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Learned magnetic map cues and two mechanisms of magnetoreception in turtles

Abstract

Growing evidence indicates that migratory animals exploit the magnetic field of the Earth for navigation, both as a compass to determine direction and as a map to determine geographical position1. It has long been proposed that, to navigate using a magnetic map, animals must learn the magnetic coordinates of the destination2,3, yet the pivotal hypothesis that animals can learn magnetic signatures of geographical areas has, to our knowledge, yet to be tested. Here we report that an iconic navigating species, the loggerhead turtle (Caretta caretta), can learn such information. When fed repeatedly in magnetic fields replicating those that exist in particular oceanic locations, juvenile turtles learned to distinguish magnetic fields in which they encountered food from magnetic fields that exist elsewhere, an ability that might underlie foraging site fidelity. Conditioned responses in this new magnetic map assay were unaffected by radiofrequency oscillating magnetic fields, a treatment expected to disrupt radical-pair-based chemical magnetoreception4,5,6, suggesting that the magnetic map sense of the turtle does not rely on this mechanism. By contrast, orientation behaviour that required use of the magnetic compass was disrupted by radiofrequency oscillating magnetic fields. The findings provide evidence that two different mechanisms of magnetoreception underlie the magnetic map and magnetic compass in sea turtles.

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Fig. 1: Results from conditioning experiments in which turtles learned to discriminate between magnetic fields replicating those that exist near New Hampshire, USA, and in the Gulf of Mexico.
Fig. 2: Results of four additional map assay experiments, in which turtles discriminated between a magnetic field in which they were fed and a magnetic field in which they were not.
Fig. 3: Data from all map assay experiments analysed cumulatively.
Fig. 4: Mismatched field experiments.
Fig. 5: Results of experiments with oscillating magnetic fields in the radiofrequency range (radiofrequency field experiments).

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Data availability

There are no restrictions on data availability. Access to the data can be found on GitHub (https://github.com/kaylago/Goforthetal_LearnedMagneticMapCuesandTwoMechanismsofMagnetoreceptioninTurtles.git). Source data are provided with this paper.

Code availability

Custom-written software by A.H. facilitated data collection in the compass and map assay experiments, but the software was not central to the research or conclusions. The code can be accessed on GitHub (https://github.com/radiotech/Caretta2_Encoder).

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Acknowledgements

We thank J. R. Brothers, D. Ernst, S. Johnsen, J. Granger, D. Steinberg, L. Naisbett-Jones, H. Havens and A. Mackiewicz for discussions of experimental design and manuscript drafts; I. Wilson, A. Barnett, J. Settelen, M. Hankins, A. Boyce, C. Manzonelli, N. Bal, N. Iverson, A. Jacks, E. Tsai, K. Steininger, D. Oakley, K. Ritterpusch, W. Jian, V. Sirupirapu, I. Taylor, G. Knaack, S. Hu, E. Cho, M. Kennedy, A. Halferty, C. Koricke, C. Herschfield, A. Ronn, I. Donnolo, V. Zhang, L. Johnson, A. Kang, T. Hinton, M. Kane, R. Davids, S. Palmieri, L. Prince, S. Nichols, W. Hammond, S. Gerber and A. Byrd for assistance with conditioning and data analyses; L. Soltan, G. Sollom, M. Babb and W. Gary for help with turtle care; L. Prince for assistance with nest marking; and A. Goforth, D. Goforth and A. Wasif for assistance with coil construction and transport.

Author information

Authors and Affiliations

Authors

Contributions

The research plan was conceived by K.M.G., K.J.L. and C.M.F.L. K.M.G. conducted the conditioning experiments and data analyses with input from K.J.L. and C.M.F.L. K.M.G., D.S.L., T.L.H., K.J.L. and C.M.F.L. conducted the compass and map assay experiments. A.H. wrote the software used in some experiments. A.G. and R.H. generated and measured the radiofrequency fields. K.M.G., K.J.L. and C.M.F.L. drafted the manuscript, which was revised with input from all authors. This research was supported by the Air Force Office of Scientific Research grant FA9550-20-1-0399 to K.J.L. and the National Science Foundation grant IOS-1456923 to K.J.L. and C.M.F.L. A.G. was supported by the National Science Foundation grant OISE-1743790. R.H. and A.G. were supported by the US Department of Energy, Office of Science, Office of Nuclear Physics grants DEFG02-97ER41041 and DEFG02- 97ER41033.

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Correspondence to Kayla M. Goforth.

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Extended data figures and tables

Extended Data Fig. 1 Results from Fig. 1 plotted on a linear scale.

Turtles learned to discriminate between magnetic fields replicating ones that exist near New Hampshire, U.S.A. and in the Gulf of Mexico. (a) Map showing relative locations of the two treatment fields. The map was created using Natural Earth (https://www.naturalearthdata.com; credit Tom Patterson and Nathaniel Vaughn Kelso). (b) In tests conducted immediately after the conditioning period, turtles exhibited significantly higher levels of turtle dance behavior when experiencing the field in which they had been fed (two-tailed Wilcoxon signed-rank test, w = 123, p = 0.003, Hedge’s g = 0.88, n = 16, = turtles rewarded in the New Hampshire field, ▲ = turtles rewarded in the Gulf of Mexico field). See Methods for details of analysis. (c) Turtles were tested a second time, four months after the initial experiments, without experiencing either the rewarded or unrewarded field in the interim. Turtles still discriminated between the two fields (two-tailed Wilcoxon signed-rank test, w = 118, p = 0.01, Hedge’s g = 0.62, n = 16). Error bars represent standard error.

