Apidologie

, Volume 48, Issue 3, pp 328–339 | Cite as

Predictive systems models can help elucidate bee declines driven by multiple combined stressors

  • Mickaël Henry
  • Matthias A. Becher
  • Juliet L. Osborne
  • Peter J. Kennedy
  • Pierrick Aupinel
  • Vincent Bretagnolle
  • François Brun
  • Volker Grimm
  • Juliane Horn
  • Fabrice Requier
Original article

Abstract

Bee declines are driven by multiple combined stresses, making it exceedingly difficult to identify experimentally the most critical threats to bees and their pollination services. We highlight here the too often ignored potential of mechanistic models in identifying critical stress combinations. Advanced bee models are now available as open access tools and offer an unprecedented opportunity for bee biologists to explore bee resilience tipping points in a variety of environmental contexts. We provide general guidelines on how to run bee models to help detect a priori critical stress combinations to be targeted in the field. This so-called funnel analysis should be performed in tight conjunction with the recent development of large-scale field monitoring programs for bee health surveillance.

Keywords

Apis mellifera field monitoring program honeybees mechanistic modeling agent-based models 

References

  1. Alaux, C., Brunet, J.-L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J., Baldy, A., Belzunces, L.P., Conte, Y.L. (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aufauvre, J., Biron, D.G., Vidau, C., Fontbonne, R., Roudel, M., Diogon, M., Viguès, B., Belzunces, L.P., Delbac, F., Blot, N. (2012) Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Sci. Rep. 2, 326CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barron, A.B. (2015) Death of the bee hive: understanding the failure of an insect society. Curr. Opin. Insect Sc. 10, 45–50CrossRefGoogle Scholar
  4. Becher, M.A., Hildenbrandt, H., Hemelrijk, C.K., Moritz, R.F.A. (2010) Brood temperature, task division and colony survival in honeybees: a model. Ecol. Model. 221, 769–776CrossRefGoogle Scholar
  5. Becher, M.A., Osborne, J.L., Thorbek, P., Kennedy, P.J., Grimm, V. (2013) Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models. J. Appl. Ecol. 50, 868–880CrossRefPubMedPubMedCentralGoogle Scholar
  6. Becher, M.A., Grimm, V., Thorbek, P., Horn, J., Kennedy, P.J., Osborne, J.L. (2014) BEEHAVE: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J. Appl. Ecol. 51, 470–482CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bretagnolle, V., Gaba, S. (2015) Weeds for bees? A review. Agron. Sustain. Dev. 35, 891–909CrossRefGoogle Scholar
  8. Bryden, J., Gill, R.J., Mitton, R.A.A., Raine, N.E., Jansen, V.A.A. (2013) Chronic sublethal stress causes bee colony failure. Ecol. Lett. 16, 1463–1469CrossRefPubMedPubMedCentralGoogle Scholar
  9. Collison, E., Hird, H., Cresswell, J., Tyler, C. (2015) Interactive effects of pesticide exposure and pathogen infection on bee health—a critical analysis. Biol. Rev. in press, doi: 10.1111/brv.12206 Google Scholar
  10. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  11. DeAngelis, D.L., Wolf, M. (2003) In praise of mechanistically rich models, in : Canham, C.D., Cole, J.J., Lauenroth, W.K. (Eds.), Models in ecosystem science, Princeton University Press, Princeton, pp. 63–82Google Scholar
  12. Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A., Suchail, S., Brunet, J.-L., Alaux, C. (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One 8, e72016CrossRefPubMedPubMedCentralGoogle Scholar
  13. Doublet, V., Labarussias, M., de Miranda, J.R., Moritz, R.F.A., Paxton, R.J. (2015) Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 17, 969–983CrossRefPubMedGoogle Scholar
  14. EPILOBEE Consortium, Chauzat, M.-P., Jacques, A., Laurent, M., Bougeard, S., Hendrikx, P., Ribière-Chabert, M. (2016) Risk indicators affecting honeybee colony survival in Europe: one year of surveillance. Apidologie, 47, 348–378.CrossRefGoogle Scholar
  15. European Academies Science Advisory Council. (2015) Ecosystem Services, Agriculture and Neonicotinoids, EASAC policy report 26, Halle, GermanyGoogle Scholar
  16. European Food Safety Authority. (2015) Statement on the suitability of the BEEHAVE model for its potential use in a regulatory context and for the risk assessment of multiple stressors in honeybees at the landscape level. EFSA Journal 13, 4125:4216Google Scholar
  17. Evans, M.R., Bithell, M., Cornell, S.J., Dall, S.R.X., Díaz, S., et al. (2013) Predictive systems ecology. Proc. R. Soc. B 280, 20131452CrossRefPubMedPubMedCentralGoogle Scholar
  18. Everaars, J., Dormann, C.F. (2014) Simulation of olitary (non-Apis) bees competing for pollen, in Devillers, J. (Ed.), in Silico Bees, CRC Press, Taylor, Francis Group, Boca Raton, pp. 209–268Google Scholar
  19. Fauser-Misslin, A., Sadd, B.M., Neumann, P., Sandrock, C. (2014) Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J. Appl. Ecol. 51, 450–459CrossRefGoogle Scholar
  20. Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., et al. (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41, 332–352CrossRefGoogle Scholar
  21. Gill, R.J., Ramos-Rodriguez, O., Raine, N.E. (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L. (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957CrossRefPubMedGoogle Scholar
  23. Grimm, V., Revilla, E., Berger, U., Jeltsch, F., Mooij, W.M., Railsback, S.F., Thulke, H.-H., Weiner, J., Wiegand, T., DeAngelis, D.L. (2005) Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310, 987–991CrossRefPubMedGoogle Scholar
  24. Grimm, V., Berger, U., Bastiansen, F., Eliassen, S., Ginot, V., et al. (2006) A standard protocol for describing individual-based and agent-based models. Ecol. Model. 198, 115–126CrossRefGoogle Scholar
