Drying responses of microbial litter decomposition and associated fungal and bacterial communities are not affected by emersion frequency

Freshwater Science

Volumn 34, Issue 4, 2015, Pages 1233-1244

  Foulquier, A ^a,b,c   Artigas, J ^a,d,e   Pesce, S ^a   Datry, T ^a  

^a UR MALY   (France)

^b UMR CARRTEL   (France)

^c UNIV GRENOBLE ALPES   (France)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

^e UNIVERSITÉ BLAISE PASCAL   (France)

Author keywords

Bacteria; Drying events; Environmental stress; Enzymatic activity; Hyphomycetes; Microbial biofilm; Structure function relationship; Temporary rivers

Indexed keywords

BACTERIUM; BIOFILM; COMMUNITY COMPOSITION; DECOMPOSITION; EMERSION; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FUNGUS; LEAF LITTER; MICROBIAL COMMUNITY;

AIN; ALBARINE RIVER; FRANCE; RHONE-ALPES;

ALNUS GLUTINOSA; BACTERIA (MICROORGANISMS); FUNGI; HYPHOMYCETES; INVERTEBRATA;

EID: 84953721943     PISSN: 21619549     EISSN: 21619565     Source Type: Journal    
DOI: 10.1086/682060     Document Type: Article

References (85)

