Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae)

R.B. Srygley, R. Dudley, E.G. Oliveira, A.J. Riveros

Resultado de la investigación: Contribución a RevistaArtículo

29 Citas (Scopus)

Resumen

We tested whether migrating Aphrissa statira butterflies orient with a magnetic compass. We captured migrants flying over Lake Gatún, Panama, and exposed experimental butterflies to a strong magnetic field. These and unmanipulated control butterflies were released back over the lake. Experimental butterflies had a more dispersed pattern of orientation than control butterflies. The average direction adopted was northeast, 160° anticlockwise to the natural migratory direction. Unmanipulated control butterflies adopted two diametrically opposed orientations: one shifted 33° clockwise, and another 147° anticlockwise, to the migratory direction. Control and experimental butterflies differed in that some controls oriented towards the migratory direction. These differences in orientation support the hypothesis of a sense for magnetic orientation cues. Unmanipulated butterflies released over the lake when the sky was completely overcast were significantly oriented towards their direction before capture (187° and 203°, respectively), further supporting the magnetic compass hypothesis. In a third experiment, we obstructed sun compass cues and reversed the horizontal component of the local geomagnetic field to position magnetic north towards the geographical south pole within a flight arena into which we released individual butterflies. Experimental butterflies experiencing the reversed magnetic field oriented on average 180° opposite to their natural migratory direction. Control butterflies, for which the position of magnetic north was unaltered, were oriented both towards and 180° opposite to the natural migratory direction. This difference between orientations of control and experimental butterflies also supports the hypothesis of a sense for magnetic orientation cues. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Idioma originalEnglish (US)
Páginas (desde-hasta)183-191
Número de páginas9
PublicaciónAnimal Behaviour
Volumen71
N.º1
DOI
EstadoPublished - 2006

Huella dactilar

Pieridae
butterfly
butterflies
Lepidoptera
magnetic fields
lakes
lake
flight
magnetic field
Panama
geomagnetic field

