Introduction

The Earth’s magnetic field plays an important role in the orientation and navigation of sea turtles (reviewed by Lohmann and Lohmann 1998, 2003).  Hatchling loggerheads have a well-developed magnetic compass that enables them to maintain consistent headings in the absence of other cues (Lohmann 1991, Light et al. 1993, Irwin and Lohmann 2003), an ability that presumably helps guide them offshore during their initial seaward migration (Lohmann and Lohmann 1996a).  In addition, sea turtles are sensitive to small differences in field inclination (Lohmann and Lohmann 1994) and intensity (Lohmann and Lohmann 1996b) and can exploit the regional fields that exist in different locations along their migratory route as navigational markers (Lohmann et al. 2001).  Finally, it has been hypothesized, though not yet demonstrated, that young turtles imprint on the magnetic fields that mark their natal beaches and use this information to return to the same region as adults (Lohmann et al. 1999).

Despite the prominent role that magnetism appears to play in the sensory world of sea turtles, little thought has been given to how anthropogenic influences in general, and conservation practices in particular, might disrupt their natural magnetic environment.  A first step toward assessing possible risks is to identify circumstances in which turtles are exposed to unnatural fields that might interfere with the development of normal magnetosensory abilities or prevent the detection of important magnetic information. 

A common conservation practice on many sea turtle nesting beaches is to cover turtle nests with galvanized wire mesh cages (Fig. 1) or screens to protect the eggs from raccoons, foxes, and other predators (Addison and Henricy 1994, Jordan 1994, Ratnaswamy et al. 1997, Yerli et al. 1997, Kinsella et al. 1998).  Here I report, however, that wire mesh cages significantly alter the magnetic field around the eggs and developing embryos.  Whether such field distortions affect the development of the turtles’ navigational system is not yet known.  In principle, however, the field changes produced by cages might produce effects on subsequent orientation ability and navigational performance, particularly if turtles do indeed imprint on the magnetic features of their natal beaches.  The results underscore the need to consider carefully the sensory biology of animals when designing conservation practices.

Methods

To assess the effect of protective cages on the ambient magnetic field, I measured the field distortions produced by 10 cages used on south Florida beaches.  Each cage was constructed in accordance with a standard cube design (Addison 1997) and had dimensions of approximately 60 x 60 x 60 cm (Fig. 1).  The local magnetic field within the test area was uniform with an intensity of 39.7 µT and an inclination angle of 58.7°.

For each measurement, I placed the probe of an Applied Physics System 520 tri-axial digital fluxgate magnetometer flat on a non-magnetic platform and aligned the probe with the north-south axis of the Earth's magnetic field.  I then adjusted the magnetometer offset readings for all three axes to zero so that I could measure the changes caused by the presence of a cage.  The cage was then placed on a second non-magnetic platform above the probe.  The cage was positioned so that one side was aligned parallel to the north-south axis and one of the test points (Fig. 1) was directly above the magnetometer probe.  The magnetic field that resulted from the presence of the cage was then recorded.  Because a field value could be either positive or negative depending on the direction the cage was facing, I used the absolute value of all measurements in calculations.  The change in magnetic field intensity and inclination angle was then calculated for each point using standard vector addition. 

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 (Fig. 1). The tracker arm could rotate freely within the horizontal plane 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. 

At the beginning of each trial, the LED in the east side of the tank was turned on.  A harnessed hatchling was then released in the arena.  The arena cover was lowered over the tank and the data acquisition computer was started.  The computer recorded the magnetic heading of the turtle every 10 sec throughout the trial.  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 the mean heading for each turtle based on all data collected during the final 60 min of the trial (i.e., the period beginning 3 min after the light was turned off). The orientation of each group of turtles was analyzed using a Rayleigh test and the distributions of the two groups were compared using Watson's U2 test (Batschelet 1981).

