Skip to main content

Electromagnetic radiation of mobile telecommunication antennas affects the abundance and composition of wild pollinators

Journal of Insect Conservation volume 20, pages 315–324 (2016)Cite this article

Abstract

The exponential increase of mobile telephony has led to a pronounced increase in electromagnetic fields in the environment that may affect pollinator communities and threaten pollination as a key ecosystem service. Previous studies conducted on model species under laboratory conditions have shown negative effects of electromagnetic radiation (EMR) on reproductive success, development, and navigation of insects. However, the potential effects that widespread mobile telecommunication antennas have on wild pollinator communities outside the laboratory microcosm are still unknown. Here we studied the effects of EMR from telecommunication antennas on key wild pollinator groups (wild bees, hoverflies, bee flies, remaining flies, beetles, butterflies, and wasps). We measured EMR at 4 distances (50, 100, 200 and 400 m) from 10 antennas (5 on Limnos Island and 5 on Lesvos Island, eastern Mediterranean, Greece), and correlated EMR values with insect abundance and richness (the latter only for wild bees and hoverflies). All pollinator groups except butterflies were affected by EMR. In both islands, beetle, wasp, and hoverfly abundance decreased with EMR, whereas the abundance of underground-nesting wild bees and bee flies unexpectedly increased with EMR. The effect of EMR on the abundance of remaining flies differed between islands. With respect to species richness, EMR only tended to have a negative effect on hoverflies in Limnos. As EMR affected the abundance of several insect guilds negatively, and changed the composition of wild pollinators in natural habitats, it might also have additional ecological and economic impacts on the maintenance of wild plant diversity, crop production and human welfare.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aguilar R, Ashworth L, Galetto L, Aizen M (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980

    Article  PubMed  Google Scholar 

  • Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

  • Atli E, Ünlü H (2006) The effects of microwave frequency electromagnetic fields on the development of Drosophila melanogaster. Int J Radiat Biol 82:435–441

    CAS  Article  PubMed  Google Scholar 

  • Atli E, Ünlü H (2007) The effects of microwave frequency electromagnetic fields on the fecundity of Drosophila melanogaster. Turkish J Biol 31:1–5

    Google Scholar 

  • Balanis C (2005) Antenna theory: analysis and design, 3rd edn. Wiley, New York

    Google Scholar 

  • Balmori A (2015) Anthropogenic radiofrequency electromagnetic fields as an emerging threat to wildlife orientation. Sci Total Environ 518–519:58–60

    Article  PubMed  Google Scholar 

  • Barton K (2014) MuMIn: Multi-model inference. R package version 1.10.0. Retrieved May 14, 2014, from http://cran.r-project.org/package=MuMIn

  • Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    CAS  Article  PubMed  Google Scholar 

  • Bjørnstad ON, Falck W (2001) Non-parametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70

    Article  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615

    CAS  Article  PubMed  Google Scholar 

  • Cammaerts M-C, Johansson O (2014) Ants can be used as bio-indicators to reveal biological effects of electromagnetic waves from some wireless apparatus. Electromagn Biol Med 33:282–288

    CAS  Article  PubMed  Google Scholar 

  • Cammaerts M-C, De Doncker P, Patris X, Bellens F, Rachidi Z, Cammaerts D (2012) GSM 900 MHz radiation inhibits ants’ association between food sites and encountered cues. Electromagn Biol Med 31:151–165

    Article  PubMed  Google Scholar 

  • Cammaerts M-C, Vandenbosch GAE, Volski V (2014) Effect of short-term GSM radiation at representative levels in society on a biological model: the ant Myrmica sabuleti. J Insect Behav 27:514–526

    Article  Google Scholar 

  • Chavdoula ED, Panagopoulus DJ, Margaritis LH (2010) Comparison of biological effects between continuous and intermittent exposure to GSM-900-MHz mobile phone radiation: detection of apoptotic cell-death features. Mutat Res 700:51–61

    CAS  Article  PubMed  Google Scholar 

  • Chittka L, Thomson JD (2001) Cognitive ecology of pollination. Cambridge University Press, Cambridge

  • Cucurachi S, Tamis WLM, Vijver MG, Peijnenburg WJGM, Bolte JFB, de Snoo GR (2013) A review of the ecological effects of radiofrequency electromagnetic fields (RF-EMF). Environ Int 51:116–140

    CAS  Article  PubMed  Google Scholar 

  • Dasdag S, Akdag MZ, Aksen F, Bashan M, Buyukbayram H (2004) Does 900 MHZ GSM mobile phone exposure affect rat brain? Electromagn Biol Med 23(3):201–214

    CAS  Article  Google Scholar 

  • Favre D (2011) Mobile phone-induced honeybee worker piping. Apidologie 42:270–279

    Article  Google Scholar 

  • Flüge S (2004) EMR-TS PC Transfer Set Narda Safety Test Solutions GmbH. BN 2244/90.36. Version 1.02 ff. http://www.narda-sts.us/software/Narda_EMR.zip

  • Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821

    Article  Google Scholar 

  • Goldsmith A (2005) Wireless communications. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208

