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Surface Water Linkages Regulate Trophic Interactions in a Groundwater Food Web

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Abstract

Groundwaters are increasingly viewed as resource-limited ecosystems in which fluxes of dissolved organic carbon (DOC) from surface water are efficiently mineralized by a consortium of microorganisms which are grazed by invertebrates. We tested for the effect of groundwater recharge on resource supply and trophic interactions by measuring physico-chemistry, microbial activity and biomass, structure of bacterial communities and invertebrate density at three sites intensively recharged with surface water. Comparison of measurements made in recharge and control well clusters at each site showed that groundwater recharge significantly increased fluxes of DOC and phosphate, elevated groundwater temperature, and diminished dissolved oxygen (DO). Microbial biomass and activity were significantly higher in recharge well clusters but stimulation of autochthonous microorganisms was not associated with a major shift in bacterial community structure. Invertebrate assemblages were not significantly more abundant in recharge well clusters and did not show any relationship with microbial biomass and activity. Microbial communities were bottom-up regulated by DOC and nutrient fluxes but trophic interactions between microorganisms and invertebrates were apparently limited by environmental stresses, particularly DO depletion and groundwater warming. Hydrological connectivity is a key factor regulating the function of DOC-based groundwater food webs as it influences both resource availability for microorganisms and environmental stresses which affect energy transfer to invertebrates and top-down control on microorganisms.

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References

  • Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46.

    Google Scholar 

  • Bady P, Dolédec S, Dumont B, Fruget JF. 2004. Multiple co-inertia analysis: a tool for assessing synchrony in the temporal variability of aquatic communities. Acad Sci C R Biol 327:29–36.

    Google Scholar 

  • Baker MA, Valett HM, Dahm CN. 2000. Organic carbon supply and metabolism in a shallow groundwater ecosystem. Ecology 81:3133–48.

    Article  Google Scholar 

  • Bengtsson G. 1989. Growth and metabolic flexibility in groundwater bacteria. Microb Ecol 18(3):235–48.

    Article  CAS  Google Scholar 

  • Blanc L, Chessel D, Dolédec S. 1998. Etude de la stabilité temporelle des structures spatiales par analyses d’une série de tableaux de relevés faunistiques totalement appariés. Bull Fr Pêche Piscic 348:1–21.

    Article  Google Scholar 

  • Boulton AJ, Fenwick GD, Hancock PJ, Harvey MS. 2008. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebr Syst 22:103–16.

    Article  Google Scholar 

  • Brunke M, Gonser T. 1997. The ecological significance of exchange process between rivers and groundwater. Freshw Biol 37:1–33.

    Article  Google Scholar 

  • Brunke M, Gonser T. 1999. Hyporheic invertebrates—the clinical nature of interstitial communities structured by hydrological exchange and environmental gradients. J N Am Benthol Soc 18:344–62.

    Article  Google Scholar 

  • Brunke M, Fischer H. 1999. Hyporheic bacteria—relationships to environmental gradients and invertebrates in a prealpine stream. Arch Hydrobiol 146:189–217.

    Google Scholar 

  • Chessel D, Hanafi M. 1996. Analyse de la co-inertie de K nuages de points. Rev Stat Appl 44:35–60.

    Google Scholar 

  • Chessel D, Dufour AB, Thioulouse J. 2004. The ade4 package-I—one-table methods. R News 4:5–10.

    Google Scholar 

  • Craft J, Stanford J, Pusch M. 2002. Microbial respiration within a floodplain aquifer of a large gravel-bed river. Freshw Biol 47:251–61.

    Article  Google Scholar 

  • Danielopol DL. 1989. Groundwater fauna associated with riverine aquifers. J N Am Benthol Soc 8:18–35.

    Article  Google Scholar 

  • Datry T. 2003. Urbanisation et qualité des nappes phréatiques: réponse des écosystèmes aquatiques souterrains aux pratiques d’infiltration d’eau pluviale. PhD thesis. Université Lyon 1, Lyon.