  25. Grimm, V., Berger, U., DeAngelis, D.L., Polhill, J.G., Giske, J., Railsback, S.F. (2010) The ODD protocol: a review and first update. Ecol. Model. 221, 2760–2768CrossRefGoogle Scholar
  26. Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P., Aptel, J., Tchamitchian, S., Decourtye, A. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350CrossRefPubMedGoogle Scholar
  27. Henry, M., Bertrand, C., Le Féon, V., Requier, F., Odoux, J.-F., Aupinel, P., Bretagnolle, V., Decourtye, A. (2014) Pesticide risk assessment in free-ranging bees is weather and landscape dependent. Nat. Commun. 5, 4359CrossRefPubMedGoogle Scholar
  28. Henry, M., Cerrutti, N., Aupinel, P., Decourtye, A., Gayrard, M., Odoux, J.-F., Pissard, A., Rüger, C., Bretagnolle, V. (2015) Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proc. R. Soc. B 282, 20152110CrossRefPubMedPubMedCentralGoogle Scholar
  29. Horn, J., Becher, M.A., Kennedy, P.J., Osborne, J.L., Grimm, V. (2016) Multiple stressors: using the honeybee model BEEHAVE to explore how spatial and temporal forage stress affects colony resilience. Oikos 125, 1001–1016CrossRefGoogle Scholar
  30. Johnson, R.M., Dahlgren, L., Siegfried, B.D., Ellis, M.D. (2013) Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS One 8, e54092CrossRefPubMedPubMedCentralGoogle Scholar
  31. Khoury, D.S., Myerscough, M.R., Barron, A.B. (2011) A quantitative model of honey bee colony population dynamics. PLoS One 6 e18491CrossRefPubMedPubMedCentralGoogle Scholar
  32. Khoury, D.S., Barron, A.B., Myerscough, M.R. (2013) Modelling food and population dynamics in honey bee colonies. PLoS One 8, e59084CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nazzi, F., Brown, S.P., Annoscia, D., Del Piccolo, F., Di Prisco, G., Varricchio, P., Della Vedova, G., Cattonaro, F., Caprio, E., Pennacchio, F. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog. 8, e1002735CrossRefPubMedPubMedCentralGoogle Scholar
  34. Odoux, J.-F., Aupinel, P., Gateff, S., Requier, F., Henry, M., Bretagnolle, V. (2014) ECOBEE: a tool for long-term bee colony monitoring at landscape scale in west European intensive agrosystems. J. Apic. Res. 53, 57–66CrossRefGoogle Scholar
  35. Park, M.G., Blitzer, E.J., Gibbs, J., Losey, J.E., Danforth, B.N. (2015) Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proc. R. Soc. B 282, 20150299CrossRefPubMedPubMedCentralGoogle Scholar
  36. Perry, C.J., Søvik, E., Myerscough, M.R., Barron, A.B. (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl. Acad. Sc. U.S.A. doi: 10.1073/pnas.1422089112 Google Scholar
  37. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353CrossRefPubMedGoogle Scholar
  38. Requier, F., Odoux, J.-F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., Bretagnolle, V. (2014) Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. Appl. 25, 881–890CrossRefGoogle Scholar
  39. Requier, F., Odoux, J.F., Henry, M., Bretagnolle, V. (2016) The carry-over effects of spring pollen shortage negatively impact the colony dynamics and survival of managed honeybees. J. Appl. Ecol, in press Google Scholar
  40. Retschnig, G., Williams, G.R., Mehmann, M.M., Yañez, O., de Miranda, J.R., Neumann, P. (2014) Sex-specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLoS One 9, e85261CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rome, Q., Muller, F.J., Touret-Alby, A., Darrouzet, E., Perrard, A., Villemant, C. (2015) Caste differentiation and seasonal changes in Vespa velutina (Hym.: Vespidae) colonies in its introduced range. J. Appl. Entomol. 139, 771–782CrossRefGoogle Scholar
  42. Rumkee, J.C.O., Becher, M.A., Thorbek, P., Kennedy, P.J., Osborne, J.L. (2015) Predicting honeybee colony failure: using the BEEHAVE model to simulate colony responses to pesticides. Environ Sci. Technol. 49, 12879–12887CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rundlöf, M., Andersson, G.K.S., Bommarco, R., Fries, I., Hederström, V., et al. (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80CrossRefPubMedGoogle Scholar
  44. Saltelli, A., Ratto, M., Andres, T., Campolongo, F., Cariboni, J., Gatelli, D., Saisana, M., Tarantola, S. (2008) Global sensitivity analysis: the primer, John Wiley Sons, Chichester.Google Scholar
  45. Schmickl, T., Crailsheim, K. (2007) HoPoMo: a model of honeybee intracolonial population dynamics and resource management. Ecol. Model. 204, 219–245CrossRefGoogle Scholar
  46. Stillman, R.A., Railsback, S.F., Giske, J., Berger, U., Grimm, V. (2015) Making predictions in a changing world: the benefits of individual-based ecology. BioScience, 65, 140–150CrossRefPubMedGoogle Scholar
  47. Stillman, R.A., Wood, K.A., Goss-Custard, J.D. (2016) Deriving simple predictions from complex models to support environmental decision-making. Ecol. Model., 10.1016/j.ecolmodel.2015.04.014. in pressGoogle Scholar
  48. Thiele, J.C., Kurth, W., Grimm, V. (2014) Facilitating parameter estimation and sensitivity analysis of agent-based models: a cookbook using NetLogo and “R”. JASSS 17, 11. doi:10.18564/jasss.2503CrossRefGoogle Scholar
  49. Torres, D.J., Ricoy, U.M., Roybal, S. (2015) Modeling honey bee populations. PLoS One 10, e0130966CrossRefPubMedPubMedCentralGoogle Scholar
  50. van Engelsdorp, D., Hayes, J., Jr., Underwood, R.M., Pettis, J. (2008) A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One 3, e4071CrossRefPubMedGoogle Scholar
  51. Vanbergen, A.J., the Insect Pollinators Initiative. (2013) Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ. 11, 251–259CrossRefGoogle Scholar
  52. Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One 6, e21550CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2016

