Microbial Ecology

, Volume 61, Issue 4, pp 968–979 | Cite as

Water–Sediment Exchanges Control Microbial Processes Associated with Leaf Litter Degradation in the Hyporheic Zone: a Microcosm Study

  • Simon Navel
  • Florian Mermillod-Blondin
  • Bernard Montuelle
  • Eric Chauvet
  • Laurent Simon
  • Pierre Marmonier
Microbiology of Aquatic Systems

Abstract

The present study aimed to experimentally quantify the influence of a reduction of surface sediment permeability on microbial characteristics and ecological processes (respiration and leaf litter decomposition) occurring in the hyporheic zone (i.e. the sedimentary interface between surface water and groundwater). The physical structure of the water–sediment interface was manipulated by adding a 2-cm layer of coarse sand (unclogged systems) or fine sand (clogged systems) at the sediment surface of slow filtration columns filled with a heterogeneous gravel/sand sedimentary matrix. The influence of clogging was quantified through measurements of hydraulic conductivity, water chemistry, microbial abundances and activities and associated processes (decomposition of alder leaf litter inserted at a depth of 9 cm in sediments, oxygen and nitrate consumption by microorganisms). Fine sand deposits drastically reduced hydraulic conductivity (by around 8-fold in comparison with unclogged systems topped by coarse sand) and associated water flow, leading to a sharp decrease in oxygen (reaching less than 1 mg L−1 at 3 cm depth) and nitrate concentrations with depth in sediments. The shift from aerobic to anaerobic conditions in clogged systems favoured the establishment of denitrifying bacteria living on sediments. Analyses performed on buried leaf litter showed a reduction by 30% of organic matter decomposition in clogged systems in comparison with unclogged systems. This reduction was linked to a negative influence of clogging on the activities and abundances of leaf-associated microorganisms. Finally, our study clearly demonstrated that microbial processes involved in organic matter decomposition were dependent on hydraulic conductivity and oxygen availability in the hyporheic zone.

Keywords

Denitrification Hydraulic Conductivity Leaf Litter Fine Sand Coarse Sand 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Bernadette Volat (Cemagref, Lyon), Félix Vallier (LEHF, Villeurbanne) and Didier Lambrigot (EcoLab, Toulouse) for their helpful assistance. We also thank Dr. K. Nelson and three anonymous reviewers for advice and constructive comments of the manuscript. This study was funded by the ANR Biodiversity programme (ANR-06-BDIV-007) InBioProcess 2007-2010.

