Skip to main content
SpringerLink
Log in

Intraspecific traits change biodiversity effects on ecosystem functioning under metal stress

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

Abstract

Studies investigating the impacts of biodiversity loss on ecosystem processes have often reached different conclusions, probably because insufficient attention has been paid to some aspects including (1) which biodiversity measure (e.g., species number, species identity or trait) better explains ecosystem functioning, (2) the mechanisms underpinning biodiversity effects, and (3) how can environmental context modulates biodiversity effects. Here, we investigated how species number (one to three species) and traits of aquatic fungal decomposers (by replacement of a functional type from an unpolluted site by another from a metal-polluted site) affect fungal production (biomass acumulation) and plant litter decomposition in the presence and absence of metal stress. To examine the putative mechanisms that explain biodiversity effects, we determined the contribution of each fungal species to the total biomass produced in multicultures by real-time PCR. In the absence of metal, positive diversity effects were observed for fungal production and leaf decomposition as a result of species complementarity. Metal stress decreased diversity effects on leaf decomposition in assemblages containing the functional type from the unpolluted site, probably due to competitive interactions between fungi. However, dominance effect maintained positive diversity effects under metal stress in assemblages containing the functional type from the metal-polluted site. These findings emphasize the importance of intraspecific diversity in modulating diversity effects under metal stress, providing evidence that trait-based diversity measures should be incorporated when examining biodiversity effects.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Azevedo MM, Cássio F (2010) Effects of metals on growth and sporulation of aquatic fungi. Drug Chem Toxicol 33:269–278. doi:10.3109/01480540903431440

    Article  PubMed  CAS  Google Scholar 

  • Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156. doi:10.1111/j.1461-0248.2006.00963.x

    Article  PubMed  Google Scholar 

  • Bärlocher F (2005) Freshwater fungal communities. In: Dighton J, Oudemans P, White J (eds) The fungal community, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Bärlocher F, Corkum M (2003) Nutrient enrichment overwhelms diversity effects in leaf decomposition by stream fungi. Oikos 101:247–252. doi:10.1034/j.1600-0706.2003.12372.x

    Article  Google Scholar 

  • Bärlocher F, Graça MAS (2002) Exotic riparian vegetation lowers fungal diversity but not leaf decomposition in Portuguese streams. Freshwater Biol 47:1123–1135. doi:10.1046/j.1365-2427.2002.00836.x

    Article  Google Scholar 

  • Bermingham S, Maltby L, Dewey FM (1996) Monoclonal antibodies as tools to quantify mycelium of aquatic hyphomycetes. New Phytol 132:593–601. doi:10.1111/j.1469-8137.1996.tb01878.x

    Article  Google Scholar 

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortiek CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848. doi:10.1038/nature00812

    Article  PubMed  CAS  Google Scholar 

  • Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. doi:10.1038/nature05202

    Article  PubMed  CAS  Google Scholar 

  • Dang CK, Chauvet E, Gessner MO (2005) Magnitude and variability of process rates in fungal diversity-litter decomposition relationships. Ecol Lett 8:1129–1137. doi:10.1111/j.1461-0248.2005.00815.x

    Article  PubMed  Google Scholar 

  • Das M, Royer TV, Leff LG (2007) Diversity of fungi, bacteria, and actinomycetes on leaves decomposing in a stream. Appl Environ Microbiol 73:756–767. doi:10.1128/AEM.01170-06

    Article  PubMed  CAS  Google Scholar 

  • Duarte S, Pascoal C, Cássio F, Bärlocher F (2006) Aquatic hyphomycete diversity and identity affect leaf litter decomposition in microcosms. Oecologia 147:658–666. doi:10.1007/s00442-005-0300-4

    Article  PubMed  Google Scholar 

  • Duarte S, Pascoal C, Garabétian F, Cássio F, Charcosset J-Y (2009) Microbial decomposer communities are mainly structured by trophic status in circumneutral and alkaline streams. Appl Environ Microbiol 79:6211–6221. doi:10.1128/AEM.00971-09

    Article  Google Scholar 

  • Ducklow H (2008) Microbial services: challenges for microbial ecologists in a changing world. Aquat Microb Ecol 53:13–19. doi:10.3354/ame01220

    Article  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039. doi:10.1126/science.1153213

    Article  PubMed  CAS  Google Scholar 

  • Fernandes I, Duarte S, Cássio F, Pascoal C (2009a) Mixtures of zinc and phosphate affect leaf litter decomposition by aquatic fungi in streams. Sci Total Environ 407:4283–4288. doi:10.1016/j.scitotenv.2009.04.007

