, Volume 97, Issue 12, pp 1077–1088 | Cite as

Light-dependent magnetic compass in Iberian green frog tadpoles

  • Francisco Javier Diego-RasillaEmail author
  • Rosa Milagros Luengo
  • John B. Phillips
Original Paper


Here, we provide evidence for a wavelength-dependent effect of light on magnetic compass orientation in Pelophylax perezi (order Anura), similar to that observed in Rana catesbeiana (order Anura) and Notophthalmus viridescens (order Urodela), and confirm for the first time in an anuran amphibian that a 90° shift in the direction of magnetic compass orientation under long-wavelength light (≥500 nm) is due to a direct effect of light on the underlying magnetoreception mechanism. Although magnetic compass orientation in other animals (e.g., birds and some insects) has been shown to be influenced by the wavelength and/or intensity of light, these two amphibian orders are the only taxa for which there is direct evidence that the magnetic compass is light-dependent. The remarkable similarities in the light-dependent magnetic compasses of anurans and urodeles, which have evolved as separate clades for at least 250 million years, suggest that the light-dependent magnetoreception mechanism is likely to have evolved in the common ancestor of the Lissamphibia (Early Permian, ~294 million years) and, possibly, much earlier. Also, we discuss a number of similarities between the functional properties of the light-dependent magnetic compass in amphibians and blue light-dependent responses to magnetic stimuli in Drosophila melanogaster, which suggest that the wavelength-dependent 90° shift in amphibians may be due to light activation of different redox forms of a cryptochrome photopigment. Finally, we relate these findings to earlier studies showing that the pineal organ of newts is the site of the light-dependent magnetic compass and recent neurophysiological evidence showing magnetic field sensitivity in the frog frontal organ (an outgrowth of the pineal).


Anuran Magnetic compass Light-dependent magnetoreception Pelophylax perezi 



We thank Marcos Diego-Gutiérrez for his valuable assistance during the study. Review by Michael Painter, Rachel Muheim and Paulo Jorge improved the manuscript. We thank three anonymous reviewers for their comments on the manuscript. The Cantabria autonomous government granted the necessary permits for the study. J.B.P. was supported by NSF IOB06-47188 during the preparation of this manuscript. The experiments reported herein comply with the current laws of Spain. The authors declare that they have no conflict of interest.


  1. Adler K, Taylor DH (1973) Extraocular perception of polarized light by orienting salamanders. J Comp Physiol 87:203–212CrossRefGoogle Scholar
  2. Ahmad M, Galland P, Ritz T, Wiltschko R, Wiltschko W (2007) Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225:615–624. doi: 10.1007/s00425-006-0383-0 CrossRefPubMedGoogle Scholar
  3. Bailey MJ, Chong NW, Xiong J, Cassone VM (2002) Chickens’ Cry2: molecular analysis of an avian cryptochrome in retinal and pineal photoreceptors. FEBS Lett 513:169–174CrossRefPubMedGoogle Scholar
  4. Banerjee R, Schleicher E, Meier S, Viana RM, Pokorny R, Ahmad M, Bittl R, Batschauer A (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J Biol Chem 282:14916–14922. doi: 10.1074/jbc.M700616200 CrossRefPubMedGoogle Scholar
  5. Batschelet E (1981) Circular statistics in biology. Academic, New YorkGoogle Scholar
  6. Biskup T, Schleicher E, Okafuji A, Link G, Hitomi K, Getzoff Elizabeth D, Weber S (2009) Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew Chem Int Ed 48:404–407. doi: 10.1002/anie.200803102 CrossRefGoogle Scholar
  7. Borsuk-Białynicka M, Evans SE (2002) The scapulocoracoid of an Early Triassic stem-frog from Poland. Acta Palaeontol Pol 47:79–96Google Scholar