  • Datry T, Malard F, Vitry L, Hervant F, Gibert J. 2003. Solute dynamics in the bed of a stormwater infiltration basin. J Hydrol 273:217–33.

    Article  CAS  Google Scholar 

  • Datry T, Malard F, Gibert J. 2005. Response of invertebrate assemblages to increased groundwater recharge rates in a phreatic aquifer. J N Am Benthol Soc 24:461–77.

    Google Scholar 

  • Daufresne M, Bady P, Fruget JF. 2007. Impacts of global changes and extreme hydro-climatic events on macroinvertebrate community structures in the French Rhône River. Oecologia 151:544–59.

    Article  PubMed  Google Scholar 

  • Dice LR. 1945. Measures of the amount of ecologic association between species. Ecology 26:297–302.

    Article  Google Scholar 

  • Dolédec S, Chessel D. 1994. Co-inertia analysis: an alternative method for studying species-environment relationships. Freshw Biol 31:277–93.

    Article  Google Scholar 

  • Dorigo U, Fontvieille D, Humbert JF. 2006. Spatial variability in the dynamic and the composition of the bacterioplankton community of the Lac du Bourget (France). FEMS Microbiol Ecol 58:109–19.

    Article  PubMed  CAS  Google Scholar 

  • Dray S, Chessel D, Thioulouse J. 2003. Co-inertia analysis and the linking of ecological data tables. Ecology 84:3078–89.

    Article  Google Scholar 

  • Dray S, Dufour AB, Chessel D. 2007. The ade4 package-II: two-table and K-table methods. R News 7:47–52.

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–6.

    Article  CAS  Google Scholar 

  • Edler CC, Dodds WK. 1996. The ecology of a subterranean isopod, Caecidotea tridentata. Freshw Biol 35:249–59.

    Article  Google Scholar 

  • Eiler A, Langenheder S, Bertilsson S, Tranvik LJ. 2003. Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69:3701–9.

    Article  PubMed  CAS  Google Scholar 

  • Foulquier A, Malard F, Barraud S, Gibert J. 2009. Thermal influence of urban groundwater recharge from stormwater infiltration basins. Hydrol Process 23:1701–13.

    Article  Google Scholar 

  • Foulquier A, Malard F, Mermillod-Blondin F, Datry T, Simon L, Montuelle B, Gibert J. 2010a. Change in dissolved organic carbon and oxygen at the water table region of an aquifer recharged with stormwater: biological uptake or mixing? Biogeochemistry 99:31–47.

    Article  CAS  Google Scholar 

  • Foulquier A, Simon L, Gilbert F, Fourel F, Malard F, Mermillod-Blondin F. 2010b. Relative influences of DOC flux and subterranean fauna on microbial abundance and activity in aquifer sediments: new insights from 13C-tracer experiments. Freshw Biol 55:1560–76.

    Article  CAS  Google Scholar 

  • Foulquier A, Mermillod-Blondin F, Malard F, Gibert J. 2011. Response of sediment biofilm to increased DOC supply in groundwater artificially recharged with stormwater. J Soils Sediments 11:382–93.

    Article  CAS  Google Scholar 

  • Franken R, Storey R, Williams D. 2001. Biological, chemical and physical characteristics of downwelling and upwelling zones in the hyporheic zone of a north-temperate stream. Hydrobiologia 444:183–95.

    Article  CAS  Google Scholar 

  • Franklin RB, Taylor DR, Mills AL. 2000. The distribution of microbial communities in anaerobic and aerobic zones of a shallow coastal plain aquifer. Microb Ecol 38:377–86.

    Article  Google Scholar 

  • Gao XQ, Olapade OA, Leff LG. 2005. Comparison of benthic bacterial community composition in nine streams. Aquat Microb Ecol 40:51–60.

    Article  Google Scholar 

  • Gasol JM, Pedros-Alio C, Vaque D. 2002. Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek 81:435–52.

