Skip to main content
SpringerLink
Log in

Changes in carbon sources fueling benthic secondary production over depth and time: coupling Chironomidae stable carbon isotopes to larval abundance

  • Global change ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Stable C isotope ratio (δ13C) values of chironomid remains (head capsules; HC) were used to infer changes in benthic C sources over the last 150 years for two French sub-Alpine lakes. The HCs were retrieved from a series of sediment cores from different depths. The HC δ13C values started to decrease with the onset of eutrophication. The HC δ13C temporal patterns varied among depths, which revealed spatial differences in the contribution of methanotrophic bacteria to the benthic secondary production. The estimates of the methane (CH4)-derived C contribution to chironomid biomass ranged from a few percent prior to the 1930s to up to 30 % in recent times. The chironomid fluxes increased concomitantly with changes in HC δ13C values before a drastic decrease due to the development of hypoxic conditions. The hypoxia reinforced the implication for CH4-derived C transfer to chironomid production. In Lake Annecy, the HC δ13C values were negatively correlated to total organic C (TOC) content in the sediment (Corg), whereas no relationship was found in Lake Bourget. In Lake Bourget, chironomid abundances reached their maximum with TOC contents between 1 and 1.5 % Corg, which could constitute a threshold for change in chironomid abundance and consequently for the integration of CH4-derived C into the lake food webs. Our results indicated that the CH4-derived C contribution to the benthic food webs occurred at different depths in these two large, deep lakes (deep waters and sublittoral zone), and that the trophic transfer of this C was promoted in sublittoral zones where O2 gradients were dynamic.

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

Similar content being viewed by others

References

  • Agasild H, Zingel P, Tuvikene L, Tuvikene A, Timm H, Feldmann T, Salujõe J, Toming K, Jones RI, Nõges T (2014) Biogenic CH4 contributes to the food web of a large, shallow lake. Freshwater Biol 59:272–285

    Article  CAS  Google Scholar 

  • Armitage P, Cranston PS, Pinder LCV (1994) The Chironomidae: biology and ecology of non-biting midges. Chapman and Hall, London

    Google Scholar 

  • Bastviken D, Cole JJ, Pace ML, Van de Bogert MC (2008) Fates of CH4 from different lake habitats: connecting whole-lake budgets and CH4 emissions. J Geophys Res Biogeosci 113:13

    Article  Google Scholar 

  • Belle S, Parent C, Frossard V, Verneaux V, Millet L, Chronopoulou P-M, Sabatier P, Magny M (2014) Temporal changes in the contribution of CH4-oxidizing bacteria to the biomass of chironomid larvae determined using stable carbon isotopes and ancient DNA. J Paleolimnol. doi:10.1007/s10933-10014-19789-z

    Google Scholar 

  • Berthon V, Alric B, Rimet F, Perga ME (2014) Sensitivity and responses of diatoms to climate warming in lakes heavily influenced by humans. Freshwater Biol. doi:10.1111/fwb.12380

    Google Scholar 

  • Blees J, Niemann H, Wenk C, Zopfi J, Schubert C, Kirf M, Veronesi M, Hitz C, Lehmann M (2014) Micro-aerobic bacterial CH4 oxidation in the chemocline and anoxic water column of deep south-Alpine Lake Lugano (Switzerland). Limnol Oceanogr 59:311–324

    Article  CAS  Google Scholar 

  • Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel JP, Peyret P, Fonty G, Lehours AC (2011) Production and consumption of CH4 in freshwater lake ecosystems. Res Microbiol 162:832–847

    Article  CAS  PubMed  Google Scholar 

  • Brodersen K, Pedersen O, Walker I, Jensen M (2008) Respiration of midges (Diptera; Chironomidae) in British Columbian lakes: oxy-regulation, temperature and their role as palaeo-indicators. Freshwater Biol 53:593–602

    Article  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  CAS  PubMed  Google Scholar 

  • Brooks SJ, Langdon PG, Heiri O (2007) The identification and use of Palaearctic Chironomidae larvae in palaeoecology. QRA technical guide no. 10 Quaternary Research Association, London

