The Science of Nature

, 104:13 | Cite as

Spontaneous magnetic alignment behaviour in free-living lizards

  • Francisco J. Diego-Rasilla
  • Valentín Pérez-Mellado
  • Ana Pérez-Cembranos
Original Paper

Abstract

Several species of vertebrates exhibit spontaneous longitudinal body axis alignment relative to the Earth’s magnetic field (i.e., magnetic alignment) while they are performing different behavioural tasks. Since magnetoreception is still not fully understood, studying magnetic alignment provides evidence for magnetoreception and broadens current knowledge of magnetic sense in animals. Furthermore, magnetic alignment widens the roles of magnetic sensitivity in animals and may contribute to shed new light on magnetoreception. In this context, spontaneous alignment in two species of lacertid lizards (Podarcis muralis and Podarcis lilfordi) during basking periods was monitored. Alignments in 255 P. muralis and 456 P. lilfordi were measured over a 5-year period. The possible influence of the sun’s position (i.e., altitude and azimuth) and geomagnetic field values corresponding to the moment in which a particular lizard was observed on lizards’ body axis orientation was evaluated. Both species exhibited a highly significant bimodal orientation along the north-northeast and south-southwest magnetic axis. The evidence from this study suggests that free-living lacertid lizards exhibit magnetic alignment behaviour, since their body alignments cannot be explained by an effect of the sun’s position. On the contrary, lizard orientations were significantly correlated with geomagnetic field values at the time of each observation. We suggest that this behaviour might provide lizards with a constant directional reference while they are sun basking. This directional reference might improve their mental map of space to accomplish efficient escape behaviour. This study is the first to provide spontaneous magnetic alignment behaviour in free-living reptiles.

Keywords

Basking behaviour Lacertidae Lizards Magnetic alignment Magnetoreception 

Supplementary material

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References

  1. Adler K, Phillips JB (1985) Orientation in a desert lizard (Uma notata): time compensated compass movement and polarotaxis. J Comp Physiol A 156:547–552. doi:10.1007/BF00613978 CrossRefGoogle Scholar
  2. Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295. doi:10.1086/285538 PubMedCrossRefGoogle Scholar
  3. Altmann GA (1981) Untersuchung zur Magnetotaxis der Honigbiene, Apis melliflica L. Schadlingskd Pflanzenschutz Umweltschutz 54:177–179CrossRefGoogle Scholar
  4. Avery RA (1976) Thermoregulation, metabolism and social behaviour in Lacertidae. In: Bellairs AA, Cox CB (eds) Morphology and biology of reptiles. Academic Press, London, pp 245–259Google Scholar
  5. Barlett PN, Gates DM (1967) The energy budget of a lizard on a tree trunk. Ecology 48:315–322. doi:10.2307/1933120 CrossRefGoogle Scholar
  6. Batschelet E (1981) Circular statistics in biology. Academic Press, New YorkGoogle Scholar
  7. Bauwens D, Castilla AM, Damme RV, Verheyen RF (1990) Field body temperatures and thermoregulatory behavior of the high altitude lizard, Lacerta bedriagae. J Herpetol 24:88–91. doi:10.2307/1564296 CrossRefGoogle Scholar
  8. Bauwens D, Hertz PE, Castilla AM (1996) Thermoregulation in a lacertid lizard: the relative contributions of distinct behavioral mechanisms. Ecology 77:1818–1830. doi:10.2307/2265786 CrossRefGoogle Scholar
  9. Becker G (1964) Reaktion von Insekten auf Magnetfelder, elektrische Felder und atmospherics. Z Angew Entomol 54:75–88. doi:10.1111/j.1439-0418.1964.tb02917.x CrossRefGoogle Scholar
