Hans G. Wallraff Avian Navigation: Pigeon Homing as a Paradigm

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3 Hans G. Wallraff Avian Navigation: Pigeon Homing as a Paradigm

4 Hans G. Wallraff Avian Navigation: Pigeon Homing as a Paradigm With 98 Figures

5 Dr. Hans G. Wallraff Max Planck Institute for Ornithology Seewiesen Germany ISBN Springer-Verlag Berlin Heidelberg New York Library of Congress Control Number: This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permissions for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer is a part of Springer Science + Business Media springeronline.com Springer-Verlag Berlin Heidelberg 2005 Printed in Germany The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Editor: Dr. Dieter Czeschlik, Heidelberg, Germany Desk editor: Anette Lindqvist, Heidelberg, Germany Cover design: Design & Production, Heidelberg Typesetting: perform electronic publishing GmbH, Heidelberg 31/3150WI Printed on acid-free paper

6 Preface Bird migration includes homing performances in almost global dimensions. After having spent the winter in South Africa, a stork or a swallow returns in spring to its old nest in a village in Denmark. A redstart, a flycatcher or a bobolink arrives in its former breeding territory after nocturnal flights covering thousands of kilometres. In what way do the birds solve the problems of navigation behind these performances? Although this book deals neither with bird migration nor with storks and flycatchers, but focuses on a domestic animal, it nevertheless deals with a central problem implicated in migrations and other long-distance flights characterizing the life cycles of many avian species. It is well known that such birds can find their way home to their breeding sites over hundreds of kilometres of unfamiliar territory, but little is known about how they achieve this admirable feat. Experiments dealing with that question in detail, with navigational strategies and with use or non-use of various environmental signals have, for good methodological reasons, predominantly been conducted with carrier pigeons. Thus, what actually can be reported is mainly our present knowledge about pigeon homing. However, there is little doubt, and there are findings suggesting, that the results and conclusions obtained with pigeons can largely be generalized towards an understanding of the navigational capabilities of other birds as well. It is not the pigeon itself as a particular bird, as a companion of man over thousands of years, that is the focus of interest of this monograph, but specifically its role as a paradigm for the study of navigation mechanisms enabling a bird to find its familiar home site from distant unfamiliar areas. The book summarizes the outcome of about half a century of research. A final solution to the homing problem has not yet been achieved during this time; substantial questions still remain. However, it seems that now, after a long period of trial-and-error searches and accumulation of initially unexplainable observations, at least the four basic categories of exploited input signals have been identified: the sun and the geomagnetic field (both used to determine compass directions), the visual landscape (used to determine the current position inside a familiar area around home), and atmospheric trace gases perceived by olfaction (used to determine the position in relation to home even from far away in unfamiliar areas). Naturally, the last category was not among the candidate input signals hypothetically envisaged from the beginning. It entered the arena unexpectedly and achieved its central position, against understandable scepticism, under the pressure of more and more compelling empir-

