Long-distance navigation and magnetosensory mechanisms in migratory songbirds [Elektronische Ressource] / Dmitry Kishkinev. Betreuer: Henrik Mouritsen

Dmitry Kishkinev

Sujets

• Biologie

Informations

• Publié par: carl_von_ossietzky_universitat_oldenburg
• Publié le: 01 janvier 2011
• Nombre de lectures: 10
• Langue: English
• Poids de l'ouvrage: 6 Mo

Extrait

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
1contribution…………………………………………………………………
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

east-west displacement in a long-distance avian migrant. The Auk, Paper II.
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
162 Learning & Behavior
Erklärungen gemäß § 10 der Promotionsordnung……………………………………... 196

3Summary 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.
4In 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