Results and Discussion

All of the cages I tested altered the inclination angle and intensity of the magnetic field at all of the test locations.  Changes to the local field decreased with distance from the cages but were present throughout the area where turtle eggs develop (Table 1). 

Whether developing in an altered magnetic field affects the subsequent behavior of turtles is not known.  In principle, however, the field in which turtles develop might influence subsequent orientation and navigation in at least three ways.  First, it might disrupt magnetic compass orientation of hatchling turtles during their offshore migration.  Second, it might alter the responses of turtles to regional magnetic fields that normally serve as open-ocean navigational markers.  Finally, it might prevent turtles from relocating their natal beaches as adults.  Below I briefly discuss each of these possibilities.

Hatchling loggerheads can orient using the Earth's magnetic field and are thought to use this ability as they migrate offshore soon after emerging from nests (Lohmann 1991, Lohmann and Lohmann 1998, Irwin and Lohmann 2003).  A similar magnetic compass sense exists in young migratory birds (reviewed by Wiltschko and Wiltschko, 1995).  However, young birds that were raised in magnetic fields that differed from those they normally encounter in their natal areas oriented differently during their first migration than did birds raised in the natural field (Bingman 1983, Weindler et al. 1995, Weindler et al. 1996).  Thus, the possibility exists that sea turtles raised in fields distorted by protective cages may also orient differently during their first migration than do those that develop under natural magnetic conditions.  If so, then deviations from the normal migratory direction might delay hatchlings in nearshore waters where predators are abundant or deplete their limited energy stores before they reach their normal offshore destination (Wyneken and Salmon 1992).

Figure 3. Potential geographic displacement

A final possibility is that turtles that develop in distorted fields might encounter difficulty in navigating to their natal beaches years later as adults.  Adult turtles are known to return to their natal areas to nest (Meylan et al. 1990, Bowen et al. 1993).  It has been hypothesized, although not yet demonstrated, that turtles imprint on the magnetic features of their natal beach and use magnetic cues to return to the same geographic region later in life (Lohmann and Lohmann 1994, Lohmann et al. 1999).  If such a process occurs, then turtles that develop in a distorted magnetic environment might imprint on magnetic fields that either do not exist in nature or else occur at distant geographic locations.  For example, in south Florida a change of 1° of inclination angle represents a geographic change of approximately 150 km.  Given that fields in many locations beneath the cages were distorted by far greater amounts (Table 1), a turtle developing beneath a cage in south Florida might hypothetically imprint on a field that exists in an oceanic location hundreds or thousands of kilometers away, or one that exists nowhere at all.  Such turtles might encounter difficulties in relocating appropriate nesting areas as adults.

Thus, in principle, the magnetic field distortions caused by wire cages might affect sea turtles in several different ways and at several different life history stages.  I emphasize, however, that no experimental evidence presently exists to confirm or refute the hypothesis that turtles are adversely affected by developing in distorted magnetic fields.  Caging and screening appear to be effective means of reducing nest depredation in many geographic areas (Addison and Henricy 1994, Jordan 1994, Ratnaswamy et al. 1997, Yerli et al. 1997, Kinsella et al. 1998).  Thus, for now, a decision about whether to use cages on a given nesting beach must balance the hypothetical possibility of adverse behavioral effects against the known threat of nest depredation.  A solution worth considering is to retain cages and screens where necessary, but to avoid the use of galvanized steel wire and instead construct protective enclosures out of magnetically-inert metal, wood, or plastic materials.

Hatchling sea turtles have been shown to derive both directional information (Lohmann 1991) and positional information (Lohmann and Lohmann 1994b, 1996b, Lohmann et al. 2001) from the Earth's magnetic field.  In principle, 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, however, the field from the magnet might have distorted the field line inclination and intensity around the turtles, so that an accurate assessment of positional information was not possible.  The present data are insufficient to distinguish among these different possibilities.

References

Batschelet, E. (1981). Circular statistics in biology. New York: Academic Press.