Citar esto

Srygley, R.B. ; Dudley, R. ; Oliveira, E.G. ; Riveros, A.J. / Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae). En: Animal Behaviour. 2006 ; Vol. 71, N.º 1. pp. 183-191.
@article{2b02f456adc94075acf8e772dd5d63b2,
title = "Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae)",
abstract = "We tested whether migrating Aphrissa statira butterflies orient with a magnetic compass. We captured migrants flying over Lake Gat{\'u}n, Panama, and exposed experimental butterflies to a strong magnetic field. These and unmanipulated control butterflies were released back over the lake. Experimental butterflies had a more dispersed pattern of orientation than control butterflies. The average direction adopted was northeast, 160° anticlockwise to the natural migratory direction. Unmanipulated control butterflies adopted two diametrically opposed orientations: one shifted 33° clockwise, and another 147° anticlockwise, to the migratory direction. Control and experimental butterflies differed in that some controls oriented towards the migratory direction. These differences in orientation support the hypothesis of a sense for magnetic orientation cues. Unmanipulated butterflies released over the lake when the sky was completely overcast were significantly oriented towards their direction before capture (187° and 203°, respectively), further supporting the magnetic compass hypothesis. In a third experiment, we obstructed sun compass cues and reversed the horizontal component of the local geomagnetic field to position magnetic north towards the geographical south pole within a flight arena into which we released individual butterflies. Experimental butterflies experiencing the reversed magnetic field oriented on average 180° opposite to their natural migratory direction. Control butterflies, for which the position of magnetic north was unaltered, were oriented both towards and 180° opposite to the natural migratory direction. This difference between orientations of control and experimental butterflies also supports the hypothesis of a sense for magnetic orientation cues. {\circledC} 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.",
author = "R.B. Srygley and R. Dudley and E.G. Oliveira and A.J. Riveros",
note = "Cited By :22 Export Date: 17 April 2018 CODEN: ANBEA Correspondence Address: Srygley, R.B.; Smithsonian Tropical Research Institute, Apdo. 2072, Balboa, Panama; email: bob.srygley@zoo.ox.ac.uk Funding details: CNPq, Conselho Nacional de Desenvolvimento Cient{\'i}fico e Tecnol{\'o}gico Funding details: National Geographic Society Funding details: STRI, Smithsonian Tropical Research Institute Funding text: This research was funded with a grant from the National Geographic Society Committee for Research and Exploration. In addition, R.B.S. was supported by a Senior Postdoctoral Fellowship from the Smithsonian Institution Office of Fellowships and Grants, Washington, DC and the Korean Science and Engineering Foundation supported preparation of the manuscript. E.G.O. was supported by a CNPq Postdoctoral Fellowship. We thank the National Geographic Society and the Smithsonian Tropical Research Institute for their continued support. We also thank Alejandro Almanza and Ana Portugal for recording behaviour of butterflies in the electromagnet. References: Able, K.P., Able, M.A., Daytime calibration of magnetic orientation in a migratory bird requires a view of skylight polarization (1993) Nature, 364, pp. 523-525; Able, K.P., Able, M.A., Evidence for calibration of magnetic migratory orientation in Savannah sparrows reared in the field (1999) Proceedings of the Royal Society of London, Series B, 266, pp. 1477-1481; Arendse, M.C., Magnetic field detection is distinct from light detection in the invertebrates Tenebrio and Talitrus (1978) Nature, 274, pp. 358-362; Baker, R.R., Integrated use of moon and magnetic compasses by the heart-and-dart moth, Agrotis exclamationis (1987) Animal Behaviour, 35, pp. 94-101; Baker, R.R., Mather, J.G., Magnetic compass sense in the large yellow underwing moth, Noctua pronuba L (1982) Animal Behaviour, 30, pp. 543-548; Banks, A.N., Srygley, R.B., Orientation of foraging leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae: Attinae), is shifted by a local reversal of the earth's magnetic field (2003) Ethology, 109, pp. 835-846; Batschelet, E., (1981) Circular Statistics in Biology, , Academic Press London; Beason, R.C., Dussourd, N., Deutschlander, M.E., Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird (1995) Journal of Experimental Biology, 198, pp. 141-146; Boles, L.C., Lohmann, K.J., True navigation and magnetic maps in spiny lobsters (2003) Nature, 421, pp. 60-63; Brower, L.P., Monarch butterfly orientation: Missing pieces of a magnificent puzzle (1996) Journal of Experimental Biology, 199, pp. 93-103; Camlitepe, Y., Stradling, D., Wood ants orient to magnetic fields (1995) Proceedings of the Royal Society of