Microbial Ecology

, Volume 72, Issue 2, pp 263–276 | Cite as

Seasonal Variability May Affect Microbial Decomposers and Leaf Decomposition More Than Warming in Streams

  • Sofia Duarte
  • Fernanda Cássio
  • Verónica Ferreira
  • Cristina Canhoto
  • Cláudia Pascoal
Microbiology of Aquatic Systems

Abstract

Ongoing climate change is expected to affect the diversity and activity of aquatic microbes, which play a key role in plant litter decomposition in forest streams. We used a before-after control-impact (BACI) design to study the effects of warming on a forest stream reach. The stream reach was divided by a longitudinal barrier, and during 1 year (ambient year) both stream halves were at ambient temperature, while in the second year (warmed year) the temperature in one stream half was increased by ca. 3 °C above ambient temperature (experimental half). Fine-mesh bags containing oak (Quercus robur L.) leaves were immersed in both stream halves for up to 60 days in spring and autumn of the ambient and warmed years. We assessed leaf-associated microbial diversity by denaturing gradient gel electrophoresis and identification of fungal conidial morphotypes and microbial activity by quantifying leaf mass loss and productivity of fungi and bacteria. In the ambient year, no differences were found in leaf decomposition rates and microbial productivities either between seasons or stream halves. In the warmed year, phosphorus concentration in the stream water, leaf decomposition rates, and productivity of bacteria were higher in spring than in autumn. They did not differ between stream halves, except for leaf decomposition, which was higher in the experimental half in spring. Fungal and bacterial communities differed between seasons in both years. Seasonal changes in stream water variables had a greater impact on the activity and diversity of microbial decomposers than a warming regime simulating a predicted global warming scenario.

Keywords

Global warming Streams Plant-litter decomposition Microbial activity and productivity BACI design 

Supplementary material

248_2016_780_MOESM1_ESM.docx (28 kb)
Table S1(DOCX 27 kb)

