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Density-dependent negative responses by bumblebees to bacteria isolated from flowers

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Abstract

Flowers offer habitats for bacterial communities that are often characterized by low diversities but high densities. The composition of these communities and the dissemination of bacteria between flowers receive increasing attention, whereas the ecological functions of flower-associated but non-phytopathogenic bacteria remain understudied. We screened bacteria isolated from nectar, petals and leaves of two plant species for their potential to affect flower–visitor interactions. We took advantage of the proboscis extension reflex (PER) of bumblebees evoked by sugar and investigated whether bacteria associated with the reward may interrupt this reflex. Cultivated bacteria were transferred into a watery glucose solution in increasing densities and their effect on the proportion of bumblebees displaying the PER after antennal contact with glucose solutions and bacteria was scored. In all but one trial, the proportion of bumblebees that accepted the watery glucose solution was negatively correlated with the bacterial density. Nearly half of the bacteria tested evoked avoidance at naturally occurring densities. Our results suggest that bacteria colonizing flowers have the potential to negatively affect the reproduction of plants via reduced visits by pollinators.

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References

  • Adler, L.S. (2000) The ecological significance of toxic nectar. Oikos 91, 409–420

    Article  Google Scholar 

  • Alvarez-Perez, S., Herrera, C.M. (2013) Composition, richness and nonrandom assembly of culturable bacterial-microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiol. Ecol. 83, 685–699

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Perez, S., Herrera, C.M., de Vega, C. (2012) Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol. Ecol. 80, 591–602

    Article  CAS  PubMed  Google Scholar 

  • Anfora, G., Rigosi, E., Frasnelli, E., Ruga, V., Trona, F., Vallortigara, G. (2011) Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee, Bombus terrestris. Plos One 6, e18903

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Belisle, M., Peay, K.G., Fukami, T. (2012) Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub. Microb. Ecol. 63, 711–718

    Article  PubMed  Google Scholar 

  • Brysch-Herzberg, M. (2004) Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiol. Ecol. 50, 87–100

    Article  CAS  PubMed  Google Scholar 

  • Buban, T., Orosz-Kovacs, Z., Farkas, A. (2003) The nectary as the primary site of infection by Erwinia amylovora (Burr.). Plant Syst. Evol. 238, 183–194

    Google Scholar 

  • Carter, C., Thornburg, R.W. (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci. 9, 320–324

    Article  CAS  PubMed  Google Scholar 

  • Crawley M. J. (2005) Statistics - An introduction using R. John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex PO19 8SQ, England.

  • Davis, T.S., Crippen, T.L., Hofstetter, R.W., Tomberlin, J.K. (2013) Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 39, 840–859

    Article  CAS  PubMed  Google Scholar 

  • Ercolani, G.L. (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb. Ecol. 21, 35–48

    Article  CAS  PubMed  Google Scholar 

  • Evangelista, C., Kraft, P., Dacke, M., Reinhard, J., Srinivasan, M.V. (2010) The moment before touchdown: landing manoeuvres of the honeybee Apis mellifera. J. Exp. Biol. 213, 262–270

    Article  CAS  PubMed  Google Scholar 

  • Ezenwa, V.O., Gerardo, N.M., Inouye, D.W., Medina, M., Xavier, J.B. (2012) Animal behavior and the microbiome. Science 338, 198–199

    Article  CAS  PubMed  Google Scholar 

  • Fouks, B., Lattorff, H.M.G. (2011) Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). Plos One 6, e26328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fridman, S., Izhaki, I., Gerchman, Y., Halpern, M. (2012) Bacterial communities in floral nectar. Environ. Microbiol. Rep. 4, 97–104

    Article  PubMed  Google Scholar 

  • Fuernkranz, M., Lukesch, B., Müller, H., Huss, H., Grube, M., Berg, G. (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb. Ecol. 63, 418–428

    Article  CAS  Google Scholar 

  • Haupt, S.S. (2004) Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 190, 735–745

    Article  CAS  PubMed  Google Scholar 

  • Herrera, C.M., Garcia, I.M., Perez, R. (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89, 2369–2376

    Article  PubMed  Google Scholar 

  • Herrera, C.M., Pozo, M.I., Medrano, M. (2013) Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94, 273–279

    Article  PubMed  Google Scholar 

  • Huang, M., Sanchez-Moreiras, A.M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J., Tholl, D. (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense against a bacterial pathogen. New Phytol. 193, 997–1008

    Article  CAS  PubMed  Google Scholar 

  • Jensen, G.B., Hansen, B.M., Eilenberg, J., Mahillon, J. (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 5, 631–640

    Article  CAS  PubMed  Google Scholar 

  • Johnson, K.B., Stockwell, V.O., Mclaughlin, R.J., Sugar, D., Loper, J.E., Roberts, R.G. (1993) Effect of Antagonistic Bacteria on Establishment of Honey Bee-Dispersed Erwinia-Amylovora in Pear Blossoms and on Fire Blight Control. Phytopathology 83, 995–1002

    Article  Google Scholar 

  • Junker, R.R., Tholl, D. (2013) Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 39, 810–825

    Article  CAS  PubMed  Google Scholar 

  • Junker, R.R., Loewel, C., Gross, R., Dötterl, S., Keller, A., Blüthgen, N. (2011) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol. 13, 918–924

    Article  CAS  PubMed  Google Scholar 

  • Kai, M., Haustein, M., Molina, F., Petri, A., Scholz, B., Piechulla, B. (2009) Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81, 1001–1012