London, Series B, 261, pp. 37-41; Deutschlander, M.E., Phillips, J.B., Borland, S.C., The case for light-dependent magnetic orientation in animals (1999) Journal of Experimental Biology, 202, pp. 891-908; Esquivel, D.M.S., Acosta-Avalos, D., El-Jaick, L.J., Cunha, A.D.M., Malheiros, M.G., Wajnberg, E., Linhares, M.P., Evidence for magnetic material in the fire ant Solenopsis sp. by electron paramagnetic resonance measurements (1999) Naturwissenschaften, 86, pp. 30-32; Froy, O., Gotter, A.L., Casselman, A.L., Reppert, S.M., Illuminating the circadian clock in monarch butterfly migration (2003) Science, 300, pp. 1303-1305; Gould, J.L., Kirschvink, J.L., Deffeyes, K.S., Brines, M.L., Orientation of demagnetized bees (1980) Journal of Experimental Biology, 86, pp. 1-8; Jones, D.S., MacFadden, B.J., Induced magnetization in the monarch butterfly, Danaus plexippus (Insecta, Lepidoptera) (1982) Journal of Experimental Biology, 96, pp. 1-9; Jungreis, S.A., Biomagnetism: An orientation mechanism in migrating insects? (1987) Florida Entomologist, 70, pp. 277-283; Kirschvink, J.L., Uniform magnetic fields and double-wrapped coil systems: Improved techniques for the design of biomagnetic experiments (1992) Bioelectromagnetics, 13, pp. 401-411; Lindauer, M., Martin, H., Die Schwereorientierung der Bienen unter dem Einfluss der Erdmagnetfelder (1968) Zeitschrift f{\"u}r Vergleichende Physiologie, 60, pp. 219-243; Lohmann, K.J., Pentcheff, N.D., Nevitt, G.A., Stetten, G.D., Zimmerfaust, R.K., Jarrard, H.E., Boles, L.C., Magnetic orientation of spiny lobsters in the ocean: Experiments with undersea coil systems (1995) Journal of Experimental Biology, 198, pp. 2041-2048; Merritt, R., Purcell, C., Stroink, G., Uniform magnetic field produced by three, four, and five square coils (1983) Review of Scientific Instruments, 54, pp. 879-882; Mouritsen, H., Frost, B.J., Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms (2002) Proceedings of the National Academy of Sciences, U.S.A., 99, pp. 10162-10166; Oliveira, E.G., Srygley, R.B., Dudley, R., Do Neotropical migrant butterflies navigate using a solar compass? (1998) Journal of Experimental Biology, 201, pp. 3317-3331; Peddie, N.W., (1993) The Magnetic Field of the Earth: 1990 Declination Chart, , US Department of Interior, US Geological Survey Reston, Virginia; Perez, S.M., Taylor, O.R., Jander, R., The effect of a strong magnetic field on monarch butterfly (Danaus plexippus) migratory behavior (1999) Naturwissenschaften, 86, pp. 140-143; Schmitt, D.E., Esch, H.E., Magnetic orientation of honeybees in the laboratory (1993) Naturwissenschaften, 80, pp. 41-43; Spieth, H.R., Kaschuba-Holtgrave, A., A new experimental approach to investigate migration in Pieris brassicae L (1996) Ecological Entomology, 21, pp. 289-294; Srygley, R.B., Oliveira, E.G., Migration patterns and orientation mechanisms within the flight boundary layer (2001) Insect Movement: Mechanisms and Consequences, pp. 183-206. , D. Reynolds C.D. Thomas I. Woiwod CAB International Oxford; Srygley, R.B., Oliveira, E.G., Dudley, R., Wind drift compensation, flyways, and conservation of diurnal, migrant Neotropical Lepidoptera (1996) Proceedings of the Royal Society of London, Series B, 263, pp. 1351-1357; Ugolini, A., Relationship between compass systems of orientation in equatorial sandhoppers (2001) Animal Behaviour, 62, pp. 193-199; Ugolini, A., Melis, C., Innocenti, R., Tiribilli, B., Castellini, C., Moon and sun compasses in sandhoppers rely on two separate chronometric mechanisms (1999) Proceedings of the Royal Society of London, Series B, 266, pp. 749-752; V{\'a}cha, M., Soukopov{\'a}, H., Magnetic orientation in the mealworm beetle Tenebrio and the effect of light (2004) Journal of Experimental Biology, 207, pp. 1241-1248; Walker, M.M., Bitterman, M.E., Honeybees can be trained to respond to very small changes in geomagnetic-field intensity (1989) Journal of Experimental Biology, 145, pp. 489-494; Walker, M.M., Baird, D.L., Bitterman, M.E., Failure of stationary but not of flying honeybees (Apis mellifera) to respond to magnetic field stimuli (1989) Journal of Comparative Psychology, 103, pp. 62-69; Wehner, R., Astronavigation in insects (1984) Annual Review of Entomology, 29, pp. 277-298; Wiltschko, R., Wiltschko, W., (1995) Magnetic Orientation in Animals, , Springer Verlag New York; Wiltschko, W., Wiltschko, R., Magnetic compass of European robins (1972) Science, 176, pp. 62-64; Wiltschko, W., Munro, U., Beason, R.C., Ford, H., Wiltschko, R., A magnetic pulse leads to temporary deflection in the orientation of migratory birds (1994) Experientia, 50, pp. 697-700; Zar, J.H., (1999) Biostatistical Analysis, , Prentice Hall Upper Saddle River, New Jersey",
year = "2006",
doi = "10.1016/j.anbehav.2005.04.013",
language = "English (US)",
volume = "71",
pages = "183--191",
journal = "Animal Behaviour",
issn = "0003-3472",
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}

Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae). / Srygley, R.B.; Dudley, R.; Oliveira, E.G.; Riveros, A.J.

En: Animal Behaviour, Vol. 71, N.º 1, 2006, p. 183-191.

Resultado de la investigación: Contribución a RevistaArtículo

TY - JOUR

T1 - Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae)

AU - Srygley, R.B.

AU - Dudley, R.

AU - Oliveira, E.G.

AU - Riveros, A.J.

N1 - Cited By :22 Export Date: 17 April 2018 CODEN: ANBEA Correspondence Address: Srygley, R.B.; Smithsonian Tropical Research Institute, Apdo. 2072, Balboa, Panama; email: bob.srygley@zoo.ox.ac.uk Funding details: CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico Funding details: National Geographic Society Funding details: STRI, Smithsonian Tropical Research Institute Funding text: This research was funded with a grant from the National Geographic Society Committee for Research and Exploration. In addition, R.B.S. was supported by a Senior Postdoctoral Fellowship from the Smithsonian Institution Office of Fellowships and Grants, Washington, DC and the Korean Science and Engineering Foundation supported preparation of the manuscript. E.G.O. was supported by a CNPq Postdoctoral Fellowship. We thank the National Geographic Society and the Smithsonian Tropical Research Institute for their continued support. We also thank Alejandro Almanza and Ana Portugal for recording behaviour of butterflies in the electromagnet. References: Able, K.P., Able, M.A., Daytime calibration of magnetic orientation in a migratory bird requires a view of skylight polarization (1993) Nature, 364, pp. 523-525; Able, K.P., Able, M.A., Evidence for calibration of magnetic migratory orientation in Savannah sparrows reared in the field (1999) Proceedings of the Royal Society of London, Series B, 266, pp. 1477-1481; Arendse, M.C., Magnetic field detection is distinct from light detection in the invertebrates Tenebrio and Talitrus (1978) Nature, 274, pp. 358-362; Baker, R.R., Integrated use of moon and magnetic compasses by the heart-and-dart moth, Agrotis exclamationis (1987) Animal Behaviour, 35, pp. 94-101; Baker, R.R., Mather, J.G., Magnetic compass sense in the large yellow underwing moth, Noctua pronuba L (1982) Animal Behaviour, 30, pp. 543-548; Banks, A.N., Srygley, R.B., Orientation of foraging leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae: Attinae), is shifted by a local reversal of the earth's magnetic field (2003) Ethology, 109, pp. 835-846; Batschelet, E., (1981) Circular Statistics in Biology, , Academic Press London; Beason, R.C., Dussourd, N., Deutschlander, M.E., Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird (1995) Journal of Experimental Biology, 198, pp. 141-146; Boles, L.C., Lohmann, K.J., True navigation and magnetic maps in spiny lobsters (2003) Nature, 421, pp. 60-63; Brower, L.P., Monarch butterfly orientation: Missing pieces of a magnificent puzzle (1996) Journal of Experimental Biology, 199, pp. 93-103; Camlitepe, Y., Stradling, D., Wood ants orient to magnetic fields (1995) Proceedings of the Royal Society of London, Series B, 261, pp. 37-41; Deutschlander, M.E., Phillips, J.B., Borland, S.C., The case for light-dependent magnetic orientation in animals (1999) Journal of Experimental Biology, 202, pp. 891-908; Esquivel, D.M.S., Acosta-Avalos, D., El-Jaick, L.J., Cunha, A.D.M., Malheiros, M.G., Wajnberg, E., Linhares, M.P., Evidence for magnetic material in the fire ant Solenopsis sp. by electron paramagnetic resonance measurements (1999) Naturwissenschaften, 86, pp. 30-32; Froy, O., Gotter, A.L., Casselman, A.L., Reppert, S.M., Illuminating the circadian clock in monarch butterfly migration (2003) Science, 300, pp. 1303-1305; Gould, J.L., Kirschvink, J.L., Deffeyes, K.S., Brines, M.L., Orientation of demagnetized bees (1980) Journal of Experimental Biology, 86, pp. 1-8; Jones, D.S., MacFadden, B.J., Induced magnetization