Naturwissenschaften

, Volume 101, Issue 11, pp 907–911

Behavioural evidence of magnetoreception in dolphins: detection of experimental magnetic fields

Authors

  • Dorothee Kremers
    • Laboratoire d’Éthologie Animale et Humaine - EthoS UMR CNRS 6552Université de Rennes 1
  • Juliana López Marulanda
    • Laboratoire d’Éthologie Animale et Humaine - EthoS UMR CNRS 6552Université de Rennes 1
  • Martine Hausberger
    • Laboratoire d’Éthologie Animale et Humaine - EthoS UMR CNRS 6552Université de Rennes 1
    • Laboratoire d’Éthologie Animale et Humaine - EthoS UMR CNRS 6552Université de Rennes 1
    • Institut Universitaire de France
Original Paper

DOI: 10.1007/s00114-014-1231-x

Cite this article as:
Kremers, D., López Marulanda, J., Hausberger, M. et al. Naturwissenschaften (2014) 101: 907. doi:10.1007/s00114-014-1231-x

Abstract

Magnetoreception, meaning the perception of magnetic fields, is supposed to play an important role for orientation/navigation in some terrestrial and aquatic species. Although some spatial observations of free-ranging cetaceans’ migration routes and stranding sites led to the assumption that cetaceans may be sensitive to the geomagnetic field, experimental evidence is lacking. Here, we tested the spontaneous response of six captive bottlenose dolphins to the presentation of two magnetized and demagnetized controlled devices while they were swimming freely. Dolphins approached the device with shorter latency when it contained a strongly magnetized neodymium block compared to a control demagnetized block that was identical in form and density and therefore undistinguishable with echolocation. We conclude that dolphins are able to discriminate the two stimuli on the basis of their magnetic properties, a prerequisite for magnetoreception-based navigation.

Keywords

Sensory perceptionMagnetic senseCetaceans

Introduction

The geomagnetic field is a dipole field generated by the Earth’s fluid outer iron core (Wiltschko and Wiltschko 1995) providing a consistent source of directional information (Winklhofer 2010). Different taxa can detect this magnetic field, although primary magnetoreceptors have not yet been unequivocally identified (Lohmann and Johnson 2000; Winklhofer 2010). Several species use geomagnetic cues for orientation during navigation and migration (Wiltschko and Wiltschko 1995). Some mammalian species respond to the geomagnetic field by spontaneously orientating their body with respect to magnetic field lines (Begall et al. 2008; Červený et al. 2011; Wang et al. 2007). Other mammals, notably rodents, build their nests by referring to the magnetic field (Kimchi and Terkel 2001; Marhold et al. 1997) or use a magnetic compass to navigate (Holland et al. 2006).

Geomagnetic information is not only available on land but also at sea, providing potential navigational cues (Walker and Dennis 2005). Observations of free-ranging cetaceans show some evidence of magnetoreception-based navigation. Fin whale migration routes are correlated with low geomagnetic intensity (Walker et al. 1992). Furthermore, offshore cetaceans’ live strandings seem to occur where valleys in the geomagnetic field cross the coast (Kirschvink et al. 1986; Klinowska 1985). However, experimental evidence for magnetoreception in cetaceans is lacking. When captive bottlenose dolphins were exposed to a magnetic field (introduced into their pool by an induction coil; magnetic field strength unknown) they did not show any spontaneous response (Bauer et al. 1985). Even during a series of conditioning experiments using two-choice discrimination and go/no-go designs (magnetic field strength 37 μT), the dolphins did not show any indication of a magnetic discrimination (Bauer et al. 1985). However, Bauer et al. (1985) admitted that “experiments that constrain the subject in time and place may be putting significant limits on appropriate orientation”. Therefore, we conducted an experiment that neither confined the dolphins spatially to one position as for example during a go/no-go experiment nor demanded a direct response as it is the case in conditioning experiments but rather observed their spontaneous reaction towards magnetized and demagnetized devices.

Methods

Study subjects and housing conditions

In January/February 2013, we studied six captive-born bottlenose dolphins (Tursiops truncatus; four males aged 5, 8, 14, and 29 years; two females aged 5 and 12 years) in the delphinarium of Planète Sauvage (Port-Saint-Père, France). Overall, this outdoor facility consists of four pools, covering 2,000 m2 water surface and containing 7,500,000 l salt water. During the entire experiment, the animals were free to move in and out the pool where the experimental device was installed (details: ESM), meaning that all six individuals were tested simultaneously while all group members were free to interact at any time with the device during a given experimental session.