1. Acuña, V. 2010. Flow regime alteration effects on the organic C dynamics in semiarid stream ecosystems. Hydrobiologia 657: 233-242.
2. Agilent Technologies. 2013. Agilent DNA 1000 Kit Guide, G2938-90014 Rev. B. Agilent Technologies, Massey, France.
3. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32-46.
4. Anderson, M. J. 2005. PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand. (Available from: http://img2.timg.co.il/forums/1-124959686 .pdf)
5. Arnell, N. W. 1999. The effect of climate change on hydrological regimes in Europe: a continental perspective. Global Environmental Change 9:5-23.
6. Artigas, J., J. Majerholc, A. Foulquier, C. Margoum, B. Volat, M. Neyra, and S. Pesce. 2012. Effects of the fungicide tebuconazole on microbial capacities for litter breakdown in streams. Aquatic Toxicology 122/123:197-205.
7. Artigas, J., A. M. Romaní, and S. Sabater. 2008. Relating nutrient molar ratios of microbial attached communities to organic matter utilization in a forested stream. Fundamental and Applied Limnology/Archiv für Hydrobiologie 173:255-264.
8. Austin, A. T., and L. Vivanco. 2006. Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature 442:555-558.
9. Baldy, V., and M. O. Gessner. 1997. Towards a budget of leaf litter decomposition in a first-order woodland stream. Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie 320:747-758.
10. Baldy, V., M. O. Gessner, and E. Chauvet. 1995. Bacteria, fungi and the breakdown of leaf litter in a large river. Oikos 74:93-102.
11. Bapiri, A., E. Baath, and J. Rousk. 2010. Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microbial Ecology 60:419-428.
12. Bärlocher, F. 1992. Effects of drying and freezing autumn leaves on leaching and colonization by aquatic hyphomycetes. Freshwater Biology 28:1-7.
13. Battin, T. J., S. Luyssaert, L. A. Kaplan, A. K. Aufdenkampe, A. Richter, and L. J. Tranvik. 2009. The boundless carbon cycle. Nature Geoscience 2:598-600.
14. Battle, J., and S. Golladay. 2001. Hydroperiod influence on breakdown of leaf litter in cypress-gum wetlands. American Midland Naturalist 146:128-145.
15. Bratbak, G., and I. Dundas. 1984. Bacterial dry matter content and biomass estimations. Applied and Environmental Microbiology 48:755-757.
16. Bruder, A., E. Chauvet, and M. O. Gessner. 2011. Litter diversity, fungal decomposers and litter decomposition under simulated stream intermittency. Functional Ecology 25:1269-1277.
17. Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L. J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J. A. Downing, J. J. Middelburg, and J. Melack. 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10:172-185.
18. Conner, W. H., and J. W. Day. 1991. Leaf litter decomposition in three Louisiana freshwater forested wetland areas with different flooding regimes. Wetlands 11:303-312.
19. Corti, R., T. Datry, L. Drummond, and S. T. Larned. 2011. Natural variation in immersion and emersion affects breakdown and invertebrate colonization of leaf litter in a temporary river. Aquatic Sciences 73:537-550.
20. Dang, C. K., E. Chauvet, and M. O. Gessner. 2005. Magnitude and variability of process rates in fungal diversity-litter decomposition relationships. Ecology Letters 8:1129-1137.
21. Dang, C. K., M. O. Gessner, and E. Chauvet. 2007. Influence of conidial traits and leaf structure on attachment success of aquatic hyphomycetes on leaf litter. Mycologia 99:24-32.
22. Das, M., T. V. Royer, and L. G. Leff. 2007. Diversity of fungi, bacteria, and actinomycetes on leaves decomposing in a stream. Applied and Environmental Microbiology 73:756-767.
23. Datry, T. 2012. Benthic and hyporheic invertebrate assemblages along a flow intermittence gradient: effects of duration of dry events. Freshwater Biology 57:563-574.
24. Datry, T., R. Corti, C. Claret, and M. Philippe. 2011. Flow intermittence controls leaf litter breakdown in a French temporary alluvial river: the "drying memory." Aquatic Sciences 73:471-483.
25. Datry, T., S. T. Larned, K. M. Fritz, M. T. Bogan, P. J. Wood, E. I. Meyer, and A. N. Santos. 2014a. Broad-scale patterns of invertebrate richness and community composition in temporary rivers: effects of flow intermittence. Ecography 37:94-104.
26. Datry, T., S. T. Larned, and K. Tockner. 2014b. Intermittent rivers: a challenge for freshwater ecology. BioScience 64:229-235.
27. Döll, P., and H. Schmied 2012 How is the impact of climate change on river flow regimes related to the impact on mean annual runoff? A global-scale analysis. Environmental Research Letters 7 014037.
28. Duarte, S., C. Pascoal, A. Alves, A. Correia, and F. Cássio. 2010. Assessing the dynamic of microbial communities during leaf decomposition in a low-order stream by microscopic and molecular techniques. Microbiological Research 165:351-362.
29. Duarte, S., C. Pascoal, F. Cássio, and F. Bärlocher. 2006. Aquatic hyphomycete diversity and identity affect leaf litter decomposition in microcosms. Oecologia (Berlin) 147:658-666.
