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Long-Distance Navigation and Magnetosensory Mechanisms in Migratory Songbirds

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Long-Distance Navigation and Magnetosensory Mechanisms in Migratory Songbirds Long-distance navigation and magnetosensory mechanisms in migratory songbirds Der Fakultät für Mathematik und Naturwissenschaften der Carl von Ossietzky Universität Oldenburg zur Erlangung des Grades und Titels eines Doktors der Naturwissenschaften (Dr. rer. nat.) angenommene Dissertation von Dmitry Kishkinev geboren am 04.05.1981 in Uljanowsk, Russland Gutachter: Prof. Dr. Henrik Mouritsen Zweitgutachter: Dr. hab. Nikita Chernetsov Tag der Disputation: 8. Juli 2011 Contents Contents……………………………………………………………………………….. 1 Summary of the Ph.D. thesis………………………………………………………… 4 Zusammenfassung der Dissertation………………………………………………… 10 Aims of my PhD project……………………………………………………………… 17 Own contribution……………………………………………………………………… 18 Introduction: 21 1. Orientation and navigation – terminology……………………………………… 21 2. Methods to study and quantify orientation and navigation…………………… 22 3. Which reference systems do migratory birds use?.................................................. 24 3.1 Sun compass………………………………………………………………… 24 3.2 Star compass………………………………………………………………… 25 3.3 Magnetoreception and the magnetic compass of the birds…………………… 26 3.3.1 The magnetic field of the Earth……………………………………………… 26 3.3.2 The magnetic compass in birds……………………………………………… 28 3.3.3 Lateralization of the bird magnetic compass: own contribution.............. 30 4. Two magnetosensory systems in birds…………………………………………… 35 4.1 Chemical magnetoreseptor: radical pair mechanism in the eye……………… 35 4.2 Iron mineral containing magnetoreceptor: the upper beak organ…………… 40 4.3 Integration of magnetic information from the eye and the upper beak: own contribution…………………………………………………………………… 43 5. An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behaviour in a migratory songbird: own contribution………… 46 6. How can juvenile birds find their way to wintering quarters?............................... 53 6.1 Reviewing the literature……………………………………………………… 53 6.2 The development of migratory program in Siberian pied flycatchers implies a detour around the Central Asia and the effect of place: own contribution…… 59 7. True navigation in experienced migratory songbirds - terminology……………. 63 8. The map of birds: a question of coordinates……………………………………… 65 8.1 Reviewing the literature……………………………………………………… 65 8.2 Testing the navigational abilities in a long-distance migrant, Eurasian reed warbler, after longitudinal displacement: own contribution……… 68 8.3 The problem of longitude and a test of the double-clock hypothesis: own 70 1 contribution………………………………………………………………… Conclusion……………………………………………………………………………… 74 Outlook………………………………………………………………………………… 77 References……………………………………………………………………………… 79 List of abbreviations………………………………………………………………....... 95 Curriculum Vitae……………………………………………………………………… 96 Acknowledgments…………………………………………………………………....... 100 Publications and manuscripts 103 Chernetsov, N., Kishkinev, D. & Mouritsen, H. (2008): A long- Paper I. distance avian migrant compensates for longitudinal displacement during spring migration. Curr. Biol. 18, 188-190. 103 Kishkinev, D., Chernetsov, N. & Mouritsen, H. (2010): A double clock or jetlag mechanism is unlikely to be involved in detection of Paper II. east-west displacement in a long-distance avian migrant. The Auk, 108 127, 773-780. Chernetsov, N., Kishkinev, D., Gashkov, S., Kosarev, S. & Bolshakov, C. (2008): Orientation programme of first-year pied Paper III. flycatchers Ficedula hypoleuca from Siberia implies an innate detour around Central Asia. Anim. Behav. 75, 539-545. 117 Zapka, M., Heyers, D., Hein, C.M., Engels, S., Schneider, N.-L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, M. & Mouritsen H. (2009): Visual, but not trigeminal, mediation of Paper IV. magnetic compass information in a migratory bird. Nature 461, 125 1274-1277. Hein, C.M., Engels, S., Kishkinev, D. & Mouritsen, H. (2011): Paper V. Robins have a magnetic compass in both eyes. Nature 471, E11. 132 Hein, C., Engels, S., Kishkinev, D., Prior, H. & Mouritsen, H. Paper VI. Robins possess a magnetic compass in both eyes. Manuscript. 136 2 Kishkinev, D., Mouritsen, H. & Mora, C.V. An attempt to develop an operant conditioning paradigm to test for magnetic Paper VII. discrimination behaviour in a migratory songbird. Submitted to Learning & Behavior 162 Erklärungen gemäß § 10 der Promotionsordnung……………………………………... 