Abstract
In a shadehouse experiment we tested the effects of light, nutrients and ectomycorrhizal fungi (EMF) on the growth of Vatica albiramis van Slooten (Dipterocarpaceae) seedlings. We hypothesised that it is more advantageous for plants to form connections with EMF and to trade carbon for nutrients with EMF under high light than low light. The relationship between seedling growth and the proportion of ectomycorrhizal root tips was expected as positive in high light and as negative in low light. Light conditions simulated the forest understory (low; 3% full sunlight), a small gap (medium; 11%) and a large gap (high; 33%) and a fully factorial combination of nutrients (F−/+) and ectomycorrhizal colonization (EMF−/+) treatments were applied within light conditions. The application of EMF and nutrients did significantly alter seedling growth across the range of forest floor light conditions, however the key hypothesis was rejected as seedling growth under low light was not affected by increased EMF colonization of root tips (light:EMF colonization χ2 = 2.97, p = 0.23). In addition, the lack of difference in morphotype abundance across light conditions indicated that light changes may not favour the association to specific EMF in seedlings of this particular dipterocarp species. Our results suggest that antagonistic (non-beneficial to the plant) effects due to ectomycorrhizal colonization under a light constrained environment may not affect seedling growth of Vatica albiramis.
Similar content being viewed by others
References
Agerer R, Rambold G (2004–2007) DEEMY—An information system for characterization and determination of ectomycorrhizae, Munich
Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility—A handbook of methods, 2nd edn. CAB International, Oxford
Appanah S (2001) Sustainable management of Malaysian rainforest. In: Evans J (ed) The forests handbook volume 2. Blackwell Science, Oxford, pp 341–356
Appanah S, Turnbull JM (1998) A review of dipterocarps: taxonomy, ecology and silviculture. Center for International Forestry Research, Bogor
Ashton PS (1982) Dipterocarpaceae. Flora Malesiana 9:237–552
Barker MG, Press MC, Brown ND (1997) Photosynthetic characteristics of dipterocarp seedlings in three tropical rain forest light environments: a basis for niche partitioning? Oecologia 112:453–463
Bebber D, Brown N, Speight M, Moura-Costa P, Wai YS (2002) Spatial structure of light and dipterocarp seedling growth in a tropical secondary forest. Forest Ecol Manag 157:65–75. doi:10.1016/S0378-1127(00)00659-9
Becker P (1983) Ectomycorrhizas in Shorea (Dipterocarpaceae) seedlings in a lowland Malaysian rainforest. Malaysian Forester 46:146–170
Bloor JMG (2003) Light responses of shade-tolerant tropical tree species in north-east Queensland: a comparison of forest- and shadehouse-grown seedlings. J Trop Ecol 19:163–170. doi:10.1017/S0266467403003183
Bray RH, Kurtz LT (1945) Determination of total organic and available forms of phosphorous in soils. Soil Sci 59:39–45
Brearley FQ (2003) The role of ectomycorrhizas in the regeneration of dipterocarp seedlings. Dissertation. University Sheffield
Brearley FQ, Scholes JD, See LS (2005) Nitrogen nutrition and isotopic discrimination in tropical ectomycorrhizal fungi. Res Microbiol 156:184–190
Brearley FQ, Scholes JD, Press MC, Palfner G (2007) How does light and phosphorus fertilisation affect the growth and ectomycorrhizal community of two contrasting dipterocarp species? Plant Ecol 192:237–249. doi:10.1007/s11258-007-9325-6
Bremner JM (1965) Total nitrogen. In: Black CA (ed) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy Inc, Madison, pp 1149–1178
Bungard RA, Press MC, Scholes JD (2000) The influence of nitrogen on rain forest dipterocarp seedlings exposed to a large increase in irradiance. Plant Cell Environ 23:1183–1194. doi:10.1046/j.1365-3040.2000.00642.x