References

  1. 1.
    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, CambridgeGoogle Scholar
  2. 2.
    Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters. Springer, DordrechtCrossRefGoogle Scholar
  3. 3.
    Stefan HG, Sinokrot BA (1993) Projected global climate change impact on water temperatures in five North Central U.S. streams. Clim Change 24:353–381CrossRefGoogle Scholar
  4. 4.
    Suberkropp K (1998) Microorganisms and organic matter decomposition. In: Naiman R, Bilby RE (eds) River ecology and management: lessons from the pacific coastal ecoregion. Springer, New York, pp 120–143CrossRefGoogle Scholar
  5. 5.
    Bärlocher F (2005) Freshwater fungal communities. Taylor and Francis, CRC Press, Boca Raton, FloridaCrossRefGoogle Scholar
  6. 6.
    Chamier A-C, Dixon PA (1982) Pectinases in leaf degradation by aquatic hyphomycetes: the enzymes and leaf maceration. J Gen Microbiol 128:2469–2483Google Scholar
  7. 7.
    Gessner MO, Gulis V, Kuehn KA, Chauvet E, Suberkropp K (2007) Fungal decomposers of plant litter in aquatic ecosystems. In: Kubicek CP, Druzhinina IS (eds) The mycota: environmental and microbial relationships, vol IV, 2nd edn. Springer, Berlin, pp 301–321Google Scholar
  8. 8.
    Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134CrossRefGoogle Scholar
  9. 9.
    Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microbiol 70:5266–5273CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Bärlocher F, Kendrick B (1975) Leaf-conditioning by microorganisms. Oecologia 20:359–362CrossRefGoogle Scholar
  11. 11.
    Graça MAS, Cressa C (2010) Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int Rev Hydrobiol 95:27–41CrossRefGoogle Scholar
  12. 12.
    Chauvet E, Suberkropp K (1998) Temperature and sporulation of aquatic hyphomycetes. Appl Environ Microbiol 64:1522–1525PubMedPubMedCentralGoogle Scholar
  13. 13.
    Duarte S, Fernandes I, Nogueira M-J, Cássio F, Pascoal C (2013) Temperature alters interspecific relationships among aquatic fungi. Fungal Ecol 6:187–191CrossRefGoogle Scholar
  14. 14.
    Dang CK, Schindler M, Chauvet E, Gessner MO (2009) Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition. Ecology 90:122–131CrossRefPubMedGoogle Scholar
  15. 15.
    Fernandes I, Uzun B, Pascoal C, Cássio F (2009) Responses of aquatic fungal communities on leaf litter to temperature-change events. Int Rev Hydrobiol 94:410–418CrossRefGoogle Scholar
  16. 16.
    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 57:2306–2317CrossRefGoogle Scholar
  17. 17.
    Ferreira V, Chauvet E (2011) Future increase in temperature more than decrease in litter quality can affect microbial litter decomposition in streams. Oecologia 167:279–291CrossRefPubMedGoogle Scholar
  18. 18.
    Ferreira V, Chauvet E (2011) Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Glob Change Biol 17:551–564CrossRefGoogle Scholar
  19. 19.
    Batista D, Pascoal C, Cássio F (2012) Impacts of warming on aquatic decomposers along a gradient of cadmium stress. Environ Pollut 169:35–41CrossRefPubMedGoogle Scholar
  20. 20.
    Geraldes P, Pascoal C, Cássio F (2012) Effects of increased temperature and aquatic fungal diversity loss on litter decomposition. Fungal Ecol 5:734–740CrossRefGoogle Scholar
  21. 21.
    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 6:546–553CrossRefGoogle Scholar
  22. 22.
    Drake JA, Huxel GR, Hewitt CL (1996) Microcosms as models for generating and testing community theory. Ecology 77:670–677CrossRefGoogle Scholar
  23. 23.
    Fraser LH (1999) The use of microcosms as an experimental approach to understanding terrestrial ecosystem functioning. Adv Sp Res 24:297–302CrossRefGoogle Scholar
  24. 24.
    Fabre E, Chauvet E (1998) Leaf breakdown along an altitudinal stream gradient. Arch Hydrobiol 141:167–179CrossRefGoogle Scholar
  25. 25.
    Taylor BR, Chauvet E (2014) Relative influence of shredders and fungi on leaf litter decomposition along a river altitudinal gradient. Hydrobiologia 721:239–250CrossRefGoogle Scholar
  26. 26.
    Irons JG, Oswood MW, Stout RJ, Pringle CM (1994) Latitudinal patterns in leaf litter breakdown: is temperature really important? Freshw Biol 32:401–411CrossRefGoogle Scholar
  27. 27.
    Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  28. 28.
    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 14:289–294CrossRefPubMedGoogle Scholar
  29. 29.
    Friberg N, Christensen JB, Olafsson JS, Gislason GM, Larsen SE, Lauridsen TL (2009) Relationship between structure and function in streams contrasting in temperature: possible impacts of climate change on running water ecosystems. Freshw Biol 54:2051–2068CrossRefGoogle Scholar
  30. 30.
    Chergui H, Pattee E (1990) The influence of season on the breakdown of submerged leaves. Arch Hydrobiol 120:1–12Google Scholar
  31. 31.
    Swan CM, Palmer MA (2004) Leaf diversity alters litter breakdown in a Piedmont stream. J N Am Benthol Soc 23:15–28CrossRefGoogle Scholar
