Increased aggression and reduced aversive learning in honey bees exposed to extremely low frequency electromagnetic fields

English version

Autoři: Sebastian Shepherd ^aff001; Georgina Hollands ^aff001; Victoria C. Godley ^aff001; Suleiman M. Sharkh ^aff003; Chris W. Jackson ^aff001; Philip L. Newland ^aff001
Působiště autorů: Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom ^aff001; Department of Entomology, Purdue University, West Lafayette, Indiana, United States of America ^aff002; Mechatronics, Mechanical Engineering, University of Southampton, Highfield Campus, Southampton, United Kingdom ^aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223614

Souhrn

Honey bees, Apis mellifera, are a globally significant pollinator species and are currently in decline, with losses attributed to an array of interacting environmental stressors. Extremely low frequency electromagnetic fields (ELF EMFs) are a lesser-known abiotic environmental factor that are emitted from a variety of anthropogenic sources, including power lines, and have recently been shown to have a significant impact on the cognitive abilities and behaviour of honey bees. Here we have investigated the effects of field-realistic levels of ELF EMFs on aversive learning and aggression levels, which are critical factors for bees to maintain colony strength. Bees were exposed for 17 h to 100 μT or 1000 μT ELF EMFs, or a sham control. A sting extension response (SER) assay was conducted to determine the effects of ELF EMFs on aversive learning, while an intruder assay was conducted to determine the effects of ELF EMFs on aggression levels. Exposure to both 100 μT and 1000 μT ELF EMF reduced aversive learning performance by over 20%. Exposure to 100 μT ELF EMFs also increased aggression scores by 60%, in response to intruder bees from foreign hives. These results indicate that short-term exposure to ELF EMFs, at levels that could be encountered in bee hives placed under power lines, reduced aversive learning and increased aggression levels. These behavioural changes could have wider ecological implications in terms of the ability of bees to interact with, and respond appropriately to, threats and negative environmental stimuli.

Klíčová slova:

Aggression – Bees – Conditioned response – Honey bees – Learning – Pollution – Electromagnetic fields

Zdroje

1. Hayes J, Underwood RM, Pettis J. A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PLoS One, 2008;3(12): e4071. doi: 10.1371/journal.pone.0004071 19115015

2. Potts SG, Roberts SP, Dean R, Marris G, Brown MA, Jones R, et al. Declines of managed honey bees and beekeepers in Europe. J Apic Res. 2010;49(1): 15–22.

3. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One. 2017;12(10): e0185809. doi: 10.1371/journal.pone.0185809 29045418

4. Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 2015;347(6229): 1255957. doi: 10.1126/science.1255957 25721506

5. Shepherd S, Lima MA, Oliveira EE, Sharkh SM, Jackson CW, Newland PL. Extremely low frequency electromagnetic fields impair the cognitive and motor abilities of honey bees. Sci Rep. 2018;8(1): 7932. doi: 10.1038/s41598-018-26185-y 29785039

6. Wyszkowska J, Shepherd S, Sharkh S, Jackson CW, Newland PL. Exposure to extremely low frequency electromagnetic fields alters the behaviour, physiology and stress protein levels of desert locusts. Sci Rep. 2016;6: 36413. doi: 10.1038/srep36413 27808167

7. World Health Organization. Extremely low frequency fields—Environmental Health Criteria. Geneva: World Health Organization Press; 2007.

8. Dimitrijević D, Savić T, Anđelković M, Prolić Z, Janać B. Extremely low frequency magnetic field (50 Hz, 0.5 mT) modifies fitness components and locomotor activity of Drosophila subobscura. Int J Radiat Biol. 2014;90(5): 337–43. doi: 10.3109/09553002.2014.888105 24475738

9. Zmejkoski D, Petković B, Pavković-Lučić S, Prolić Z, Anđelković M, Savić T, 2017. Different responses of Drosophila subobscura isofemale lines to extremely low frequency magnetic field (50 Hz, 0.5 mT): fitness components and locomotor activity. Int J Radiat Biol. 2017;93(5): 544–52. doi: 10.1080/09553002.2017.1268281 27921519

10. Maliszewska J, Marciniak P, Kletkiewicz H, Wyszkowska J, Nowakowska A, Rogalska J. Electromagnetic field exposure (50 Hz) impairs response to noxious heat in American cockroach. J Comp Physiol A. 2018;204(6): 605–11.