Goff, M., Salmon, M. and Lohmann, K. J. (1998). Hatchling sea turtles use surface waves to establish a magnetic compass direction. Anim. Behav. 55, 69-77.

Haugh, C. V., Davison, M., Wild, M. and Walker, M. M. (2001). P-gps (pigeon geomagnetic positioning system): I. Conditioning analysis of magnetoreception and its mechanism in the homing pigeon (Columbia livia). In RIN 01,  Paper No. 7. Oxford: Royal Institute of Navigation.

Keeton, W. T. (1971). Magnets interfere with pigeon homing. PNAS 68, 102-106.

Kirschvink, J. L. (1992). Uniform magnetic fields and double-wrapped coil systems: improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401-411.

Light, P., Salmon, M. and Lohmann, K. J. (1993). Geomagnetic orientation of loggerhead sea turtles: evidence for an inclination compass. J. Exp. Biol. 182, 1-10.

Lohmann, K. J. (1991). Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). J. Exp. Biol. 155, 37-49.

Lohmann, K. J., Cain, S. D., Dodge, S. A. and Lohmann, C. M. F. (2001). Regional magnetic fields as navigational markers for sea turtles. Science 294, 364-6.

Lohmann, K. J. and Lohmann, C. M. F. (1993). A light-independent magnetic compass in the leatherback sea turtle. Biol. Bull. 185, 149-151.

Lohmann, K. J. and Lohmann, C. M. F. (1994a). Acquisition of magnetic directional preference in hatchling loggerhead sea turtles. J. Exp. Biol. 190, 1-8.

Lohmann, K. J. and Lohmann, C. M. F. (1994b). Detection of magnetic inclination angle by sea turtles: A possible mechanism for determining latitude. J. Exp. Biol. 194, 23-32.

Lohmann, K. J. and Lohmann, C. M. F. (1996a). Detection of magnetic field intensity by sea turtles. Nature 380, 59-61.

Lohmann, K. J. and Lohmann, C. M. F. (1996b). Orientation and open-sea navigation in sea turtles. J. Exp. Biol. 199, 73-81.

Mathis, A. and Moore, F. R. (1988). Geomagnetism and the homeward orientation of the box turtle, Terrapene carolina. Ethology 78, 265-274.

Merritt, R., Purcell, C. and Stroink, G. (1983). Uniform magnetic field produced by three, four, and five square coils. Rev. Sci. Instrum. 54, 879-882.

Salmon, M. and Wyneken, J. (1987). Orientation and swimming behavior of hatchling loggerhead turtles Caretta caretta  L. during their offshore migration. J. Exp. Mar. Biol. Ecol. 109, 137-153.

Walcott, C. and Green, R. P. (1974). Orientation of homing pigeons altered by a change in direction of an applied magnetic field. Science 184, 180-182.

Walker, M. M. and Bitterman, M. E. (1989). Attached magnets impair magnetic field discrimination by honeybees. J. Exp. Biol. 141, 447-451.

Walker, M. M., Diebel, C. E., Haugh, C. V., Pankhurst, P. M., Montgomery, J. C. and Green, C. R. (1997). Structure and function of the vertebrate magnetic sense. Nature 390, 371-376.

Wiltschko, R. and Wiltschko, W. (1995). Magnetic orientation in animals. Berlin: Springer-Verlag.

Witherington, B. E. (1995). Observations of hatchling loggerhead turtles during the first few days of the lost year(s). In Proceeding of the Twelfth Annual Workshop on Sea Turtle Biology and Conservation, (eds. J. I. Richardson and T. H. Richardson): NOAA Tech. Memo. NMFS-SEFSC-361, Miami, FL. pp. 194-197.

Witherington, B. E., Bjorndal, K. A. and McCabe, C. M. (1990). Temporal pattern of nocturnal emergence of loggerhead turtle hatchlings from natural nests. Copeia 1990, 1165-1168.