  10. Becker G (1974) Einfluss des Magnetfelds auf das Richtungsverhalten von Goldfischen. Naturwissenschaften 61:220–221. doi:10.1007/BF00599929 PubMedCrossRefGoogle Scholar
  11. Becker G, Speck U (1964) Untersuchungen ueber die Magnetfeldorientierung von Dipteren. Z Vergl Physiol 49:301–340. doi:10.1007/BF00302681 CrossRefGoogle Scholar
  12. Begall S, Burda H, Červený J, Gerter O, Neef-Weisse J, Němec P (2011) Further support for the alignment of cattle along magnetic field lines: reply to Hert et al. J Comp Physiol A 197:1127–1133. doi:10.1007/s00359-011-0674-1 CrossRefGoogle Scholar
  13. Begall S, Červený J, Neef J, Vojtech O, Burda H (2008) Magnetic alignment in grazing and resting cattle and deer. Proc Natl Acad Sci U S A 105:13451–13455. doi:10.1073/pnas.0803650105 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Begall S, Malkemper EP, Červený J, Němec P, Burda H (2013) Magnetic alignment in mammals and other animals. Mamm Biol 78:10–20. doi:10.1016/j.mambio.2012.05.005 CrossRefGoogle Scholar
  15. Bohórquez-Alonso ML, Molina-Borja M, Font E (2011) Activity and body orientation of Gallotia galloti in different habitats and daily times. Amphibia-Reptilia 32:93–103. doi:10.1163/017353710X542994 CrossRefGoogle Scholar
  16. Braña F (1991) Summer activity patterns and thermoregulation in the wall lizard, Podarcis muralis. Herpetol J 1:544–549Google Scholar
  17. Brown RP, Pérez-Mellado V (1994) Ecological energetics and food acquisition in dense Menorcan islet populations of the lizard Podarcis lilfordi. Funct Ecol 8:427–434. doi:10.2307/2390065 CrossRefGoogle Scholar
  18. Burda H, Begall S, Červený J, Neef J, Nemec P (2009) Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants. Proc Natl Acad Sci U S A 106:5708–5713. doi:10.1073/pnas.0811194106 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Castilla AM, Damme RV, Bauwens D (1999) Field body temperatures, mechanisms of thermoregulation and evolution of thermal characteristics in lacertid lizards. Natura Croatica 8:253–274Google Scholar
  20. Červený J, Begall S, Koubek P, Nováková P, Burda H (2011) Directional preference may enhance hunting accuracy in foraging foxes. Biol Letters 7:355–357. doi:10.1098/rsbl.2010.1145 CrossRefGoogle Scholar
  21. Chelazzi G, Delfino G (1986) A field test on the use of olfaction in homing by Testudo hermanni (Reptilia: Testudinidae). J Herpetol 20:451–455. doi:10.2307/1564513 CrossRefGoogle Scholar
  22. Chew GL, Brown GE (1989) Orientation of rainbow trout (Salmo gairdneri) in normal and null magnetic fields. Can J Zool 67:641–643. doi:10.1139/z89-092 CrossRefGoogle Scholar
  23. Deoras PJ (1960) Some observations on the termites of Bombay. In: Termites in the humid tropics, vol Proc New Delhi Symp 1960. UNESCO, Paris, New Delhi, pp 101–103Google Scholar
  24. Deutschlander ME, Borland SC, Phillips JB (1999a) Extraocular magnetic compass in newts. Nature 400:324–325. doi:10.1038/22450 PubMedCrossRefGoogle Scholar
  25. Deutschlander ME, Phillips JB, Borland SC (1999b) The case for light-dependent magnetic orientation in animals. J Exp Biol 202:891–908PubMedGoogle Scholar
  26. Díaz JA (1991) Temporal patterns of basking behaviour in a Mediterranean lacertid lizard. Behaviour 118:1–14. doi:10.1163/156853991X00166 CrossRefGoogle Scholar
  27. Díaz JA, Bauwens D, Asensio B (1996) A comparative study of the relation between heating rates and ambient temperatures in lacertid lizards. Physiol Zool 69:1359–1383CrossRefGoogle Scholar