Data collection

We used a neodymium block (10 × 10 × 1.5 cm) with a magnetic field strength of 1.2 T (Ingeniería Magnética Aplicada, S.L., Barcelona, Spain; ESM Fig. 1) that was placed in an opaque plastic barrel (20 × 26 cm). During an experimental session, the barrel hung in the water at a depth of 50 cm, 40 cm away from the pool wall (details: ESM). Because the barrel was perforated, the magnet inside was in contact with the pool water. At the end of a session, the device was removed from the pool. The magnet remained at the same position in the barrel during all the experiment so that magnetic field direction never changed. As control stimulus we used the exact same (size/density) but demagnetized neodymium block. During an experimental session, only one device was used, containing either the magnetized or the demagnetized neodymium block, and was installed by a person blind to the content of the barrel.

Before the experiment started, we conducted 51 sessions with an empty barrel to habituate the dolphins. Thereafter, 30 sessions with the magnetized block and 30 sessions with the demagnetized block were done on 13 consecutive days, presenting the two stimuli in a randomized order (1–6 experimental sessions per day). An experimental session started at the moment the barrel was placed in the water (experimenter left) and lasted 15 min during which the individual responses of the six dolphins were filmed by a video camera (Sony HDR-XR155) on a tripod behind the device. Sessions continued no matter if some dolphins stayed or swam out of the pool.

Later, the videos were analysed by an observer who was able to identify the dolphins but was blind to the content of the barrel visible in the video. The observation followed a continuous and simultaneous individual sampling of the six dolphins (sampling all occurrences of some previously defined behaviours), thus different behaviours that occurred during the 15 min within a range of 1.5 m around the barrel, defined as the experimental area, were measured or counted for each individual dolphin (even if several individuals were present at the same time): latency for the first approach (i.e. entering the experimental area), proximity duration (i.e. time spent within the experimental area), latencies for the first rostrum contact and the first body contact (i.e. contact with another part of the body), number and duration of rostrum and body contacts. If an individual did not approach or touch the device during a session, the session’s total duration (900 s) was used for statistical analysis on latencies. As the dolphins were not tested with individuals isolated and as dolphins were free to approach or not, the number of times a given dolphin was close to the barrel differed between individuals.

Data analysis

Due to very strong sun reflections from the water surface, one magnet session and five control sessions had to be removed from further analysis, because visibility did not allow for dolphin identification. Statistical analyses were ran using R software (version 2.15.0). We compared all variables (approach latency, proximity duration, latencies for first rostrum and body contact, number and duration of rostrum and body contacts) between magnet and control sessions with Wilcoxon signed-rank tests using the mean values for each individual. In the text, values present mean ± SE.

Results

Although the six tested dolphins showed some individual differences in their responses towards the magnetized and the demagnetized stimulus (Table 1), we found that the individuals behaved overall in the same way. On the one hand, most behaviour did not differ between sessions using the magnet and sessions using the control. Dolphins spent similar durations in the presence of both devices (magnet 26.3 ± 5.2 s, control 26.6 ± 5.0 s, p = 0.5625, V = 14). The latencies for the first contact (rostrum contacts: magnet and control 11.6 ± 0.4 min, p = 1, V = 11; body contacts: magnet 14.0 ± 0.2 min, control 13.5 ± 0.3 min, p = 0.1056, V = 1), number of contacts (rostrum contacts: magnet 2.4 ± 0.5, control 3.4 ± 0.8, p = 0.2188, V = 17; body contacts: magnet and control 0.2 ± 0.1, p = 0.7874, V = 9) and the duration of contacts (rostrum contacts: magnet 2.9 ± 0.6 s, control 3.8 ± 0.9 s, p = 0.3125, V = 16; body contacts: magnet 0.4 ± 0.1 s, control 0.3 ± 0.1 s, p = 1, V = 7) did not differ statistically. One behaviour, however, differed between sessions using the magnet and sessions using the control: Dolphins approached the magnetized device with significantly shorter latency than the control device (magnet 5.7 ± 0.5 min, control 6.2 ± 0.5 min, p = 0.0313, V = 21; Fig. 1).
Table 1