    CAS  Article  PubMed  Google Scholar 

  • Harst W, Kuhn J, Stever H (2006) Can electromagnetic exposure cause a change in behaviour? Studying possible non-thermal influences on honeybees—an approach within the framework of educational informatics. Acta Syst IIAS Int J 6(1):1–6

    Google Scholar 

  • Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195

    Article  PubMed  Google Scholar 

  • Kearns C, Inouye D, Waser N (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kirschvink JL, Walker MM, Diebel C (2001) Magnetite-based magnetoreception. Curr Opin Neurobiol 11:462–467

    CAS  Article  PubMed  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Dewenter IS, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 274:303–313

    Article  Google Scholar 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314

    Article  PubMed  Google Scholar 

  • Lázaro A, Tscheulin T, Devalez J, Nakas G, Petanidou T (2016) Effects of grazing intensity on pollinator abundance and diversity, and on pollination services. Ecol Entom. doi:10.1111/een.12310

    Google Scholar 

  • Lever JJ, van Nes EH, Scheffer M, Bascompte J (2014) The sudden collapse of pollinator communities. Ecol Lett 17:350–359

    Article  PubMed  Google Scholar 

  • Löscher W, Käs G (1998) Behavioural abnormalities in a dairy cow herd near a TV and radio transmitting antenna. Prakt Tierarzt 79:437

    Google Scholar 

  • Marks TA, Ratke CC, English WO (1995) Stray voltage and developmental, reproductive and other toxicology problems in dogs, cats and cows—a discussion. Vet Hum Toxicol 37:163–172

    CAS  PubMed  Google Scholar 

  • Maskey D, Kim M, Aryal B, Pradhan J, Choi I-Y, Park K-S, Son T, Hong S-Y, Kim SB, Kim HG, Kim MJ (2010) Effect of 835 MHz radiofrequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain Res 1313:232–241

    CAS  Article  PubMed  Google Scholar 

  • Maskey D, Kim H-J, Kim HG, Kim MJ (2012) Calcium-binding proteins and GFAP immunoreactivity alterations in murine hippocampus after 1 month of exposure to 835 MHz radiofrequency at SAR values of 1.6 and 4.0 W/kg. Neurosci Lett 506:292–296

    CAS  Article  PubMed  Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. John Hopkins University Press, Baltimore

    Google Scholar 

  • Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A-M, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314

    Article  PubMed  Google Scholar 

  • Müller A (2015) Palaearctic osmiine bees. ETH Zürich. http://blogs.ethz.ch/osmiini

  • Narayanan SN, Kumar RS, Karun KM, Nayak SB, Bhat PG (2015) Possible cause for altered spatial cognition of prepubescent rats exposed to chronic radiofrequency electromagnetic radiation. Metab Brain Dis 30(5):1193–1206

    CAS  Article  PubMed  Google Scholar 

  • Nielsen A, Steffan-Dewenter I, Westphal C, Messinger O, Potts SG, Roberts SPM, Settele J, Szentgyorgyi H, Vaissière BE, Vaitis M, Woyciechowski M, Bazos I, Biesmeijer JC, Bommarco R, Kunin WE, Tscheulin T, Lamborn E, Petanidou T (2011) Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques. Ecol Res 26:969–983

    Article  Google Scholar 

  • Panagopoulos DJ, Margaritis LH (2010) The effect of exposure duration on the biological activity of mobile telephony radiation. Mutat Res 699:17–22

    CAS  Article  PubMed  Google Scholar 

  • Panagopoulos DJ, Karabarbounis A, Margaritis LH (2004) Effect of GSM 900-MHz mobile phone radiation on the reproductive capacity of Drosophila melanogaster. Electromagn Biol Med 23:29–43

    Article  Google Scholar 

  • Panagopoulos DJ, Chavdoula ED, Nezis IP, Margaritis LH (2007) Cell death induced by GSM 900-MHz and DCS 1800-MHz mobile telephony radiation. Mutat Res 626:69–78

    CAS  Article  PubMed  Google Scholar 

  • Panagopoulos DJ, Chavdoula ED, Margaritis LH (2010) Bioeffects of mobile telephony radiation in relation to its intensity or distance from the antenna. Int J Radiat Biol 86:345–357

    CAS  Article  PubMed  Google Scholar 

  • Pauw A (2007) Collapse of a pollination web in small conservation areas. Ecology 88:1759–1769

    Article  PubMed  Google Scholar 

  • Petanidou T, Ellis WN (1993) Pollinating fauna of a phryganic ecosystem: composition and diversity. Biodiv Lett 1:9–22

    Article  Google Scholar 

  • Petanidou T, Ståhls G, Vujić A, Olesen JM, Rojo S, Thrasyvoulou A, Sgardelis S, Kallimanis AS, Kokkini S, Tscheulin T (2013) Investigating plant–pollinator relationships in the Aegean: the approaches of the project POL-AEGIS (The Pollinators of the Aegean Archipelago: Diversity and Threats). J Apicult Res 52:106–117