  28. Diego-Rasilla FJ, Luengo RM, Phillips JB (2010) Light-dependent magnetic compass in Iberian green frog tadpoles. Naturwissenschaften 97:1077–1088. doi:10.1007/s00114-010-0730-7 PubMedCrossRefGoogle Scholar
  29. Diego-Rasilla FJ, Luengo RM, Phillips JB (2013) Use of a light-dependent magnetic compass for y-axis orientation in European common frog (Rana temporaria) tadpoles. J Comp Physiol A 199:619–628. doi:10.1007/s00359-013-0811-0 CrossRefGoogle Scholar
  30. Diego-Rasilla FJ, Luengo RM, Phillips JB (2015) Evidence of light-dependent magnetic compass orientation in urodele amphibian larvae. Behav Process 118:1–7. doi:10.1016/j.beproc.2015.05.007 CrossRefGoogle Scholar
  31. Dodt E, Heerd E (1962) Mode of action of pineal nerve fibers in frogs. J Neurophysiol 25:405–429PubMedGoogle Scholar
  32. Dundee H, Miller M III (1968) Aggregative behavior and habitat conditioning by the prairie ringneck snake, Diadophis punctatus arnyi. Tulane Stud Zool Bot 15:41–58Google Scholar
  33. Eldred WD, Nolte J (1978) Pineal photoreceptors: evidence for a vertebrate visual pigment with two physiologically active states. Vis Res 18:29–32PubMedCrossRefGoogle Scholar
  34. Ellis-Quinn BA, Simon CA (1991) Lizard homing behavior: the role of the parietal eye during displacement and radio-tracking, and time-compensated celestial orientation in the lizard Sceloporus jarrovi. Behav Ecol Sociobiol 28:397–407. doi:10.1007/BF00164121 CrossRefGoogle Scholar
  35. Freake MJ (1999) Evidence for orientation using the e-vector direction of polarised light in the sleepy lizard Tiliqua rugosa. J Exp Biol 202:1159–1166PubMedGoogle Scholar
  36. Freake MJ (2001) Homing behaviour in the sleepy lizard (Tiliqua rugosa): the role of visual cues and the parietal eye. Behav Ecol Sociobiol 50:563–569. doi:10.1007/s002650100387 Google Scholar
  37. Graham T, Georges A, McElhinney N (1996) Terrestrial orientation by the eastern long-necked turtle, Chelodina longicollis, from Australia. J Herpetol 30:467–477. doi:10.2307/1565689 CrossRefGoogle Scholar
  38. Grant BW, Dunham AE (1988) Thermally imposed time constraints on the activity of the desert lizard Sceloporus merriami. Ecology 69:167–176. doi:10.2307/1943171 CrossRefGoogle Scholar
  39. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9 ppGoogle Scholar
  40. Hart V, Kušta T, Němec P, Bláhová V, Ježek M, Nováková P, Begall S, Cervený J, Hanzal V, Malkemper EP, Stípek K, Vole C, Burda H (2012) Magnetic alignment in carps: evidence from the Czech Christmas fish market. PLoS One 7:e51100. doi:10.1371/journal.pone.0051100 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hart V, Malkemper EP, Kušta T, Begall S, Nováková P, Hanzal V, Pleskač L, Ježek M, Policht R, Husinec V, Cervený J, Burda H (2013a) Directional compass preference for landing in water birds. Front Zool 10:38. doi:10.1186/1742-9994-10-38 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hart V, Nováková P, Malkemper EP, Begall S, Hanzal V, Ježek M, Kušta T, Němcová V, Adámková J, Benediktová K, Cervený J, Burda H (2013b) Dogs are sensitive to small variations of the Earth’s magnetic field. Front Zool 10:80. doi:10.1186/1742-9994-10-80 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Heath JE (1965) Temperature regulation and diurnal activity in horned lizards. Univ Cal Pub Zool 64:97–136Google Scholar
  44. Henbest KB, Kukura P, Rodgers CT, Hore PJ, Timmel CR (2004) Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. J Am Chem Soc 126:8102–8103. doi:10.1021/ja048220q PubMedCrossRefGoogle Scholar
  45. Herczeg G, Gonda A, Saarikivi J, Merilä J (2006) Experimental support for the cost-benefit model of lizard thermoregulation. Behav Ecol Sociobiol 60:405–414. doi:10.1007/s00265-006-0180-6 CrossRefGoogle Scholar