Mean ± SE values and ranges for each variable measured (minimum–maximum) for each individual dolphin (sex/age given in parenthesis after the name) during magnet (N = 29) and control (N = 25) sessions. Interpretation of latency variables: 0.0 min = dolphin approached/touched experimental device as soon as it was placed in the water; 15 min = dolphin never approached/touched experimental device during a session

Variable

Stimulus

Amtan

(♀, 12)

Cecil

(♂, 29)

Kite

(♂, 8)

Parel

(♀, 5)

Peos

(♂, 14)

Spat

(♂, 5)

Latency for 1st approach [min]

Magnet

5.7 ± 1.1

2.5 ± 0.7

11.9 ± 1.0

3.8 ± 1.0

5.0 ± 0.9

5.6 ± 1.0

0.0–15

0.0–15

0.05–15

0.0–15

0.03–15

0.0–15

Control

7.0 ± 1.2

2.9 ± 0.7

12.0 ± 1.0

3.9 ± 1.1

5.5 ± 1.0

5.9 ± 1.2

0.0–15

0.1–14.0

1.2–15

0.0–15

0.0–15

0.03–15

Proximity duration [sec]

Magnet

30.6 ± 7.9

25.5 ± 3.2

1.6 ± 0.7

49.3 ± 18.2

18.9 ± 7.0

32.0 ± 21.9

0–193

0–70

0–18

0–484

0–183

0–653

Control

34.9 ± 11.5

15.8 ± 2.5

2.1 ± 0.9

52.4 ± 15.4

22.9 ± 9.3

31.8 ± 19.5

0–216

2–43

0–19

0–288

0–226

0–505

Latency for 1st rostrum contact [min]

Magnet

9.0 ± 1.2

13.4 ± 0.7

15.0 ± 0.0

7.6 ± 1.3

11.9 ± 1.0

13.0 ± 0.8

0.0–15

0.8–15

15

0.0–15

0.5–15

0.3–15

Control

9.9 ± 1.2

13.3 ± 0.7

14.4 ± 0.5

7.8 ± 1.3

12.5 ± 0.9

11.8 ± 1.1

0.02–15

0.8–15

1.1–15

0.03–15

0.3–15

0.03–15

Number of rostrum contacts

Magnet

4.2 ± 1.6

1.3 ± 0.6

0

6.0 ± 1.9

1.8 ± 1.1

0.9 ± 0.5

0–44

0–13

0

0–38

0–30

0–12

Control

4.7 ± 1.6

0.8 ± 0.4

0.2 ± 0.2

9.2 ± 2.6

1.6 ± 0.9

3.9 ± 2.9

0–28

0–9

0–6

0–39

0–20

0–74

Duration of rostrum contacts [sec]

Magnet

5.8 ± 2.1

0.8 ± 0.3

0

9.1 ± 2.7

1.5 ± 1.0

0.7 ± 0.4

0–53.5

0–8

0

0–55.5

0–28.5

0–9

Control

5.1 ± 1.9

0.6 ± 0.3

0.5 ± 0.5

11.6 ± 3.7

1.6 ± 1.0

3.7 ± 2.7

0–40.5

0–6.5

0–13.5

0–64

0–24

0–68

Latency for 1st body contact [min]

Magnet

15.0 ± 0.0

14.9 ± 0.1

15.0 ± 0.0

12.7 ± 0.9

14.5 ± 0.5

12.1 ± 0.9

15

11.4–15

15

0.9–15

0.1–15

0.7–15

Control

15.0 ± 0.0

14.6 ± 0.1

14.4 ± 0.04

10.7 ± 0.1

14.6 ± 0.1

11.9 ± 0.3

15

10.0–15

1.2–15

0.7–15

5.8–15

0.3–15

Number of body contacts

Magnet

0

0.03 ± 0.03

0

0.7 ± 0.3

0.1 ± 0.1

0.7 ± 0.2

0

0–1

0

0–6

0–2

0–6

Control

0

0.2 ± 0.1

0.04 ± 0.04

0.4 ± 0.1

0.1 ± 0.1

0.7 ± 0.3

0

0–2

0–1

0–1

0–1

0–6

Duration of body contacts [sec]

Magnet

0

0.03 ± 0.03

0

1.1 ± 0.5

0.1 ± 0.1

1.2 ± 0.6

0

0–1

0

0–14.5

0–2

0–18.5

Control

0

0.3 ± 0.2

0.1 ± 0.1

0.5 ± 0.2

0.1 ± 0.1

0.9 ± 0.4

0

0–6

0–3

0–3

0–1

0–8.5

https://static-content.springer.com/image/art%3A10.1007%2Fs00114-014-1231-x/MediaObjects/114_2014_1231_Fig1_HTML.gif
Fig. 1

