. Water Resources Research, 1986, 22: 1891-1899
[48] Tripathi SK, Sumida A, Shibata H, et al. Growth and substrate quality of fine root and soil nitrogen availability in a young Betula ermanii forest of northern Japan: Effects of the removal of understory dwarf bamboo (Sasa kurilensis). Forest Ecology and Management, 2005, 212: 278-290
[49] Tripathi SK, Sumida A, Ono K, et al. The effects of understorey dwarf bamboo (Sasa kurilensis) removal on soil fertility in a Betula ermanii forest of northern Japan. Ecological Research, 2006, 21: 315-320
[50] Xiong YM, Xia HP, Li ZA, et al. Impacts of litter and understory removal on soil properties in a subtropical Acacia mangium plantation in China. Plant and Soil, 2008, 304: 179-188
[51] Zhao J, Wang XL, Shao YH, et al. Effects of vegetation removal on soil properties and decomposer organisms. Soil Biology & Biochemistry, 2011, 43: 954-960
[52] Wang FM, Li ZA, Xia HP, et al. Effects of nitrogen-fixing and non-nitrogen-fixing tree species on soil properties and nitrogen transformation during forest restoration in southern China. Soil Science and Plant Nutrition, 2010, 56: 297-306
[53] Zhao J, Wan SZ, Fu SL, et al. Effects of understory removal and nitrogen fertilization on soil microbial communities in Eucalyptus plantations. Forest Ecology and Management, 2013, 310: 80-86
[54] Liu ZF, Wu JP, Zhou LX, et al. Effect of understory fern (Dicranopteris dichotoma) removal on substrate utilization patterns of culturable soil bacterial communities in subtropical Eucalyptus plantations. Pedobiologia, 2012, 55: 7-13
[55] Liu ZF, Wu JP, Zhou LX, et al. Tree girdling effect on bacterial substrate utilization pattern depending on stand age and soil microclimate in Eucalyptus plantations. Applied Soil Ecology, 2012, 54: 7-13
[56] Zhao J, Wan SZ, Li ZA, et al. Dicranopteris-dominated understory as major driver of intensive forest ecosystem in humid subtropical and tropical region. Soil Biology & Biochemistry, 2012, 49: 78-87
[57] Huang Y-M (黄玉梅), Yang W-Q (杨万勤), Zhang J (张健), et al. Response of soil faunal community to simulated understory plant loss in the subalpine conife-rous plantation of western Sichuan. Acta Ecologica Sinica (生态学报), 2010, 30(8): 2018-2025 (in Chinese)
[58] Wardle DA, Nilsson MC, Zackrisson O, et al. Determinants of litter mixing effects in a Swedish boreal forest. Soil Biology & Biochemistry, 2003, 35: 827-835
[59] Aerts R. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: A triangular relationship. Oikos, 1997, 79: 439-449
[60] Zhang DQ, Hui DF, Luo YQ, et al. Rates of litter decomposition in terrestrial ecosystems: Global patterns and controlling factors. Journal of Plant Ecology, 2008, 1: 85-93
[61] Wardle DA, Zackrisson O, HÖrnberg G, et al. Influence of island area on ecosystem properties. Science, 1997, 277: 1296-1299
[62] Gurlevik N, Kelting DL, Allen HL. Nitrogen mineralization following vegetation control and fertilization in a 14-year-old loblolly pine plantation. Soil Science Society of America Journal, 2004, 68: 272-281
[63] Zak DR, Groffman PM, Pregitzer KS, et al. The vernal dam: Plant microbe competition for nitrogen in northern hardwood forests. Ecology, 1990, 71: 651-656
[64] Li QC, Allen HL, Wilson CA. Nitrogen mineralization dynamics following the establishment of a loblolly pine plantation. Canadian Journal of Forest Research, 2003, 33: 364-374
[65] Takahashi K. Regeneration and coexistence of two subalpine conifer species in relation to dwarf bamboo in the understorey. Journal of Vegetation Science, 1997, 8: 529-536
[66] Kume A, Satomura T, Tsuboi N, et al. Effects of understory vegetation on the ecophysiological characteristics of an overstory pine, Pinus densiflora. Forest Ecology and Management, 2003, 176: 195-203
[67] Kitao M, Lei TT, Koike T, et al. Higher electron transport rate observed at low intercellular CO₂ concentration in long-term drought-acclimated leaves of Japanese mountain birch (Betula ermanii). Physiologia Plantarum, 2003, 118: 406-413
[68] Takahashi K, Matsuki S, Uemura S, et al. Variations in the maximum photosynthetic rate of Betula ermanii in relation to soil water potential. Vegetation Science, 2004, 21: 103-108
[69] Kobayashi T, Miki N, Kato K, et al. Understory remo-val increases carbon gain and transpiration in the overstory of birch (Betula ermanii) stands in northern Hokkaido, Japan: Trends in leaf, shoot, and canopy. Proceedings of the International Workshop on H₂O and CO₂ Exchanges in Siberia (2nd International WS on C/H₂O/Energy Balance and Climate Over Boreal Regions with Special Emphasis on Eastern Siberia), Nagoya, 2006: 19-22
[70] Ishii HT, Kobayashi T, Uemura S, et al. Removal of understory dwarf bamboo (Sasa kurilensis) induces changes in water-relations characteristics of overstory Betula ermanii trees. Journal of Forest Research, 2008, 13: 101-109
[71] Morgan JM. Osmoregulation and water stress in higher plants. Annual Review of Plant Physiology, 1984, 35: 299-319