    Article  Google Scholar 

  • Potts SG, Petanidou T, Roberts S, O’Toole C, Hulbert A, Willmer P (2006) Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Conserv 129:519–529

    Article  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Sahib SS (2011) Impact of mobile phones on the density of honeybees. J Public Adm Policy Res 3:131–137

    Google Scholar 

  • Sahin A, Aslan A, Bas O, Ikinci A, Özyilmaz C, Sönmez OF, Çolakoglu OE (2015) Deleterious impacts of a 900-MHz electromagnetic field on hippocampal pyramidal neurons of 8-week-old Sprague Dawley male rats. Brain Res 1624:232–238

    CAS  Article  PubMed  Google Scholar 

  • Sharma VP, Kumar NR (2010) Changes in honeybee behaviour and biology under the influence of cellphone radiations. Curr Sci 98:1376–1378

    Google Scholar 

  • Tscheulin T, Spyropoulos A, Petanidou T (2010) Impacts of mobile phone masts on the abundance of pollinators. In: 5th Conference of the Hellenic Ecological Society, Patras, p 201

  • Vácha, M, Půžová T, Kvíčalová M (2009) Radio-frequency magnetic fields disrupt magnetoreception in American cockroach. J Exp Biol 212:3473–3477

    Article  PubMed  Google Scholar 

  • Válková T, Vácha M (2012) How do honeybees use their magnetic compas? Can they see the North? Bull Entomol Res 102:461–467

    Article  PubMed  Google Scholar 

  • Vijver MG, Bolte JFB, Evans TR, Tamis WLM, Peijnenburg WJGM, Musters CJM, de Snoo GR (2013) Investigating short-term exposure to electromagnetic fields on reproductive capacity of invertebrates in the field situation. Electromagn Biol Med 33(1):21–28

    Article  PubMed  Google Scholar 

  • Wajnberg E, Acosta-Avalos D, Alves OC, de Oliviera JF, Srygley RB, Esquivel DM (2010) Magnetoreception in eusocial insects: an update. J R Soc Interface 7:S207–S225

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Warnke U (2009) Bees, birds and mankind: destroying nature by ‘Electrosmog’ effects of wireless communication technologies. A Brochure series by the competence initiative for the protection of humanity, environment and democracy, Kempten, 1st edn, November 2007, ISBN: 978-3-00-023124-7, English edn, March 2009, pp 14–33

  • Weisbrot D, Lin H, Ye L, Blank M, Goodman R (2003) Effects of mobile phone radiation on reproduction and development in Drosophila melanogaster. J Cell Biochem 89:48–55

    CAS  Article  PubMed  Google Scholar 

  • Westphal C, Bommarco R, Carre G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyorgyi H, Tscheulin T, Vaissière BE, Woyciechowski M, Biesmeijer JC, Kunin WE, Settele J, Steffan-Dewenter I (2008) Measuring bee biodiversity in different European habitats and biogeographical regions. Ecol Monogr 78:653–671

    Article  Google Scholar 

  • Yeates DK, Greathead DJ (1997) The evolutionary pattern of host use in the Bombyliidae (Diptera): a diverse family of parasitoid flies. Biol J Linn Soc 60:149–185

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  • Zuur AF, Hilbe JM, Ieno EN (2013) Beginner’s guide to GLM and GLMM with R. Highland Statistics, Newburgh

    Google Scholar 

Download references

Acknowledgments

The research has been co-financed by the European Union (European Social Fund—ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF)—Research Funding Program: THALES: Investing in knowledge society through the European Social Fund. We would like to thank W. Arens, H. Dathe, J. Dils, A. Ebmer, M. Kuhlmann, V. Mizerakis, A. Mueller, A. Pauly, C. Praz, M. Quaranta, S. Risch, W. Schedl, E. Scheuchl, M. Schwarz, M. Terzo and A. Vujic for insect identification.

Author information

Authors and Affiliations

  1. Laboratory of Biogeography and Ecology, Department of Geography, University of the Aegean, University Hill, 81100, Mytilene, Greece

    A. Lázaro, A. Chroni, T. Tscheulin, J. Devalez & T. Petanidou

  2. Mediterranean Institute for Advanced Studies, C/Miquel Marquès 21, 07190, Esporles, Balearic Islands, Spain

    A. Lázaro

  3. Department of Environment, University of the Aegean, University Hill, 81100, Mytilene, Greece

    C. Matsoukas

Authors
  1. A. Lázaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Chroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Tscheulin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Devalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Matsoukas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Petanidou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Lázaro.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1063 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lázaro, A., Chroni, A., Tscheulin, T. et al. Electromagnetic radiation of mobile telecommunication antennas affects the abundance and composition of wild pollinators. J Insect Conserv 20, 315–324 (2016). https://doi.org/10.1007/s10841-016-9868-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-016-9868-8

Keywords

  • Bee flies
  • Beetles
  • Butterflies
  • Distance to the antenna
  • Electromagnetic smog
  • EMR
  • Hoverflies
  • Species richness
  • Wasps
  • Wild bees