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Learned magnetic map cues and two mechanisms of magnetoreception in turtles

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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.
Data from all map assay experiments analysed cumulatively a, 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 = 2,676, P = 1.6 × 10⁻⁸, Hedge’s g = 0.50, n = 78). Each dot represents an individual response. Remaining conventions are as in Fig. 1. Extended Data Fig. 3 shows the same data plotted on a linear scale. b, Percentage change in turtle dancing responses in the rewarded field relative to the unrewarded field for all conditioned turtles. For each turtle, percentage change was defined as: Rewardedfieldturtledancing−unrewardedfieldturtledancingunrewardedfieldturtledancing×100\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\frac{{\rm{R}}{\rm{e}}{\rm{w}}{\rm{a}}{\rm{r}}{\rm{d}}{\rm{e}}{\rm{d}}\,{\rm{f}}{\rm{i}}{\rm{e}}{\rm{l}}{\rm{d}}\,{\rm{t}}{\rm{u}}{\rm{r}}{\rm{t}}{\rm{l}}{\rm{e}}\,{\rm{d}}{\rm{a}}{\rm{n}}{\rm{c}}{\rm{i}}{\rm{n}}{\rm{g}}-{\rm{u}}{\rm{n}}{\rm{r}}{\rm{e}}{\rm{w}}{\rm{a}}{\rm{r}}{\rm{d}}{\rm{e}}{\rm{d}}\,{\rm{f}}{\rm{i}}{\rm{e}}{\rm{l}}{\rm{d}}\,{\rm{t}}{\rm{u}}{\rm{r}}{\rm{t}}{\rm{l}}{\rm{e}}\,{\rm{d}}{\rm{a}}{\rm{n}}{\rm{c}}{\rm{i}}{\rm{n}}{\rm{g}}}{{\rm{u}}{\rm{n}}{\rm{r}}{\rm{e}}{\rm{w}}{\rm{a}}{\rm{r}}{\rm{d}}{\rm{e}}{\rm{d}}\,{\rm{f}}{\rm{i}}{\rm{e}}{\rm{l}}{\rm{d}}\,{\rm{t}}{\rm{u}}{\rm{r}}{\rm{t}}{\rm{l}}{\rm{e}}\,{\rm{d}}{\rm{a}}{\rm{n}}{\rm{c}}{\rm{i}}{\rm{n}}{\rm{g}}}\times 100$$\end{document}. The red dashed line indicates a 0% change in turtle dancing behaviour relative to the unrewarded field. The dots represent the percentage change in turtle dancing for individual turtles. The percentage change in turtle dancing behaviour was significantly greater than 0 (one-tailed Wilcoxon signed-rank test, w = 2,833, P = 6.2 × 10⁻¹¹, Hedge’s g = 0.55, n = 78). Source data
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Mismatched field experiments a, Experimental design. Turtles conditioned to discriminate between magnetic fields near Maine and Florida (see Fig. 2b) were exposed to three magnetic fields: the rewarded field, the unrewarded field and one of two mismatched fields, consisting either of rewarded inclination and unrewarded intensity or unrewarded inclination and rewarded intensity. The map was created using Natural Earth (https://www.naturalearthdata.com; credit Tom Patterson and Nathaniel Vaughn Kelso). b, Amount of time spent turtle dancing. The field treatment was a significant predictor of time spent turtle dancing (see Extended Data Table 1; analysis of variance, F(2,30) = 5.9, P = 0.007). Benjamini–Hochberg pairwise comparisons indicated that turtles danced significantly longer in their rewarded field than in the unrewarded field (P = 0.01, Hedge’s g = 0.97) or to the mismatched fields (P = 0.01, Hedge’s g = 0.67); responses to the mismatched fields and the unrewarded field did not differ (P = 0.9, Hedge’s g = 0.032). Conventions are as in Fig. 3. c, Percentage change in turtle dancing behaviour relative to the unrewarded field. The red dashed line indicates a 0% change. One-tailed Wilcoxon signed-rank tests indicate that the percentage change significantly exceeded 0 for the rewarded field (w = 133, ***P = 0.00008, Hedge’s g = 0.88, n = 16), but not for either of the mismatched fields (w = 17, P = 0.58, Hedge’s g = 0.18, n = 8 for the unrewarded inclination and rewarded intensity field; w = 26, P = 0.16, Hedge’s g = 0.42, n = 8 for the rewarded inclination and unrewarded intensity field). Responses to the rewarded field were not equivalent to the responses to either of the mismatched fields (unrewarded inclination and rewarded intensity: Wilcoxon two one-sided tests (TOST), w = 50, P = 0.20); rewarded inclination and unrewarded intensity field: Wilcoxon TOST, w = 44, P = 0.12). The black dots represent individual responses. The boxes span the first to third quartile, the centre line represents the median, and the whiskers represent the 5th and 95th percentiles. NS, not significant. Source data
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Results of experiments with oscillating magnetic fields in the radiofrequency range (radiofrequency field experiments) a, Results of the map assay. Responses to the initial behavioural tests showed that turtles successfully learned to discriminate between magnetic fields that exist near Maine (the rewarded field) and near Florida (the unrewarded field); these data (grey bars) are reproduced from Fig. 2b as a convenient reference. In the radiofrequency field experiments, responses to the rewarded field did not differ regardless of whether radiofrequency (RF) was absent (blue bar) or present (red bar; two-tailed Wilcoxon signed-rank test, w = 65, P = 0.9, Hedge’s g = 0.076, n = 16). Each dot represents results from a single individual. Conventions are as in Fig. 3. b, Results from the compass and map assay. Turtles exposed to a magnetic field that exists near the Cape Verde Islands swam approximately westwards and were significantly oriented (Rayleigh test, r = 0.53, P = 0.0004, mean angle = 293.2° (95% CI = 269.5–324.5°), n = 26, left circular plot). Turtles exposed to the same Cape Verde field but with radiofrequency present had orientation statistically indistinguishable from random (Rayleigh test, r = 0.19, P = 0.42, mean angle = 47.9°, n = 24, right circular plot). The two distributions were significantly different (Watson test, U² = 0.35, P < 0.01). The dots represent the swimming directions of individual turtles; in the left circular diagram, the black arrow represents the mean swimming direction of the entire group, and the dashed lines represent 95% confidence intervals. Data are plotted relative to magnetic north. In a,b, blue indicates treatments without radiofrequency fields, and red corresponds to treatments with radiofrequency fields. Source data
