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Use of sun compass orientation during natal dispersal in Blanding’s turtles: in situ field experiments with clock-shifting and disruption of magnetoreception

  • John D. Krenz
  • Justin D. Congdon
  • Meredith A. Schlenner
  • Michael J. Pappas
  • Bruce J. Brecke
Original Article

Abstract

When hatchling freshwater turtles emerge from nests and first experience environmental stimuli, they primarily use visual cues to disperse toward nearby open horizons or far dark horizons. Within hours, hatchling Blanding’s turtles (Emydoidea blandingii) develop compass mechanisms to maintain their headings when the initial dispersal targets become invisible. We captured hatchling Blanding’s turtles during dispersal in natural habitat, attached a magnetic or non-magnet disk to each turtle, translocated them into an arena in a visually uniform field of corn, and measured their compass orientation (heading). Hatchlings from the magnet and no-magnet groups were evenly divided into two environmental chambers (6-h clock-shift or non-clock-shift) to create four experimental treatments. After 5 to 11 days hatchlings were re-released in the arena. If hatchlings used a time-compensated sun compass, then clock-shifting would cause a ~90° change in heading. If they used a geomagnetic compass, disruption of magnetoreception would cause wandering. If both compasses were used simultaneously or sequentially, we predicted a range of outcomes. All four treatment groups dispersed directionally during both trials, maintaining their prior headings in natural habitat except for the clock-shift treatment which changed heading ~90° as predicted. The ability of hatchlings to maintain prior headings despite the disruption of geomagnetism supports the absence, inactivity, or disregard of a geomagnetic compass. Only a time-compensated sun compass coupled with an internal clock was necessary and sufficient for hatchlings to maintain compass headings during natal dispersal when relocated from natural prairie habitat to a monoculture habitat with a relatively uniform visual horizon.

Significance statement

Individuals moving long distances (e.g., migrating birds or dispersing salamanders) often maintain their movement headings using compass orientation (i.e., a geomagnetic or time-compensated sun compass). When hatchling freshwater turtles emerge from underground terrestrial nests they initiate dispersal in search of wetlands primarily based on visual horizon cues. Because such cues often become obscured by uneven terrain or dense vegetation and because straight-line travel is more efficient and less risky, hatchlings soon develop a mechanism of compass orientation to maintain their dispersal headings. We disrupted their ability to use magnetoreception by attaching magnets to their shells, manipulated their sense of time-of-day with clock-shifting, and then monitored their dispersal in a visually uniform field of mature corn. Our results demonstrated that a sun compass was necessary and sufficient for hatchlings with dispersal experience to maintain their dispersal headings when natural environmental cues were not visible.

Keywords

Biological clock Clock-shift Geomagnetic compass Natal dispersal Orientation Sun compass 

Notes

Acknowledgments

The success of this study was greatly enhanced by the late John Danckwart who graciously allowed us to create an arena in his corn field in 2012 and 2013. Abigail Armstrong, Leslie Schroeder, Robert Stewert, Amanda Sausen, Sarah Bonnell, Josephine Hartung, Steve Freedberg, Anne Yen, and Martha Sichko assisted in the field and laboratory. Michael Bottesch and Henrik Mouritsen assisted in conducting the Hotelling tests. St. Olaf College and The Nature Conservancy allowed us the use of the Weaver Dunes field station. Earlier drafts of the manuscript were improved by Nancy Dickson. Minnesota State University provided sabbatical leave to JDK during 2012.

Author contributions

Experimental design for sun compass: JDK, MAS. Experimental design for geomagnetic compass: JDK, JDC, MJP. Clock-shifting treatments: JDK, MAS. Capture, handling and care of animals, and the execution of arena trials: all authors. Analysis of data: JDK, JDC, MAS. Writing: JDK, JDC.