30. Dudgeon, D., A. H. Arthington, M. O. Gessner, Z.-I. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A.-H. Prieur-Richard, D. Soto, M. L. J. Stiassny, and C. A. Sullivan. 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81:163-182.
31. Febria, C. M., P. Beddoes, R. R. Fulthorpe, and D. D. Williams. 2012. Bacterial community dynamics in the hyporheic zone of an intermittent stream. ISME Journal 6:1078-1088.
32. Ferreira, V., and E. Chauvet. 2012. Changes in dominance among species in aquatic hyphomycete assemblages do not affect litter decomposition rates. Aquatic Microbial Ecology 66:1-11.
33. Findlay, S., J. Tank, S. Dye, H. M. Valett, P. J. Mulholland, W. H. McDowell, S. L. Johnson, S. K. Hamilton, J. Edmonds, W. K. Dodds, and W. B. Bowden. 2002. A cross-system comparison of bacterial and fungal biomass in detritus pools of headwater streams. Microbial Ecology 43:55-66.
34. Fischer, H., J. Bergfur, W. Goedkoop, and L. Tranvik. 2009. Microbial leaf degraders in boreal streams: bringing together stochastic and deterministic regulators of community composition. Freshwater Biology 54:2276-2289.
35. Foulquier, A., B. Volat, M. Neyra, G. Bornette, and B. Montuelle. 2013. Long-term impact of hydrological regime on structure and functions of microbial communities in riverine wetland sediments. FEMS Microbiology Ecology 85:211-226.
36. Gessner, M. O., and E. Chauvet. 1993. Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Applied and Environmental Microbiology 59:502-507.
37. Gessner, M. O., and E. Chauvet. 1994. Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75:1807-1817.
38. Gessner, M. O., and E. Chauvet. 2002. A case for using litter breakdown to assess functional stream integrity. Ecological Applications 12:498-510.
39. Gessner, M. O., V. Gulis, K. Kuehn, E. Chauvet, and K. Suberkropp. 2007. Fungal decomposers of plant litter in aquatic ecosystems. Pages 301-324 in C. P. Kubicek and I. S. Druzhinina (editors). Environmental andMicrobial Relationships. Springer, Berlin, Germany.
40. Gessner, M. O., and A. L. Schmitt. 1996. Use of solid-phase extraction to determine ergosterol concentrations in plant tissue colonized by fungi. Applied and Environmental Microbiology 62:415-419.
41. Gessner, M. O., C. M. Swan, C. K. Dang, B. G. McKie, R. D. Bardgett, D. H. Wall, and S. Hättenschwiler. 2010. Diversity meets decomposition. Trends in Ecology and Evolution 25: 372-380.
42. Gleick, P. 2003. Global freshwater resources: soft-path solutions for the 21st century. Science 302:1524-1528.
43. Graça, M. A. S. 2001. The role of invertebrates on leaf litter decomposition in streams - A review. International Review of Hydrobiology 86:383-393.
44. Hieber, M., and M. O. Gessner. 2002. Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026-1038.
45. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6:65-70.
46. Kremen, C. 2005. Managing ecosystem services: what do we need to know about their ecology? Ecology Letters 8:468-479.
47. Lake, P. S. 2003. Ecological effects of perturbation by drought in flowing waters. Freshwater Biology 48:1161-1172.
48. Lake, P. S. 2011. Drought and aquatic ecosystems: effects and responses. John Wiley and Sons, New York.
49. Langhans, S. D., and K. Tockner. 2006. The role of timing, duration, and frequency of inundation in controlling leaf litter decomposition in a river-floodplain ecosystem (Tagliamento, northeastern Italy). Oecologia (Berlin) 147:501-509.
50. Larned, S. T., T. Datry, D. B. Arscott, and K. Tockner. 2010. Emerging concepts in temporary-river ecology. Freshwater Biology 55:717-738.
51. Larned, S. T., T. Datry, and C. T. Robinson. 2007. Invertebrate and microbial responses to inundation in an ephemeral river reach in New Zealand: effects of preceding dry periods. Aquatic Sciences 69:554-567.
52. Larned, S. T., J. Schmidt, T. Datry, C. P. Konrad, J. K. Dumas, and J. C. Diettrich. 2011. Longitudinal river ecohydrology: flow variation down the lengths of alluvial rivers. Ecohydrology 4:532-548.
53. Ledger, M. E., R. M. Harris, P. D. Armitage, and A. M. Milner. 2012. Climate change impacts on community resilience: evidence from a drought disturbance experiment. Advances in Ecological Research 46:211.
54. Lehner, B., P. Döll, J. Alcamo, T. Henrichs, and F. Kaspar. 2006. Estimating the impact of global change on flood and drought risks in Europe: a continental, integrated analysis. Climatic Change 75:273-299.
55. Maamri, A., H. Chergui, and E. Pattee. 1997. Leaf litter processing in a temporary northeastern Moroccan river. Archiv für Hydrobiologie 140:513-531.
56. Marks, J. C., G. A. Haden, B. L. Harrop, E. G. Reese, J. L. Keams, M. E. Watwood, and T. G. Whitham. 2009. Genetic and environmental controls of microbial communities on leaf litter in streams. Freshwater Biology 54:2616-2627.
57. Marxsen, J., A. Zoppini, and S. Wilczek. 2010. Microbial communities in streambed sediments recovering from desiccation. FEMS Microbiology Ecology 71:374-386.
58. Mille-Lindblom, C., H. Fischer, and L. J. Tranvik. 2006. Litterassociated bacteria and fungi-a comparison of biomass and communities across lakes and plant species. Freshwater Biology 51:730-741.
