Magnetic orientation in Homarus americanus
Larval American lobsters (Homarus americanus) live suspended in surface waters, carried long distances by ocean currents. After their pelagic phase, lobsters become competent forward-swimming post-larvae (stage IV) and settle as they encounter suitable habitat (Factor 1995). Settlement is influenced by physical processes, but there is also evidence of complex navigation (Kingsford et al 2002, Cooper & Uzmann 1971). They use photo- and geotaxis in search of shelter (Kingsford et al 2002), can swim upstream, and even follow odors over long distances (Boudreau et al 1993). Foraging juveniles return to the same shelter night after night without visual cues (Karnofsky et al 1989). Adults embark on migrations >200 km, and displacement trials show that lobsters can home to known geographic areas (Cooper & Uzmann 1971). The similar migratory behavior of the spiny lobster (Panulirus argus) is accomplished by magnetic orientation, demonstrated by displacement (Boles & Lohmann 2003) and induced directional preference (Lohmann et al 1995) trials. Marine and terrestrial organisms are known to sense field inclination and polarity, and use geomagnetic cues to migrate (Cain et al 2005). The navigation capability of H. americanus anecdotally suggests they might share this sensory mechanism. This study demonstrates re-orientation in response to manipulation of the local geomagnetic field.
Lohmann et al (1995) used electromagnetic fields (EMF) to study navigation by P. argus. Two square coils in series create overlapping EMFs with an area of magnetic uniformity (Firester 1966). By applying appropriate voltage, the apparent geomagnetic polarity within this area can be reversed. For this design, 22 turns of 16-gauge insulated copper wire were wound around a PVC frame. Side length was 150 cm, with a coil separation of 82 cm (Figure 1). The uniform EMF of this configuration has <0.5% deviation within a 50 cm diameter area (Firester 1966).
The effect of rounded instead of square corners was ignored (pipe diameter = 5.08 cm). Firester’s (1966) equation for the central field strength of a Helmholtz coil (, gauss) was used with Ohm’s law to calculate the voltage necessary to reverse the magnetic field, .
The resistance of the conductor (Ω/ft) is important here. Flux density and magnetic field strength can be used interchangeably in this case (Diament 2000). Additionally, air and water have similar magnetic permeability, so is accurate in either media (Lohmann et al 1995). Magnetic deviation as great as 40° existed in some areas of the lab (attributable to HVAC). The coils were aligned using a compass in an area with minimal interference, such that north varied 5° between sides.
The horizontal geomagnetic component for Boston has a magnitude of 0.198 G (National Geophysical Data Center), but in situ magnetometer readings were 0.238–0.245 G. Therefore =0.478 G. Two DC power supplies (3.41 and 3.50 V) were connected to the coils. Coil resistance was 1.85 and 2.05 Ω, including power supply leads (Fluke 8050A multimeter). The difference in current was under <5 mA. The coils produced B=0.415 G, falling short of 0.478 G.
Ten H. americanus from the New England Aquarium were used in baseline tests, and a subset of those in EMF tests. During the experiment they were stage VI-VII (CL=8.8±0.5 mm), and molted before trials began. Lobsters were kept in individual mesh tubes in a flow-through tray with aerated 15 °C artificial seawater, under a 12:12 hr light schedule. They were fed Artemia daily.
Lohmann et al. (1995) covered the eyestalks of adult P argus in magnetic experiments to prevent orienting to the sun (Deutschlander et al 1999). In this study lobsters were blindfolded with black plastic, wrapped under the rostrum and eyes and secured to the carapace with SuperGlue. Blindfolded lobsters did not react to motion, and their ability to eat and walk was unaffected. A cotton thread was glued to the plastic on the dorsal carapace to limit movement to a radius short of the tank walls. Individuals made unsuccessful attempts to remove tethers immediately after affixing, but otherwise ignored them.
The arena was a circular basin (28 cm ø). The bottom was covered with a uniform layer of mixed fine and coarse sand. The tank was centered in the coils at 75 cm height. Water was replaced between trials (depth = 5 cm) and sediment allowed to settle. A transparent plastic cover was divided into 30° sectors, with north marked, and a hole for securing the tether. A tripod-mounted DV camera filmed downward through the cover. The PVC frame for the coils was draped with black plastic sheet to prevent glare in the recording, and to reduce shadows that might bias unblinded trials.
In baseline trials (I) lobsters were corralled (4 cm ø) during a 5 minute acclimation, then freely wandered for 20 minutes. Video was converted to an image sequence with one minute intervals, starting when the corral was removed. EMF control trials (II) were conducted with blindfolds and tethers. There was no acclimation period. Runtime and photo interval were again 20 min and 60 s. For two trials the coil was activated at 10 min remained on for 10 min (IIIa). Two further trials had coil state toggled every 2 min (IIIb). One trial had coil state toggled preferentially while the lobster was traversing the arena, every 15–60 seconds (IIIc).