    Article  CAS  PubMed  Google Scholar 

  • Knuth, P. (1908) Handbook of flower pollination. Clarendon, Oxford

    Google Scholar 

  • Krimm, U., Abanda-Nkpwatt, D., Schwab, W., Schreiber, L. (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol. Ecol. 53, 483–492

    Article  CAS  PubMed  Google Scholar 

  • Lachance, M.A., Starmer, W.T., Rosa, C.A., Bowles, J.M., Barker, J.S.F., Janzen, D.H. (2001) Biogeography of the yeasts of ephemeral flowers and their insects. Fems Yeast Res. 1, 1–8

    Article  CAS  PubMed  Google Scholar 

  • Leroy P. D., Sabri A., Heuskin S., Thonart P., Lognay G., Verheggen F. J., Francis F., Brostaux Y., Felton G. W., Haubruge E. (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2, doi:10.1038/ncomms1347

  • Lindow, S.E., Brandl, M.T. (2003) Microbiology of the phyllosphere. Appl. Environ. Microb. 69, 1875–1883

    Article  CAS  Google Scholar 

  • Lunau, K., Unseld, K., Wolter, F. (2009) Visual detection of diminutive floral guides in the bumblebee Bombus terrestris and in the honeybee Apis mellifera. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 195, 1121–1130

    Article  PubMed  Google Scholar 

  • Maccagnani, B., Giacomello, F., Fanti, M., Gobbin, D., Maini, S., Angeli, G. (2009) Apis mellifera and Osmia cornuta as carriers for the secondary spread of Bacillus subtilis on apple flowers. Biocontrol 54, 123–133

    Article  Google Scholar 

  • Mattila, H.R., Rios, D., Walker-Sperling, V.E., Roeselers, G., Newton, I.L.G. (2012) Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. Plos One 7

  • Ondov B. D., Bergman N. H., Phillippy A. M. (2011) Interactive metagenomic visualization in a Web browser. Bmc Bioinforma. 12, doi:10.1186/1471-2105-1112-1385

  • Ponnusamy, L., Xu, N., Nojima, S., Wesson, D.M., Schal, C., Apperson, C.S. (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 105, 9262–9267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pozo, M.I., Lachance, M.A., Herrera, C.M. (2012) Nectar yeasts of two southern Spanish plants: the roles of immigration and physiological traits in community assembly. FEMS Microbiol. Ecol. 80, 281–293

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. ed.^eds.), p.^pp. R Foundation for Statistical Computing, Vienna.

  • Sanchez, M.G.D. (2011) Taste Perception in Honey Bees. Chem. Senses 36, 675–692

    Article  Google Scholar 

  • Schulz, S., Dickschat, J. (2007) Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24, 814–842

    Article  CAS  PubMed  Google Scholar 

  • Shade, A., McManus, P.S., Handelsman, J. (2013) Unexpected diversity during community succession in the apple flower microbiome. mBio 4, e00602–e00612

    Article  PubMed Central  PubMed  Google Scholar 

  • Stensmyr, M.C., Dweck, H.K.M., Farhan, A., Ibba, I., Strutz, A., Mukunda, L., Linz, J., Grabe, V., Steck, K., Lavista-Llanos, S., Wicher, D., Sachse, S., Knaden, M., Becher, P.G., Seki, Y., Hansson, B.S. (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345–1357

    Article  CAS  PubMed  Google Scholar 

  • van der Steen, J.J.M., Langerak, C.J., van Tongeren, C.A.M., Dik, A.J. (2004) Aspects of the use of honeybees and bumblebees as vector of antagonistic micro-organisms in plant disease control. Proc. Neth. Entomol. Soc. 15, 41–46

    Google Scholar 

  • Vannette, R.L., Gauthier, M.-P.L., Fukami, T. (2012) Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proc. R. Soc. B 280, 20122601

    Article  PubMed  Google Scholar 

  • Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang, C.-H., Crowley, D.E., Borneman, J., Keen, N.T. (2001) Microbial phyllosphere populations are more complex than previously realized. Proc. Natl. Acad. Sci. U. S. A. 98, 3889–3894

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Christina Loewel for helpful advices and Karl Köhrer for technical support. The project was supported by the Deutsche Forschungsgemeinschaft (DFG, JU 2856/1-1).

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Author notes

  1. Robert R. Junker

    Present address: Present Address: Department of Organismic Biology, University Salzburg, Hellbrunnerstr. 34, 5020, Salzburg, Austria

Authors and Affiliations

  1. Institute of Sensory Ecology, Department Biology, Heinrich-Heine University Düsseldorf, Universitätsstr. 1, 40225, Düsseldorf, Germany

    Robert R. Junker, Tanja Romeike & Daniela Langen

  2. DNA Analytics Core Facility, Department of Animal Ecology and Tropical Biology, University Würzburg, Am Hubland, 97074, Würzburg, Germany

    Alexander Keller

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  1. Robert R. Junker
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  2. Tanja Romeike
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Correspondence to Robert R. Junker.

Additional information

Manuscript editor: Bernd Grünewald

Réponses négatives densité-dépendantes des bourdons aux bactéries isolées à partir des fleurs

Aversion / bactérie / Bombus terrestris / interactions plante–bactérie–animal / PER / réflexe d’extension du proboscis

Hummeln vermeiden Bakterien auf Blüten in natürlichen Dichten

Abneigung / Bacilli / Bombus terrestris / Pflanzen–Bakterien–Tier Interaktionen / Rüsselreflex

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Junker, R.R., Romeike, T., Keller, A. et al. Density-dependent negative responses by bumblebees to bacteria isolated from flowers. Apidologie 45, 467–477 (2014). https://doi.org/10.1007/s13592-013-0262-1

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  • DOI: https://doi.org/10.1007/s13592-013-0262-1

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