Journal of Avian Biology 46: 001–002, 2015 doi: 10.1111/jav.00593 © 2015 The Author. Journal of Avian Biology © 2015 Nordic Society Oikos Subject Editor: Thomas Alerstam. Editor-in-Chief: Jan-Åke Nilsson. Accepted 2 December 2014
Avian compass systems: do all migratory species possess all three? Nikita Chernetsov N. Chernetsov (
[email protected]), Biological Station Rybachy, Zoological Inst. RAS, 238535 Rybachy, Kaliningrad Region, Russia, and Dept Vertebrate Zoology, St Petersburg State Univ., 7/9 Universitetskaya Emb., 199034 St Petersburg, Russia.
A reader of almost any more or less recent review on avian orientation (Wiltschko and Wiltschko 1999b, Muheim et al. 2006a, Fraser 2010) is most likely to learn that migrating birds are known to possess at least three mechanisms of direction finding, namely the solar compass (Kramer 1953, Wiltschko 1980, 1981), the stellar compass (Emlen 1967a, b, 1970) and the magnetic compass (Wiltschko and Wiltschko 1972). These three compass systems have been shown to exist in migrating birds, their existence has been independently replicated multiple times and can now be considered an established fact rather than a hypothesis. Redundancy of compass systems of avian migrants naturally raised the question how these systems integrate. Quite a lot of controversial evidence has been collected over the decades [reviewed by Wiltschko and Wiltschko (1999a) and Muheim et al. (2006a)]. The prevailing view has been that during the premigratory period, celestial rotation (primarily stellar patterns; but the actually stellar pattern may be successfully replaced in the experiment by completely artificial ‘skies’; Emlen 1970, Wiltschko et al. 1987, Michalik et al. 2014) is given the greatest salience and is used to recalibrate the magnetic compass, whereas during actual migration, the magnetic compass takes over the primary role and is used to recalibrate celestial information. However, some data contradicted this view (Moore 1985), and two studies published in the mid 2000s managed to convince the orientation community that many, if not all, migrating songbirds calibrate their magnetic compass daily from sunset (i.e. celestial) cues (Cochran et al. 2004, Muheim et al. 2006b). Later research showed that the pattern is more complex, with some species calibrating their magnetic compass from polarisation patterns at sunset and sunrise (Muheim et al. 2007, 2009, Guinchi et al. 2014) and some apparently not (Rabøl 2010, Chernetsov et al. 2011, Schmaljohann et al. 2013). The reasons behind this between-species variation have been speculated upon but remain not known with any certainty (Liu and Chernetsov 2012). The possibilities include e.g. variation in the range of magnetic declinations regularly traversed by a species or population: some birds, e.g. Eurasian reed warblers Acrocephalus scirpaceus breeding in England and wintering in west Africa, may remain within virtually the same values of magnetic declination (ca –2° to –3°) throughout their annual cycle, whereas e.g. a
Swainson’s thrush Catharus ustulatus breeding in Yukon or Alaska and wintering in Brazil may annually visit areas with declinations varying between 20° and –20°. The latter species would then be predicted to have a stronger need to regularly calibrate its magnetic compass from celestial cues. Another possibility might be that different migratory routes may demand varying accuracy of orientation and navigation (cf. species migrating to oceanic islands and those not crossing any major barriers). Most authors who contributed to this debate seem to have implicitly assumed that every species of migrants (and probably every individual migrant) possess all three compass systems known to exist in birds, i.e. magnetic, solar (including the use of polarisation patterns) and magnetic compass. However, there is some evidence suggesting that it may not be the case. For instance, Swainson’s thrushes and grey-cheeked thrushes C. minimus studied by Cochran et al. (2004) after pre-exposure to the artificial magnetic field rotated 80° clockwise in the horizontal plane changed the direction of their nocturnal migratory flight 80° anticlockwise, which is consistent with calibration of the magnetic cues from sunset. Most of these birds had access to the correct stellar compass information during take-off and actual flight, but for whatever reason they did not make use of this information and flew in the wrong direction. In these two species, stellar information seems to be very low in the hierarchy of compass cues, if they are able to use it at all. In our recent study, garden warblers Sylvia borin exposed at sunset to the vertical magnetic field that did not contain any compass information were not able to orient in the seasonally appropriate direction later during the night in the natural magnetic field (Pakhomov and Chernetsov 2014), which is consistent with the idea of compass calibration at sunset and the crucial role of polarisation cues. Interestingly (and unexpectedly for us), not only birds deprived of celestial information were disoriented, but also those that had access to the correct stellar information throughout the experiment. In the case of North American thrushes one can speculate that the (wrong) magnetic compass information has overridden the (correct) stellar cues, but garden warblers just failed to orient in spite of having access to stellar cues. This species is known to develop stellar compass in the EV-1
ontogeny (Wiltschko et al. 1987), but it does not seem to always use it during actual migration. One can argue that the magnetic compass may calibrate the stellar one not just early in the ontogeny, but also later during the migration, and if this calibration is not allowed to occur, as in our expriments (Pakhomov and Chernetsov 2014), the birds cannot use the stars for orientation. Saying this would actually mean saying that stars do not provide any independent orientation cue that can be used without reference to other cues, e.g. geomagnetic ones. There is no doubt that some songbird migrants have a stellar compass and use it during migration (Emlen 1967a, b, 1970, Mouritsen and Larsen 2001, Michalik et al. 2014), and e.g. in pied flycatchers Ficedula hypoleuca it seems to have a higher priority than the magnetic cues (Guinchi et al. 2014). However, this ability seems to be less universal across nocturnally migrating birds, or even songbirds, than hitherto assumed. This means that the question of compass cue integration is even more complicated than usually thought. Not just cue hierarchy differs between the species of songbird migrants, but some species may not possess or use the full set of independent compass systems, e.g. stellar compass is either not available in some species or is consequently ignored by them. One reason behind this might be that learning to use the time-independent stellar compass (Emlen 1975) is timeconsuming (Michalik et al. 2014) and possibly cognitively challenging, and some species or individuals may be less efficient than others in doing that. All this makes disentangling the compass systems of migrating birds and how they are used during migration even less straightforward. Acknowledgements – The author is acknowledging the support for avian orientation research provided by Russian Foundation for Basic Research through grant 12-04-00296 and by St Petersburg State Univ. through research grant 1.37.149.2014. Constructive comments by Rachel Muheim were most helpful when revising an earlier draft.
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