[72] Hébert F, Thiffault N, Ruel JC, et al. Ericaceous shrubs affect black spruce physiology independently form inhe-rent site fertility. Forest Ecology and Management, 2010, 260: 219-228
[73] Takahashi K, Yogo M, Ishibashi S. Stand development and regeneration during a 33-year period in a seral Picea glehnii forest, northern Japan. Ecological Research, 2006, 21: 35-42
[74] LeBel P, Thiffault N, Bradley RL. Kalmia removal increases nutrient supply and growth of black spruce seedlings: An effect fertilizer cannot emulate. Forest Ecology and Management, 2008, 256: 1780-1784
[75] Busse MD, Cochran PH, Barrett JW. Changes in ponderosa pine site productivity following removal of understory vegetation. Soil Science Society of America Journal, 1996, 60: 1614-1621
[76] Wagner RG, Little KM, Richardson B, et al. The role of vegetation management for enhancing productivity of the world’s forests. Forestry, 2006, 79: 57-79
[77] Stokes VJ, Willoughby IH. Early weed control can increase long-term growth, yield and carbon sequestration of Sitka spruce stands in Britain. Forestry, 2014, 87: 425-435
[78] Richardson B. The effects of weeds on tree growth// Menzies M, Parrott J, Whitehouse L, eds. Efficiency of Stand Establishment Operations. Rotorua, New Zealand: New Zealand Forest Research Institute, 1991: 242-249
[79] Zhang JW, Powers RF, Oliver WW, et al. Response of ponderosa pine plantations to competing vegetation control in Northern California, USA: A meta-analysis. Forestry, 2013, 86: 3-11
[80] Zeng Q (曾青), Zhu J-G (朱建国). Elevated atmospheric CO₂ and crop/weed competition. Chinese Journal of Applied Ecology (应用生态学报), 2002, 13(10): 1339-1343 (in Chinese)
[81] Polley HW, Johnson HB, Derner JD. Increasing CO₂ from subambient to superambient concentrations alters species composition and increases above-ground biomass in a C3/C4 grassland. New Phytologist, 2003, 160: 319-327
[82] Belote RT, Weltzin JF, Norby RJ. Response of an understory plant community to elevated CO₂ depends on differential responses of dominant invasive species and is mediated by soil water availability. New Phytologist, 2004, 161: 827-835
[83] Gunnarsson U, Granberg G, Nilsson MC. Growth, production and interspecific competition in Sphagnum: Effects of temperature, nitrogen and sulphur treatments ona boreal mire. New Phytologist, 2004, 163: 349-359
[84] Casper BB, Jackson RB. Plant competition underground. Annual Review of Ecology and Systematics, 1997, 28: 545-570
[85] Blank RR, Qualls RG, Young JA. Lepidium latifolium: Plant nutrient competition-soil interactions. Biology and Fertility of Soils, 2002, 35: 458-464
[86] Chang SX, Weetman GF, Preston CM. Understory competition effect on tree growth and biomass allocation on a coastal old-growth forest cutover site in British Columbia. Forest Ecology and Management, 1996, 83: 1-11
[87] Staples TE, Van Rees KCJ, Van Kessel C. Nitrogen competition using ¹⁵N between early successional plants and planted white spruce seedlings. Canadian Journal of Forest Research, 1999, 29: 1282-1289
[88] Ostertag, R, Verville JH. Fertilization with nitrogen and phosphorus increases abundance of non-native species in Hawaiian montane forests. Plant Biology, 2002, 162: 77-90
[89] Goodman LF, Hungate BA. Managing forests infested by spruce beetles in south-central Alaska: Effects on nitrogen availability, understory biomass, and spruce rege-neration. Forest Ecology and Management, 2006, 227: 267-274
[90] Yang X-Y (杨贤燕), Jiang Q-Q (蒋琦清), Tang J-J (唐建军), et al. Effects of smiulated nitrogen deposition on competition of weedy species (Echinochloa crusgalli) and upland rice (Oryza sativa) under different air temperatures. Chinese Journal of Applied Ecology (应用生态学报), 2007, 18(4): 848-852 (in Chinese)
[91] Souza L, Belote RT, Kardol P, et al. CO₂ enrichment accelerates successional development of an understory plant community. Journal of Plant Ecology, 2010, 3: 33-39
[92] Silvertown J. Plant coexistence and the niche. Trends in Ecology & Evolution, 2004, 19: 605-611
[93] Tremmel DC, Bazzaz FA. Plant architecture and allocation in different neighborhoods: Implications for compe-titive success. Ecology, 1995, 76: 262-271
[94] Grams TEE, Kozovits AR, Reiter IM, et al. Quantifying competitiveness in woody plants. Plant Biology, 2002, 4: 153-158
[95] Zhang JY, Cheng GW, Yu FH, et al. Intensity and importance of competition for a grass (Festuca rubra) and a legume (Trifolium pratense) vary with environmental changes. Journal of Integrative Plant Biology, 2008, 50: 1570-1579
[96] Zhang JY, Cheng GW, Yu FH, et al. Interspecific variations in responses of Festuca rubra L. and Trifolium pra-tense L. to a severe clipping under environmental changes. Biologia, 2009, 64: 292-298
[97] Kuppers BIL. Nitrogen and rubisco contents in eucalypt canopies as affected by Acacia neighbourhood. Plant Physiology and Biochemistry, 1996, 34: 753-760
[98] Umeki K. Importance of crown position and morphological plasticity in competitive interaction in a population of Xanthium canadense. Annals of Botany, 1995, 75: 259-265