    Article  PubMed  CAS  Google Scholar 

  • Fernandes I, Uzun B, Pascoal C, Cássio F (2009b) Responses of aquatic fungal communities on leaf litter to temperature-change events. Int Rev Hydrobiol 94:410–418. doi:10.1002/iroh.200811163

    Article  Google Scholar 

  • Ferreira V, Gulis V, Graça MAS (2006) Whole-stream nitrate addition affects litter decomposition and associated fungi but not invertebrates. Oecologia 149:718–729. doi:10.1007/s00442-006-0478-0

    Article  PubMed  Google Scholar 

  • Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on ecosystem function. Ecol Lett 8:846–856. doi:10.1111/j.1461-0248.2005.00795.x

    Article  Google Scholar 

  • Gamfeldt L, Hillebrand H (2008) Biodiversity effects on aquatic ecosystem functioning—maturation of a new paradigm. Int Rev Hydrobiol 93:550–564. doi:10.1002/iroh.200711022

    Article  Google Scholar 

  • Gamfeldt L, Källström B (2007) Increasing intraspecific diversity increases predictability in population survival in the face of perturbations. Oikos 116:700–705. doi:10.1111/j.0030-1299.2007.15382.x

    Article  Google Scholar 

  • Gessner MO (2005) Ergosterol as a measure of fungal biomass. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 189–196

    Chapter  Google Scholar 

  • Hector A, Bell T, Connolly J, Finn J, Fox J, Kirwan L, Loreau M, McLaren J, Schmid B, Weigelt A (2009) The analysis of biodiversity experiments: from pattern toward mechanism. In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C (eds) Biodiversity, ecosystem functioning, and human wellbeing. An ecological and economic perspective. Oxford University Press, New York, pp 94–104

    Chapter  Google Scholar 

  • Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. doi:10.1890/04-0922

    Article  Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002. doi:10.1073/pnas.0402642101

    Article  PubMed  CAS  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi:10.1111/j.1461-0248.2008.01179.x

    Article  PubMed  Google Scholar 

  • Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, Bohannan BJM (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189–197. doi:10.1016/j.tree.2004.01.008

    Article  PubMed  Google Scholar 

  • Kanagawa T (2003) Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96:317–323. doi:10.1016/S1389-1723(03)90130-7

    PubMed  CAS  Google Scholar 

  • Kennedy PG, Bergemann SE, Hortal S, Bruns TD (2007) Determining the outcome of field-based competition between two Rhizopogon species using real-time PCR. Mol Ecol 16:881–890. doi:10.1111/j.1365-294X.2006.03191.x

    Article  PubMed  CAS  Google Scholar 

  • Kominoski JS, Hoellein TJ, Kelly JJ, Pringle CM (2009) Does mixing litter of different qualities alter stream microbial diversity and functioning on individual litter species? Oikos 118:457–463. doi:10.1111/j.1600-0706.2008.17222.x

    Article  Google Scholar 

  • Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonák J, Lind K, Sindelka R, Sjöback R, Sjögreen B, Strömbom L, Ståhlberg A, Zoric N (2006) The real-time polymerase chain reaction. Mol Asp Med 27:95–125. doi:10.1016/j.mam.2005.12.007

    Article  CAS  Google Scholar 

  • Lecerf A, Dobson M, Dang CK, Chauvet E (2005) Riparian plant species loss alters trophic dynamics in detritus-based ecosystems. Oecologia 146:432–442. doi:10.1007/s00442-005-0212-3

    Article  PubMed  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. doi:10.1038/35083573

    Article  PubMed  CAS  Google Scholar 

  • Marks JC, Haden GA, Harrop BL, Reese EG, Keams JL, Watwood ME, Whitham TG (2009) Genetic and environmental controls of microbial communities on leaf litter in streams. Freshwater Biol 54:2616–2627. doi:10.1111/j.1365-2427.2009.02270.x

    Article  CAS  Google Scholar 

  • McKie BG, Schindler M, Gessner MO, Malmqvist B (2009) Placing biodiversity and ecosystem functioning in context: environmental perturbations and the effects of species richness in a stream field experiment. Oecologia 160:757–770. doi:10.1007/s00442-009-1336-7

    Article  PubMed  Google Scholar 

  • Mulder CPH, Uliassi DD, Doak DF (2001) Physical stress and diversity-productivity relationships: the role of positive interactions. Proc Natl Acad Sci USA 98:6704–6708. doi:10.1073/pnas.111055298

    Article  PubMed  CAS  Google Scholar 

  • Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microbiol 70:5266–5273. doi:10.1128/AEM.70.9.5266-5273.2004