Dolphins’ mean ± SE latency [min] to approach the magnetized stimulus (in black) is shorter compared to the control (in white; Wilcoxon signed-rank test; *p ≤ 0.05)

Discussion

The responses of six captive bottlenose dolphins towards visually identical devices containing either a magnetized or a demagnetized neodymium block suggest that this species is capable of perceiving magnetic fields. The dolphins approached the device with shorter latency when it contained the magnetized neodymium block compared to the control that was identical in form and density, thus they discriminated between the two stimuli. To do so, already at a distance of more than 1.5 m implies that dolphins’ perceptual abilities must be very sensitive. The fact that all other behaviours did not differ between magnetized and control stimulus may reflect that magnetic fields are neither particularly attractive nor repulsive to dolphins. This is, to our knowledge, the first experimentally obtained behavioural evidence for sensitivity to magnetic stimuli in cetaceans. However, we acknowledge that, although our findings suggest that dolphins are magnetosensitive, the fact that not all behaviours differed between magnetized and control stimulus indicate the importance of further studies to yield a more precise and conclusive result.

That dolphins can sense magnetic fields was already previously suggested by Stafne and Manger (2004) who observed that captive bottlenose dolphins in the northern hemisphere swim predominantly in counter clockwise direction, while dolphins in the southern hemisphere swim predominantly in clockwise direction, although they could not finally conclude what the reason for this behaviour was. There are not many studies testing for magnetoreception in dolphins. Kuznetsov (1999; only abstract available) reported that dolphins’ vegetative characteristics such as electrocardiogram, galvanic skin responses and respiration responded to changes in the magnetic field, interpreting this as “a high sensitivity of the dolphin to changes in the permanent magnetic field (a ‘magnetic sense’)”. However, as details of this study are unknown, it is difficult to evaluate.

One reason why previous experiments failed to detect a behavioural response of the dolphins towards magnetized stimuli might be the magnetic field strength. The magnet used in this study (details: ESM) created a magnetic field with a strength of approximately 0.051–0.240 T at a distance of 2–5 cm from the magnet. This means, when touching the barrel, the magnetic field was roughly 1,000–6,000 times stronger than the magnetic field used in the conditioning experiments of Bauer et al. (1985).

In view of the fact that the geomagnetic field is on average 4.5 μT strong (Wiltschko and Wiltschko 1995), it seems questionable whether or not dolphins’ sensitivity is high enough to perceive and use geomagnetic cues for navigation. However, we did not test dolphins’ perception threshold, and there are several observations that found a correlation between cetaceans’ occurrence and geomagnetic characteristics (Kirschvink et al. 1986; Klinowska 1985; Walker et al. 1992). Further studies are needed to address the importance of magnetic field intensity and direction on the behaviour of dolphins.

One possible mechanism to perceive magnetic fields is the presence of ferromagnetic particles, such as magnetite, in the organism’s body. These miniature magnets align themselves in the magnetic field and seem to transmit this information through a connection with the central nervous system (Wiltschko and Wiltschko 1995), although further studies are also needed to really understand this process. However, a magnetite-based system is the only one yet proposed for cetaceans (Walker et al. 1992). Magnetite has indeed been found in the dura mater of dolphins (Bauer et al. 1985; Zoeger et al. 1981), although this finding alone does not provide sufficient evidence for magnetite-based magnetoreception. Regardless the mechanism, cetaceans may have inherited this sensory ability from their ancestors because some of the closely related artiodactyls (Thewissen et al. 2009) are also magnetosensitive (Begall et al. 2008).

Our results provide new, experimentally obtained evidence that this phylogenetic group should be added to the list of magnetosensitive species, broadening the evolutionary view on magnetoreception.

Acknowledgments

We thank Planète Sauvage and the dolphin trainers for their cooperation, as well as Martin Böye, Françoise Joubaud and Maxime Hervé for their assistance. This study was funded by A.N.R. (grant ORILANG), I.U.F, and A.N.R.T. (grant CIFRE).

Conflict of interest

The experiments described in this paper comply with the current laws of the country in which they were performed. The authors declare that they have no conflict of interest.

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