  8. Bouly JP, Schleicher E, Dionisio-Sese M, Vandenbussche F, Van Der Straeten D, Bakrim N, Meier S, Batschauer A, Galland P, Bittl R, Ahmad M (2007) Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J Biol Chem 282:9383–9391. doi: 10.1074/jbc.M609842200 CrossRefPubMedGoogle Scholar
  9. Busza A, Emery-Le M, Rosbash M, Emery P (2004) Roles of the two Drosophila cryptochrome structural domains in circadian photoreception. Science 304:1503–1506CrossRefPubMedGoogle Scholar
  10. Cannatella DC, Vieites DR, Zhang P, Wake MH, Wake DB (2009) Amphibians (Lissamphibia). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 353–356Google Scholar
  11. Cashmore A, Jarillo JA, Wu Y, Liu D (1999) Cryptochromes: blue light receptors for plants and animals. Science 284:760–765CrossRefPubMedGoogle Scholar
  12. Cintolesi F, Ritz T, Kay CWM, Timmel CR, Hore PJ (2003) Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor. Chem Phys 294:385–399. doi: 10.1016/S0301-0104(03)00320-3 CrossRefGoogle Scholar
  13. Deutschlander ME, Borland SC, Phillips JB (1999a) Extraocular magnetic compass in newts. Nature 400:324–325. doi: 10.1038/22450 CrossRefPubMedGoogle Scholar
  14. Deutschlander ME, Phillips JB, Borland SC (1999b) The case for light-dependent magnetic orientation in animals. J Exp Biol 202:891–908PubMedGoogle Scholar
  15. Deutschlander ME, Phillips JB, Borland SC (2000) Magnetic compass orientation in the eastern red-spotted newt, Notophthalmus viridescens: rapid acquisition of the shoreward axis. Copeia 2000:413–419CrossRefGoogle Scholar
  16. Diego-Rasilla FJ (2003) Homing ability and sensitivity to the geomagnetic field in the alpine newt, Triturus alpestris. Ethol Ecol Evol 15:251–259CrossRefGoogle Scholar
  17. Diego-Rasilla FJ, Phillips JB (2007) Magnetic compass orientation in larval Iberian green frogs, Pelophylax perezi. Ethology 113:1–6. doi: 10.1111/j.1439-0310.2007.01334.x CrossRefGoogle Scholar
  18. Dodt E, Heerd E (1962) Mode of action of pineal nerve fibers in frogs. J Neurophysiol 25:405–429PubMedGoogle Scholar
  19. Eldred WD, Nolte J (1978) Pineal photoreceptors: evidence for a vertebrate visual pigment with two physiologically active states. Vis Res 18:29–32. doi: 10.1016/0042-6989(78)90073-1 CrossRefPubMedGoogle Scholar
  20. Ferguson DE, Landreth HF (1966) Celestial orientation of Fowler’s toad (Bufo fowleri). Behaviour 26:105–123CrossRefGoogle Scholar
  21. Ferguson DE, Landreth HF, McKeown JP (1967) Sun compass orientation of the northern cricket frog, Acris crepitans. Anim Behav 15:45–53CrossRefPubMedGoogle Scholar
  22. Freake MJ, Phillips JB (2005) Light-dependent shift in bullfrog tadpole magnetic compass orientation: evidence for a common magnetoreception mechanism in anuran and urodele amphibians. Ethology 111:241–254. doi: 10.1111/j.1439-0310.2004.01067.x CrossRefGoogle Scholar
  23. Freake MJ, Borland SC, Phillips JB (2002) Use of a magnetic compass for Y-axis orientation in larval bullfrogs (Rana catesbeiana). Copeia 2002:466–471CrossRefGoogle Scholar
  24. Gegear RJ, Casselman A, Waddell S, Reppert SM (2008) Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454:1014–1018. doi: 10.1038/nature07183 CrossRefPubMedGoogle Scholar
  25. Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat Struct Biol 10:489–490CrossRefPubMedGoogle Scholar
  26. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  27. Gradstein FM, Ogg JG, Smith AG, Agterberg FP, Bleeker W, Cooper RA, Davydov V, Gibbard P, Hinnov LA, House MR, Lourens L, Luterbacher HP, McArthur J, Melchin MJ, Robb LJ, Shergold J, Villeneuve M, Wardlaw BR, Ali J, Brinkhuis H, Hilgen FJ, Hooker J, Howarth RJ, Knoll AH, Laskar J, Monechi S, Plumb KA, Powell J, Raffi I, Röhl U, Sadler P, Sanfilippo A, Schmitz B, Shackleton NJ, Shields GA, Strauss H, Dam JV, Tv K, Veizer J, Wilson DM (2004) A geologic time scale. Cambridge University Press, CambridgeGoogle Scholar