11. Todorović D, Mirčić D, Ilijin L, Mrdaković M, Vlahović M, Prolić Z, et al. Effect of magnetic fields on antioxidative defense and fitness-related traits of Baculum extradentatum (insecta, phasmatodea). Bioelectromagnetics. 2012;33(3): 265–73. doi: 10.1002/bem.20709 21953292

12. Li SS, Zhang ZY, Yang CJ, Lian HY, Cai P. Gene expression and reproductive abilities of male Drosophila melanogaster subjected to ELF–EMF exposure. Mutat Res Genet Toxicol Environ Mutagen. 2013;758(1–2): 95–103.

13. Valadez-Lira JA, Medina-Chavez NO, Orozco-Flores AA, Heredia-Rojas JA, Rodriguez-de la Fuente AO, Gomez-Flores R, et al. Alterations of immune parameters on Trichoplusia ni (Lepidoptera: Noctuidae) larvae exposed to extremely low-frequency electromagnetic fields. Environ Entomol. 2017;46(2): 376–82. doi: 10.1093/ee/nvx037 28334331

14. Rogers LE, Warren JT, Hinds NR, Gano KA, Fitzner RE, Piepel GF. Environmental studies of a 1100-kV prototype transmission line: an annual report for the 1981 study period. Richland (WA): Battelle Pacific Northwest Laboratories; 1982.

15. Wellenstein G. The influence of high-tension lines on honeybee colonies (translation from the original German). J Appl Entomol. 1973;74: 86–94.

16. Morse RA, Hooper T. The Illustrated Encyclopedia of Beekeeping. lst ed. New York: Dutton Adult; 1985.

17. Greenberg B, Bindokas VP, Frazier MJ, Gauger JR. Response of honey bees, Apis mellifera L., to high-voltage transmission lines. Environ Entomol. 1981;10(5): 600–10.

18. Lee JM. Electrical and Biological Effects of Transmission Lines: A Review. Portland (OR): USDOE Bonneville Power Administration; 1989.

19. Wright GA, Mustard JA, Simcock NK, Ross-Taylor AA, McNicholas LD, Popescu A, et al. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr Biol. 2010;20(24): 2234–40. doi: 10.1016/j.cub.2010.11.040 21129969

20. Cappa F, Bruschini C, Protti I, Turillazzi S, Cervo R. Bee guards detect foreign foragers with cuticular chemical profiles altered by phoretic varroa mites. J Apic Res. 2016;55(3): 268–77.

21. Goulson D, O’Connor ST, Park KJ. The impacts of predators and parasites on wild bumblebee colonies. Ecol Entomol. 2018;43(2): 168–81.

22. Nouvian M, Reinhard J, Giurfa M. The defensive response of the honeybee Apis mellifera. J Exp Biol. 2016;219(22): 3505–17.

23. Tan K, Dong S, Li X, Liu X, Wang C, Li J, et al. Honey bee inhibitory signaling is tuned to threat severity and can act as a colony alarm signal. PLoS Biol. 2016;14(3): e1002423. doi: 10.1371/journal.pbio.1002423 27014876

24. Maschwitz UW. Alarm substances and alarm behaviour in social Hymenoptera. Nature. 1964;204(4956): 324.

25. Collins AM, Rinderer TE, Tucker KW, Sylvester HA, Lackett JJ. A model of honeybee defensive behaviour. J Apic Res. 1980;19(4): 224–31.

26. Núñez J, Maldonado H, Miralto A, Balderrama N. The stinging response of the honeybee: effects of morphine, naloxone and some opioid peptides. Pharmacol Biochem Behav. 1983;19(6): 921–4.

27. Vergoz V, Roussel E, Sandoz JC, Giurfa M. Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One. 2007;2(3): e288. doi: 10.1371/journal.pone.0000288 17372627

28. McNally GP, Westbrook RF. Predicting danger: the nature, consequences, and neural mechanisms of predictive fear learning. Learn Mem. 2006;13(3): 245–53. doi: 10.1101/lm.196606 16741278

29. Zhang E, Nieh JC. The neonicotinoid imidacloprid impairs honey bee aversive learning of simulated predation. J Exp Biol. 2015;218(20): 3199–205.

