Skip to main content

Advertisement

SpringerLink
Log in

Responses of Aquatic Hyphomycetes to Temperature and Nutrient Availability: a Cross-transplantation Experiment

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Aquatic hyphomycetes represent a large component of the microbial assemblage that decomposes submerged leaf-litter in fluvial ecosystems. The structure and activity of these fungal decomposers depend on environmental factors. Fungal communities may adapt to local habitat conditions; however, little is known about how fungal communities respond to abrupt changes in factors such as nutrient availability and temperature. To respond to this question, we carried out a cross-transplantation experiment, which assessed the decomposer activity and structure of this microbial community on decaying leaves transplanted from a cold and oligotrophic stream (S1) to a warmer and nitrogen-richer one (S2) and vice versa. Results were compared to those from untransplanted leaves decomposing either at S1 or at S2. In terms of days, untransplanted leaves were decomposed at a similar rate in both streams; the change to warmer and nitrogen-richer waters (S1 ➔ S2) significantly enhanced the decomposition process while the reciprocal transplantation (S2 ➔ S1) did not alter decomposition rate. However, when standardizing the temperature effects by using degree-days, microbial decomposers under colder conditions were more efficient in terms of accumulated heat, independent of the initial or final incubation site. Regarding community structure, taxa richness and diversity of aquatic hyphomycetes appear to be favoured under warmer and richer conditions, increasing after transplantation to S2 but with little effect on the predominant taxa. However, the reciprocal transplantation (S2 ➔ S1) yielded a clear decline of the dominant taxa at S2 (Lunulospora curvula) in favour of the local dominant ones. Thus, effects of environmental changes on activity and community structure can be highly variable and not always clearly linked or reciprocal. Therefore, results from simplified experimental designs (e.g. artificial assemblages under laboratory conditions) must be taken with caution. Additional field studies and manipulative experimentation dealing with natural communities are required when trying to extend individual results to complex scenarios such as those projected by global change.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Wallace JB, Eggert SL, Meyer JL, Webster JR (1999) Effects of resource limitation on a detrital-based ecosystem. Ecol Monogr 69:409–442

    Article  Google Scholar 

  2. Bärlocher F (1992) The ecology of aquatic hyphomycetes. Springer, Berlin

    Book  Google Scholar 

  3. Ferreira V, Chauvet E (2011) Future increase in temperature more than decrease in litter quality can affect microbial litter decomposition in streams. Oecologia 67:279–291

    Article  Google Scholar 

  4. Suberkropp K, Chauvet E (1995) Regulation of leaf breakdown by fungi in streams: influences of water chemistry. Ecology 76:1433–1445

    Article  Google Scholar 

  5. Canhoto C, Graça MAS (2008) Interactions between fungi and stream invertebrates: back to the future. In: Novel techniques and ideas in mycology. Sridhar S, Bärlocher F, Hyde KD (eds) Fungal Diversity Research Series 20: 205–325

  6. Tant CJ, Rosemond AD, First MR (2013) Stream nutrient enrichment has a greater effect on coarse than on fine benthic organic matter. Freshw Sci 32:1111–1121

    Article  Google Scholar 

  7. Bärlocher F (2005a) Freshwater fungal communities. In: Deighton J, White Jr JF, Oudemans P (eds) The fungal community: its organization and role in the ecosystem3rd edn. Taylor and Francis, CRC, Boca Raton, pp 39–59

    Chapter  Google Scholar 

  8. Webster JR, Newbold JD, Thomas SA, Valett HM, Mulholland PJ (2009) Nutrient uptake and mineralization during leaf decay in streams—a model simulation. Int Rev Hydrobiol 94:372–390

    Article  CAS  Google Scholar 

  9. Pérez J, Descals E, Pozo J (2012) Aquatic hyphomycete communities associated with decomposing alder leaf litter in reference headwater streams of the Basque Country (northern Spain). Microb Ecol 64:279–290