  32. 32.
    Woodward G, Dybkjaer JB, Ólafsson JS, Gíslason GM, Hannesdóttir ER, Friberg N (2010) Sentinel systems on the razor’s edge: effects of warming on Arctic geothermal stream ecosystems. Glob Change Biol 16:1979–1991CrossRefGoogle Scholar
  33. 33.
    Hogg ID, Williams DD (1996) Response of stream invertebrates to a global-warming thermal regime: an ecosystem-level manipulation. Ecology 77:395–407CrossRefGoogle Scholar
  34. 34.
    Bärlocher F, Seena S, Wilson KP, Williams DD (2008) Raised water temperature lowers diversity of hyporheic aquatic hyphomycetes. Freshw Biol 53:368–379Google Scholar
  35. 35.
    Canhoto C, de Lima J, Traça de Almeida A (2013) Warming up a stream reach: design of a hydraulic and heating system. Limnol Oceanogr Methods 11:410–417CrossRefGoogle Scholar
  36. 36.
    Ferreira V, Canhoto C (2014) Effect of experimental and seasonal warming on litter decomposition in a temperate stream. Aquat Sci 76:155–163CrossRefGoogle Scholar
  37. 37.
    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 60:881–892CrossRefGoogle Scholar
  38. 38.
    Ylla I, Canhoto C, Romaní AM (2014) Effects of warming on stream biofilm organic matter use capabilities. Microbiol Ecol 68:132–145CrossRefGoogle Scholar
  39. 39.
    Miranda P, Coelho FES, Tomé AR, Valente MA (2002) 20th century Portuguese climate and climate scenarios. In: Santos FD, Forbes K, Moita R (eds) Climate change in Portugal. Scenarios, impacts and adaptation measures. SIAM project, Gradiva Publications, Lda, Lisbon, pp 23–83Google Scholar
  40. 40.
    Ferreira V, Encalada AC, Graça MAS (2012) Effects of litter diversity on decomposition and biological colonization of submerged litter in temperate and tropical streams. Freshw Sci 31:945–962CrossRefGoogle Scholar
  41. 41.
    Pozo J, González E, Díez JR, Molinero J, Elósegui A (1997) Inputs of particulate organic matter to streams with different riparian vegetation. J North Am Benthol Soc 16:602–611CrossRefGoogle Scholar
  42. 42.
    González E, Pozo J (1996) Longitudinal and temporal patterns of benthic coarse particulate organic matter in the Agüera stream (northern Spain). Aquat Sci 58:355–366CrossRefGoogle Scholar
  43. 43.
    Morrill JC, Bales RC, Conklin MH (2005) Estimating stream temperature from air temperature: implications for future water quality. J Environ Eng 131:131–139CrossRefGoogle Scholar
  44. 44.
    Gore JA (1996) Discharge measurements and stream flow analysis. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology. Academic press, New York, pp 53–74Google Scholar
  45. 45.
    APHA (1995) Standard methods for the examination of water and watershed. American Public Health Association, Washington DCGoogle Scholar
  46. 46.
    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 Press Inc, New York, pp 315–322Google Scholar
  47. 47.
    Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedPubMedCentralGoogle Scholar
  48. 48.
    Bärlocher F (2005) Sporulation by aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, pp 185–188CrossRefGoogle Scholar
  49. 49.
    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 153–168CrossRefGoogle Scholar
  50. 50.
    Suberkropp K, Weyers H (1996) Application of fungal and bacterial production methodologies to decomposing leaves in streams. Appl Environ Microbiol 62:1610–1615PubMedPubMedCentralGoogle Scholar
  51. 51.
    Gessner MO, Newell SY (2002) Biomass, growth rate, and production of filamentous fungi in plant litter. In: Hurst CJ, Crawford RL, Knudsen C, McIerney M, Stetzenbach LD (eds) Manual of environmental microbiology, 2nd edn. ASM Press, Washington DC, pp 390–408Google Scholar
  52. 52.
    Kirchman DL (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 509–512Google Scholar
  53. 53.
    Zar JH (2010) Biostatistical analysis. Pearson Prentice-Hall, Upper Saddle RiverGoogle Scholar
  54. 54.
    Kruskal JB, Wish M (1978) Multidimensional scaling. Sage Publications, Beverley HillsCrossRefGoogle Scholar
  55. 55.
    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46Google Scholar
  56. 56.
    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 59:2390–2399CrossRefGoogle Scholar
  57. 57.
    Nikolcheva LG, Bärlocher F (2005) Seasonal and substrate preferences of fungi colonizing leaves in streams: traditional versus molecular evidence. Environ Microbiol 7:270–280CrossRefPubMedGoogle Scholar
  58. 58.
    Duarte S, Pascoal C, Alves A, Correia A, Cássio F (2010) Assessing the dynamic of microbial communities during leaf decomposition in a low-order stream by microscopic and molecular techniques. Microbiol Res 165:351–362CrossRefPubMedGoogle Scholar
  59. 59.
    Das M, Royer TV, Leff LG (2007) Diversity of fungi, bacteria, and actinomycetes on leaves decomposing in a stream. Appl Environ Microbiol 73:756–767CrossRefPubMedGoogle Scholar
  60. 60.