Funding

Research was supported by the authors and research and manuscript preparation were aided by the Office of Biological and Environmental Research, U.S. Department of Energy through Financial Assistant Award No. DE-FC09-96SR18546 to the University of Georgia Research Foundation and by the Savannah River Ecology Laboratory.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The study was conducted under permits (13808 and 15422) from Richard Baker, Jaime Edwards, Gary Nelson, and Don Ramsden of the Minnesota Department of Natural Resources, and permit 2007-17R from Richard Biske of The Nature Conservancy.

The methods of care and use for this study were approved by the Institutional Animal Care and Use Committee at Minnesota State University.

References

  1. Able KP (1980) Mechanisms of orientation, navigation and homing. In: Gauthreaux SA Jr (ed) Animal migration, orientation, and navigation. Academic Press, New York, pp 283–373CrossRefGoogle Scholar
  2. Anderson PK (1958) The photic responses and water-approach behavior of hatchling turtles. Copeia 1958:211–215CrossRefGoogle Scholar
  3. Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James P, Rosenberg M, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575CrossRefPubMedGoogle Scholar
  4. Avens L, Lohmann KJ (2003) Use of multiple orientation cues by juvenile loggerhead sea turtles (Caretta caretta). J Exp Biol 206:4317–4325CrossRefPubMedGoogle Scholar
  5. Butler BO, Graham TE (1995) Early post-emergent behavior and habitat selection in hatchling Blanding’s turtles, Emydoidea blandingii, in Massachusetts. Chelonian Conserv Bi 1:187–196Google Scholar
  6. Caldwell IR, Nams VO (2006) A compass without a map: tortuosity and orientation of eastern painted turtles (Chrysemys picta picta) released in unfamiliar territory. Can J Zool 84:1129–1137CrossRefGoogle Scholar
  7. Congdon JD, Pappas MJ, Brecke BJ, Capps JD (2011) Conservation implications of initial orientation of naïve hatchling snapping turtles (Chelydra serpentina) and painted turtles (Chrysemys picta belli) dispersing from experimental nests. Chelonian Conserv Bi 10:42–53CrossRefGoogle Scholar
  8. Congdon JD, Pappas MJ, Krenz JD, Brecke BJ, Schlenner MA (2015) Compass orientation during dispersal of freshwater hatchling snapping turtles (Chelydra serpentina) and Blanding’s turtles (Emydoidea blandingii). Ethology 120:1–10Google Scholar
  9. Crawford JA, Semlitsch RD (2007) Estimation of core terrestrial habitat for stream-breeding salamanders and delineation of riparian buffers for protection of biodiversity. Conserv Biol 21:152–158CrossRefPubMedGoogle Scholar
  10. DeRosa CT, Taylor DH (1978) Sun-compass orientation in the painted turtle, Chrysemys picta (Reptilia, Testudines, Testudinidae). J Herpetol 12:25–28CrossRefGoogle Scholar
  11. DeRosa CT, Taylor DH (1982) A comparison of compass orientation mechanisms in three turtles (Trionyx spinifer, Chrysemys picta, and Terrapene carolina). Copeia 1982:394–399CrossRefGoogle Scholar
  12. Iverson JB, Prosser RL, Dalton EN (2009) Orientation in juveniles of a semiaquatic turtle Kinosternon flavescens. Herpetology 65:237–245CrossRefGoogle Scholar
  13. Johnsen S, Lohmann KJ (2008) Magnetoreception in animals. Phys Today 61:29–35CrossRefGoogle Scholar
  14. Krochmal AR, Roth TC Jr, Rush S, Wachter K (2015) Turtles outsmart rapid environmental change: the role of cognition in navigation. Commun Integr Biol 8:e1052922CrossRefPubMedGoogle Scholar
  15. Landler L, Painter MS, Youmans PW, Hopkins WA, 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:e0124728CrossRefPubMedPubMedCentralGoogle Scholar