    Article  PubMed  CAS  Google Scholar 

  • Gibert J, Deharveng L. 2002. Subterranean ecosystems: a truncated functional biodiversity. Bioscience 52:473–81.

    Article  Google Scholar 

  • Goldscheider N, Hunkeler D, Rossi P. 2006. Review: microbial biocenosis in pristine aquifers and an assessment of investigation methods. Hydrogeol J 14:926–41.

    Article  CAS  Google Scholar 

  • Groffman PM, Bohlen PJ, Fisk MC, Fahey TJ. 2004. Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54.

    Article  CAS  Google Scholar 

  • Haack SK, Bekins BB. 2000. Microbial populations in contaminant plumes. Hydrogeol J 8:63–76.

    Article  Google Scholar 

  • Hahn MW, Höfle MG. 2001. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35:113–21.

    Article  PubMed  CAS  Google Scholar 

  • Hedde M, Lavelle P, Joffre R, Jiménez JJ, Decaëns T. 2005. Specific functional signature in soil macro-invertebrate biostructures. Funct Ecol 19:785–93.

    Article  Google Scholar 

  • Houri-Davignon C, Relexans JC, Etcheher H. 1989. Measurements of actual electron transport system (ETS) activity in marine sediments by incubation with INT. Environ Technol 10:91–100.

    Article  CAS  Google Scholar 

  • Hunter MD, Price PW. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–32.

    Google Scholar 

  • Huxel GR, McCann K. 1998. Food web stability: the influence of trophic flows across habitats. Am Nat 152:460–9.

    Article  PubMed  CAS  Google Scholar 

  • Issartel J, Hervant F, Voituron Y, Renault D, Vernon P. 2005. Behavioural, ventilatory and respiratory responses of epigean and hypogean crustaceans to different temperatures. Comp Biochem Physiol A 141:1–7.

    Google Scholar 

  • Jones JB, Fisher SG, Grimm NB. 1995. Vertical hydrological exchange and ecosystem metabolism in a Sonoran Desert stream. Ecology 76:942–52.

    Article  Google Scholar 

  • Jørgensen PE, Eriksen T, Jensen BK. 1992. Estimation of viable biomass in wastewater and activated sludge by determination of ATP, oxygen utilization rate and FDA hydrolysis. Water Res 26:1495–501.

    Article  Google Scholar 

  • Kazumi J, Capone DG. 1994. Heterotrophic microbial activity in shallow aquifer sediments of Long Island, New York. Microb Ecol 28:19–37.

    Article  CAS  Google Scholar 

  • Langenheder S, Jürgens K. 2001. Regulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnol Oceanogr 46:121–34.

    Article  Google Scholar 

  • Lazarova V, Manem J. 1995. Biofilm characterization and activity analysis in water and wastewater treatment. Water Res 29:2227–45.

    Article  CAS  Google Scholar 

  • Leibold MA, Chase JM, Shurin JB, Downing AL. 1997. Species turnover and the regulation of trophic structure. Annu Rev Ecol Syst 28:467–94.

    Article  Google Scholar 

  • Malard F, Hervant F. 1999. Oxygen supply and the adaptations of animals in groundwater. Freshw Biol 41:1–30.

    Article  Google Scholar 

  • Marmonier P, Fontvieille D, Gibert J, Vanek V. 1995. Distribution of dissolved organic carbon and bacteria at the interface between the Rhone River and its alluvial aquifer. J N Am Benthol Soc 14:382–92.

    Article  Google Scholar 

  • Mauclaire L, Gibert J, Claret C. 2000. Do bacteria and nutrients control faunal assemblages in alluvial aquifers? Arch Hydrobiol 148:85–98.

    CAS  Google Scholar 

  • Menge BA, Sutherland J. 1976. Species diversity gradients: synthesis of the roles of predation, competition and temporal heterogeneity. Am Nat 110:351–69.