  46. Hertz PE (1992) Temperature regulation in Puerto Rican Anolis lizards: a field test using null hypotheses. Ecology 73:1405–1417. doi:10.2307/1940686 CrossRefGoogle Scholar
  47. Huey RB (1974) Behavioral thermoregulation in lizards: importance of associated costs. Science 184:1001–1003CrossRefGoogle Scholar
  48. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the Reptilia, Physiology (C). Academic Press, London, vol 12 pp 25–91Google Scholar
  49. Huey RB, Pianka ER (1977) Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology 58:1066–1075. doi:10.2307/1936926 CrossRefGoogle Scholar
  50. Jammalamadaka SR, Sengupta A (2001) Topics in circular statistics. World Scientific Publishing Co, SingaporeGoogle Scholar
  51. Korf HW, Liesner R, Meissl H, Kirk A (1981) Pineal complex of the clawed toad, Xenopus laevis Daud.: structure and function. Cell Tissue Res 216:113–130PubMedCrossRefGoogle Scholar
  52. Landler L, Painter MS, Youmans PW, Wa H, Phillips JB (2015) Spontaneous magnetic alignment by yearling snapping turtles: rapid association of radio frequency dependent pattern of magnetic input with novel surroundings. PLoS One 10:e0124728. doi:10.1371/journal.pone.0124728 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lawson PA, Secoy DM (1991) The use of solar cues as migratory orientation guides by the plains garter snake, Thamnophis radix. Can J Zool 69:2700–2702. doi:10.1139/z91-380 CrossRefGoogle Scholar
  54. Lohmann KJ (1991) Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). J Exp Biol 155:37–49PubMedGoogle Scholar
  55. Lohmann KJ, Lohmann CMF (1993) A light-independent magnetic compass in the leatherback sea turtle. Biol Bull 185:149–151. doi:10.2307/1542138 CrossRefGoogle Scholar
  56. Lohmann KJ, Lohmann CMF, Ehrhart LM, Bagley DA, Swing T (2004) Geomagnetic map used in sea-turtle navigation. Nature 428:909–910. doi:10.1038/428909a PubMedCrossRefGoogle Scholar
  57. Malkemper EP, Eder SHK, Begall S, Phillips JB, Winklhofer M, Hart V, Burda H (2015) Magnetoreception in the wood mouse (Apodemus sylvaticus): influence of weak frequency-modulated radio frequency fields. Scientific Reports 4:9917. doi:10.1038/srep09917 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Malkemper EP, Painter MS, Landler L (2016) Shifted magnetic alignment in vertebrates: evidence for neural lateralization? J Theor Biol 399:141–147. doi:10.1016/j.jtbi.2016.03.040 PubMedCrossRefGoogle Scholar
  59. Mardia KV, Jupp PE (2000) Directional statistics. Wiley, New YorkGoogle Scholar
  60. Marek C, Bissantz N, Curio E, Siegert A, Tacud B, Ziggel D (2010) Spatial orientation of the Philippine bent-toed gecko (Cyrtodactylus philippinicus ) in relation to its home range. Salamandra 46:93–97Google Scholar
  61. Martín J, López P, Carrascal LM, Salvador A (1995) Adjustment of basking postures in the high-altitude Iberian rock lizard (Lacerta monticola). Can J Zool 73:1065–1068. doi:10.1139/z95-126 CrossRefGoogle Scholar
  62. Mathis A, Moore FR (1988) Geomagnetism and the homeward orientation of the box turtle, Terrapene carolina. Ethology 78:265–274. doi:10.1111/j.1439-0310.1988.tb00238.x CrossRefGoogle Scholar
  63. Meyer-Rochow VB (2014a) Polarization sensitivity in amphibians. In: Horváth G (ed) Polarized light and polarization vision in animal sciences. Springer-Verlag, Berlin Heidelberg, pp 249–263. doi:10.1007/978-3-642-54718-8_10 Google Scholar
  64. Meyer-Rochow VB (2014b) Polarization sensitivity in reptiles. In: Horváth G (ed) Polarized light and polarization vision in animal sciences. Springer-Verlag, Berlin Heidelberg, pp 265–274. doi:10.1007/978-3-642-54718-8_11 Google Scholar