  28. Hoang N, Schleicher E, Kacprzak S, Bouly J-P, Picot M, Wu W, Berndt A, Wolf E, Bittl R, Ahmad M (2008) Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol 6:e160. doi: 10.1371/journal.pbio.0060160 CrossRefPubMedGoogle Scholar
  29. Klarsfeld A, Malpel S, Michard-Vanhee C, Picot M, Chelot E, Rouyer F (2004) Novel features of cryptochrome-mediated photoreception in the brain of the circadian clock of Drosophila. J Neurosci 24:1468–1477CrossRefPubMedGoogle Scholar
  30. Koyanagi M, Kawano E, Kinugawa Y, Oishi T, Shichida Y, Tamotsu S, Terakita A (2004) Bistable UV pigment in the lamprey pineal. Proc Natl Acad Sci USA 101:6687–6691. doi: 10.1073/pnas.0400819101 CrossRefPubMedGoogle Scholar
  31. Kyriacou CP (2009) Clocks, cryptochromes and Monarch migrations. J Biol 8:55.3–55.4. doi: 10.1186/jbiol153 CrossRefGoogle Scholar
  32. Landreth HF, Ferguson DE (1967) Newts: sun-compass orientation. Science 158:1459–1461CrossRefPubMedGoogle Scholar
  33. Landreth HF, Ferguson DE (1968) The sun compass of Fowler’s toad, Bufo woodhousei fowleri. Behaviour 30:27–43CrossRefGoogle Scholar
  34. Lee MSY, Anderson JS (2006) Molecular clocks and the origin(s) of modern amphibians. Mol Phylogenet Evol 40:635–639CrossRefPubMedGoogle Scholar
  35. Liedvogel M, Mouritsen H (2010) Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know? J R Soc Interface 7:S147–S162. doi: 10.1098/rsif.2009.0411.focus CrossRefPubMedGoogle Scholar
  36. Liedvogel M, Maeda K, Henbest K, Schleicher E, Simon T, Timmel CR, Hore PJ, Mouritsen H (2007) Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS ONE 2:e1106. doi: 10.1371/journal.pone.0001106 CrossRefPubMedGoogle Scholar
  37. Lin C (2004) Photoreceptors and associated signaling II: cryptochromes. In: Encyclopedia of plant and crop science. University of California, Los Angeles, California, USAGoogle Scholar
  38. Mardia KV, Jupp PE (2000) Directional statistics. Wiley, New YorkGoogle Scholar
  39. Marjanović D, Laurin M (2007) Fossils, molecules, divergence times, and the origin of Lissamphibians. Syst Biol 56:369–388CrossRefPubMedGoogle Scholar
  40. Milner AR (1990) The radiations of temnospondyl amphibians. In: Taylor PD, Larwood GP (eds) Major evolutionary radiations. Clarendon, Oxford, pp 321–349Google Scholar
  41. Möller A, Sagasser S, Wiltschko W, Schierwater B (2004) Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585–588. doi: 10.1007/s00114-004-0578-9 CrossRefPubMedGoogle Scholar
  42. Mouritsen H, Ritz T (2005) Magnetoreception and its use in bird navigation. Curr Opin Neurobiol 15:406–414CrossRefPubMedGoogle Scholar
  43. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J, Dirks P, Weiler R (2004) Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc Natl Acad Sci USA 101:14294–14299. doi: 10.1073/pnas.0405968101 CrossRefPubMedGoogle Scholar
  44. Öztürk N, Song S-H, Selby CP, Sancar A (2008) Animal type 1 cryptochromes: analysis of the redox state of the flavin cofactor by site-directed mutagenesis. J Biol Chem 283:3256–3263. doi: 10.1074/jbc.M708612200 CrossRefPubMedGoogle Scholar
  45. Phillips JB (1986) Magnetic compass orientation in the Eastern red-spotted newt (Notophthalmus viridescens). J Comp Physiol A 158:103–109CrossRefPubMedGoogle Scholar
  46. Phillips JB, Borland SC (1992a) Behavioral evidence for the use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359:142–144. doi: 10.1038/359142a0 CrossRefGoogle Scholar
  47. Phillips JB, Borland SC (1992b) Magnetic compass orientation is eliminated under near-infrared light in the Eastern red-spotted newt (Notophthalmus viridescens). Anim Behav 44:796–797. doi: 10.1016/S0003-3472(05)80311-2 CrossRefGoogle Scholar
  48. Phillips JB, Borland SC (1992c) Wavelength-specific effects of light on magnetic compass orientation of the Eastern red-spotted newt (Notophthalmus viridescens). Ethol Ecol Evol 4:33–42CrossRefGoogle Scholar