    Article  Google Scholar 

  • Menge BA. 2000. Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–89.

    Article  PubMed  Google Scholar 

  • Menge BA, Olson AM, Dahlhoff EP. 2002. Environmental stress, bottom-up effects, and community dynamics: integrating molecular-physiological and ecological approaches. Integr Comp Biol 42:892–908.

    Article  PubMed  Google Scholar 

  • 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 39:1687–98.

    Article  PubMed  CAS  Google Scholar 

  • Mikola J, Setälä H. 1998a. No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153–64.

    Article  Google Scholar 

  • Mikola J, Setälä H. 1998b. Productivity and trophic-level biomasses in a microbial-based soil food web. Oikos 82:158–68.

    Article  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC, De Ruiter PC, Dong Q, Hastings A et al. 2004. Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600.

    Article  Google Scholar 

  • Mösslacher F, Notenboom J. 1999. Groundwater biomonitoring. Biomonitoring of polluted water. Zürich: Trans Tech Publications.

    Google Scholar 

  • Muyzer M, Smalla K. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73:127–41.

    Article  PubMed  CAS  Google Scholar 

  • Oksanen L, Fretwell SD, Arruda J, Niemela P. 1981. Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–61.

    Article  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Stevens MHH, Wagner H. 2008. Vegan: community ecology package (http://vegan.r-forge.r-project.org).

  • Pace ML, Cole JJ. 1994. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb Ecol 28:181–93.

    Article  Google Scholar 

  • Perlmutter DG, Meyer JL. 1991. The impact of a stream-dwelling harpacticoid copepod upon detritally associated bacteria. Ecology 71:2170–80.

    Article  Google Scholar 

  • Peterson GL. 1977. A modification of the protein assay method of Lowry and others which is more generally applicable. Anal Biochem 83:346–56.

    Article  PubMed  CAS  Google Scholar 

  • Polis GA, Strong DR. 1996. Food web complexity and community dynamics. Am Nat 147:813–46.

    Article  Google Scholar 

  • Porter KS, Feig YS. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–8.

    Article  Google Scholar 

  • Pusch M, Fiebig D, Brettar I, Eisenmann H, Ellis BK, Kaplan LA, Lock MA, Naegeli MW, Traunspurger W. 1998. The role of micro-organisms in the ecological connectivity of running waters. Freshw Biol 40:453–95.

    Article  Google Scholar 

  • R Development Core Team. 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing: Vienna. http://www.R-project.org.

  • Robert P, Escoufier Y. 1976. A unifying tool for linear multivariate statistical methods: the RV-coefficient. Appl Stat 25:257–65.

    Article  Google Scholar 

  • Röling WFM, Van Breukelen BM, Braster M, Lin B, Van Verseveld HW. 2001. Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl Environ Microbiol 67:4619–29.

    Article  PubMed  Google Scholar 

  • Rønn R, McCaig A, Griffiths B, Prosser J. 2002. Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–105.

    Article  PubMed  Google Scholar 

  • Rosemond AD, Pringle CM, Ramirez A, Paul MJ. 2001. A test of top-down and bottom-up control in a detritus-based food web. Ecology 82:2279–93.

    Article  Google Scholar 

  • Schauer M, Massana R, Pedrós-Alió C. 2000. Spatial differences in bacterioplankton composition along the Catalon coast (NW Mediterranean) assessed by molecular fingerprinting. FEMS Microbiol Ecol 33:51–9.

    Article  PubMed  CAS  Google Scholar 

  • Šimek K, Pernthaler J, Weinbauer MG, Hornák K, Dolan JR, Nedoma J, Mašín M, Amann R. 2001. Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl Environ Microbiol 67:2723–33.

    Article  PubMed  Google Scholar 

  • Simon KS, Benfield EF, Macko SA. 2003. Food web structure and the role of epilithic biofilms in cave streams. Ecology 84:2395–406.