  65. Murphy PA (1981) Celestial compass orientation in juvenile american alligators (Alligator mississippiensis). Copeia 1981:638–645. doi:10.2307/1444569 CrossRefGoogle Scholar
  66. Muth A (1977) Thermoregulatory postures and orientation to the sun: a mechanistic evaluation for the zebra-tailed lizard Callisaurus draconoides. Copeia 1977:710–720. doi:10.2307/1443171 CrossRefGoogle Scholar
  67. Newcomer RT, Taylor DH, Guttman SI (1974) Celestial orientation in two species of water snakes (Natrix sipedon and Regina septemvittata). Herpetologica 30:194–200Google Scholar
  68. Nishimura T, Okano H, Tada H, Nishimura E, Sugimoto K, Mohri K, Fukushima M (2010) Lizards respond to an extremely low-frequency electromagnetic field. J Exp Biol 213:1985–1990. doi:10.1242/jeb.031609 PubMedCrossRefGoogle Scholar
  69. Obleser P, Hart V, Malkemper EP, Begall S, Holá M, Painter MS, Červený J, Burda H (2016) Compass-controlled escape behavior in roe deer. Behav Ecol Sociobiol 70:1345–1355. doi:10.1007/s00265-016-2142-y CrossRefGoogle Scholar
  70. Ortega Z, Pérez-Mellado V, Garrido M, Guerra C, Villa-García A, Alonso-Fernández T (2014) Seasonal changes in thermal biology of Podarcis lilfordi (Squamata, Lacertidae) consistently depend on habitat traits. J Therm Biol 39:32–39. doi:10.1016/j.jtherbio.2013.11.006 CrossRefGoogle Scholar
  71. Painter MS, Dommer DH, Altizer WW, Muheim R, Phillips JB (2013) Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice. J Exp Biol 216:1307–1316. doi:10.1242/jeb.077404 PubMedCrossRefGoogle Scholar
  72. Pérez-Mellado V (1983) Activity and thermoregulation patterns in two species of Lacertidae: Podarcis hispanica (Steindachner, 1870) and Podarcis bocagei (Seoane, 1884). Cienc Biol Ecol Syst 5:5–12Google Scholar
  73. Pérez-Mellado V (1998a) Podarcis muralis (Laurenti, 1768). In: Ramos MA et al. (eds) Fauna Ibérica. Museo Nacional de Ciencias Naturales, CSIC, Madrid, vol 10 pp 283–294Google Scholar
  74. Pérez-Mellado V (1998b) Podarcis lilfordi (Günther, 1874). In: Ramos MA et al. (eds) Fauna Ibérica., Museo Nacional de Ciencias Naturales, CSIC, Madrid, vol 10 pp 272–282Google Scholar
  75. Phillips JB (1986) Two magnetoreception pathways in a migratory salamander. Science 233:765–767PubMedCrossRefGoogle Scholar
  76. Phillips JB, Borland SC (1994) Use of a specialized magnetoreception system for homing by the eastern red-spotted newt Notophthalmus viridescens. J Exp Biol 188:275–291PubMedGoogle Scholar
  77. Phillips JB, Borland SC, Freake MJ, Brassart J, Kirschvink JL (2002) ‘Fixed-axis’ magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J Exp Biol 205:3903–3914PubMedGoogle Scholar
  78. 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
  79. Phillips JB, Jorge PE, Muheim R (2010a) 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 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Phillips JB, Muheim R, Jorge PE (2010b) A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J Exp Biol 213:3247–3255. doi:10.1242/jeb.020792 PubMedCrossRefGoogle Scholar
  81. Phillips JB, Youmans P, Muheim R (2013) Rapid learning of magnetic compass direction by C57BL/6 mice in a 4-armed ‘plus’ water maze. PLoS One 8:e73112. doi:10.1371/journal.pone.0073112 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Plotkin PT (2002) Adult migrations and habitat use. In: Lutz PL, Musick J, Wyneken J (eds) The biology of sea turtles, CRC Press, vol 2. Boca Raton, FL, pp 225–241CrossRefGoogle Scholar