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Nature | Vol 638 | 27 February 2025 | 1015
Article
Learned magnetic map cues and two
mechanisms of magnetoreception in turtles
Kayla M. Goforth1,3 ✉, Catherine M. F. Lohmann1, Andrew Gavin2, Reyco Henning2,
Andrew Harvey1, Tara L. Hinton1, Dana S. Lim1 & Kenneth J. Lohmann1
Growing evidence indicates that migratory animals exploit the magnetic eld 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 elds replicating those that exist in particular oceanic
locations, juvenile turtles learned to distinguish magnetic elds in which they
encountered food from magnetic elds that exist elsewhere, an ability that might
underlie foraging site delity. Conditioned responses in this new magnetic map assay
were unaected by radiofrequency oscillating magnetic elds, a treatment expected
to disrupt radical-pair-based chemical magnetoreception4–6, 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 elds. The ndings provide evidence that two
dierent mechanisms of magnetoreception underlie the magnetic map and magnetic
compass in sea turtles.
Diverse animals migrate immense distances between specific areas used
in foraging, reproduction and seasonal sheltering
7–9
. How long-distance
migrant animals navigate to specific locations has remained enigmatic,
but the ability to exploit the magnetic field of the Earth as a source of
both directional information (that is, for a magnetic compass sense)
and positional information (that is, for a magnetic map sense) is an
important element in the navigational repertoire of many species
1,8,10
.
Magnetically sensitive animals can derive compass information
either from the direction (polarity) of field lines or from the relation-
ship between the tilt of magnetic field lines and gravity
10
. Magnetic map
information can be derived from several geomagnetic parameters that
vary predictably across the globe, including the intensity, or strength, of
the field and the inclination angle (the angle formed between magnetic
field lines and the surface of the Earth)1. The particular magnetic field
parameters that exist at a location, which are sometimes collectively
referred to as the ‘magnetic signature’ or ‘magnetic coordinates’ of a
site, can potentially provide an animal with a way to recognize a place
and return to it11–13.
Navigating to a known destination with a magnetic map presumably
requires an animal to learn and remember the magnetic signature of the
goal
2,3,12,13
. Nevertheless, despite strong evidence that sea turtles and
other animals possess magnetic maps
1
, an ability to learn the magnetic
signature of a location has yet to be demonstrated. Here we describe a
new behavioural assay in an iconic navigating species, the loggerhead
turtle (C. caretta), that relies on the ability of turtles to detect magnetic
map information. Our work provides direct evidence that an animal can
learn and remember the natural magnetic signature of a geographical
area. This ability may enable turtles and other animals to learn the
locations of ecologically important destinations and return to them
after long migrations.
A noteworthy feature of this new magnetic map assay is that turtles
respond to learned magnetic signatures without using the magnetic
compass; thus, the new assay effectively decouples the magnetic map
and compass senses. We used this decoupling to explore two major
questions of magnetic navigation research: first, how sea turtles
and other animals sense the magnetic field of the Earth, and second,
whether the same biophysical mechanism underlies the magnetic map
and compass. Using the magnetic map assay in combination with a sec-
ond, established assay that requires the magnetic compass, we report
strong evidence that two different mechanisms of magnetoreception
exist in sea turtles.
Learning magnetic signatures (map assay)
Sea turtles are renowned for their long-distance migrations and extraor-
dinary navigational abilities. At the beginning of their lives, logger
-
head turtles respond to magnetic signatures along their transoceanic
migratory route by swimming in directions that help them to remain
within favourable ocean currents and advance along the migratory
pathway14,15. Following this initial migration, turtles take up residence
https://doi.org/10.1038/s41586-024-08554-y
Received: 30 November 2023
Accepted: 19 December 2024
Published online: 12 February 2025
Check for updates
1Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA. 2Department of Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
3Present address: Department of Biology, Texas A&M University, College Station, TX, USA. e-mail: kmgoforth@tamu.edu
Content courtesy of Springer Nature, terms of use apply. Rights reserved
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