Should animals navigating over short distances switch to a magnetic compass sense?

Abstract

Magnetoreception can play a substantial role in long distance navigation by animals. I hypothesize that locomotion guided by a magnetic compass sense could also play a role in short distance navigation. Animals identify mates, prey, or other short distance navigational goals using different sensory modalities (olfaction, vision, audition, etc.) to detect sensory cues associated with those goals. In conditions where these cues become unreliable for navigation (due to flow changes, obstructions, noise interference, etc.), switching to a magnetic compass sense to guide locomotion toward the navigational goals could be beneficial. Using simulations based on known locomotory and flow parameters, I show this strategy has strong theoretical benefits for the nudibranch mollusk Tritonia diomedea navigating toward odor sources in variable flow. A number of other animals may garner similar benefits, particularly slow-moving species in environments with rapidly changing cues relevant for navigation. Faster animals might also benefit from switching to a magnetic compass sense, provided the initial cues used for navigation (acoustic signals, odors, etc.) are intermittent or change rapidly enough that the entire navigation behavior cannot be guided by a continuously detectable cue. Examination of the relative durations of navigational tasks, the persistence of navigational cues, and the stability of both navigators and navigational targets will identify candidates with the appropriate combination of unreliable initial cues and relatively immobile navigational goals for which this hypothetical behavior could be beneficial. Magnetic manipulations can then test whether a switch to a magnetic compass sense occurs. This hypothesis thus provides an alternative when considering the behavioral significance of a magnetic compass sense in animals.

Keywords: Tritonia; acoustic signaling; magnetic compass sense; magnetoreception; navigation; odor-gated rheotaxis; short distance; simulation.

Figure 1

Four examples of flow patterns from the habitat of Tritonia diomedea with frequent flow direction changes that could render strict odor-gated rheotaxis unusable as an odor source search strategy. Note the compass headings are circular data, and thus the y-axis maxima and minima both indicate magnetic North (0°). Chemical plumes spread ∼30° in the habitat, and thus any flow direction change greater than 30° (the distance between y-axis tick marks) will likely sweep an odor plume away from an animal, forcing it to either stop or use a different strategy to find the odor plume source. On average, the flow remains within a 30° sector for only 5 min in this habitat, less than the 8 min average slugs spend navigating in a single direction (Wyeth and Willows, ; Wyeth et al., 2006).

Figure 2

An example of how switching to a magnetic compass sense can improve navigation. Three simulated Tritonia diomedea start at the same location, 2 m distant from an odor source (X), and then use three strategies for to find the source. (1) Strict odor-gated rheotaxis (OGR), stopping once the odor plume is no longer detected (red); (2) OGR followed by rheotaxis for 10 min after odors are no longer detected (blue); (3) OGR, followed by a switch to a magnetic compass sense to follow last known heading for 10 min after odors are no longer detected (black). As the simulation progresses (A–H, time indicated in lower right for each frame), the slug using strict OGR moves only a short distance toward the target since it is only intermittently in contact with the odor plume (A,D). The slug that continues rheotaxis crawls much further, but is lead away from the source by the variable currents (E–G). These problems are overcome by the slug that switches to a magnetic compass, following the last heading from which odor was detected, as it makes continuous progress toward the odor source despite the intermittent odor plume (A–G), and makes a final approach to the source while in the odor plume (H). (I) The movement tracks for the three strategies demonstrate that for this particular flow pattern, switching to a magnetic compass sense was the best strategy to find the odor source. Movie versions of this figure using both simulation methods are available in the Supplementary Material.

Figure 3

Two simulation methods for odor plumes. (A) In one set of simulations, the region with detectable odors (gray) was defined by the location of an odor source (x) and expanding circles (outlined) moved by the current (arrow). (B) In the second set of simulations, the region with detectable odors (gray) was defined by a trapezoidal region (outlined, cut off at right) oriented around the odor source (x) by the current (arrow). Inset: trapezoid schematic indicating segments for which dimensions are given in Table 1. Movies in Supplementary Material demonstrate the differences between the two simulation methods.

Figure 4

Switching to a magnetic compass sense is consistently the best strategy for simulated T. diomedea that lose contact with an odor plume due to flow heading changes. Shown are minimum distances that simulated slugs reached relative to an odor source for each of three strategies invoked over five different durations after an odor plume was no longer detected. Values are means normalized to the initial distance from the source, with standard errors. Strategies: continued rheotaxis (gray), switching to a magnetic compass to crawl along the last heading from which odor was detected (black), and unguided crawling initiated along the last heading from which odor was detected (white). Over all non-zero durations, switching to magnetically guided crawling was consistently the best strategy. The zero duration strategies (which are the same for all three strategies types since, in all three cases, the strategy is strict odor-gated rheotaxis followed by no subsequent strategy) were the worst strategies for finding the odor source.