    Article  Google Scholar 

  • Steiner CF. 2001. The effects of prey heterogeneity and consumer identity on the limitation of trophic-level biomass. Ecology 82:2495–506.

    Article  Google Scholar 

  • Storey RG, Williams DD. 2004. Spatial responses of hyporheic invertebrates to seasonal changes in environmental parameters. Freshw Biol 49:1468–86.

    Article  Google Scholar 

  • Strayer DL, May SE, Nielsen P, Wolheim W, Hausam S. 1997. Oxygen, organic matter, and sediment granulometry as controls on hyporheic animal communities. Arch Hydrobiol 140:131–44.

    CAS  Google Scholar 

  • Strong DR. 1992. Are trophic cascades all wet? The redundant differentiation in trophic architecture of high diversity ecosystems. Ecology 73:747–54.

    Article  Google Scholar 

  • Sutherland IW. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9.

    PubMed  CAS  Google Scholar 

  • Townsend CR, Dolédec S, Norris R, Peacock K, Arbuckle C. 2003. The influence of scale and geography on relationships between stream community composition and landscape variables: description and prediction. Freshw Biol 48:768–85.

    Article  Google Scholar 

  • Ward JV, Bretschko G, Brunke M, Danielopol D, Gibert J, Gonser T, Hildrew AG. 1998. The boundaries of river systems: the metazoan perspective. Freshw Biol 40:531–69.

    Article  Google Scholar 

  • Wintzingerode FV, Göbel UB, Stackebrandt E. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–29.

    Article  Google Scholar 

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Acknowledgments

This study was conducted within the framework of the experimental Observatory for Urban Hydrology (OTHU, http://www.graie.org/othu/). It was funded by the French National Research Agency (project ANR-05-ECOT-006; http://www.graie.org/ecopluies/), the French programme EC2CO-Cytrix from INSU/CNRS (project “NAPCOD”), the Urban Community of Lyon, and the Rhône-Alpes Region. We are indebted to G. Bouger, E. Malet, Y. Negrutiu, L. Simon, D. Ferreira and F. Vallier for their most dedicated support with the field and laboratory work. We thank two anonymous reviewers for their comments that improved an earlier version of the manuscript.

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Authors and Affiliations

  1. Université de Lyon, 69000, Lyon, France

    Arnaud Foulquier, Florian Malard, Florian Mermillod-Blondin, Sylvain Dolédec & Janine Gibert

  2. Université Lyon 1, 69622, Lyon, France

    Arnaud Foulquier, Florian Malard, Florian Mermillod-Blondin, Sylvain Dolédec & Janine Gibert

  3. CNRS, UMR 5023, Laboratoire d’Écologie des Hydrosystèmes Naturels et Anthropisés, 43 Bd du 11 Novembre 1918, 69622, Villeurbanne, France

    Arnaud Foulquier, Florian Malard, Florian Mermillod-Blondin, Sylvain Dolédec & Janine Gibert

  4. Cemagref, Groupement de Lyon, UR Milieux Aquatiques, Écologie et Pollutions, Laboratoire d’Écologie Microbienne des Hydrosystèmes Anthropisés, 3 bis Quai Chauveau, CP 220, 69336, Lyon Cedex 09, France

    Arnaud Foulquier, Bernard Montuelle & Bernadette Volat

  5. INRA, UMR CARRTEL, 75 av. de Corzent, BP 511, 74203, Thonon-les-Bains Cedex, France

    Bernard Montuelle

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  1. Arnaud Foulquier
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Correspondence to Arnaud Foulquier.

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FA, MF, MBF, and GJ designed the study. FA, MF, MBF, MB, and VB performed research. FA and DS analyzed data. FA wrote the article with assistance from all authors.

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Foulquier, A., Malard, F., Mermillod-Blondin, F. et al. Surface Water Linkages Regulate Trophic Interactions in a Groundwater Food Web. Ecosystems 14, 1339–1353 (2011). https://doi.org/10.1007/s10021-011-9484-0

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