Oecologia

, Volume 181, Issue 2, pp 519–532 | Cite as

Pathogens trigger top-down climate forcing on ecosystem dynamics

  • Eric Edeline
  • Andreas Groth
  • Bernard Cazelles
  • David Claessen
  • Ian J. Winfield
  • Jan Ohlberger
  • L. Asbjørn Vøllestad
  • Nils C. Stenseth
  • Michael Ghil
Community ecology – original research

Abstract

Evaluating the effects of climate variation on ecosystems is of paramount importance for our ability to forecast and mitigate the consequences of global change. However, the ways in which complex food webs respond to climate variations remain poorly understood. Here, we use long-term time series to investigate the effects of temperature variation on the intraguild-predation (IGP) system of Windermere (UK), a lake where pike (Esox lucius, top predator) feed on small-sized perch (Perca fluviatilis) but compete with large-sized perch for the same food sources. Spectral analyses of time series reveal that pike recruitment dynamics are temperature controlled. In 1976, expansion of a size-truncating perch pathogen into the lake severely impacted large perch and favoured pike as the IGP-dominant species. This pathogen-induced regime shift to a pike-dominated IGP apparently triggered a temperature-controlled trophic cascade passing through pike down to dissolved nutrients. In simple food chains, warming is predicted to strengthen top–down control by accelerating metabolic rates in ectothermic consumers, while pathogens of top consumers are predicted to dampen this top–down control. In contrast, the local IGP structure in Windermere made warming and pathogens synergistic in their top–down effects on ecosystem functioning. More generally, our results point to top predators as major mediators of community response to global change, and show that size-selective agents (e.g. pathogens, fishers or hunters) may change the topological architecture of food webs and alter whole ecosystem sensitivity to climate variation.

Keywords

Body size Parasites Population structure Singular spectrum analysis Wavelet analysis 

Notes

Acknowledgments

We thank Janice Fletcher, Ben James and other colleagues for undertaking the field and laboratory work of the Windermere fish monitoring programme and Lorenzo Ciannelli for useful discussions. We are also grateful to the Freshwater Biological Association who collected the data at the beginning of the time series. It is a pleasure to thank two anonymous reviewers for their detailed and constructive comments. The Natural Environment Research Council of the UK and the Norwegian Research Council supported part of this work. E. E. and D. C. received financial support from the French National Research Agency through projects ANR-10-CEPL-0010 PULSE and ANR-10-BLAN-1709 PHYTBACK. A. G. was supported by a post-doctoral fellowship of the Groupement d’Intérêt Scientifique Réseau de Recherche sur le Développement Soutenable of the Région Ile-de-France. I. J. W.’s contribution was part funded by the Managing Aquatic Ecosystems and Water Resources under Multiple Stress project under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), contract no. 603378. M. G. acknowledges support from the US National Science Foundation through grants DMS-1049253 and OCE-1243175.

Author contribution statement

E. E. led manuscript writing, I. J. W. provided the data, A. G. and B. C. ran the analyses and produced associated figures, and all authors contributed to results’ interpretation and manuscript improvement.

Supplementary material

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Supplementary material 1 (JPEG 452 kb)
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Supplementary material 2 (JPEG 174 kb)
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Supplementary material 3 (JPEG 2754 kb)
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Electronic Supplemental MaterialOne single file containing: supplemental materials and methods with references, supplemental figures S1 to S3, supplemental figure legends (PDF 1448 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Eric Edeline
    • 1
  • Andreas Groth
    • 2
    • 3
  • Bernard Cazelles
    • 4
    • 5
  • David Claessen
    • 2
    • 5
  • Ian J. Winfield
    • 6
  • Jan Ohlberger
    • 7
    • 8
  • L. Asbjørn Vøllestad
    • 7
  • Nils C. Stenseth
    • 7
  • Michael Ghil
    • 2
    • 3
    • 9
  1. 1.Institut d’Ecologie et des Sciences de l’Environnement-Paris (iEES-Paris)Sorbonne Universités/UPMC Université Paris 06/CNRS/INRA/IRD/Paris Diderot Université Paris 07/UPECParisFrance
  2. 2.Environmental Research and Teaching Institute (CERES-ERTI)Paris Cedex 05France
  3. 3.Department of Atmospheric and Oceanic Sciences and Institute of Geophysics and Planetary PhysicsUniversity of California at Los AngelesLos AngelesUSA
  4. 4.IRD-UPMCBondyFrance
  5. 5.Eco-Evolutionary MathematicsParis Cedex 05France
  6. 6.Lake Ecosystems Group, Centre for Ecology & Hydrology, Lancaster Environment CentreBailrigg, LancasterUK
  7. 7.Department of Biosciences, Center for Ecological and Evolutionary Synthesis (CEES)University of OsloOsloNorway
  8. 8.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA
  9. 9.Laboratoire de Météorologie DynamiqueCNRS and IPSLParis Cedex 05France

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