    Article  PubMed  CAS  Google Scholar 

  • Pascoal C, Cássio F (2008) Linking fungal diversity to the functioning of freshwater ecosystems. In: Sridhar KR, Bärlocher F, Hyde KD (eds) Novel techniques and ideas in mycology. Fungal Diversity Research Series, Fungal Diversity Press, Hong Kong, pp 1–15

    Google Scholar 

  • Pascoal C, Cássio F, Marvanová L (2005a) Anthropogenic stress may affect aquatic hyphomycete diversity more than leaf decomposition in a low-order stream. Arch Hydrobiol 162:481–496. doi:10.1127/0003-9136/2005/0162-0481

    Article  Google Scholar 

  • Pascoal C, Marvanová L, Cássio F (2005b) Aquatic hyphomycete diversity in streams of Northwest Portugal. Fungal Divers 19:109–128

    Google Scholar 

  • Pascoal C, Cássio F, Nikolcheva L, Bärlocher F (2010) Realized fungal diversity increases functional stability of leaf litter decomposition under zinc stress. Microb Ecol 59:84–93. doi:10.1007/s00248-009-9567-z

    Article  PubMed  CAS  Google Scholar 

  • Raviraja NS, Sridhar KR, Bärlocher F (1998) Breakdown of Ficus and Eucalyptus leaves in an organically polluted river in India: fungal diversity and ecological functions. Freshwater Biol 39:537–545. doi:10.1046/j.1365-2427.1998.00303.x

    Article  Google Scholar 

  • Raviraja NS, Nikolcheva LG, Bärlocher F (2006) Fungal growth and leaf decomposition are affected by amount and type of inoculum and by external nutrients. Sydowia 58:91–104

    Google Scholar 

  • Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514. doi:10.1016/j.tree.2009.03.018

    Article  PubMed  Google Scholar 

  • Reiss J, Forster J, Cássio F, Pascoal C, Stewart R, Hirst AG (2010) When microscopic organisms inform general ecological theory. Adv Ecol Res 43:45–85. doi:10.1016/B978-0-12-385005-8.00002-2

    Article  Google Scholar 

  • Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831. doi:10.1073/pnas.0500008102

    Article  PubMed  CAS  Google Scholar 

  • Soares HMVM, Boaventura RAR, Machado AASC, Esteves da Silva JCG (1999) Sediments as monitors of heavy metal contamination in the Ave river basin (Portugal): multivariate analysis of data. Environ Pollut 105:311–323. doi:10.1016/S0269-7491(99)00048-2

    Article  PubMed  CAS  Google Scholar 

  • Sridhar KR, Krauss G, Bärlocher F, Wennrich R, Krauss G-J (2000) Fungal diversity in heavy metal polluted waters in Central Germany. Fungal Divers 5:119–129

    Google Scholar 

  • Sridhar KR, Krauss G, Bärlocher F, Raviraja NS, Wennrich R, Baumbach R, Krauss G-J (2001) Decompostion of alder leaves in two heavy metal-polluted streams in central Germany. Aquat Microb Ecol 26:73–80. doi:10.3354/ame026073

    Article  Google Scholar 

  • Suberkropp K, Arsuffi TL, Anderson JP (1983) Comparison of degradative ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Appl Environ Microbiol 46:237–244

    PubMed  CAS  Google Scholar 

  • Treton C, Chauvet E, Charcosset J-Y (2004) Competitive interaction between two aquatic hyphomycete species and increase in leaf litter breakdown. Microb Ecol 48:439–446. doi:10.1007/s00248-003-0195-8

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Englewood Cliffs, Prentice-Hall

    Google Scholar 

  • Zhang Q-G, Zhang D-Y (2006) Species richness destabilizes ecosystem functioning in experimental aquatic microcosms. Oikos 112:218–226. doi:10.1111/j.0030-1299.2006.14220.x

    Article  Google Scholar 

Download references

Acknowledgments

The Portuguese Foundation for Science and Technology supported I. Fernandes (SFRH/BD/42215/2007). We are grateful to M.O. Gessner, R.O. Hall, Jr, and two anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Isabel Fernandes, Cláudia Pascoal & Fernanda Cássio

Authors
  1. Isabel Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cláudia Pascoal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernanda Cássio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernanda Cássio.

Additional information

Communicated by Robert Hall.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 26 kb)

Supplementary material 2 (PDF 11 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernandes, I., Pascoal, C. & Cássio, F. Intraspecific traits change biodiversity effects on ecosystem functioning under metal stress. Oecologia 166, 1019–1028 (2011). https://doi.org/10.1007/s00442-011-1930-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-1930-3

Keywords

Search

Navigation