Authors and Affiliations

  • Mickaël Henry
    • 1
    • 2
  • Matthias A. Becher
    • 3
  • Juliet L. Osborne
    • 3
  • Peter J. Kennedy
    • 3
  • Pierrick Aupinel
    • 4
  • Vincent Bretagnolle
    • 5
    • 6
  • François Brun
    • 7
  • Volker Grimm
    • 8
  • Juliane Horn
    • 8
  • Fabrice Requier
    • 1
    • 2
  1. 1.INRA, UR406 Abeilles et EnvironnementAvignonFrance
  2. 2.UMT Protection des Abeilles dans l’Environnement, Site AgroparcAvignonFrance
  3. 3.Environment and Sustainability InstituteUniversity of Exeter, Penryn CampusPenrynUK
  4. 4.INRA, UE1255, UE EntomologieSurgèresFrance
  5. 5.Centre d’Etudes Biologiques de Chizé, UMR 7372, CNRS & Université de La RochelleBeauvoir-sur-NiortFrance
  6. 6.LTER Zone Atelier Plaine & Val de Sèvre, Centre d’Etudes Biologiques de Chizé, CNRSVilliers-en-BoisFrance
  7. 7.ACTA INRA, UMR 1248 AGIRCastanet Tolosan cedexFrance
  8. 8.UFZ, Helmholtz Centre for Environmental Research – UFZLeipzigGermany

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