References

  1. 1.
    Abelho M (2001) From litterfall to breakdown in streams: a review. Sci World 1:656–680CrossRefGoogle Scholar
  2. 2.
    Battin TJ, Sengschmitt D (1999) Linking sediment biofilms, hydrodynamics, and river bed clogging: evidence from a large river. Microb Ecol 37:185–196PubMedCrossRefGoogle Scholar
  3. 3.
    Blaschke AP, Steiner K-H, Schmalfuss R, Gutknecht D, Sengschmitt D (2003) Clogging processes in hyporheic interstices of an impounded river, the Danube at Vienna, Austria. Int Rev Hydrobiol 88:397–413CrossRefGoogle Scholar
  4. 4.
    Boulton AJ, Foster JG (1998) Effects of buried leaf litter and vertical hydrologic exchange on hyporheic water chemistry and fauna in a gravel-bed river in northern New South Wales, Australia. Freshw Biol 40:229–243CrossRefGoogle Scholar
  5. 5.
    Castela J, Ferreira V, Graça MAS (2008) Evaluation of stream ecological integrity using litter decomposition and benthic invertebrates. Environ Pollut 153:440–449PubMedCrossRefGoogle Scholar
  6. 6.
    Chauvet E (1988) Influence of the environment on willow leaf litter decomposition in the alluvial corridor of the Garonne River. Arch Hydrobiol 112:371–386Google Scholar
  7. 7.
    Claret C, Boulton AJ (2009) Integrating hydraulic conductivity with biogeochemical gradients and microbial activity along river–groundwater exchange zones in a subtropical stream. Hydrogeol J 17:151–160CrossRefGoogle Scholar
  8. 8.
    Cornut J, Elger A, Lambrigot D, Marmonier P, Chauvet E (2010) Early leaf decomposition stages are mediated by aquatic hyphomycetes in the hyporheic zone of woodland streams. Freshw Biol 55:2541–2556.CrossRefGoogle Scholar
  9. 9.
    Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. Wiley, New YorkGoogle Scholar
  10. 10.
    Crenshaw CL, Valett HM (2002) The effect of coarse particulate organic matter on fungal biomass and invertebrate density in the subsurface of a headwater stream. J N Am Benthol Soc 21:28–42CrossRefGoogle Scholar
  11. 11.
    Dahm CN, Trotter EH, Sedell JR (1987) Role of anaerobic zones and processes in stream ecosystem productivity. In: Averett RC, McKnight DM (eds) Chemical quality of water and the hydrologic cycle. Lewis, Chelsea, pp 157–178Google Scholar
  12. 12.
    Dangles O, Gessner MO, Guerold F, Chauvet E (2004) Impacts of stream acidification on litter breakdown: implications for assessing ecosystem functioning. J Appl Ecol 41:365–378CrossRefGoogle Scholar
  13. 13.
    Fellows CS, Valett HM, Dahm CN (2001) Whole-stream metabolism in two montane streams: contribution of the hyporheic zone. Limnol Oceanogr 46:523–531CrossRefGoogle Scholar
  14. 14.
    Findlay S, Smith PJ, Meyer JL (1986) Effect of detritus addition on metabolism of river sediment. Hydrobiologia 137:257–263CrossRefGoogle Scholar
  15. 15.
    Fischer H, Wanner SC, Pusch M (2002) Bacterial abundance and production in river sediments as related to the biochemical composition of particulate organic matter (POM). Biogeochemistry 61:37–55CrossRefGoogle Scholar
  16. 16.
    Franken RJM, Storey RG, Williams DD (2001) Biological, chemical and physical characteristics of downwelling and upwelling zones in the hyporheic zone of a north-temperate stream. Hydrobiologia 444:183–195CrossRefGoogle Scholar
  17. 17.
    Furutani A, Rudd JW, Kelly CA (1984) A method for measuring the response of sediment microbial communities to environmental perturbations. Can J Microbiol 30:1408–1414CrossRefGoogle Scholar
  18. 18.
    Gayraud S, Philippe M (2003) Influence of bed-sediment features on the interstitial habitat available for macroinvertebrates in 15 French streams. Int Rev Hydrobiol 88:77–93CrossRefGoogle Scholar
  19. 19.
    Gessner MO, Bärlocher F, Chauvet E (2003) Qualitative and quantitative analyses of aquatic hyphomycetes in streams. In: Tsui CKM, Hyde KD (eds) Freshwater mycology, Fungal Diversity research series 10. Fungal Diversity, Hong Kong, pp 127–157Google Scholar
  20. 20.
    Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol 59:502–507PubMedGoogle Scholar
  21. 21.
    Gessner MO, Chauvet E (2002) A case for using leaf litter breakdown to assess functional stream integrity. Ecol Appl 12:498–510CrossRefGoogle Scholar
  22. 22.
    Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, BerlinGoogle Scholar
  23. 23.