in the monarch butterfly, Danaus plexippus (Insecta, Lepidoptera) (1982) Journal of Experimental Biology, 96, pp. 1-9; Jungreis, S.A., Biomagnetism: An orientation mechanism in migrating insects? (1987) Florida Entomologist, 70, pp. 277-283; Kirschvink, J.L., Uniform magnetic fields and double-wrapped coil systems: Improved techniques for the design of biomagnetic experiments (1992) Bioelectromagnetics, 13, pp. 401-411; Lindauer, M., Martin, H., Die Schwereorientierung der Bienen unter dem Einfluss der Erdmagnetfelder (1968) Zeitschrift für Vergleichende Physiologie, 60, pp. 219-243; Lohmann, K.J., Pentcheff, N.D., Nevitt, G.A., Stetten, G.D., Zimmerfaust, R.K., Jarrard, H.E., Boles, L.C., Magnetic orientation of spiny lobsters in the ocean: Experiments with undersea coil systems (1995) Journal of Experimental Biology, 198, pp. 2041-2048; Merritt, R., Purcell, C., Stroink, G., Uniform magnetic field produced by three, four, and five square coils (1983) Review of Scientific Instruments, 54, pp. 879-882; Mouritsen, H., Frost, B.J., Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms (2002) Proceedings of the National Academy of Sciences, U.S.A., 99, pp. 10162-10166; Oliveira, E.G., Srygley, R.B., Dudley, R., Do Neotropical migrant butterflies navigate using a solar compass? (1998) Journal of Experimental Biology, 201, pp. 3317-3331; Peddie, N.W., (1993) The Magnetic Field of the Earth: 1990 Declination Chart, , US Department of Interior, US Geological Survey Reston, Virginia; Perez, S.M., Taylor, O.R., Jander, R., The effect of a strong magnetic field on monarch butterfly (Danaus plexippus) migratory behavior (1999) Naturwissenschaften, 86, pp. 140-143; Schmitt, D.E., Esch, H.E., Magnetic orientation of honeybees in the laboratory (1993) Naturwissenschaften, 80, pp. 41-43; Spieth, H.R., Kaschuba-Holtgrave, A., A new experimental approach to investigate migration in Pieris brassicae L (1996) Ecological Entomology, 21, pp. 289-294; Srygley, R.B., Oliveira, E.G., Migration patterns and orientation mechanisms within the flight boundary layer (2001) Insect Movement: Mechanisms and Consequences, pp. 183-206. , D. Reynolds C.D. Thomas I. Woiwod CAB International Oxford; Srygley, R.B., Oliveira, E.G., Dudley, R., Wind drift compensation, flyways, and conservation of diurnal, migrant Neotropical Lepidoptera (1996) Proceedings of the Royal Society of London, Series B, 263, pp. 1351-1357; Ugolini, A., Relationship between compass systems of orientation in equatorial sandhoppers (2001) Animal Behaviour, 62, pp. 193-199; Ugolini, A., Melis, C., Innocenti, R., Tiribilli, B., Castellini, C., Moon and sun compasses in sandhoppers rely on two separate chronometric mechanisms (1999) Proceedings of the Royal Society of London, Series B, 266, pp. 749-752; Vácha, M., Soukopová, H., Magnetic orientation in the mealworm beetle Tenebrio and the effect of light (2004) Journal of Experimental Biology, 207, pp. 1241-1248; Walker, M.M., Bitterman, M.E., Honeybees can be trained to respond to very small changes in geomagnetic-field intensity (1989) Journal of Experimental Biology, 145, pp. 489-494; Walker, M.M., Baird, D.L., Bitterman, M.E., Failure of stationary but not of flying honeybees (Apis mellifera) to respond to magnetic field stimuli (1989) Journal of Comparative Psychology, 103, pp. 62-69; Wehner, R., Astronavigation in insects (1984) Annual Review of Entomology, 29, pp. 277-298; Wiltschko, R., Wiltschko, W., (1995) Magnetic Orientation in Animals, , Springer Verlag New York; Wiltschko, W., Wiltschko, R., Magnetic compass of European robins (1972) Science, 176, pp. 62-64; Wiltschko, W., Munro, U., Beason, R.C., Ford, H., Wiltschko, R., A magnetic pulse leads to temporary deflection in the orientation of migratory birds (1994) Experientia, 50, pp. 697-700; Zar, J.H., (1999) Biostatistical Analysis, , Prentice Hall Upper Saddle River, New Jersey

