Magnetic map navigation in a migratory songbird requires trigeminal input

Abstract

Recently, virtual magnetic displacement experiments have shown that magnetic cues are indeed important for determining position in migratory birds; but which sensory system(s) do they use to detect the magnetic map cues? Here, we show that Eurasian reed warblers need trigeminal input to detect that they have been virtually magnetically displaced. Birds with bilaterally ablated ophthalmic branches of the trigeminal nerves were not able to re-orient towards their conspecific breeding grounds after a virtual magnetic displacement, exactly like they were not able to compensate for a real physical displacement. In contrast, sham-operated reed warblers re-oriented after the virtual displacement, like intact controls did in the past. Our results show that trigeminally mediated sensory information is necessary for the correct function of the reed warblers’ magnetic positioning system.

Anosmic migrating songbirds demonstrate a compensatory response following long-distance translocation: a radio-tracking study

“…1a for scenarios 2−4). This would be in general agreement with the result from birds tested in Emlen funnels (Chernetsov et al 2008;Kishkinev et al 2013Kishkinev et al , 2015Pakhomov et al 2018) and/or with the real movements of displaced Common Cuckoos (Cuculus canorus) according to Willemoes et al's (2015) satellite tracking study. If the olfactory system plays a necessary role in true navigation, we predicted that birds without a functional sense of smell would not be able to determine their new location and either show disorientation (departure in random directions) or fall back to the normal migratory direction, as has been seen in other studies (Holland et al 2009;Wikelski et al 2015), whereas the control group would adjust to the displacement by shifting their orientation anti-clockwise, as mentioned above.…”

“…A further displacement experiment from the Courish Spit to Moscow demonstrated that an intact trigeminal nerve is necessary for the compensatory response shown by Reed Warblers (Kishkinev et al 2013). Following on from this, exposure to a changed magnetic field alone at the capture site simulating the displacement site in Zvenigorod elicited a compensatory goal-ward anti-clockwise re-orientation similar to the one documented after a real geographic displacement (Kishkinev et al 2015), and these compensatory responses also required intact trigeminal nerves (Pakhomov et al 2018). Another experiment at this capture site in which only declination was changed to match a location in Scotland showed that this magnetic parameter appears to be used to calculate longitudinal position, at least in Western Europe (Chernetsov et al 2017).…”

“…The birds' orientation was not tested in Emlen funnels at the capture site to allow enough time for habituation to captivity, transportation, post-transportation rest and time for radio-tracking at the displacement site before the end of the spring migratory state (mid-June for this species). Based on the numerous orientation tests of these migrants at the same capture site in 2004−2017 (Chernetsov et al 2008;Kishkinev et al 2013Kishkinev et al , 2015Pakhomov et al 2018), there is good reason to assume that the control orientation of transit birds in spring is towards the northeast (Fig. 1b).…”

“…This result suggested that Reed Warblers were able to determine that they were at a new location and to compensate for the translocation. Which natural cues the Reed Warblers use to be able to determine their displacement to Zvenigorod has been the focus of the subsequent studies (Kishkinev et al 2010(Kishkinev et al , 2013(Kishkinev et al , 2015Pakhomov et al 2018).…”

“…Given the mismatch between the results of experiments on Reed Warblers and other migratory species tested, and the fact we did not precisely control odours and the sense of smell during our virtual magnetic displacements (Kishkinev et al 2015;Pakhomov et al 2018), in this study we aimed to explicitly examine the role of the olfactory sense in the compensatory behaviour of Reed Warblers after displacement, by studying their orientation during free flight after take-off, rather than in Emlen funnels, as free-ranging birds have been used in other studies (Holland et al 2009;Wikelski et al 2015). If the magnetic map hypothesis reported above is correct, we expected that the ability to determine their position should remain intact in both control and anosmic birds so that they would be able to compensate for the translocation and show their initial flight directions shifted anti-clockwise, compared to their normal migratory direction (see Fig.…”