Magnetoreception in Social Wasps: An Update

Maria da Graça Cardoso Pereira-Bomfim; William Fernando Antonialli-Junior; Daniel Acosta-Avalos

doi:10.12741/ebrasilis.v9i1.526

Authors

Maria da Graça Cardoso Pereira-Bomfim Universidade Federal da Grande Dourados
William Fernando Antonialli-Junior Universidade Estadual de Mato Grosso do Sul
Daniel Acosta-Avalos Centro Brasileiro de Pesquisas Físicas

DOI:

https://doi.org/10.12741/ebrasilis.v9i1.526

Keywords:

Hymenoptera, Magnetic Field, Magnetosensibility, Vespidae, Campo Magnético, Magnetossensibilidade, Vespidae.

Abstract

Abstract. Magnetoreception is a mechanism of active orientation that occurs in animals with nervous systems. Social insects such as bees, ants, wasps and termites have been studied on the influence of the magnetic field exerts on its biology. The social wasps comprise species represented in Stenogastrinae, Vespinae and Polistinae, however studies on the influence of magnetic field on wasps Vespinae address only. The areas studied include the biomineralization of magnetic material and behavioral aspects related to changes in local intensity of the geomagnetic field. The objective of this review is to integrate knowledge of social wasps’ magnetoreception in order to build an instructive overview of the current situation of studies, therefore, provide the conceptual framework for the development of future work on the topic.

Magnetorrecepção em Vespas Sociais: Uma Atualização

Resumo. Magnetorrecepção é um mecanismo de orientação ativa que ocorre em animais com sistema nervoso. Insetos sociais tais como abelhas, formigas, vespas e cupins são estudados sobre a influência que o campo magnético exerce em sua biologia. As vespas sociais compreendem espécies representadas em Stenogastrinae, Vespinae e Polistinae, no entanto os estudos sobre a influência do campo magnético em vespas abordam somente Vespinae. As áreas de estudo incluem a biomineralização do material magnético e aspectos comportamentais relacionados a mudanças na intensidade do campo geomagnético local. O objetivo desta revisão é integrar o conhecimento sobre magnetorrecepção em vespas sociais, a fim de construir um panorama elucidativo da atual situação dos estudos, e assim fornecer uma estrutura conceitual para o desenvolvimento de trabalhos futuros sobre o tema.

References

Abra

Acosta-Avalos, D., D.M.S. Esquivel, E. Wajnberg, H.G.P. Lins de Barros, P.S. Oliveira & I. Leal, 2001. Seasonal patterns in the orientation system of the migratory ant Pachycondyla marginata. Naturwissenschaften, 88: 343-346. DOI:

http://dx.doi.org/10.1007/s001140100245.

Acosta-Avalos, D., E. Wajnberg, D.M.S. Esquivel & L.J. El-Jaick, 2000. Insetos sociais: um exemplo de magnetismo animal. Revista Brasileira de Ensino de F

Alves, O.C., E. Wajnberg, J.F. Oliveira & D.M.S. Esquivel, 2004. Magnetic material arrangement in oriented termites: a magnetic resonance study. Journal of Magnetic Resonance, 168: 246-251. DOI: http://dx.doi.org/10.1016/j.jmr.2004.03.010.

Anderson, J.B. & R.K. Vander der Meer, 1993. Magnetic orientation in fire ant, Solenopsis invicta. Naturwissenschaften, 80: 568-570. DOI: http://dx.doi.org/10.1007/BF01149274.

Banks, A.N. & R.B. Srygley, 2003. Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae). Ethology, 109: 835-846. DOI: http://.doi.org/10.1046/j.0179-1613.2003.00927.x.

Bean, C.P. & J.D. Livingston, 1959. Superparamagnetism. Journal of Applied Physics, 30: S120-S129.

Bellini, S., 2009. On a unique behavior of freshwater bacteria. Chinese Journal of Oceanology and Limnology, 27: 3-5.

Blackemore, R.P., 1975. Magnetotactic bacteria. Science, 19: 377-379. DOI: http://dx.doi.org/10.1126/science.170679.

Camlitepe, Y. & D.J. Stradling, 1995. Wood ants orient to magnetic fields. Proceedings of the Royal Society of London, 261: 37-41. DOI: http://dx.doi.org/10.1098/rspb.1995.0114.

Carpenter, J.M, 1982. The philogenetic relationships and natural classification of the Vespoidea (Hymenoptera). Systematic Entomology, 7: 11-38. DOI: http://dx.doi.org/10.1111/j.1365-3113.1982.tb00124.x.