PY - 2006

Y1 - 2006

N2 - We tested whether migrating Aphrissa statira butterflies orient with a magnetic compass. We captured migrants flying over Lake Gatún, Panama, and exposed experimental butterflies to a strong magnetic field. These and unmanipulated control butterflies were released back over the lake. Experimental butterflies had a more dispersed pattern of orientation than control butterflies. The average direction adopted was northeast, 160° anticlockwise to the natural migratory direction. Unmanipulated control butterflies adopted two diametrically opposed orientations: one shifted 33° clockwise, and another 147° anticlockwise, to the migratory direction. Control and experimental butterflies differed in that some controls oriented towards the migratory direction. These differences in orientation support the hypothesis of a sense for magnetic orientation cues. Unmanipulated butterflies released over the lake when the sky was completely overcast were significantly oriented towards their direction before capture (187° and 203°, respectively), further supporting the magnetic compass hypothesis. In a third experiment, we obstructed sun compass cues and reversed the horizontal component of the local geomagnetic field to position magnetic north towards the geographical south pole within a flight arena into which we released individual butterflies. Experimental butterflies experiencing the reversed magnetic field oriented on average 180° opposite to their natural migratory direction. Control butterflies, for which the position of magnetic north was unaltered, were oriented both towards and 180° opposite to the natural migratory direction. This difference between orientations of control and experimental butterflies also supports the hypothesis of a sense for magnetic orientation cues. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

AB - We tested whether migrating Aphrissa statira butterflies orient with a magnetic compass. We captured migrants flying over Lake Gatún, Panama, and exposed experimental butterflies to a strong magnetic field. These and unmanipulated control butterflies were released back over the lake. Experimental butterflies had a more dispersed pattern of orientation than control butterflies. The average direction adopted was northeast, 160° anticlockwise to the natural migratory direction. Unmanipulated control butterflies adopted two diametrically opposed orientations: one shifted 33° clockwise, and another 147° anticlockwise, to the migratory direction. Control and experimental butterflies differed in that some controls oriented towards the migratory direction. These differences in orientation support the hypothesis of a sense for magnetic orientation cues. Unmanipulated butterflies released over the lake when the sky was completely overcast were significantly oriented towards their direction before capture (187° and 203°, respectively), further supporting the magnetic compass hypothesis. In a third experiment, we obstructed sun compass cues and reversed the horizontal component of the local geomagnetic field to position magnetic north towards the geographical south pole within a flight arena into which we released individual butterflies. Experimental butterflies experiencing the reversed magnetic field oriented on average 180° opposite to their natural migratory direction. Control butterflies, for which the position of magnetic north was unaltered, were oriented both towards and 180° opposite to the natural migratory direction. This difference between orientations of control and experimental butterflies also supports the hypothesis of a sense for magnetic orientation cues. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

U2 - 10.1016/j.anbehav.2005.04.013

DO - 10.1016/j.anbehav.2005.04.013

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VL - 71

SP - 183

EP - 191

JO - Animal Behaviour

JF - Animal Behaviour

SN - 0003-3472

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