Bungard RA, Zipperlen SA, Press MC, Scholes JD (2002) The influence of nutrients on growth and photosynthesis of seedlings of two rainforest dipterocarp species. Funct Plant Biol 29:505–515
Burslem DFRP, Grubb PJ, Turner IM (1995) Responses to nutrient addition among shade-tolerant tree seedlings of lowland tropical rain forest in Singapore. J Ecol 83:113–122
Chazdon RL, Pearcy RW (1991) The importance of sunflecks for forest understory plants—Photosynthetic machinery appears adapted to brief, unpredictable periods of radiation. Bioscience 41:760–766
Dalling JW, Lovelock CE, Hubbell SP (1999) Growth responses of seedlings of two neotropical pioneer species to simulated forest gap environments. J Trop Ecol 15:827–839. doi:10.1017/S0266467499001200
Dalling JW, Winter K, Hubbell SP (2004) Variation in growth responses of neotropical pioneers to simulated forest gaps. Funct Ecol 18:725–736. doi:10.1111/j.0269-8463.2004.00868.x
Eschenbach C, Glauner R, Kleine M, Kappen L (1998) Photosynthesis rates of selected tree species in lowland dipterocarp rainforest of Sabah, Malaysia. Trees-Struct Funct 12:356–365. doi:10.1007/s004680050162
Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New York
Gillman GP, Bruce RC, Davey BG, Kimble JM, Searle PL, Skjemstid JO (1983) Comparison of methods used for determination of cation exchange capacity. Commun Soil Sci Plant Anal 14:1005–1014
Hunt R (1990) Basic growth analysis. Unwyn Hyman, London
Ingleby K, Munro RC, Noor M, Mason PA, Clearwater M (1998) Ectomycorrhizal populations of dipterocarp seedlings regenerating under three different forest canopy treatments. Forest Ecol Manag 111:171–179
Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae. Ecol Appl 3:749–757
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585
Kamaluddin M, Grace J (1996) Acclimatisation of seedlings of Bischofia javanica and Hopea odorata to light and nutrient supply. In: Appanah S, Khoo KC (eds) Proceedings Fifth Round-Table Conference on Dipterocarps. Forest Research Institute Malaysia, Kuala Lumpur
Leakey ADB, Scholes JD, Press MC (2004) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482. doi:10.1093/jxb/eri055
Lee SS, Alexander IJ (1994) The response of seedlings of two dipterocarp species to nutrient additions and ectomycorrhizal infection. Plant Soil 163:299–306. doi:10.1007/BF00007979
Lee SS, Watling R, Turnbull E (1995) Ectomycorrhizal fungi as possible bio-indicators in forest management. Conf. Forestry and Forest Products Research, pp 63–68
Lemmon PE (1956) A spherical densiometer for estimating forest over-story density. Forest Sci 2:314–320
Limin SH, Ermiasi Y, Selviana EI (2007) History of the development of tropical peatland in central Kalimantan, Indonesia. Centre for International Cooperation in Management of Tropical Peatland, Palangka Raya
Majalap N, Chu NH (1992) Laboratory manual for chemical analysis. Forestry Department, Sandakan
Marsh CW, Greer AG (1992) Forest land-use in Sabah, Malaysia—an introduction to Danum Valley. Proc Roy Soc Lond B Bio 335:331–339
Moura-Costa P, Sau Wai Y, Ong Chye L, Ganing A, Nussbaum R, Mojiun T (1994) Large scale enrichment planting with dipterocarps as an alternative for carbon offset—methods and preliminary results. In: Appanah S, Khoo KC (eds) Proceedings Fifth Round-Table Conference on Dipterocarps. Forest Research Institute Malaysia, Kuala Lumpur
Nicieza AG, Alvarez D (2009) Statistical analysis of structural compensatory growth: how can we reduce the rate of false detection? Oecologia 159:27–39
Nussbaum R, Anderson J, Spencer T (1995) Factors limiting the growth of indigenous tree seedlings planted on degraded rain forest soils in Sabah, Malaysia. Forest Ecol Manag 74:149–159. doi:10.1016/0378-1127(94)03496-J