  83. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ritz T, Ahmad M, Mouritsen H, Wiltschko R, Wiltschko W (2010) Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing. J R Soc Interface 7:S135–S146. doi:10.1098/rsif.2009.0456.focus PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 PubMedCrossRefGoogle Scholar
  86. Rocha CFD, Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidade) in an area of Amazonian Brazil. Ethol Ecol Evol 2:263–268CrossRefGoogle Scholar
  87. Rodda GH (1984a) Homeward paths of displaced juvenile alligators as determined by radiotelemetry. Behav Ecol Sociobiol 14:241–246CrossRefGoogle Scholar
  88. Rodda GH (1984b) The orientation and navigation of juvenile alligators: evidence of magnetic sensitivity. J Comp Physiol A 154:649–658. doi:10.1007/BF01350218 CrossRefGoogle Scholar
  89. Rodda GH (1985) Navigation in juvenile alligators. Z Tierpsychol 68:65–77. doi:10.1111/j.1439-0310.1985.tb00115.x CrossRefGoogle Scholar
  90. Rodgers CT, Hore PJ (2009) Chemical magnetoreception in birds: the radical pair mechanism. Proc Natl Acad Sci U S A 106:353–360. doi:10.1073/pnas.0711968106 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Roonwal ML (1958) Recent work on termite research in India (1947–57). Trans Bose Res Inst 22:77–100Google Scholar
  92. 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-Verlag, Berlin Heidelberg, pp 151–203. doi:10.1007/3-540-26604-6_7 CrossRefGoogle Scholar
  93. Schlegel P (2007) Spontaneous preferences for magnetic compass direction in the American red-spotted newt, Notophthalmus viridescens (Salamandridae, Urodela). J Ethol 25:177–184. doi:10.1007/s10164-006-0016-x CrossRefGoogle Scholar
  94. Schlegel P, Renner H (2007) Innate preference for magnetic compass direction in the Alpine newt, Triturus alpestris (Salamandridae, Urodela)? J Ethol 25:185–193. doi:10.1007/s10164-006-0017-9 CrossRefGoogle Scholar
  95. Schlegel PA (2008) Magnetic and other non-visual orientation mechanisms in some cave and surface urodeles. J Ethol 26:347–359. doi:10.1007/s10164-007-0071-y CrossRefGoogle Scholar
  96. Shine R, Kearney M (2001) Field studies of reptile thermoregulation: how well do physical models predict operative temperatures? Funct Ecol 15:282–288CrossRefGoogle Scholar
  97. Skiles DD (1985) The geomagnetic field: its nature, history and biological relevance. In: Kirschvink JL, Jones DS, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms: a new biomagnetism. Plenum Press, New York, pp 43–102CrossRefGoogle Scholar
  98. Slaby P, Tomanova K, Vácha M (2013) Cattle on pastures do align along the north--south axis, but the alignment depends on herd density. J Comp Physiol A 199:695–701. doi:10.1007/s00359-013-0827-5 CrossRefGoogle Scholar
  99. Solessio E, Engbretson GA (1993) Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature 364:442–445. doi:10.1038/364442a0 PubMedCrossRefGoogle Scholar
  100. Southwood A, Avens L (2010) Physiological, behavioral, and ecological aspects of migration in reptiles. J Comp Physiol B 180:1–23. doi:10.1007/s00360-009-0415-8 PubMedCrossRefGoogle Scholar
  101. Stapput K, Thalau P, Wiltschko R, Wiltschko W (2008) Orientation of birds in total darkness. Curr Biol 18:602–606. doi:10.1016/j.cub.2008.03.046 PubMedCrossRefGoogle Scholar
  102. Stevenson RD (1985) The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126:362–386CrossRefGoogle Scholar
  103. Taylor DH, Adler K (1978) The pineal body: site of extraocular perception of celestial cues for orientation in the tiger salamander (Ambystoma tigrinum). J Comp Physiol A 124:357–361. doi:10.1007/BF00661385 CrossRefGoogle Scholar
  104. 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-Verlag, Berlin, pp 334–346. doi:10.1007/978-3-662-11147-5_33 CrossRefGoogle Scholar
