Abstract
Bacteria and fungi drive the cycling of plant litter in forests, but little is known about their role in tropical rain forest nutrient cycling, despite the high rates of litter decay observed in these ecosystems. However, litter decay rates are not uniform across tropical rain forests. For example, decomposition can differ dramatically over small spatial scales between low-diversity, monodominant rain forests, and species-rich, mixed forests. Because the climatic patterns and soil parent material are identical in co-occurring mixed and monodominant forests, differences in forest floor accumulation, litter production, and decomposition between these forests may be biotically mediated. To test this hypothesis, we conducted field and laboratory studies in a monodominant rain forest in which the ectomycorrhizal tree Dicymbe corymbosa forms >80% of the canopy, and a diverse, mixed forest dominated by arbuscular mycorrhizal trees. After 2 years, decomposition was significantly slower in the monodominant forest (P < 0.001), but litter production was significantly greater in the mixed forest (P < 0.001). In the laboratory, we found microbial community biomass was greater in the mixed forest (P = 0.02), and the composition of fungal communities was distinct between the two rain forest types (P = 0.001). Sequencing of fungal rDNA revealed a significantly lower richness of saprotrophic fungi in the monodominant forest (19 species) relative to the species-rich forest (84 species); moreover, only 4% percent of fungal sequences occurred in both forests. These results show that nutrient cycling patterns in tropical forests can vary dramatically over small spatial scales, and that changes in microbial community structure likely drive the observed differences in decomposition.
Similar content being viewed by others
References
Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449
Altschul SF et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anderson JM, Swift MJ (1983) Decomposition in tropical forests. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forests: ecology and management. Blackwell, Oxford, pp 287–309
Ayres E, Steltzer H, Berg S, Wall DH (2009a) Soil biota accelerate decomposition in high-elevation forests by specializing in the breakdown of litter produced by the plant species above them. J Ecol 97:901–912
Ayres E et al (2009b) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem 41:606–610
Baldrian P (2009) Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia 161:657–660
Batjes NH (1996) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 47:151–163
Berg B, McClaugherty C (2007) Chapter 3 decomposer organisms. In: Plant litter: decomposition, humus formation, carbon sequestration. Springer, Berlin, pp 35–52
Bligh EG, Dyer WJ (1954) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Carney KM, Matson PA (2006) The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52:226–238
Connell JH, Lowman MD (1989) Low-diversity tropical rain forests: some possible mechanisms for their existence. Am Nat 134:88–119
Couteaux MM, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10:63–66
Cullings K, Ishkhanova G, Henson J (2008) Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park. Oecologia 158:77–83
Degagne RS, Henkel TW, Steinberg SJ, Fox L (2009) Identifying Dicymbe corymbosa monodominant forests in Guyana using satellite imagery. Biotropica 41:7–15
Dixon RK, Brown S, Houghton RA, Solomon AM, Trexler MC, Wisniewski J (1994) Carbon pools and flux of global forest ecosystems. Science 263:185–190
Felsenstein J (2005) PHYLIP (Phylogeny Inference Package). In: 3.6 edn. Department of Genome Sciences, University of Washington, Seattle
Gadgil RL, Gadgil GD (1971) Mycorrhiza and litter decomposition. Nature 233:133
Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal foots of Pinus radiata. N Z J For Sci 5:35–41
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246
Gause GF (1934) The struggle for existence. Williams & Wilkins, Baltimore
Gentry AH (1992) Tropical forest biodiversity—distributional patterns and their conservational significance. Oikos 63:19–28
Gholz HL, Wedin DA, Smitherman SM, Harmon ME, Parton WJ (2000) Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Glob Change Biol 6:751–765
Hart TB (1990) Monospecific dominance in tropical rain forests. Trends Ecol Evol 5:6–11
Hattenschwiler S, Tiunov A, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218
Henkel TW (2003) Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J Trop Ecol 19:417–437
Janos DP (1985) Mycorrhizal fungi: agents or symptoms of tropical community composition. In: Molina R (ed) Proceedings of the 6th North American Conference on Mycorrhizae. Oregon State University, Corvallis
Jimenez JJ, Lal R (2006) Mechanisms of C sequestration in soils of Latin America. Crit Rev Plant Sci 25:337–365
Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407
Lindahl B, Stenlid J, Olsson S, Finlay R (1999) Translocation of P-32 between interacting mycelia of a wood-decomposing fungus and ectomycorrhizal fungi in microcosm systems. New Phytol 144:183–193
Lozupone C, Knight R (2005) UniFrac—a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228-8235
Lynch MDJ, Thorn RG (2006) Diversity of basidiomycetes in Michigan agricultural soils. Appl Environ Microbiol 72:7050–7056
Mayor JR, Henkel TW (2006) Do ectomycorrhizas alter leaf-litter decomposition in monodominant tropical forests of Guyana? New Phytol 169:579–588
McGuire KL (2008) Ectomycorrhizal associations function to maintain tropical monodominance. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Netherlands, pp 287–302
McGuire KL, Henkel TW, Granzow de la Cerda I, Villa G, Edmund F, Andrew C (2008) Dual mycorrhizal colonization of forest-dominating tropical trees and the mycorrhizal status of non-dominant tree and liana species. Mycorrhiza 18:217–222
Olson JS (1963) Energy-storage and balance of producers and decomposers in ecological-systems. Ecology 44:322
Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) 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 Phytol 185:529–542
Potvin C, Lechowicz MJ, Tardif S (1990) The statistical-analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400
Proctor J (1983) Tropical forest litter fall. I. Problems of data comparison. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forests: ecology and management. Blackwell, Oxford, pp 267–285
Sayer EJ, Powers JS, Tanner EVJ (2007) Increased litterfall in tropical forests boosts the transfer of soil CO2 to the atmosphere. PLos ONE 2:1–6
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506
Singer R, Araujo IdJdSAraujo (1979) Litter decomposition and ectomycorrhizas in Amazonian forests. Acta Amazon 9:25–41
Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Blackwell, Oxford
Swofford DL (2003) PAUP*. Phylogentic analysis using parsimony (*and other methods), 4 edn. Sinauer, Sunderland
Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850
Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354
Tedersoo L, Suva T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748
Ter Braak CJF (1986) Canonical correspondence analysis—a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167-1179
Thacker JR, Henkel TW (2004) New species of Clavulina from Guyana. Mycologia 96:650–657
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
Torti SD, Coley PD, Kursar TA (2001) Causes and consequences of monodominance in tropical lowland forests. Am Nat 157:141–153
Townsend AR, Vitousek PM, Holland EA (1992) Tropical soils could dominate the short-term carbon-cycle feedbacks to increased global temperatures. Climatic Change 22:293–303
Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936
Valencia RH, Balslev H, Paz H, Mino CG (1994) High tree alpha-diversity in Amazonian Ecuador. Biodivers Conserv 3:21–28
Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298
Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167
White DC, Stair JO, Ringelberg DB (1997) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol 17:185–196
Woolley LP, Henkel TW, Sillett SC (2008) Reiteration in the monodominant tropical tree Dicymbe corymbosa (Caesalpiniaceae) and its potential adaptive significance. Biotropica 40:32–43
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soi: a review. Biol Fertil Soils 29:111–129
Zhu WX, Ehrenfeld JG (1996) The effects of mycorrhizal roots on litter decomposition, soil biota, and nutrients in a spodosolic soil. Plant Soil 179:109–118
Acknowledgments
We thank the Patamona Amerindian tribe, Margaret Chana-Sue, Malcolm Chana-Sue, Terry Henkel, and Raquel Thomas for logistical support with field expeditions. Christopher Andrew, Estine Andrew, Francino Edmund, Leonard Williams, Primus Peters, Dan Griffith, Jesse Knapp, Dana Revallo, and Matt Pierle were of particular assistance in the field. We also thank John Vandermeer, Deborah Goldberg, Kathleen Treseder, Íñigo Granzow de la Cerda, Terry Henkel, and two anonymous reviewers for valuable intellectual contribution to this work. Funding was provided by the University of Michigan Wehmeyer endowment, the University of Michigan International Institute, and the National Science Doctoral Dissertation Improvement Grant (No. 0508585). Permits were granted by the Guyana Environmental Protection Agency and the Guyana Ministry of Amerindian Affairs.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Stephan Hättenschwiler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
McGuire, K.L., Zak, D.R., Edwards, I.P. et al. Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164, 785–795 (2010). https://doi.org/10.1007/s00442-010-1686-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1686-1