A reorientation event was defined as a 90° change in heading, not caused by interaction with the arena or tether. These corresponded to EMF reversal event if it occurred within 5 seconds. Continuous circling within a quadrant was evaluated as an event for every revolution. Events occurring within 60 seconds following any disturbance were ignored. Plots of vector averages were used to evaluate directional preference (Lohmann 1995). The number of distinct reorientation events (total and corresponding to reversals) was compared to runtime (considered in 5 s bins).
Baseline trials (I) did not show obvious directional preference (Figure 2). Lobsters tended to reach the wall of the tank and follow it, reversing direction occasionally and at random. Most settled in the relative safety of depressions against the tank wall. This necessitated the use of a tether in control trials. Control trials (II) showed erratic movement (Figure 3), but no settling.
Lobsters reaching the end of a tether would either (a) strain against it, (b) turn tangential to the radius and walk at the limit of the string, or (c) be lifted off the substrate by tension. Entanglement occurred in only one case, though in several cases the tether fouled on itself. This did not affect mobility, only the radius of movement. Slack was added in cases where the small radius caused constant directional change. If the lobster reached the wall, the tether was shortened, the next time it was not under tension.
In two trials (IIIa) a reversed horizontal field caused an instantaneous heading change (100%, N=2). One lobster was at the limit of the tether in the southern arena, heading east. It turned inward and completed a narrow loop before again reaching the end of the tether an resuming its counterclockwise course. The second was straining against the tether and moving clockwise in the northern arena; it also turned in and passed through the center of the arena, and reaching the opposite wall began a counterclockwise course. These behaviors were observed in (II).
A series of reversals (IIIb) showed discernible reactions in some cases (44%, N=18), but the circular course imposed by the tether made it difficult to establish the cause of directional changes. This increased to 72% if including reactions that may have been related but were not the defined >90° turn. Of 27 non-random reversals (IIIc) performed over 11.75 min, 9 were ignored because the lobster was at the extent of the tether (including positive, negative and possible reactions). An obvious change in behavior occurred in 12 cases (67%, N=18). With a more lenient criteria for a related event there potentially would be 89% coincidence. There were 47 total reorientation events, occurring in 33% of 5 s time intervals.
Figure 2: average heading during baseline trials (I) (N=6). Direction is vector average of 20 positions, length is an indicator of course consistency. Following the tank wall results in a short vector.
Figure 3: Sector positions of two lobsters during blind tether trials with no reversals (II). This shows a possible bias to 270° (West), but seems coincidental when examining video instead of still images.
A major concern in evaluating frequency of reactions was the functional definition of what constituted a response. In general, non-associated events were given more leniency, and associated events only counted if there appeared to be no other justifiable cause. Simply reducing the correspondence interval after a switch in polarity to 3 s reduces the probability of a single event occurring in any given time bin to 29% and reduces definite responses (IIIc) to 50% of reversals.
If using instantaneous reactions (1 s), the probably of an event happening in any second is 0.07; and a definite responses occurred in 39% of reversals. Simplifying the lobsters behavior by giving more room to establish linear paths would aid in recognizing true events (and not throwing away potential data because of confounding factors).
Regardless, reorientation occurred in both moving and stationary lobsters at the instant of reversal. Particularly spectacular changes in orientation matched exactly the rotation of the compass arm used to confirm field change. Two other behavioral responses were observed. In cases of frequent reversal for more than 15 min two lobster made jerky vibratory movements and appeared agitated. This happened after reversals, and was followed by the lobster grasping one claw with the other, like wringing hands. When lobsters were stationary during reorientation, they would sometimes roll their tail in and pause before or during a turn. Lobsters would also stop and exhibit this behavior during field reversals. This might indicate that tail is acting as a sort of biological Hall effect sensor. Analyses of trace metals and electric fields in the lobster body might reveal more regarding the sensory mechanism. I have no explanation for the claw-wringing behavior.
Because of the simplicity of component vector addition, three such arrays can be aligned to x- y- and z-axes, and allow greater control of the uniform area. If the design includes Hall probes to sense each axial component of the field, a CPU can dynamically shift the power supplied to the coils. A moored system in constant motion could maintain a field of uniform magnitude a direction regardless of its instantaneous orientation; DC supplied devices are also inherently suited to battery operation.
The ability to change the apparent orientation of the Earth’s field has applications in study of competent dispersal and population connectivity which may be driven by magnetic navigation. One possible application is in situ testing of larval orientation, particularly whether H. americanus post-larvae utilize a polarity compass in their settlement strategy and how this might affect species distribution.
Many thanks to the people whose enthusiastic generosity made this possible: Anita Metzler and the New England Aquarium for the lobsters; Eric Hazen and Paul Bohn of the BU Electronics Design Facility for power, parts and knowledge; Michael Ruane and Robert Kotiuga of BU Electrical and Computer Engineering for testing equipment and EM theory consultation; Jonathan Perry and Justin Scace for use of their tools and time; and Jelle Atema and Julia Spät for encouraging something ambitious.
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