  • Carpenter SR, Ludwig D, Brock W (1999) Management of eutrophicaiton for lakes subject to potentially irreversible change. Ecol Appl 9:751–771

    Article  Google Scholar 

  • Cole J, Carpenter S, Kitchell J, Pace M, Solomon C, Weidel B (2011) Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. PNAS 108:1975–1980

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Danis PA, von Grafenstein U, Masson-Delmotte V, Planton V, Gerdeaux D, Moisselin JM (2004) Vulnerability of two European lakes in response to future climatic changes. Geophys Res Lett 31:L21507

    Article  Google Scholar 

  • Deines P, Wooller MJ, Grey J (2009) Unravelling complexities in benthic food webs using a dual stable isotope (hydrogen and carbon) approach. Freshwater Biol 54:2243–2251

    Article  CAS  Google Scholar 

  • Devlin SP, Vander Zanden MJ, Vadeboncoeur Y (2013) Depth-specific variation in carbon isotopes demonstrates resource partitioning among the littoral zoobenthos. Freshwater Biol 58:2389–2400

    CAS  Google Scholar 

  • Eller G, Känel L, Krüger M (2005) Cooccurrence of aerobic and anaerobic CH4 oxidation in the water column of lake Plußsee. Appl Environ Microbiol 71:8925–8928

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eller G, Deines P, Krüger M (2007) Possible sources of CH4-derived carbon for chironomid larvae. Aquat Microb Ecol 46:283–293

    Article  Google Scholar 

  • Espitalié J, Deroo G, Marquis F (1985a) La pyrolyse rock Eval et ses applications 2de partie. Rev Inst Fr Pet 40:755–784

    Google Scholar 

  • Espitalié J, Deroo G, Marquis F (1985b) La pyrolyse rock Eval et ses applications. 3ème partie. Rev Inst Fr Pet 41:73–89

    Google Scholar 

  • France RL (1995) Carbon-13 depletion in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312

    Article  Google Scholar 

  • Frossard V (2013c) Trajectoires écologiques des lacs d’Annecy et du Bourget au cours des 150 dernières années: approche paléolimnologique par analyse des assemblages de Chironomidae (Diptera) et de leurs signatures isotopiques en carbone. Ph.D. thesis, Université Franche-Comté, France

  • Frossard V, Belle S, Verneaux V, Millet L, Magny M (2013a) A study of the δ13C offset between chironomid larvae and their exuvial head capsules: a contribution to palaeoecology. J Paleolimnol 50:379–386

    Article  Google Scholar 

  • Frossard V, Millet L, Verneaux V, Jenny JP, Arnaud F, Magny M, Poulenard J, Perga ME (2013b) Chironomid assemblage reconstructions at multiple depths describe the O2-driven changes in a deep French lake during the last 150 years. J Paleolimnol 50:257–273

    Article  Google Scholar 

  • Frossard V, Verneaux V, Millet L, Jenny JP, Arnaud F, Magny M, Perga ME (2014a) Depth-specific responses of the chironomid community to contrasting anthropogenic pressures: a paleolimnological perspective of 150 years. Freshwater Biol 59:26–40

    Article  Google Scholar 

  • Frossard V, Verneaux V, Millet L, Jenny JP, Arnaud F, Magny M, Perga ME (2014b) Reconstructing long-term changes (150 years) in the carbon cycle of a clear-water lake based on the stable carbon isotope composition (d13C) of chironomid and cladoceran subfossil remains. Freshwater Biol. doi:10.1111/fwb.12304

    Google Scholar 

  • Grey J, Deines P (2005) Differential assimilation of methanotrophic and chemoautotrophic bacteria by lake chironomid larvae. Aquat Microb Ecol 40:61–66

    Article  Google Scholar 

  • Hanson R, Hanson T (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hastie T, Tibshirani R (1990) Generalized additive models. Chapman and Hall, London

    Google Scholar 

  • Heiri O, Schilder J, van Hardenbroek M (2012) Stable isotopic analysis of fossil chironomids as an approach to environmental reconstruction: state of development and future challenges. Fauna Nor 31:7–18

