Localizing the Magnetoreception System

Introduction

Although the ability of sea turtles to detect magnetic fields has been clearly established, the way in which turtles and other animals do so has remained enigmatic, and primary magnetoreceptors have not yet been identified with certainty in any animal (Wiltschko and Wiltschko 1995, Deutschlander et al. 1999, Lohmann and Johnsen 2000).  One factor that has made locating magnetoreceptors particularly difficult is that magnetic fields pass freely through biological tissue.  Thus, magnetoreceptors need not contact the external environment and might plausibly be located nearly anywhere within an animal’s body.  Magnetoreceptors might also be tiny and dispersed throughout a large volume of tissue (Kirschvink and Gould 1981, Walker 1997, Lohmann and Johnsen 2000), or the transduction process might involve a sequence of chemical reactions (Schulten and Windemuth 1996, Ritz et al. 2000), so that no obvious organ or structure devoted to magnetoreception necessarily exists.  Moreover, accessory structures such as lenses, which focus sensory stimuli on receptors and are often conspicuous, are unlikely to have evolved for magnetic field sensing because few biomaterials affect magnetic field lines (Lohmann and Johnsen 2000).

Previous experiments with hatchling loggerhead turtles have shown that magnetic orientation behavior is disrupted by small magnets that distort the ambient field over the entire body of the turtle (Irwin and Lohmann, 2003).  As a first step toward localizing the magnetoreception system in sea turtles, I conducted additional experiments using small magnets that distorted the field only over specific anatomical regions.  By comparing the orientation of turtles with magnets attached to different parts of the body, I have obtained evidence that the sea turtle magnetoreception system is located in or very near the head.


Methods

Animals

Hatchling loggerheads were obtained from nests at a beach hatchery several hours before they would otherwise have emerged naturally and were immediately placed into lightproof coolers.  They were then transported to a laboratory and maintained in darkness.  Each hatchling was tested only once and released on the beach following experiments each night.

 Experimnetal Arena

Experiments were conducted in a black, plastic, circular pool filled with water and enclosed by a removable lightproof cover (Fig. 1).  A light-emitting diode was attached to the inside wall of the pool directly east of the center of the arena.  The LED could be turned on and off as needed (see below). 

Figure 1. Experimental Arena

Procedure

Turtles were randomly assigned to one of four groups.  On each turtle, either a small magnet or a magnetically inert brass bar of similar size and weight was placed in three locations: on the posterior carapace, the mid-carapace, and the head (Fig. 2).  The control group had brass rods at all three locations.  Each of the other three groups had a small magnet placed at one of the locations and brass bars at the other two.  Each piece was attached to the turtles with a drop of cyanoacrylate adhesive.  The mean pole strength of the magnets at 0.5 cm was 20 µT (measured with a Magnetic Instrumentation, Inc. model 912 gaussmeter) and field strength diminished rapidly with distance from the magnet.  At a distance > 2.0 cm from the magnets, the field produced by the magnet was less than measurement discrimination of the magnetometer (1 µT).

Figure 2. Turtle with a magnet on the head (red arrow) and brass bars on the mid and posterior carapace (green arrows)

For each trial, a hatchling was placed in a Lycra harness that encircled the carapace but did not inhibit swimming movements (Salmon and Wyneken 1987).  The harness was attached by monofilament line to a wooden tracker arm that was affixed to a rotary digital encoder mounted above the center of the pool. The tracker arm could rotate freely and thus tracked the movement of the turtle as it swam.  Information was relayed, via the digital encoder, to a data acquisition computer that continuously monitored the heading of the turtle throughout each trial.

Harnessed hatchlings were released in the north quadrant of the arena, the arena cover was lowered over the tank and the data acquisition computer was started.  The turtle was allowed to swim toward the light for 60 min.  The light was then turned off.  After a 3 min adjustment period, the orientation of the turtle was monitored as it swam in darkness during the next 60 min.

Data analysis and statistics

The data-acquisition computer calculated a mean heading for each turtle based on all data collected during the first 60 min. of the trial (when turtles were swimming toward the light source) and during the final 60 min of the trial (when turtles were swimming in darkness).  A Rayleigh test was used to determine whether each group (control turtles and pulsed turtles) was significantly oriented during the light and dark periods.  In addition, the distributions of the two groups were compared using Watson's U2 test (Batschelet 1981) for both the light and dark periods .

Results and Discussion

Turtles in the control group, with only brass bars attached, were significantly oriented (Fig. 3A) as were turtles with a magnet placed on the posterior carapace (Fig. 3B) and turtles with a magnet on the mid-carapace (Fig. 3C).  In all three cases, the 95% confidence interval of these distributions overlapped the direction of the initial light stimulus (90°).  This continued eastward orientation after the light stimulus was removed probably represents a magnetic directional preference acquired on the basis of light cues (Lohmann and Lohmann 1994a). 

In contrast, the group of turtles with a magnet placed on the head was not significantly oriented (Fig. 3D).  This disorientation presumably resulted from a distortion caused by the magnet (Irwin and Lohmann 2003).  Thus, the reception system is likely located within the head or anterior portion of the neck of sea turtles as these were the areas over which the field was most distorted when a magnet was placed on the head.  The magnetoreception system presumably is not located in the vicinity of the mid or posterior carapace because magnets in these areas had no apparent effect on magnetic orientation behavior.

This finding is in agreement with other attempts to localize the magnetoreception system in vertebrate animals.  Several candidate receptor locations have been identified in cephalic structures including the ophthalmic nerve in birds (Beason and Semm 1987, 1996, Semm and Beason 1990), the ethmoid region of fish (Mann et al. 1988, Walker et al. 1988, Diebel et al. 2000) and the pineal complex in newts (Deutschlander et al. 1999).

Figure 3. Results
Because sea turtles derive both directional information (Lohmann, 1991) and positional information (Lohmann and Lohmann 1994b, 1996, Lohmann et al. 2001, Lohmann et al. 2004) from the Earth's magnetic field, the magnets attached to the turtles might have interfered with either or both of these abilities.  One possibility is that the field disrupted the turtles’ magnetic compass sense, so that they could not hold a reliable course.  Alternatively or additionally, the field from the magnet might have altered the field line inclination and intensity around the turtles, so that an accurate assessment of positional information was not possible.  At present I cannot distinguish among these different possibilities.

References

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A manuscript of his experiment is currently in review.
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