  49. Phillips JB, Sayeed O (1993) Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster. J Comp Physiol A 172:303–308. doi: 10.1007/BF00216612 CrossRefPubMedGoogle Scholar
  50. Phillips JB, Deutschlander ME, Freake MJ, Borland SC (2001) The role of extraocular photoreceptors in newt magnetic compass orientation: evidence for parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J Exp Biol 204:2543–2552PubMedGoogle Scholar
  51. Phillips JB, Jorge PE, Muheim R (2010) Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms. J R Soc Interface 7:S241–S256. doi: 10.1098/rsif.2009.0459.focus CrossRefPubMedGoogle Scholar
  52. Rage JC, Roček Z (1989) Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the Early Triassic. Palaeontogr A 206:1–16Google Scholar
  53. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718. doi: 10.1016/S0006-3495(00)76629-X CrossRefPubMedGoogle Scholar
  54. Ritz T, Phillips JB, Dommer DH (2002) Shedding light on vertebrate magnetoreception. Neuron 34:503–506. doi: 10.1016/S0896-6273(02)00707-9 Google Scholar
  55. Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical pair mechanism for avian magnetic compass. Nature 429:177–180. doi: 10.1038/nature02534 CrossRefPubMedGoogle Scholar
  56. Robinson R (2008) Monarchs, Cry2 is king of the clock. PLoS Biol 6:e12CrossRefPubMedGoogle Scholar
  57. Rodgers CT, Hore PJ (2009) Chemical magnetoreception in birds: the radical pair mechanism. Proc Nat Acad Sci USA 106:353–360. doi: 10.1073/pnas.0711968106 CrossRefPubMedGoogle Scholar
  58. Rodríguez-García L, Diego-Rasilla FJ (2006) Use of a magnetic compass for Y-axis orientation in premetamorphic newts (Triturus boscai). J Ethol 24:111–116. doi: 10.1007/s10164-005-0169-z CrossRefGoogle Scholar
  59. Rosato E, Codd V, Mazzotta G, Piccin A, Zordan M, Costa R, Kyriacou CP (2001) Light-dependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr Biol 11:909–917CrossRefPubMedGoogle Scholar
  60. Rubens SM (1945) Cube-surface coil for producing a uniform magnetic field. Rev Sci Instrum 16:243–245CrossRefGoogle Scholar
  61. Russell AP, Bauer AM, Johnson MK (2005) Migration in amphibians and reptiles: an overview of patterns and orientation mechanisms in relation to life history strategies. In: Elewa AMT (ed) Migration of organisms. Climate. Geography. Ecology. Springer, Berlin, pp 151–203Google Scholar
  62. Ruta M, Coates MI, Quicke DDL (2003) Early tetrapod relationships revisited. Biol Rev 78:251–345CrossRefPubMedGoogle Scholar
  63. Sancar A (2004) Regulation of the mammalian circadian clock by cryptochrome. J Biol Chem 279:34079–34082. doi: 10.1074/jbc.R400016200 CrossRefPubMedGoogle Scholar
  64. Schoch RR, Milner AR (2004) Structure and implications of theories on the origin of lissamphibians. In: Arratia G, Wilson MVH, Cloutier R (eds) Recent advances in the origin and early radiations of vertebrates. Dr. Friedrich Pfeil, Munich, pp 345–377Google Scholar
  65. Schulten K (1982) Magnetic field effects in chemistry and biology. In: Treusch J (ed) Festkörperprobleme [Advances in solid state physics], vol 22. Vieweg, Braunschweig, pp 61–83Google Scholar
  66. Schulten K, Windemuth A (1986) Model for a physiological magnetic compass. In: Maret G, Boccara N, Kiepenheuer J (eds) Biophysical effects of steady magnetic fields. Springer, Berlin, pp 99–106Google Scholar
  67. Schulten K, Swenberg CE, Weller A (1978) A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z Phys Chem NF 111:1–5Google Scholar
  68. Solov’yov IA, Schulten K (2009) Magnetoreception through cryptochrome may involve superoxide. Biophys J 96:4804–4813. doi: 10.1016/j.bpj.2009.03.048 CrossRefPubMedGoogle Scholar
  69. Solov’yov IA, Chandler D, Schulten K (2007) Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys J 92:2711–2726CrossRefPubMedGoogle Scholar