    Google Scholar 

  • Jenny JP, Arnaud F, Dorioz JM, Giguet Covex C, Frossard V, Sabatier P, Millet L, Reyss JL, Tachikawa K, Bard E, Pignol C, Soufi F, Romeyer O, Perga ME (2013) A spatiotemporal sediment investigation highlights the dynamics of hypolimnetic hypoxia in a large hard water lake over 150 years. Limnol Oceanogr 58:1395–1408

    CAS  Google Scholar 

  • Jones R, Grey J (2011) Biogenic CH4 in freshwater food webs. Freshwater Biol 56:213–229

    Article  CAS  Google Scholar 

  • Jones SE, Lennon JT (2009) Evidence for limited microbial transfer of CH4 in a planktonic food web. Aquat Microb Ecol 58:45–53

    Article  Google Scholar 

  • Jones RI, Carter CE, Kelly A, Ward S, Kelly DJ, Grey J (2008) Widespread contribution of CH4cycle bacteria to the diets of lake profundal chironomid larvae. Ecology 89:857–864

    Article  PubMed  Google Scholar 

  • Jyväsjärvi J, Boros G, Jones R, Hämäläinen H (2013) The importance of sedimenting organic matter, relative to O2 and temperature, in structuring lake profundal macroinvertebrate assemblages. Hydrobiologia 709:55–72

    Article  Google Scholar 

  • Kankaala P, Taipale S, Grey J, Sonninen E, Arvola L, Jones R (2006) Experimental d13C evidence for a contribution of CH4 to pelagic food webs in lakes. Limnol Oceanogr 51:2821–2827

    Article  CAS  Google Scholar 

  • Karlsson J (2007) Different carbon support for respiration and secondary production in unproductive lakes. Oikos 116:1691–1696

    Article  CAS  Google Scholar 

  • Kiyashko S, Narita T, Wada E (2001) NOTE: contribution of methanotrophs to freshwater macroinvertebrates: evidence from stable isotope ratios. Aquat Microb Ecol 24:203–207

    Article  Google Scholar 

  • Lehmann M, Bernasconi S, Barbieri A, Simona M, McKenzie J (2004) Interannual variation of the isotopic composition of sedimenting organic carbon and nitrogen in Lake Lugano: a long-term sediment trap study. Limnol Oceanogr 49:839–849

    Article  CAS  Google Scholar 

  • Low-Décarie E, Fussmann GF, Bell G (2014) Aquatic primary production in a high-CO2 world. Trends Ecol Evol (Personal Edn) 29:223–232

    Article  Google Scholar 

  • Meyers P, Ishiwatari R (1993) Lacustrine organic geochemistry: an overview of indicators of organic matter sources and diagenesis in lake sediments. Org Geochem 20:867–900

    Article  CAS  Google Scholar 

  • Millet L, Giguet-Covex C, Verneaux V, Druart JC, Adatte T, Arnaud F (2010) Reconstruction of the recent history of a large deep prealpine lake (Lake Bourget, France) using subfossil chironomids, diatoms, and organic matter analysis: towards the definition of a lake-specific reference state. J Paleolimnol 44:963–978

    Article  Google Scholar 

  • Moller Pillot HKM (2009) Chironomidae larvae volume 2. Biology and ecology of the Chironomini. KNNV

  • Moog O (2002) Fauna Aquatica Austriaca: a comprehensive species inventory of Austrian aquatic organisms with ecological notes, 2nd edn. Federal Ministry of Agriculture, Forestry, Environment and Water Management, Division VII (Water), Vienna

    Google Scholar 

  • Noël H, Garbolino E, Brauer A, Lallier-Vergès E, de Beaulieu JL, Disnar JR (2001) Human impact and soil erosion during the last 5,000 years as recorded in lacustrine sedimentary organic matter at Lac d’Annecy, the French Alps. J Paleolimnol 25:229–244

    Article  Google Scholar 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    Article  CAS  PubMed  Google Scholar 