    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 75:6211–6221CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Muyzer G, Brinkoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (2004) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, The Netherlands, pp 743–770Google Scholar
  62. 62.
    Suberkropp K (1984) The effect of temperature on the seasonal occurrence of aquatic hyphomycetes. Trans Br Mycol Soc 82:53–62CrossRefGoogle Scholar
  63. 63.
    Bärlocher F (2000) Water-borne conidia of aquatic hyphomycetes: seasonal and yearly patterns in Catamaran Brook, New Brunswick, Canada. Can J Bot 78:157–167Google Scholar
  64. 64.
    Ferreira V, Chauvet E, Canhoto C (2015) Effects of experimental warming, litter species, and presence of macroinvertebrates on litter decomposition and associated decomposers in a temperate mountain stream. Can J Fish Aquat Sci 72:206–216CrossRefGoogle Scholar
  65. 65.
    Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Towards a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  66. 66.
    Mas-Martí E, Muñoz I, Oliva F, Canhoto C (2015) Effects of increased water temperature on leaf litter quality and detritivore performance: a whole-reach manipulative experiment. Freshw Biol 60:184–197CrossRefGoogle Scholar
  67. 67.
    Lecerf A, Dobson M, Dang CK, Chauvet E (2005) Riparian plant species loss alters trophic dynamics in detritus-based stream ecosystems. Oecologia 146:432–442CrossRefPubMedGoogle Scholar
  68. 68.
    Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12:1319–1333CrossRefPubMedGoogle Scholar
  69. 69.
    Flury S, Gessner MO (2011) Experimentally simulated global warming and nitrogen enrichment effects on microbial litter decomposers in a marsh. Appl Environ Microbiol 77:803–809CrossRefPubMedGoogle Scholar
  70. 70.
    Finlay BJ, Maberly SC, Cooper JI (1997) Microbial diversity and ecosystem function. Oikos 80:209–213CrossRefGoogle Scholar
  71. 71.
    Verma B, Robarts RD, Headley JV (2003) Seasonal changes in fungal production and biomass on standing dead Scirpus lacustris litter in a Northern prairie wetland. Appl Environ Microbiol 69:1043–1050CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Buesing N, Gessner MO (2006) Benthic bacterial and fungal productivity and carbon turnover in a freshwater marsh. Appl Environ Microbiol 72:596–605CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Acuña V, Wolf A, Uehlinger U, Tockner K (2008) Temperature dependence of stream benthic respiration in an Alpine river network under global warming. Freshw Biol 53:2076–2088CrossRefGoogle Scholar
  74. 74.
    Young RG, Matthaei CD, Townsend CR (2008) Organic matter breakdown and ecosystem metabolism: functional indicators for assessing river ecosystem health. J N Am Benthol Soc 27:605–625CrossRefGoogle Scholar
  75. 75.
    Gulis V, Ferreira V, Graça MAS (2006) Stimulation of leaf litter decomposition and associated fungi and invertebrates by moderate eutrophication: implications for stream assessment. Freshw Biol 51:1655–1669CrossRefGoogle Scholar
  76. 76.
    Woodward G, Gessner MO, Giller PS, Gulis V, Hladyz S, Lecerf A et al (2012) Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336:1438–1440CrossRefPubMedGoogle Scholar
  77. 77.
    Park S, Cho KH (2003) Nutrient leaching from leaf litter of emergent macrophyte (Zizania latifolia) and the effects of water temperature on the leaching process. Korean J Biol Sci 7:289–294CrossRefGoogle Scholar
  78. 78.
    Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V (2012) Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem 56:60–68CrossRefGoogle Scholar
  79. 79.
    Murdoch PS, Baron JS, Miller TL (2000) Potential effects of climate change on surface-water quality in North America. J Am Water Res Assoc 36:347–366CrossRefGoogle Scholar
  80. 80.
    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 87:257–267CrossRefPubMedGoogle Scholar
  81. 81.
    Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283CrossRefGoogle Scholar
  82. 82.
    Lecerf A, Richardson J (2010) Litter decomposition can detect effects of high and moderate levels of forest disturbance on stream condition. Forest Ecol Manag 259:2433–2443CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Sofia Duarte
    • 1
  • Fernanda Cássio
    • 1
    • 2
  • Verónica Ferreira
    • 3
  • Cristina Canhoto
    • 4
  • Cláudia Pascoal
    • 1
    • 2
  1. 1.Centre of Molecular and Environmental Biology (CBMA), Department of BiologyUniversity of MinhoBragaPortugal
  2. 2.Institute of Science and Innovation for Bio-Sustainability (IB-S)University of MinhoBragaPortugal
  3. 3.Marine and Environmental Sciences Centre (MARE), Department of Life SciencesUniversity of CoimbraCoimbraPortugal
  4. 4.Centre for Functional Ecology (CFE), Department of Life SciencesUniversity of CoimbraCoimbraPortugal

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