Skip to main content

Advertisement

Log in

Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest

  • Ecosystem ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

    Article  Google Scholar 

  • Altschul SF et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Ayres E et al (2009b) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem 41:606–610

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Batjes NH (1996) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 47:151–163

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Carney KM, Matson PA (2006) The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52:226–238

    Article  PubMed  Google Scholar 

  • Connell JH, Lowman MD (1989) Low-diversity tropical rain forests: some possible mechanisms for their existence. Am Nat 134:88–119

    Article  Google Scholar 

  • Couteaux MM, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10:63–66

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Degagne RS, Henkel TW, Steinberg SJ, Fox L (2009) Identifying Dicymbe corymbosa monodominant forests in Guyana using satellite imagery. Biotropica 41:7–15

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal foots of Pinus radiata. N Z J For Sci 5:35–41

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246

    Article  Google Scholar 

  • Gause GF (1934) The struggle for existence. Williams & Wilkins, Baltimore

    Google Scholar 

  • Gentry AH (1992) Tropical forest biodiversity—distributional patterns and their conservational significance. Oikos 63:19–28

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hart TB (1990) Monospecific dominance in tropical rain forests. Trends Ecol Evol 5:6–11

    Article  Google Scholar 

  • Hattenschwiler S, Tiunov A, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218

    Article  Google Scholar 

  • Henkel TW (2003) Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J Trop Ecol 19:417–437

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Jimenez JJ, Lal R (2006) Mechanisms of C sequestration in soils of Latin America. Crit Rev Plant Sci 25:337–365

    Article  CAS  Google Scholar 

  • Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac—a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228-8235

    Google Scholar 

  • Lynch MDJ, Thorn RG (2006) Diversity of basidiomycetes in Michigan agricultural soils. Appl Environ Microbiol 72:7050–7056

    Article  CAS  PubMed  Google Scholar 

  • Mayor JR, Henkel TW (2006) Do ectomycorrhizas alter leaf-litter decomposition in monodominant tropical forests of Guyana? New Phytol 169:579–588

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Olson JS (1963) Energy-storage and balance of producers and decomposers in ecological-systems. Ecology 44:322

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Potvin C, Lechowicz MJ, Tardif S (1990) The statistical-analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Singer R, Araujo IdJdSAraujo (1979) Litter decomposition and ectomycorrhizas in Amazonian forests. Acta Amazon 9:25–41

    Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Blackwell, Oxford

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ter Braak CJF (1986) Canonical correspondence analysis—a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167-1179

    Google Scholar 

  • Thacker JR, Henkel TW (2004) New species of Clavulina from Guyana. Mycologia 96:650–657

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Torti SD, Coley PD, Kursar TA (2001) Causes and consequences of monodominance in tropical lowland forests. Am Nat 157:141–153

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Valencia RH, Balslev H, Paz H, Mino CG (1994) High tree alpha-diversity in Amazonian Ecuador. Biodivers Conserv 3:21–28

    Article  Google Scholar 

  • Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298

    Article  CAS  Google Scholar 

  • Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • White DC, Stair JO, Ringelberg DB (1997) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol 17:185–196

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Krista L. McGuire.

Additional information

Communicated by Stephan Hättenschwiler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 26 kb)

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1686-1

Keywords

Navigation