  • Perga ME, Gerdeaux D (2004) Changes in the δ13C of pelagic food webs: the influence of lake area and trophic status on the isotopic signature of whitefish (Coregonus lavaretus). Can J Fish Aquat Sc 61:1485–1492

    Article  CAS  Google Scholar 

  • Perga ME, Desmet M, Enters D, Reyss JL (2010) A century of bottom-up- and top-down-driven changes on a lake planktonic food web: a paleoecological and paleoisotopic study of Lake Annecy, France. Limnol Oceanogr 55:803–816

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1-103

  • Popp BN, Laws EA, Bidigare RR, Dore JE, Hanson KL, Wakeham SG (1998) Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochim Cosmochim Acta 62:69–77

    Article  CAS  Google Scholar 

  • Quinlan R, Smol JP (2001) Chironomid-based inference models for estimating end-of-summer hypolimnetic O2 from south-central Ontario shield lakes. Freshwater Biol 46:1529–1551

    Article  CAS  Google Scholar 

  • Rau G (1978) Carbon-13 depletion in a subalpine lake: carbon flow implications. Science 201:901–902

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Johnston AM, Newman JR, Scrimgeour CM (1994) Inorganic carbon acquisition by aquatic photolithoatrophs of the Dighty Burn, Angus, UK: uses and limitations of natural abundance measurements of carbon isotopes. New Phytol 127:271–286

    Article  CAS  Google Scholar 

  • Ravinet M, Syväranta J, Jones R, Grey J (2010) A trophic pathway from biogenic CH4 supports fish biomass in a temperate lake ecosystem. Oikos 119:409–416

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, http://www.R-project.org/

  • Reuss N, Hamerlik L, Velle G, Michelsen A, Pedersen O, Brodersen K (2013) Stable isotopes reveal that chironomids occupy several trophic levels within West Greenland lakes: implications for food web studies. Limnol Oceanogr 58:1023–1034

    Article  CAS  Google Scholar 

  • Reynolds CS (2008) A changing paradigm of pelagic food webs. Int Rev Hydrobiol 93:517–531

    Article  CAS  Google Scholar 

  • Rooney N, McCann K (2012) Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–46

    Article  PubMed  Google Scholar 

  • Schippers P, Lürling M, Scheffer M (2004) Increase of atmospheric CO2 promotes phytoplankton productivity. Ecol Lett 7:446–451

    Article  Google Scholar 

  • Smyntek P, Maberly S, Grey J (2012) Dissolved carbon dioxide concentration controls baseline stable carbon isotope signatures of a lake food web. Limnol Oceanogr 57:1292–1302

    Article  CAS  Google Scholar 

  • Solomon C, Carpenter S, Clayton M, Cole J, Coloso J, Pace M, Vander Zanden J, Weidel B (2011) Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model. Ecology 92:1115–1125

    Article  PubMed  Google Scholar 

  • Squires MM, Lesack LFW (2003) The relation between sediment nutrient content and macrophyte biomass and community structure along a water transparency gradient among lakes of the Mackenzie Delta Can. J Fish Aquat Sci 60:333–343

    Article  CAS  Google Scholar 

  • Summons RE (1994) Carbon isotopic fractionation in lipids from methanotrophic bacteria: relevance for interpretation of the geochemical record of biomarkers. Geochim Cosmochim Acta 58:2853–2863

    Article  CAS  PubMed  Google Scholar 

  • Takagi S, Kikuchi E, Doi H, Shikano S (2005) Swimming behaviour of Chironomus acerbiphilus larvae in Lake Katanuma. Hydrobiologia 548:153–165

    Article  Google Scholar 

  • Talbot M, Livingstone D (1989) Hydrogen index and carbon isotopes of lacustrine organic matter as lake level indicators. Palaeogeogr Palaeoclim Palaeoecol 70:121–137

    Article  Google Scholar 

  • Vadeboncoeur Y, Vander Zanden J, Lodge D (2002) Putting the lake back together: reintegrating benthic pathways into Lake food web models. Bioscience 52:44