Nussbaum R, Anderson J, Spencer T (1996) Planting dipterocarps for rehabilitation of log landings and skid trails in Sabah, Malaysia. In: Appanah S, Khoo KC (eds) Proceedings Fifth Round-Table Conference on Dipterocarps. Forest Research Institute Malaysia, Kuala Lumpur
Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-Plus. Springer, New York
Philipson CD (2009) Plant growth analysis of Bornean Dipterocarpaceae seedlings. Dissertation. University Zurich
R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
Raja Barizan RS (1996) Growth and survival of planted seedlings of Hopea odorata under different light conditions and fertiliser levels in a logged-over forest. In: Appanah S, Khoo KC (eds) Proceedings Fifth Round-Table Conference on Dipterocarps. Forest Research Institute Malaysia, Kuala Lumpur
Romell E, Hallsby G, Karlsson A, Garcia C (2008) Artificial canopy gaps in a Macaranga spp. dominated secondary tropical rain forest—effects on survival and above ground increment of four under-planted dipterocarp species. Forest Ecol Manag 255:1452–1460. doi:10.1016/j.foreco.2007.11.003
Saner P (2005) Does the growth performance of dipterocarp saplings in different light conditions follow an ecological trade-off? Diploma. University Zurich
Saner P (2009) Ecosystem carbon dynamics in logged forest of Malaysian Borneo. Dissertation. University Zurich
Saner P, Lim R, Burla B, Scherer-Lorenzen M, Hector A (2009) Reduced soil respiration in gaps in logged lowland dipterocarp forests. Forest Ecol Manag 258:2007–2012. doi:10.1016/j.foreco.2009.07.048
Scholes JD, Press MC, Zipperlen SW (1997) Differences in light energy utilisation and dissipation between dipterocarp rain forest tree seedlings. Oecologia 109:41–48
Selosse MA, Richard F, He XH, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628
Symington CF (1943) Foresters’ manual of dipterocarps. Penerbit Universiti Malaya, Kuala Lumpur
Turjaman M, Tamai Y, Segah H, Limin SH, Osaki M, Tawaraya K (2006) Increase in early growth and nutrient uptake of Shorea seminis seedlings inoculated with two ectomycorrhizal fungi. J Trop For Sci 18:243–249
Turner IM, Brown ND, Newton AC (1993) The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. Forest Ecol Manag 57:329–337
Venables WN, Ripley BD (2003) Modern applied statistics with S. Springer, New York
Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25
Yasman I (1995) Dipterocarpaceae: tree-mycorrhizae-seedling connections. Dissertation. University Wageningen
Zipperlen SW, Press MC (1996) Photosynthesis in relation to growth and seedling ecology of two dipterocarp rain forest tree species. J Ecol 84:863–876
Acknowledgements
We thank: Martina Peter and Lee Su See for helpful discussion of the experimental design and morphotype identification; Charles Godfray and Glen Reynolds for their efforts in setting up and supporting the Sabah Biodiversity Experiment; Karin Beer together with research assistants from the Malua Field Station for providing field assistance; Jake Snaddon, Michael O’Brien, Thom W. Kuyper and two anonymous reviewers for comments on the manuscript. The Economic Planning Unit Sabah, Malaysia and the Danum Valley Management Committee approved this field study. This project was funded by the University Zurich, with financial support from the Darwin Initiative fund and is part of the Royal Society South-East Asia Rainforest Research Programme (Project No. RS243). This is paper no. 3 of the Sabah Biodiversity Experiment.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Thom W. Kuyper.
Rights and permissions
About this article
Cite this article
Saner, P., Philipson, C., Ong, R.C. et al. Positive effects of ectomycorrhizal colonization on growth of seedlings of a tropical tree across a range of forest floor light conditions. Plant Soil 338, 411–421 (2011). https://doi.org/10.1007/s11104-010-0555-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-010-0555-3