  16. Lanzerotti LJ, Krimigis SM (1985) Comparative magnetospheres. Phys Today 38:25–34CrossRefGoogle Scholar
  17. Lohmann KJ, Lohmann CM (1996) Detection of magnetic field intensity by sea turtles. Nature 380:5–61CrossRefGoogle Scholar
  18. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511CrossRefPubMedGoogle Scholar
  19. Noble GK, Breslau AM (1938) The senses involved in the migration of young fresh-water turtles after hatching. J Comp Psychol 25:175–193CrossRefGoogle Scholar
  20. Pappas MJ, Congdon JD, Brecke BJ, Capps JD (2009) Orientation and dispersal of hatchling Blanding’s turtles (Emydoidea blandingii) from experimental nests. Can J Zool 87:755–766CrossRefGoogle Scholar
  21. Pappas MJ, Congdon JD, Brecke BJ, Freedberg S (2013) Orientation of freshwater hatchling Blanding's (Emydoidea blandingii) and snapping turtles (Chelydra serpentina) dispersing from experimental nests in agricultural fields. Herpetol Conserv Biol 8:385–399Google Scholar
  22. Phillips JB, Moore FR (1992) Calibration of the sun compass by sunset polarized light patterns in a migratory bird. Behav Ecol Sociobiol 31:189–193CrossRefGoogle Scholar
  23. Pyke GH (1984) Optimal foraging theory: a critical review. Annu Rev Ecol Syst 15:523–575CrossRefGoogle Scholar
  24. Roth TC, Krochmal AR (2015) The role of age-specific learning and experience for turtles navigating a changing landscape. Curr Biol 25:333–337CrossRefPubMedGoogle Scholar
  25. Semlitsch RD, Bodie JR (2003) Biological criteria for buffer zones around wetlands and riparian habitats for amphibians and reptiles. Conserv Biol 17:1219–1228CrossRefGoogle Scholar
  26. Semlitsch RD, Jensen JB (2001) Core habitat, not buffer zone. Natl Wetl Newsl 23:5–11Google Scholar
  27. Sumner J, Rousset F, Estoup A, Moritz C (2001) ‘Neighbourhood’ size, dispersal and density estimates in the prickly forest skink (Gnypetoscincus queenslandiae) using individual genetic and demographic methods. Mol Ecol 10:1917–1927CrossRefPubMedGoogle Scholar
  28. Tuttle SE, Carroll DM (2005) Movements and behavior of hatchling wood turtles (Glyptemys insculpta). Northeast Nat 12:331–348CrossRefGoogle Scholar
  29. Van Dyck H, Baguette M (2005) Dispersal behaviour in fragmented landscapes: routine or special movements? Basic Appl Ecol 6:535–545CrossRefGoogle Scholar
  30. Wiltschko W (1983) Compasses used by birds. Comp Biochem Phys A 76:709–717CrossRefGoogle Scholar
  31. Wiltschko W, Wiltschko R (1976) Interrelation of magnetic compass and star orientation in night-migrating birds. J Comp Physiol 109:91–99CrossRefGoogle Scholar
  32. Wiltschko W, Wiltschko R (1996) Magnetic orientation in birds. J Exp Biol 199:29–38Google Scholar
  33. Wiltschko R, Wiltschko W (2001) Clock-shift experiments with homing pigeons: a compromise between solar and magnetic information? Behav Ecol Sociobiol 49:393–400CrossRefGoogle Scholar
  34. Wiltschko W, Wiltschko R, Keeton WT, Brown AI (1987) Pigeon homing: the orientation of young birds that had been prevented from seeing the sun. Ethology 76:27–32CrossRefGoogle Scholar
  35. Wu J (2006) Landscape ecology, cross-disciplinarity, and sustainability science. Landsc Ecol 21:1–4CrossRefGoogle Scholar
  36. Wyeth RC (2010) Should animals navigating over short distances switch to a magnetic compass sense? Front Behav Neurosci 4:42PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesMinnesota State UniversityMankatoUSA
  2. 2.Savannah River Ecology LaboratoryAikenUSA
  3. 3.Bar Boot RanchDouglasUSA
  4. 4.North BendUSA
  5. 5.WelchUSA

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