  70. Song S-H, Öztürk N, Denaro TR, NÃz A, Kao Y-T, Zhu H, Zhong D, Reppert SM, Sancar A (2007) Formation and function of flavin anion radical in cryptochrome 1 blue-light photoreceptor of monarch butterfly. J Biol Chem 282:17608–17612. doi: 10.1074/jbc.M702874200 CrossRefPubMedGoogle Scholar
  71. Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681–692. doi: 10.1016/S0092-8674(00)81638-4 CrossRefPubMedGoogle Scholar
  72. Stebbins RC, Cohen NW (1997) A natural history of amphibians. Princeton University Press, PrincetonGoogle Scholar
  73. Taylor DH (1972) Extra-optic photoreception and compass orientation in larval and adult salamanders (Ambystoma tigrinum). Anim Behav 20:233–236CrossRefPubMedGoogle Scholar
  74. Taylor DH, Adler K (1973) Spatial orientation by salamanders using plane-polarized light. Science 181:285–287CrossRefPubMedGoogle Scholar
  75. Taylor DH, Auburn J (1978) Orientation of amphibians by linearly polarized light. In: Schmidt-Koenig K, Keeton W (eds) Animal migration, navigation and homing. Springer, Berlin, pp 334–346Google Scholar
  76. Taylor DH, Ferguson DE (1970) Extraoptic celestial orientation in the southern cricket frog Acris gryllus. Science 168:390–392CrossRefPubMedGoogle Scholar
  77. Trueb L, Cloutier R (1991) A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). In: Schultze H-P, Trueb L (eds) Origins of the higher groups of Tetrapods—controversy and consensus. Cornell University Press, Ithaca, pp 223–313Google Scholar
  78. Tu DC, Batten ML, Palczewski K, Van Gelder RN (2004) Nonvisual photoreception in the chick iris. Science 306:129–131. doi: 10.1126/science.1101484 CrossRefPubMedGoogle Scholar
  79. van der Horst GTJ, Muijtjens M, Kobayashi K, Takano R, Kanno S-I, Takao M, Jd W, Verkerk A, Eker APM, Dv L, Buijs R, Bootsma D, Hoeijmakers JHJ, Yasui A (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627–630. doi: 10.1038/19323 CrossRefPubMedGoogle Scholar
  80. van Gelder RN, Wee R, Lee JA, Tu DC (2003) Reduced pupillary light responses in mice lacking cryptochromes. Science 299:222CrossRefPubMedGoogle Scholar
  81. Van Vickle-Chavez SJ, Van Gelder RN (2007) Action spectrum of Drosophila cryptochrome. J Biol Chem 282:10561–10566. doi: 10.1074/jbc.M609314200 CrossRefGoogle Scholar
  82. Wells DK (2007) The ecology and behavior of amphibians. The University of Chicago Press, ChicagoGoogle Scholar
  83. Wiltschko R, Wiltschko W (2006) Magnetoreception. BioEssays 28:157–168CrossRefPubMedGoogle Scholar
  84. Yoshii T, Ahmad M, Helfrich-Förster C (2009) Cryptochrome mediates light-dependent magnetosensitivity of Drosophila’s circadian clock. PLoS Biol 7:e1000086. doi: 10.1371/journal.pbio.1000086 CrossRefPubMedGoogle Scholar
  85. Zhang P, Wake DB (2009) Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogenet Evol 53:492–508CrossRefPubMedGoogle Scholar
  86. Zhu H, Green CB (2001) Three cryptochromes are rhythmically expressed in Xenopus laevis retinal photoreceptors. Mol Vis 7:210PubMedGoogle Scholar
  87. Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol 6:e4. doi: 10.1371/journal.pbio.0060004 CrossRefPubMedGoogle Scholar
  88. Zikihara K, Ishikawa T, Todo T, Tokutomi S (2008) Involvement of electron transfer in the photoreaction of zebrafish cryptochrome-DASH. Photochem Photobiol 84:1016–1023. doi: 10.1111/j.1751-1097.2007.00364.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Francisco Javier Diego-Rasilla
    • 1
    Email author
  • Rosa Milagros Luengo
    • 2
  • John B. Phillips
    • 3
  1. 1.Departamento de Biología AnimalUniversidad de SalamancaSalamancaSpain
  2. 2.Gabinete de Iniciativas Socioculturales y de Formación S.L.SalamancaSpain
  3. 3.Department of Biological SciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA

Personalised recommendations