    Article  PubMed  Google Scholar 

  10. Manning DWP, Rosemond AD, Kominoski JS, Gulis V, Benstead JP, Maerz JC (2015) Detrital stoichiometry as a critical nexus for the effects of streamwater nutrients on leaf litter breakdown rates. Ecology 96:2214–2224

    Article  PubMed  Google Scholar 

  11. Perkins DM, Reiss J, Yvon-Durocher G, Woodward G (2010) Global changes and food webs in running waters. Hydrobiologia 657:181–198

    Article  Google Scholar 

  12. Battin TJ, Luyssaert S, Kaplan LA, Aufdenkampe AK, Richter A, Tranvik LJ (2009) The boundless carbon cycle. Nat Geosci 2:598–600

    Article  CAS  Google Scholar 

  13. Duarte S, Pascoal C, Cássio F (2008) High diversity of fungi may mitigate the impact of pollution on plant litter decomposition in streams. Microb Ecol 56:688–695

    Article  PubMed  CAS  Google Scholar 

  14. Sridhar KR, Bärlocher F, Krauss G-J, Krauss G (2005) Response of aquatic hyphomycete communities to changes in heavy metal exposure. Int Rev Hydrobiol 90:21–32

    Article  CAS  Google Scholar 

  15. Ferreira V, Elosegi A, Gulis V, Pozo J, Graça MAS (2006) Eucalyptus plantations affect fungal communities associated with leaf-litter decomposition in Iberian streams. Arch Hydrobiol 166:467–490

    Article  CAS  Google Scholar 

  16. Gonçalves AL, Graça MAS, Canhoto C (2013) The effect of temperature on leaf decomposition and diversity of associated aquatic hyphomycetes depends on the substrate. Fungal Ecol 6:546–553

    Article  Google Scholar 

  17. Murdoch PS, Baron JS, Miller TL (2000) Potential effects of climate change on surface-water quality in North America. J Am Water Resour Assoc 36:347–366

    Article  CAS  Google Scholar 

  18. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  19. Docherty KM, Gutknecht JLM (2012) The role of environmental microorganisms in ecosystem responses to global change: current state of research and future outlooks. Biogeochemistry 109:1–6

    Article  Google Scholar 

  20. Fenoy E, Casas JJ, Díaz-López M, Rubio J, Guil-Guerrero JL, Moyano-López FJ (2016) Temperature and substrate chemistry as major drivers of interregional variability of leaf microbial decomposition and cellulolytic activity in headwater streams. FEMS Microbiol Ecol 92. https://doi.org/10.1093/femsec/fiw169

  21. Dang CK, Schindler M, Chauvet E, Gessner MO (2009) Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition. Ecology 90:122–132

    Article  PubMed  Google Scholar 

  22. Geraldes P, Cláudia P, Cássio F (2012) Effects of increased temperature and aquatic fungal diversity on litter decomposition. Fung Ecol 5:734–740

    Article  Google Scholar 

  23. Fernandes I, Pascoal C, Guimarães H, Pinto R, Sousa I, Cássio F (2012) Higher temperature reduces the effects of litter quality on decomposition by aquatic fungi. Freshw Biol 57:2306–2317

    Article  Google Scholar 

  24. Ferreira V, Castagneyrol B, Koricheva J, Gulis V, Chauvet E, Graça MAS (2015) A meta-analysis of the effects of nutrient enrichment on litter decomposition in streams. Biol Rev 90:669–688

    Article  PubMed  Google Scholar 

  25. Ferreira V, Chauvet E (2011b) Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Glob Chang Biol 17:551–565

    Article  Google Scholar 

  26. Fernandes I, Seena S, Pascoal C, Cássio F (2014) Elevated temperature may intensify the positive effects of nutrients on microbial decomposition in streams. Freshw Biol 59:2390–2399

    Article  CAS  Google Scholar 

  27. Ferreira V, Voronina E (2016) Impact of climate change on aquatic hypho- and terrestrial macromycetes. In: Marxsen J (ed) Climate change and microbial ecology: current research and future trends. Caister Academic Press, Norfolk, pp 53–72