30. Breed MD. Nestmate recognition in honey bees. Anim Behav. 1983;31(1): 86–91.

31. Richard FJ, Holt HL, Grozinger CM. Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics. 2012;13(1): 558.

32. Li-Byarlay H, Rittschof CC, Massey JH, Pittendrigh BR, Robinson GE. Socially responsive effects of brain oxidative metabolism on aggression. Proc Natl Acad Sci USA. 2014;111(34): 12533–7. doi: 10.1073/pnas.1412306111 25092297

33. Rittschof CC, Coombs CB, Frazier M, Grozinger CM, Robinson GE. Early-life experience affects honey bee aggression and resilience to immune challenge. Sci Rep. 2015;5: 15572. doi: 10.1038/srep15572 26493190

34. Snodgrass RE. Anatomy and physiology of the honey bee. London: Constable and Company; 1956.

35. Dade HA. Anatomy and dissection of the honeybee. Cardiff: International Bee Research Association; 1962.

36. Ogawa H, Kawakami Z, Yamaguchi T. Motor pattern of the stinging response in the honeybee Apis mellifera. J Exp Biol. 1995;198(1): 39–47.

37. Menzel R, Müller U. Learning and memory in honeybees: from behavior to neural substrates. Annual Rev Neurosci. 1996;19(1): 379–404.

38. Hammer M. The neural basis of associative reward learning in honeybees. Trends Neurosci. 1997;20(6): 245–52. doi: 10.1016/s0166-2236(96)01019-3 9185305

39. Hammer M, Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem. 1998;5(1): 146–56.

40. Jarriault D, Fuller J, Hyland BI, Mercer AR. Dopamine release in mushroom bodies of the honey bee (Apis mellifera L.) in response to aversive stimulation. Sci Rep. 2018;8(1): 16277. doi: 10.1038/s41598-018-34460-1 30389979

41. Nouvian M, Mandal S, Jamme C, Claudianos C, d’Ettorre P, Reinhard J, et al. Cooperative defence operates by social modulation of biogenic amine levels in the honey bee brain. Proc Biol Sci. 2018;285(1871): 20172653. doi: 10.1098/rspb.2017.2653 29367399

42. Todorović D, Marković T, Prolić Z, Mihajlović S, Rauš S, Nikolić L, et al. The influence of static magnetic field (50 mT) on development and motor behaviour of Tenebrio (Insecta, Coleoptera). Int J Radiat Biol. 2013;89(1): 44–50. doi: 10.3109/09553002.2012.715786 22849716

43. Jankowska M, Pawlowska-Mainville A, Stankiewicz M, Rogalska J, Wyszkowska J. Exposure to 50 Hz electromagnetic field changes the efficiency of the scorpion alpha toxin. J Venom Anim Toxins Incl Trop Dis. 2015;21(1): 38.

44. Hermann HR. Sting autotomy, a defensive mechanism in certain social Hymenoptera. Insectes Soc. 1971;18(2): 111–20.

45. Cunard SJ, Breed MD. Post-stinging behavior of worker honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am. 1998;91(5): 754–7.

46. Russell KN, Ikerd H, Droege S. The potential conservation value of unmowed powerline strips for native bees. Biol Conserv. 2005;124(1):133–48.

47. Wojcik VA, Buchmann S. Pollinator conservation and management on electrical transmission and roadside rights-of-way: a review. J Pollinat Ecol. 2012;7.

48. Wagner DL, Ascher JS, Bricker NK. A transmission right-of-way as habitat for wild bees (Hymenoptera: Apoidea: Anthophila) in Connecticut. Ann Entomol Soc Am. 2014;107(6): 1110–20.

49. Berg Å, Bergman KO, Wissman J, Żmihorski M, Öckinger E. Power-line corridors as source habitat for butterflies in forest landscapes. Biol Conserv. 2016;201: 320–6.

50. Hill B, Bartomeus I. The potential of electricity transmission corridors in forested areas as bumblebee habitat. R Soc Open Sci. 2016;3(11): 160525. doi: 10.1098/rsos.160525 28018640

Increased aggression and reduced aversive learning in honey bees exposed to extremely low frequency electromagnetic fields

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