    Grimm NB, Fisher SG (1984) Exchange between interstitial and surface water: implication for stream metabolism and nutrient cycling. Hydrobiologia 111:219–228CrossRefGoogle Scholar
  24. 24.
    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
  25. 25.
    Gulis V, Suberkropp K (2003) Effect of inorganic nutrients on relative contributions of fungi and bacteria to carbon flow from submerged decomposing leaf litter. Microb Ecol 45:11–19PubMedCrossRefGoogle Scholar
  26. 26.
    Hedin LO, von Fischer JC, Ostrom NE, Kennedy BP, Brown MG, Robertson GP (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil–stream interfaces. Ecology 79:684–703Google Scholar
  27. 27.
    Hendricks SP (1993) Microbial ecology of the hyporheic zone: a perspective integrating hydrology and biology. J N Am Benthol Soc 12:70–78CrossRefGoogle Scholar
  28. 28.
    Hulthe G, Hulth S, Hall POJ (1998) Effect of oxygen on degradation rate of refractory and labile organic matter in continental margin sediments. Geochim Cosmochim Ac 62:1319–1328CrossRefGoogle Scholar
  29. 29.
    Hvitved-Jacobsen T, Raunkjaer K, Nielsen PH (1995) Volatile fatty acids and sulfide in pressure mains. Water Sci Technol 31:169–179Google Scholar
  30. 30.
    Karner M, Fuhrman JA (1997) Determination of active marine bacterioplankton: a comparison of universal 16S rRNA probes, autoradiography, and nucleoid staining. Appl Environ Microbiol 63:1208–1213PubMedGoogle Scholar
  31. 31.
    Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426:1–24CrossRefGoogle Scholar
  32. 32.
    Lefebvre S, Marmonier P, Pinay G (2004) Stream regulation and nitrogen dynamics in sediment interstices: comparison of natural and straightened sectors of a third-order stream. River Res Appl 20:499–512CrossRefGoogle Scholar
  33. 33.
    Lefebvre S, Marmonier P, Pinay G, Bour O, Aquilina L, Baudry J (2005) Nutrient dynamics in interstitial habitats of low-order rural streams with different bedrock geology. Arch Hydrobiol 164:169–191CrossRefGoogle Scholar
  34. 34.
    Leichtfried M (2007) The energy basis of the consumer community in streams yesterday, today and tomorrow…. Int Rev Hydrobiol 92:363–377CrossRefGoogle Scholar
  35. 35.
    Lowell JL, Gordon N, Engstrom D, Stanford JA, Holbe WE, Gannon JE (2009) Habitat heterogeneity and associated microbial community structure in a small-scale floodplain hyporheic flow path. Microb Ecol 58:611–620PubMedCrossRefGoogle Scholar
  36. 36.
    Marmonier P, Piscart C, Sarriquet P-E, Azam D, Chauvet E (2010) Relevance of large litter bag burial for the study of leaf breakdown in the hyporheic zone. Hydrobiologia 641:203–214CrossRefGoogle Scholar
  37. 37.
    Marxsen J (2006) Bacterial production in the carbon flow of a central European stream, the Breitenbach. Freshw Biol 51:1838–1861CrossRefGoogle Scholar
  38. 38.
    Maurice L (1993) Modelling of degradation of organic matter by bacterial populations. Applications to the zone of maximum turbidity of the Loire estuary. Hydroécol Appl 5:71–96CrossRefGoogle Scholar
  39. 39.
    McNamara CJ, Leff LG (2004) Response of biofilm to dissolved organic matter from decomposing maple leaves. Microb Ecol 48:324–330PubMedCrossRefGoogle Scholar
  40. 40.
    Medeiros AO, Pascoal C, Graca MAS (2009) Diversity and activity of aquatic fungi under low oxygen conditions. Freshw Biol 54:142–149CrossRefGoogle Scholar
  41. 41.
    Mermillod-Blondin F, des Chatellier MC, Gerino M, Gaudet JP (2000) Testing the effect of Limnodrilus sp. (Oligochaeta, Tubificidae) on organic matter and nutrient processing in the hyporheic zone: a microcosm method. Arch Hydrobiol 149:467–487Google Scholar
  42. 42.
    Mermillod-Blondin F, Mauclaire L, Montuelle B (2005) Use of slow filtration columns to assess oxygen respiration, consumption of dissolved organic carbon, nitrogen transformations, and microbial parameters in hyporheic sediments. Water Res 39:1687–1698PubMedCrossRefGoogle Scholar
  43. 43.
    Mermillod-Blondin F, Nogaro G, Vallier F, Gibert J (2008) Laboratory study highlights the key influences of stormwater sediment thickness and bioturbation by tubificid worms on dynamics of nutrients and pollutants in stormwater retention systems. Chemosphere 72:213–223PubMedCrossRefGoogle Scholar
  44. 44.
    Montuelle B, Volat B (1997) Influence of oxygen and temperature on exoenzyme activities in freshwater sediments. Verh Int Ver Limnol 26:373–376Google Scholar