    Chapter  Google Scholar 

  28. Duarte S, Cássio F, Ferreira V, Canhoto C, Pascoal C (2016) Seasonal variability may affect microbial decomposers and leaf decomposition more than warming in streams. Microb Ecol 72:263–276

    Article  PubMed  CAS  Google Scholar 

  29. Martínez A, Larrañaga A, Pérez J, Descals E, Pozo J (2014) Temperature affects leaf litter decomposition in low-order forest streams: field and microcosm approaches. FEMS Microbiol Ecol 87:257–267

    Article  PubMed  CAS  Google Scholar 

  30. Ferreira V, Canhoto C (2015) Future increase in temperature may stimulate litter decomposition in temperate mountain streams: evidence from a stream manipulation experiment. Freshw Biol 60:881–892

    Article  Google Scholar 

  31. Pérez J, Galán J, Descals E, Pozo J (2014) Effects of fungal inocula and habitat conditions on alder and eucalyptus leaf litter decomposition in streams of northern Spain. Microb Ecol 67:245–255

    Article  PubMed  Google Scholar 

  32. Suberkropp K (1984) Effect of temperature on seasonal occurrence of aquatic hyphomycetes. Trans Br Mycol Soc 82:53–62

    Article  Google Scholar 

  33. 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

    Article  PubMed  CAS  Google Scholar 

  34. Sridhar KR, Duarte S, Cássio F, Pascoal C (2009) The role of early fungal colonizers in leaf-litter decomposition in Portuguese streams impacted by agricultural runoff. Int Rev Hydrobiol 94:399–409

    Article  CAS  Google Scholar 

  35. Molinero J, Larrañaga A, Pérez J, Martínez A, Pozo J (2013) Evaluation of the ACR SmartButton thermometer and a low-cost protective case for continuous stream temperature measurement. Limnetica 32:11–22

    Google Scholar 

  36. Molinero J, Larrañaga A, Pérez J, Martínez A, Pozo J (2016) Stream temperature in the Basque Mountains during winter: thermal regimes and sensitivity to air warming. Clim Change 134:593–604

    Article  Google Scholar 

  37. IPCC (2014) Summary for policymakers. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part a: global and sectoral aspects. Contribution of working group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK

  38. Taylor BR, Chauvet E (2014) Relative influence of shredders and fungi on leaf litter decomposition along a river altitudinal gradient. Hydrobiologia 721:239–250

    Article  CAS  Google Scholar 

  39. Bärlocher F (2005b) Leaf mass loss estimated by litter bag technique. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 37–42

    Chapter  Google Scholar 

  40. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC

    Google Scholar 

  41. Allen SE, Grimshaw HM, Parkinson JA, Quarmby C (1974) Chemical analysis and ecological materials. Blackwell, Oxford

    Google Scholar 

  42. Graça MAS, Abelho M (2005) Respirometry. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 231–236

    Chapter  Google Scholar 

  43. Bärlocher F (2005c) Sporulation of aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 185–188

    Chapter  Google Scholar 

  44. Duarte S, Pascoal C, Garabétian F, Cássio F, Charcosset JY (2009) Microbial decomposer communities are mainly structured by trophic status in circumneutral and alkaline streams. Appl Environ Microbiol 75:6211–6222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Descals E (2005) Techniques for handling Ingoldian fungi. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 129–143

    Chapter  Google Scholar 

  46. Gulis V, Marvanová L, Descals E (2005) An illustrated key to the common temperate species of aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 153–168

    Chapter  Google Scholar 

  47. Pozo J, Casas JJ, Menéndez M, Mollá S, Arostegui I, Basaguren A, Casado C, Descals E, García-Avilés J, González JM, Larrañaga A, López E, Lusi M, Moya O, Pérez J, Riera T, Roblas N, Salinas MJ (2011) Leaf-litter decomposition in headwater streams: a comparison of the process among four climatic regions. J N Am Benthol Soc 30:935–950