59. MP Biomedicals. 2007. FastDNA SPIN kit for soil, catalog number 6560-200, protocol revision 6560-200-07DEC. MP Biomedicals, Solon, Ohio.
60. Nikolcheva, L. G., T. Bourque, and F. Bärlocher. 2005. Fungal diversity during initial stages of leaf decomposition in a stream. Mycological Research 109:246-253.
61. Nikolcheva, L. G., A. M. Cockshutt, and F. Bärlocher. 2003. Determining diversity of freshwater fungi on decaying leaves: comparison of traditional and molecular approaches. Applied and Environmental Microbiology 69:2548-2554.
62. Oksanen, J., F. Blanchet, R. Kindt, P. Legendre, P. Minchin, R. O'Hara, G. Simpson, P. Solymos, M. Stevens, and H. Wagner. 2012. vegan: community ecology package. R package version 2.0-3. R Project for Statistical Computing, Vienna, Austria. (Available from: http://CRAN.R-project.org/package=vegan)
63. Pascoal, C., and F. Cássio. 2004. Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Applied and Environmental Microbiology 70:5266-5273.
64. Petersen, R. C., and K. W. Cummins. 1974. Leaf processing in a woodland stream. Freshwater Biology 4:343-368.
65. Poff, N. L., J. D. Allan, M. B. Bain, J. R. Karr, K. L. Prestegaard, B. D. Richter, R. E. Sparks, and J. C. Stromberg. 1997. The natural flow regime. BioScience 47:769-784.
66. Poff, N. L., and J. K. H. Zimmerman. 2010. Ecological responses to altered flow regimes: a literature review to inform the science and management of environmental flows. Freshwater Biology 55:194-205.
67. Porter, K. G., and Y. S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25:943-948.
68. Rees, G. N., G. O. Watson, D. S. Baldwin, and A. M. Mitchell. 2006. Variability in sediment microbial communities in a semipermanent stream: impact of drought. Journal of the North American Benthological Society 25:370-378.
69. Romaní, A. M., H. Fischer, C. Mille-Lindblom, and L. J. Tranvik. 2006. Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87: 2559-2569.
70. Ryder, D., and P. Horwitz. 1995. Seasonal water regimes and leaf litter processing in a wetland on the Swan Coastal Plain, Western Australia. Marine and Freshwater Research 46:1077-1084.
71. Schimel, J. P., T. C. Balser, and M. Wallenstein. 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386-1394.
72. Steward, A., D. von Schiller, K. Tockner, J. Marshall, and S. Bunn. 2012. When the river runs dry: human and ecological values of dry riverbeds. Frontiers in Ecology and the Environment 10:202-209.
73. Strickland, M. S., C. Lauber, N. Fierer, and M. A. Bradford. 2009. Testing the functional significance of microbial community composition. Ecology 90:441-451.
74. Suberkropp, K., T. L. Arsuffi, and J. P. Anderson. 1983. Comparison of degradative ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Applied and Environmental Microbiology 46:237-244.
75. Theil-Nielsen, J., and M. Søndergaard. 1998. Bacterial carbon biomass calculated from biovolumes. Archiv für Hydrobiologie 141:195-207.
76. Timoner, X., V. Acuña, D. von Schiller, and S. Sabater. 2012. Functional responses of stream biofilms to flow cessation, desiccation and rewetting. Freshwater Biology 57:1565-1578.
77. Treplin, M., and M. Zimmer. 2012. Drowned or dry: a crosshabitat comparison of detrital breakdown processes. Ecosystems 15:477-491.
78. Vinebrooke, R. D., K. L. Cottingham, J. Norberg, M. Scheffer, S. I. Dodson, S. C. Maberly, and U. Sommer. 2004. Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104:451-457.
79. von Schiller, D., R. Marcé, B. Obrador, L. Gómez, J. P. Casas, V. Acuña, and M. Koschorreck. 2014. Carbon dioxide emissions from dry watercourses. Inland Waters 4:377-382.
80. Vörösmarty, C. J., P. B. McIntyre, M. O. Gessner, D. Dudgeon, A. Prusevich, P. Green, S. Glidden, S. E. Bunn, C. A. Sullivan, C. R. Liermann, and P. M. Davies. 2010. Global threats to human water security and river biodiversity. Nature 467:555-561.
81. Webster, J. R., and J. L. Meyer. 1997. Organic matter budgets for streams: a synthesis. Journal of the North American Benthological Society 16:141-161.
82. Wilhelm, L., G. A. Singer, C. Fasching, T. J. Battin, and K. Besemer. 2013. Microbial biodiversity in glacier-fed streams. ISME Journal 7:1651-1660.
83. Wintzingerode, F., U. B. Göbel, and E. Stackebrandt. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiology Reviews 21:213-229.
84. Woodward, G., M. O. Gessner, P. S. Giller, V. Gulis, S. Hladyz, A. Lecerf, B. Malmqvist, B. G. McKie, S. D. Tiegs, H. Cariss, M. Dobson, A. Elosegi, V. Ferreira, M. A. S. Graça, T. Fleituch, J. O. Lacoursière, M. Nistorescu, J. Pozo, G. Risnoveanu, M. Schindler, A. Vadineanu, L. B.-M. Vought, and E. Chauvet. 2012. Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336:1438-1440.
85. Yannarell, A. C., R. R. Busby, M. L. Denight, D. L. Gebhart, and S. J. Taylor. 2011. Soil bacteria and fungi respond on different spatial scales to invasion by the legume Lespedeza cuneata. Frontiers in Microbiology 2:127.