Carpenter, J.M. & O.M. Marques, 2001. Contribui

El-Jaick, L.J., D. Acosta-Avalos, D.M.S. Esquivel, E. Wajnberg & M.P. Linhares, 2001. Electron paramagnetic resonance study of Honeybee Apis mellifera abdomens. European Biophysics Journal, 29: 579-586. DOI: http://dx.doi.org/10.1007/s002490000115.

Esquivel, D.M.S., D. Acosta-Avalos, L.J. El-Jaick, A.D.M. Cunha, M.G. Malheiros, E. Wajnberg & M.P. Linhares, 1999. Evidence for magnetic material in the fire ant Solenopsis sp. By Electron Paramagnetic Resonance measurements. Naturwissenschaften, 86: 30-32. DOI: http://dx.doi.org/10.1007/s001140050564.

Ferreira, J., G. Cernicchiaro, M. Winklhofer, H. Dutra, P.S. Oliveira, D.M.S. Esquivel, E. Wajnberg, 2005. Comparative magnetic measurements on social insects. Journal of Magnetism and Magnetic Materials, 289: 442-444.

Frier, H.J., E. Edwards, C. Smith, S. Neale & T.S. Collet, 1996. Magnetic compass cues and visual pattern learning in honeybees. Journal of Experimental Biology, 199: 1353-1361.

Gould, J.L., 2008. Animal navigation: the evolution of magnetic orientation. Current Biology, 18: R482-R484. DOI:

http://dx.doi.org/10.1016/j.cub.2008.03.052.

Gould, J.L., J.L. Kirschvink & K.S. Deffyes, 1978. Bees have magnetic remanence. Science, 201: 1026-1028. DOI:

http://dx.doi.org/10.1126/science.201.4360.1026.

Gould, J.L., J.L. Kirschvink, K.S. Deffeyes & M.L. Brines, 1980. Orientation of Demagnetized Bees. Journal of Experimental Biology, 86: 1-8.

Hepworth, D., R.S. Pickard & K.J. Overshott, 1980. Effects of the periodically intermittent application of a constant magnetic field on the mobility in darkness of worker honeybees. Journal of Apicultural Research, 19: 179-186.

Hsu, C.Y. & C.W. Li, 1994. Magnetoreception in honeybees. Science, 265: 95-96. DOI: http://dx.doi.org/10.1126/science.265.5168.95.

Hsu, C.Y., 2002. Magnetic remanence in common hornet (Vespa aff?nis). Journal of Minghsin Institute of Technology, 28: 181-186.

Hsu, C.Y., 2004. The process of iron deposition in the common hornet (Vespa affinis). Biology of the Cell, 96: 529-537. DOI: http://dx.doi.org/10.1016/j.biolcel.2004.05.001.

Ishay, J. & D. Sadeh, 1975. Direction finding by hornets under gravitational and centrifugal forces. Science, 190: 802-804. DOI: http://dx.doi.org/10.1126/science.1198099.

Ishay, J.S., Z. Barkay, N. Eliaz, M. Plotkin, S. Volynchik & D.J. Bergman, 2008. Gravity orientation in social wasp comb cells (Vespinae) and the possible role of embedded minerals. Naturwissenschaften, 95: 333-342. DOI: http://dx.doi.org/10.1007/s00114-007-0334-z.

Jander, R. & U. Jander, 1998. The light and magnetic compass of the weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae). Ethology, 104: 743-758.

Jardine, M., 2010. Sunscreen for the young earth. Science, 327: 1206-1207.

Johnsen, S. & K.J. Lohmann, 2005. The physics and neurobiology of magnetoreception. Nature Reviews Neuroscience 6, 703-712. DOI: http://dx.doi.org/10.1038/nrn1745.

Kirschvink, J.L., A.K. Kirschvink & B. Woodford, 1992. Magnetite biomineralization in the human brain. Proceedings of the National Academy of Sciences USA, 26: 7683-7687.

Kisliuk, M. & J. Ishay, 1977. Influence of an additional magnetic field on hornet nest architecture. Experientia, 33: 885-887.

Korall, H., T. Leucht & H. Martin, 1988. Bursts of magnetic fields induce jumps of misdirection in bees by a mechanism of magnetic resonance. Journal of Comparative Physiology A, 162: 279-284.

Kuterbach, D.A. & B. Walcott, 1986. Iron containing cells in the honeybee (Apis mellifera). I. Adult morphology and physiology. Journal of Experimental Biology, 126: 375-387.

Lindauer, M. & H. Martin, 1968. Die Schwereoientierung der Biene unter dem Einfluss des Erdmagnetfelds. Zeitschrift fur vergleichende physiologie, 60: 219-243.