    Article  Google Scholar 

  48. Boyero L, Pearson RG, Gessner MO, Barmuta LA, Ferreira V, Graça MAS et al (2011) A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration. Ecol Lett 14:289–294

    Article  PubMed  Google Scholar 

  49. Zar JH (2010) Biostatistical analysis5th edn. Pearson, Upper Saddle River

    Google Scholar 

  50. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. PNAS 102:11512–11519

    Article  Google Scholar 

  51. Bergfur J, Friberg N (2012) Trade-offs between fungal and bacterial respiration along gradients in temperature, nutrients and substrata: experiments with stream derived microbial communities. Fungal Ecol 5:46–52

    Article  Google Scholar 

  52. Chauvet E, Suberkropp K (1998) Temperature and sporulation of aquatic hyphomycetes. Appl Environ Microbiol 64:1522–1526

    PubMed  PubMed Central  CAS  Google Scholar 

  53. Fernandes I, Uzun B, Pascoal C, Cássio F (2009) Responses of aquatic fungal communities on leaf litter to temperature-change events. Int Rev Hydrobiol 94:410–419

    Article  Google Scholar 

  54. Bärlocher F, Seena S, Wilson KP, Williams DD (2008) Raised water temperature lowers diversity of hyporheic aquatic hyphomycetes. Freshw Biol 53:368–379

    Google Scholar 

  55. Cross WF, Benstead JP, Frost PC, Thomas SA (2005) Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Freshw Biol 50:1895–1912

    Article  CAS  Google Scholar 

  56. Benstead JP, Rosemond AD, Cross WF, Wallace JB, Eggert SL, Suberkropp K, Gulis V, Greenwood JL, Tant CJ (2009) Nutrient enrichment alters storage and fluxes of detritus in a headwater stream ecosystem. Ecol Soc Am 90:2556–2566

    Google Scholar 

  57. Pérez J, Basaguren A, Descals E, Larrañaga A, Pozo J (2013) Leaf-litter processing in headwater streams of northern Iberian Peninsula: moderate levels of eutrophication do not explain breakdown rates. Hydrobiologia 718:41–57

    Article  Google Scholar 

  58. Pozo J (1993) Leaf litter processing of alder and eucalyptus in the Agüera stream system (North Spain) I. Chemical changes. Arch Hydrobiol 127:299–317

    Google Scholar 

  59. Webster J, Moran ST, Davey RA (1976) Growth and sporulation of Tricladium chaetocladium and Lunulospora curvula in relation to temperature. Trans Br Mycol Soc 67:491–496

    Article  Google Scholar 

Download references

Acknowledgments

S. Monroy, S. Padilla and U. Txurruka helped in field visits and laboratory processing of samples. The authors thank the technicians of SGIker’s SCAB Service of the University of the Basque Country, UPV/EHU, for the nitrate measurements. J. Molinero and A. Larrañaga helped with the assessment of leaf-P concentrations and O2 consumption rates.

Funding

This work was funded by the Ministry of Science and Innovation of the Spanish Government (projects CGL2010-22129-C04-01 and CGL2011-23984) and by the Basque Government (projects IT-422-07 and IT-302-10). J. Pérez and A. Martínez were supported by UPV/EHU grants.

Author information

Authors and Affiliations

  1. Laboratory of Stream Ecology, Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), P.O. Box 644, 48080, Bilbao, Spain

    Javier Pérez, Aingeru Martínez & Jesús Pozo

  2. Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC), Miquel Marquès 21, 07190, Esporles, Mallorca, Spain

    Enrique Descals

Authors
  1. Javier Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aingeru Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrique Descals
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jesús Pozo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Pérez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez, J., Martínez, A., Descals, E. et al. Responses of Aquatic Hyphomycetes to Temperature and Nutrient Availability: a Cross-transplantation Experiment. Microb Ecol 76, 328–339 (2018). https://doi.org/10.1007/s00248-018-1148-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1148-6

Keywords

Search

Navigation