196 3 Summary of the Ph.D. thesis The question how migratory birds can find the way to their wintering grounds and back has been puzzling researchers for decades. Migratory birds travel thousands of kilometres over apparently featureless landscape, and some species even fly alone at nighttime. Since the 1950s, it has become clear that, to find and maintain their headings, migratory birds are able to use rather sophisticated mechanisms to derive orientation information from different natural cues: the sun and the star compass use respective celestial cues (the Sun: e.g., Kramer 1950a, 1950b; and stars: e.g., Sauer 1956, 1957a, 1957b; Emlen 1967a, 1967b, 1975) and the magnetic compass uses the Earth’s magnetic field (e.g., Merkel and Wiltschko 1965; Wiltschko and Wiltschko 1972). Despite significant progress in our understanding of the orientation and navigation mechanisms of migratory birds, there are still many open questions. For example, the mechanisms underlying long-distance navigation, i.e., the ability to reach goals without perceiving any direct information from them or to compensate for huge geographical displacements, still remain poorly understood. Particularly, we still do not know which natural cues migratory birds can use as surrogates for geographical coordinates. Since the 1960s, there is evidence that birds are able to use the Earth’s magnetic field as a directional reference (e.g., Wiltschko and Wiltschko 1972; Cochran et al. 2004). But only recently, researchers started understanding the neurophysiological mechanisms underlying magnetoreception. Nowadays, there is a growing body of facts strongly suggesting that birds possess two different magnetosensory systems: i) a chemical sensor in the bird’s eye based on a radical pair mechanism (Ritz et al. 2000; see Ritz et al. 2010 and Liedvogel and Mouritsen 2010 for reviews), and ii) iron mineral containing sensors in the upper beak (Fleissner et al. 2003, 2007). However, the neurophysiological substrates and interaction between these two putative magnetosensory systems are still the subjects of research. Magnetoreceptive mechanisms, in turn, may be closely related to navigational abilities of migratory birds. It has been proposed that natural cue(s) used to determine position on the globe must meet the following requirements: they must provide consistent information, must vary systematically so that single points on the surface of the Earth can be identified uniquely, must be sufficiently stable over time to permit natural selection for navigation, must be detected and used to determine position with sufficient resolution to meet needs of the animal (Walker et al. 2002). The parameters of the Earth’s magnetic field, at least in part, meet these requirements and, therefore, understanding magnetoreception may help us answer the question how birds can navigate. 4 In my PhD work, I mainly focus on the following questions: i) are migratory birds able to detect a geographical displacement along east-west axis?; ii) if they are, which mechanism(s) may underlie this ability?; iii) which properties do the two putative magnetosensory systems possess? Specifically, what is the function of Cluster N and the beak organ?; and, finally, iv) is the avian magnetic compass strongly lateralized? Because human navigation techniques are based on two coordinates (latitude and longitude), it is not surprising that most authors assume that migratory birds should also use bi-coordinate navigation (e.g., Berthold 1991, 1996; Rabøl 1978). However, this assumption may be too anthropocentric and, therefore, has to be experimentally tested. Theoretically, it is much easier to propose a mechanism detecting position along north-south axis. For instance, this mechanism may measure the height of starry sky’s rotation center above the horizon (Sauer and Sauer 1960; Able 1980; Mouritsen 2003; Gould 2004, 2008), magnetic inclination and/or magnetic intensity. However, it is much harder to imagine which natural parameters may serve for detection of east-west position – the analogue of longitude (Åkesson and Alerstam 1998; Mouritsen 2003; Gould 2004, 2008). Therefore, it was plausibly hypothesized that migratory birds, particularly young birds on their first spring migration yet having no experience with finding their natal area, may use an one-coordinate navigation strategy (Mouritsen 2003). It implies that the birds may remember and identify latitude, but not longitude, of their natal area as well as landmarks around it before their first autumn migration. Next spring, young birds may travel north (situation for the northern hemisphere considered) until they reach latitude of their natal site destination. If a bird has made a small navigational mistake, but reached an area with visually known landmarks, it may easily pinpoint the natal area using landmark-based map. If a larger navigational mistake has been made, a bird may start searching for the goal moving back and forth along latitude of the natal site and trying to find known landmarks (Mouritsen 2003). Using Eurasian reed warblers (Acrocephalus scirpaceus) as model long distance migrants, I together with my co-workers
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