Lohmann, K.J. & S. Johnsen, 2000. The neurobiology of magnetoreception in vertebrate animals. Tins - Trends in Neurosciences, 23: 153-159.

Lucano, M.J., G. Cernicchiaro, E. Wajnberg & D.M.S. Esquivel, 2006. Stingless Bee Antennae: a magnetic sensory organ? BioMetals, 19: 295-300. DOI: http://dx.doi.org/10.1007/s10534-005-0520-4.

Martin, H. & M. Lindauer, 1977. Der Einflu? des Erdmagnetfeldes auf die Schwereorientierung der Honigbiene (Apis mellifica). Journal of Comparative Physiology A, 122: 145-187.

Martin, H., H. Korall & B. Forster, 1989. Magnetic field effects on activity and ageing in honeybees. Journal of Comparative Physiology A, 164: 423-431.

Oliveira, J.F., E. Wajnberg, D.M. Esquivel, S. Weinkauf, M. Winklhofer, M. Hanzlik, 2010. Ant antennae: are they sites for magnetoreception? Journal of the Royal Society, Interface 7: 143-152. DOI: http://dx.doi.org/10.1098/rsif.2009.0102.

Paz, H., M.A. Vargas, O.A. Forero, J.F. Pab

Pereira-Bomfim, M.G.C., W.F. Antonialli-Junior, D. Acosta-Avalos, 2015. Effect of magnetic field on the foraging rhythm and behavior of the swarm-founding paper wasp Polybia paulista Ihering (Hymenoptera: Vespidae). Sociobiology, 62: 99-104.

Sandoval, E.L., E. Wajnberg, D.M.S. Esquivel, H. Lins de Barros & D. Acosta-Avalos, 2012. Magnetic orientation in Solenopsis sp. ants. Journal of Insect Behavior, 25: 612-619.

Schiff, H. & G. Canal, 1993. The magnetic and electric ?elds induced by superparamagnetic magnetite in honeybees. Biological Cybernetics, 69: 7-17.

Schiff, H., 1991. Modulation of spike frequencies by varying the ambient magnetic field and magnetite candidates in bees (Apis mellifera). Comparative Biochemistry and Physiology A, 4: 975-985. DOI: http://dx.doi.org/10.1016/0300-9629(91)90325-7.

Shcherbakov, V.P. & M. Winklhofer, 1999. The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. European Biophysics Journal, 28: 380-392. DOI: http://dx.doi.org/10.1007/s002490050222.

Skiles, D.D., 1985. The geomagnetic field: its nature, history and biological relevance, p. 43-102. In: Kirschvink, J.L., D.S. Jones & B.J. MacFadden, (Eds.). Magnetite Biomineralization and Magnetoreception in Organisms. A new biomagnetism. New York, Plenum Press, 682p.

Stokroos, I., L. Litinetsky, J.J.L.Van der Want & J.S. Ishay, 2001. Keystone-like crystals in cells of hornet combs. Nature, 411: 654.

Towne, W.F. & J.L. Gould, 1985. Magnetic field sensitivity in honeybees, p. 385-406. In: Magnetite Biomineralization and Magnetoreception in Organisms. A new biomagnetism. Kirschvink, J. L., Jones, D.S. & MacFadden B.J. (Eds). Plenum Press

V

Wajnberg, E., D. Acosta-Avalos, L.J. El-Jaick, L.G. Abra

Wajnberg, E., D. Acosta-Avalos, O.C. Alves, J.F. Oliveira, R.B. Srygley & D.M.S. Esquivel, 2010. Magnetoreception in eusocial insects: an update. Journal of the Royal Society Interface, 7: S207-S226. DOI: http://dx.doi.org/10.1098/rsif.2009.0526.focus.

Wajnberg, E., G. Cernicchiaro & D.M.S. Esquivel, 2004. Antennae: the strongest magnetic part of the migratory ant. BioMetals, 17: 467-470. DOI: http://dx.doi.org/10.1023/B:BIOM.0000029443.93732.62.

Walcott, B., 1985. The cellular localization of particulate iron, p. 417-438. In: Kirschvink, J.L., D.S. Jones & B.J. MacFadden (Eds.). Magnetite biomineralization and magnetoreception in organisms: A new biomagnetism. New York, Plenum Press. 682p.

Walker, M.M. & M.E. Bitterman, 1985. Conditioned responding to magnetic ?eld by honeybees. Journal of Comparative Physiology A, 157: 67-71. DOI: http://dx.doi.org/10.1007/BF00611096.

Wiltschko, W. & R. Wiltschko, 2006. Magnetoreception. BioEssays, 28: 157-168.