  45. 45.
    Naegeli MW, Uehlinger U (1997) Contribution of the hyporheic zone to ecosystem metabolism in a prealpine gravel-bed river. J N Am Benthol Soc 16:794–804CrossRefGoogle Scholar
  46. 46.
    Navel S, Mermillod-Blondin F, Montuelle B, Chauvet E, Simon L, Piscart C, Marmonier P (2010) Interactions between fauna and sediment control the breakdown of plant matter in river sediments. Freshw Biol 55:753–766CrossRefGoogle Scholar
  47. 47.
    Nogaro G, Datry T, Mermillod-Blondin F, Descloux S, Montuelle B (2010) Influence of streambed sediment clogging on microbial processes in the hyporheic zone. Freshw Biol 55:1288–1302CrossRefGoogle Scholar
  48. 48.
    Nogaro G, Mermillod-Blondin F, Montuelle B, Boisson JC, Bedell JP, Ohannessian A, Volat B, Gibert J (2007) Influence of a stormwater sediment deposit on microbial and biogeochemical processes in infiltration porous media. Sci Total Environ 377:334–348PubMedCrossRefGoogle Scholar
  49. 49.
    Nogaro G, Mermillod-Blondin F, Montuelle B, Boisson JC, Gibert J (2008) Chironomid larvae stimulate biogeochemical and microbial processes in a riverbed covered with fine sediment. Aquat Sci 70:156–168CrossRefGoogle Scholar
  50. 50.
    Orghidan T (1959) Ein neuer Lebensraum des unterirdischen Wassers: Der hyporheische Biotop. Arch Hydrobiol 55:392–414Google Scholar
  51. 51.
    Petersen RC, Cummins KW (1974) Leaf processing in woodland stream. Freshw Biol 4:343–368CrossRefGoogle Scholar
  52. 52.
    Pusch M (1996) The metabolism of organic matter in the hyporheic zone of a mountain stream, and its spatial distribution. Hydrobiologia 323:107–118CrossRefGoogle Scholar
  53. 53.
    Rehg KJ, Packman AI, Ren JH (2005) Effects of suspended sediment characteristics and bed sediment transport on streambed clogging. Hydrol Proc 19:413–427CrossRefGoogle Scholar
  54. 54.
    Robinson CT, Gessner MO (2000) Nutrient addition accelerates leaf breakdown in an alpine springbrook. Oecologia 122:258–263CrossRefGoogle Scholar
  55. 55.
    Santmire JA, Leff LG (2007) The effect of sediment grain size on bacterial communities in streams. J N Am Benthol Soc 26:601–610CrossRefGoogle Scholar
  56. 56.
    Santmire JA, Leff LG (2007) The influence of stream sediment particle size on bacterial abundance and community composition. Aquat Ecol 41:153–160CrossRefGoogle Scholar
  57. 57.
    Schälchli U (1992) The clogging of coarse gravel river beds by fine sediment. Hydrobiologia 235(236):189–197CrossRefGoogle Scholar
  58. 58.
    Sinsabaugh RL, Carreiro MM, Alvarez S (2002) Enzyme and microbial dynamics during litter decomposition. In: Burns R, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 249–266Google Scholar
  59. 59.
    Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215CrossRefGoogle Scholar
  60. 60.
    Suberkropp K, Chauvet E (1995) Regulation of leaf breakdown by fungi in streams: influences of water chemistry. Ecology 76:1433–1445CrossRefGoogle Scholar
  61. 61.
    Tillman DC, Moerke AH, Ziehl CL, Lamberti GA (2003) Subsurface hydrology and degree of burial affect mass loss and invertebrate colonisation of leaves in a woodland stream. Freshw Biol 48:98–107CrossRefGoogle Scholar
  62. 62.
    EPA US (1991) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. EPA/600/4-90/027, 4th edn. US Environmental Protection Agency, Washington, DC, pp 34–35Google Scholar
  63. 63.
    Wood PJ, Armitage PD (1997) Biological effects of fine sediment in the lotic environment. Environ Manage 21:203–217PubMedCrossRefGoogle Scholar
  64. 64.
    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
  65. 65.
    Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Simon Navel
    • 1
    • 2
    • 3
  • Florian Mermillod-Blondin
    • 1
    • 2
    • 3
  • Bernard Montuelle
    • 4
    • 7
  • Eric Chauvet
    • 5
    • 6
  • Laurent Simon
    • 1
    • 2
    • 3
  • Pierre Marmonier
    • 1
    • 2
    • 3
  1. 1.Université de LyonLyonFrance
  2. 2.Université Lyon 1VilleurbanneFrance
  3. 3.CNRS, UMR 5023, Laboratoire d’Ecologie des Hydrosystèmes FluviauxVilleurbanneFrance
  4. 4.CEMAGREFCemagref LyonLyon Cedex 09France
  5. 5.Université de Toulouse; UPS, INPEcoLab (Laboratoire d’écologie fonctionnelle)ToulouseFrance
  6. 6.CNRSEcoLabToulouseFrance
  7. 7.INRA—UMR CARRTELThonon-les-bains CedexFrance

Personalised recommendations