    Article  Google Scholar 

  • van Hardenbroek M, Heiri O, Grey J, Bodelier P, Verbruggen F, Lotter A (2010) Fossil chironomid δ13C as a proxy for past methanogenic contribution to benthic food webs in lakes? J Paleolimnol 43:235–245

    Article  Google Scholar 

  • van Hardenbroek M, Heiri O, Wilhelm M, Lotter A (2011) How representative are subfossil assemblages of Chironomidae and common benthic invertebrates for the living fauna of Lake De Waay, the Netherlands? Aquatic Science 73:247–259

    Article  CAS  Google Scholar 

  • van Hardenbroek M et al (2013) Evidence for past variations in CH4 availability in a Siberian thermokarst lake based on d13C of chitinous invertebrate remains. Quat Sci Rev 66:74–84

    Article  Google Scholar 

  • van Hardenbroek M, Lotter AF, Bastviken D, Andersen TJ, Heiri O (2014) Taxon-specific δ13C analysis of chitinous invertebrate remains in sediments from Strandsjön, Sweden. J Paleolimnol 52:95–105

    Article  Google Scholar 

  • Verneaux V, Verneaux J, Schmitt A, Lambert JC (2004) Relationship of macrobenthos with dissolved O2 and organic matter at the sediment-water interface in ten French lakes. Fundam Appl Limnol/Archiv Hydrobiol 160:247–259

    CAS  Google Scholar 

  • Wagner A, Volkmann S, Dettinger-Klemm PMA (2012) Benthic–pelagic coupling in lake ecosystems: the key role of chironomid pupae as prey of pelagic fish. Ecosphere 3:2–17

    Article  Google Scholar 

  • Wanninkhof R (1992) Relationship between wind-speed and gas exchange over the ocean. J Geophys Res Oceans 97:7373–7382

    Article  Google Scholar 

  • Wood SN (2006) Generalized additive models: an introduction with R. Chapman & Hall, London

    Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc B 73:3–36

    Article  Google Scholar 

  • Wooller M et al (2012) Reconstruction of past CH4 availability in an Arctic Alaska wetland indicates climate influenced CH4 release during the past ~12,000 years. J Paleolimnol 48:27–42

    Article  Google Scholar 

  • Yang C, Wilkinson G, Cole J, Macko S, Pace M (2014) Assigning hydrogen, carbon, and nitrogen isotope values for phytoplankton and terrestrial detritus in aquatic food web studies. Inland Waters 4:233–242

    Article  CAS  Google Scholar 

  • Zuür A, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, Berlin

Download references

Acknowledgments

We are indebted to two anonymous reviewers and the editor for comments that greatly improved the manuscript, as well as to Clémentine Fritsch (UMR-CNRS 6249, Besançon) for her advice on statistical analyses. This study is a contribution to the program Impact des Perturbations sur les Réseaux Trophiques en lacs (IPER-RETRO) and was financially supported by the French National Research Agency (ANR VUL 005).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Université Savoie Mont Blanc, UMR42 CARRTEL, 73376, Le-Bourget-du-lac, France

    Victor Frossard

  2. Laboratoire Chrono-Environnement, UMR6249, 16 route de Gray, 25030, Besançon Cedex, France

    Victor Frossard, Valérie Verneaux, Laurent Millet & Michel Magny

  3. INRA, UMR42 CARRTEL, 75 avenue de Corzent, 74203, Thonon les Bains Cedex, France

    Marie-Elodie Perga

Authors
  1. Victor Frossard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valérie Verneaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laurent Millet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michel Magny
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marie-Elodie Perga
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor Frossard.

Additional information

Communicated by Robert O. Hall.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TXT 9 kb)

Supplementary material 2 (XLSX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frossard, V., Verneaux, V., Millet, L. et al. Changes in carbon sources fueling benthic secondary production over depth and time: coupling Chironomidae stable carbon isotopes to larval abundance. Oecologia 178, 603–614 (2015). https://doi.org/10.1007/s00442-015-3225-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3225-6

Keywords

Search

Navigation