Extended Data Fig. 2 Results of additional map assay experiments plotted on a linear scale.

In four additional experiments, turtles discriminated between a magnetic field in which they were fed and one in which they were not. Turtles differentiated between magnetic fields that exist near: (a) Delaware, U.S.A. and Cuba (two-tailed Wilcoxon signed-rank test, w = 108, p = 0.04, Hedge’s g = 0.50, n = 16); (b) Maine and Florida, U.S.A. (two-tailed Wilcoxon signed-rank test, w = 121, p = 0.004, Hedge’s g = 0.63, n = 16); (c) Newfoundland, Canada and Virginia, U.S.A. (two-tailed Wilcoxon signed-rank test, w = 115, p = 0.01, Hedge’s g = 0.60, n = 16); and (d) the Turks and Caicos Islands and Haiti (two-tailed Wilcoxon signed-rank test, w = 97, p = 0.003, Hedge’s g = 0.60, n = 14). The data in (c) represent a second conditioning experiment conducted with the same turtles used in (b) and thus indicate that turtles can learn magnetic fields that exist at multiple locations. For each pair of magnetic fields, the rewarded field for the turtle is indicated by either or ▲ as indicated on the figure. Remaining conventions as in Fig. 1. The maps were created using Natural Earth (https://www.naturalearthdata.com; credit Tom Patterson and Nathaniel Vaughn Kelso).

Extended Data Fig. 3 Data from all map assay experiments (Fig. 3a) plotted on a linear scale.

Turtles learned to discriminate between a magnetic field in which they received food and one in which they did not (two-tailed Wilcoxon signed-rank test, w = 2676, p = 1.6 × 10−8, Hedge’s g = 0.50, n = 78). Conventions as in Fig. 3a.

Extended Data Fig. 4 Percent change in turtle dancing responses for all turtles.

Percent change = \(\frac{{Rewarded\; field\; turtle\; dancing}-{Unrewarded\; field\; turtle\; dancing}}{{Unrewarded\; field\; turtle\; dancing}}\,* \,100\). Red dotted lines indicate 0% change relative to the unrewarded field. Dots represent the percent change for individuals; dot color corresponds to the rewarded magnetic field as indicated on the figure. All data were analyzed with one-tailed Wilcoxon signed-rank tests. (a) Turtles conditioned to magnetic fields near New Hampshire, U.S.A. and the Gulf of Mexico had a percent change in dancing behavior significantly greater than zero (w = 127, p = 0.0005, Hedge’s g = 0.80, n = 16). (b) When these same turtles were tested four months after conditioning ended, without exposure to either field in the interim, percent change in dancing was again significantly greater than zero (w = 124, p = 0.001, Hedge’s g = 0.85, n = 16). (c) Turtles conditioned to Delaware, U.S.A. and Cuba had a percent change in dancing behavior significantly greater than zero (w = 118, p = 0.004, Hedge’s g = 0.45, n = 16). (d) Turtles with a rewarded field of Maine, U.S.A. had a percent change in dancing significantly greater than zero (w = 121, p = 0.002, Hedge’s g = 0.80, n = 16). (e) Turtles conditioned to Newfoundland, Canada and Virginia, U.S.A., had a percent change in dancing significantly greater than zero (w = 120, p = 0.003, Hedge’s g = 0.63, n = 16). (f) Turtles conditioned to Haiti and the Turks and Caicos had a percent change in dancing significantly greater than zero (w = 99, p = 0.0009, Hedge’s g = 0.94, n = 14). Collectively, these analyses of percent change corroborate the findings based on raw data in Figs. 1 and 2.

Extended Data Fig. 5 Measured RF magnetic flux at water level in the testing environments in the two RF experiments.

(a) Magnetic flux density of the broadband oscillating magnetic fields, as well as the background magnetic field fluctuations, produced during the map assay experiments. Single runs (a single measurement of the field) are displayed as vertical dashed lines and are digitized with 25 MHz sampling frequency and a 2048 sample buffer. Measurements extended to 12 MHz but only values in the targeted range (0.1–10 MHz) were included in calculations. (b) Magnetic flux density of the broadband magnetic fields produced and the background magnetic field fluctuations during the compass & map assay experiments. Single runs are displayed as vertical dashed lines and are digitized with 20 MHz sampling frequency and a 1200 sample buffer. In (a) and (b) solid lines represent the average magnetic noise density, calculated from 10 and 8 repeated measurements respectively.

Extended Data Table 1 Results of the linear mixed effects model for the mismatched field experiments
Extended Data Table 2 Magnetic fields used to approximate conditions in different geographic areas

Supplementary information

Reporting Summary

Supplementary Video 1

Turtle dance behavior. The video shows one sequence of vigorous turtle dance behavior in the presence of food, followed by several more subtle instances of turtle dance behavior when a turtle was in the rewarded magnetic field but food was absent. Turtles swimming in the unrewarded field are also shown to illustrate baseline behavior for comparative purposes.

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Goforth, K.M., Lohmann, C.M.F., Gavin, A. et al. Learned magnetic map cues and two mechanisms of magnetoreception in turtles. Nature 638, 1015–1022 (2025). https://doi.org/10.1038/s41586-024-08554-y

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