  105. Tesch FW, Lelek A (1973) Directional behaviour of transplanted stationary and migratory forms of the eel, Anguilla anguilla, in a circular tank. Neth J Sea Res 7:46–52. doi:10.1016/0077-7579(73)90031-8 CrossRefGoogle Scholar
  106. Tosini G (1997) The pineal complex of reptiles: physiological and behavioral roles. Ethol Ecol Evol 9:313–333. doi:10.1080/08927014.1997.9522875 CrossRefGoogle Scholar
  107. Vácha M, Kvíčalová M, Půžová T (2010) American cockroaches prefer four cardinal geomagnetic positions at rest. Behaviour 147:425–440CrossRefGoogle Scholar
  108. Vitt LJ, Caldwell JP (2009) Herpetology: an introductory biology of amphibians and reptiles, 3rd edn. Academic Press, New YorkGoogle Scholar
  109. Wada S, Kawano-Yamashita E, Koyanagi M, Terakita A (2012) Expression of UV-sensitive parapinopsin in the iguana parietal eyes and its implication in UV-sensitivity in vertebrate pineal-related organs. PLoS One 7:e39003. doi:10.1371/journal.pone.0039003 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Waldschmidt S (1980) Orientation to the sun by the iguanid lizards Uta stansburiana and Sceloporus undulatus: hourly and monthly variations. Copeia 1980:458–462. doi:10.2307/1444522 CrossRefGoogle Scholar
  111. Walker MM, Dennis TE, Kirschvink JL (2002) The magnetic sense and its use in long-distance navigation by animals. Curr Opin Neurobiol 12:735–744. doi:10.1016/S0959-4388(02)00389-6 PubMedCrossRefGoogle Scholar
  112. Wiltschko R, Stapput K, Ritz T, Thalau P, Wiltschko W (2007) Magnetoreception in birds: different physical processes for two types of directional responses. HFSP J 1:41–48. doi:10.2976/1.2714294 PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wiltschko R, Wiltschko W (1995) Magnetic orientation in animals. Springer-Verlag, Berlin, Heidelberg, New York. doi:10.1007/978-3-642-79749-1 Google Scholar
  114. Wiltschko R, Wiltschko W (2006) Magnetoreception. BioEssays 28:157–168. doi:10.1002/bies.20363 PubMedCrossRefGoogle Scholar
  115. Wiltschko R, Wiltschko W (2013) The magnetite-based receptors in the beak of birds and their role in avian navigation. J Comp Physiol A 199:89–98. doi:10.1007/s00359-012-0769-3 CrossRefGoogle Scholar
  116. Wiltschko W, Munro U, Ford H, Wiltschko R (2003) Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis. Aust J Zool 51:1–6. doi:10.1071/ZO03022 CrossRefGoogle Scholar
  117. Wiltschko W, Ritz T, Stapput K, Thalau P (2005) Two different types of light-dependent responses to magnetic fields in birds. Curr Biol 15:1518–1523. doi:10.1016/j.cub.2005.07.037 PubMedCrossRefGoogle Scholar
  118. Wiltschko W, Traudt J, Gunturkun O, Prior H, Wiltschko R (2002) Lateralisation of magnetic compass orientation in a migratory birds. Nature 419:467–470. doi:10.1038/nature00958 PubMedCrossRefGoogle Scholar
  119. Wiltschko W, Wiltschko R (2002) Magnetic compass orientation in birds and its physiological basis. Naturwissenschaften 89:445–452. doi:10.1007/s00114-002-0356-5 PubMedCrossRefGoogle Scholar
  120. Wiltschko W, Wiltschko R (2005) Magnetic orientation and magnetoreception in birds and other animals. J Comp Physiol A 191:675–693. doi:10.1007/s00359-005-0627-7 CrossRefGoogle Scholar
  121. Wiltschko W, Wiltschko R, Ritz T (2011) The mechanism of the avian magnetic compass. Procedia Chem 3:276–284. doi:10.1016/j.proche.2011.08.035 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Francisco J. Diego-Rasilla
    • 1
  • Valentín Pérez-Mellado
    • 1
  • Ana Pérez-Cembranos
    • 1
  1. 1.Departamento de Biología AnimalUniversidad de Salamanca, Campus Miguel de UnamunoSalamancaSpain

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