7 VI Preface ical findings. Presentation of these findings, discussion of their significance and theoretical consequence, and a proper look at the atmosphere make up the longest chapter of the book. Other sections proved necessary in order to show that initially favoured physical cues, especially the earth s magnetic field or the sun, are apparently not used by birds to determine their current position with respect to home, but are nevertheless substantial components of the homing process as a whole. Further, it was necessary to describe the pigeons homing behaviour in some detail and to separate its navigationally relevant parts from concomitant peculiarities which must be considered for methodological reasons and whose disregard may lead to misinterpretation of results. The book tries to give a state-of-the-art survey for everyone interested, but also tries to meet the demands of a critical readership being more or less familiar with the field. Considering the former group, the main text does not aim to report comprehensively on all pigeon homing experiments conducted over five decades and on all debates and controversies connected with them. I focus on those findings and ideas that I consider sound and relevant and that formed my current picture of the field. Being selective in the interest of keeping the text sufficiently fluent and attaining comprehensible conclusions,however,implies the danger and the possible reproach that the presented picture has been made coherent at the cost of objectiveness. Therefore, I did not simply ignore findings and opinions that might confuse the picture, but deal with them in a separate section (Sect. 7.8), in a chapter on research history (Chap. 11) and in the Appendix at the end, in which selected particulars are discussed in some detail. Even readers who are not ready to accept my style of presentation, my arguments and conclusions may profit from the book, as it facilitates access to the extensive literature from which everybody can derive his or her own view of a field and a period of research that now possibly approaches its end phase. I may be wrong, but I feel that the types of pigeon releases, field glass observations and statistical analyses, as initiated by G. Kramer and G.V.T. Matthews in the 1950s and described in the following pages, have largely done their task. On the one hand, these experiments probably revealed the most fundamental peculiarities of pigeon homing (albeit many particulars are not yet clarified), while, on the other hand, future progress in solving the remaining most fundamental questions will require more sophisticated methods intruding deeper into the environment and into the animals neural mechanisms of signal processing. This monograph attempts to provide the material basis from which more refined research may commence. The book has a personal touch insofar as it includes a retrospect of my own research over a period of about 45 years, i.e. over almost the whole period during which pigeon homing has been intensely investigated. Naturally, my mode of looking at the accumulated material agrees most properly with the mode in which I have previously designed experiments aimed at achieving some understanding of the pigeons homing behaviour. Therefore, and because other

8 Preface VII corresponding data are often unavailable, many of the figures show results obtained by me and by colleagues with whom I worked.i thank all those who contributed to produce the related data files, in particular Silvano Benvenuti, Augusto Foà, Jakob Kiepenheuer, Michael Neumann, Ulrich Sinsch, Andrea Streng and my technical assistants Rainer Wahl and Karl Wielander. I remember most gratefully the productive collaborations I had over the years with Floriano Papi and his associates in Pisa, whose outcomes are included in the following pages. Last, but not least, I thank Floriano for his readiness to read a draft of the whole manuscript and for his helpful advice resulting in a number of improvements. Seewiesen / Starnberg, May 2004 Hans G. Wallraff

9 Contents 1 Introduction Avian Migration and Navigation Why Investigate Domestic Homing Pigeons? On Terms and Definitions Observation Data Used to Investigate Pigeon Homing Initial Orientation Homing Performance Homing Routes Recoveries Cage Experiments Basic Features of Pigeon Homing Homing of Inexperienced Pigeons Peculiarities of Initial Orientation The Problem of Motivation Limited Significance of Exercise Flights at Home Experience Gained by Homing Flights Number and Range of Previous Homing Flights Directions of Previous Homing Flights Familiarity with the Release Site or Area Temporal Variability Annual Periodicity Aperiodic Fluctuations Accuracy of Homeward Orientation Distance of Displacement Geographical Variability Distraction by Landscape Configurations Stochastic Noise Spatial Range of Pigeon Homing Multiple and Mobile Home Sites Conclusions and Perspectives Home-Related and Home-Independent Components of Initial Orientation Motivation, Selection and Homing Experience Inaccuracy and Variability of Homing Orientation... 51

10 X Contents 4 Potential Input Signals Exploitable for Home-Finding Directional References Indicators of Position Motion-Bound Signals Location-Bound Signals TheRoleoftheSun Effects of Shifting the Birds Circadian Clock Linkage Between Sun Compass and Map Orientation Under Overcast Skies Conclusions and Perspectives The Role of the Geomagnetic Field Effects of Artificial Magnetic Fields Magnets or Coils During Flight Magnetic Fields Before Release Geomagnetic Irregularities Spatial Magnetic Anomalies Temporal Magnetic Fluctuations Conclusions and Perspectives The Interference with the Stress Issue The Magnetic Compass Issue The Magnetic Map Issue The Path Integration Issue The Magnetic Sense Issue Overall Conclusions and Outlook The Role of the Chemical Atmosphere Effects of Olfactory Deprivation Olfactory Nerve Section Inactivation of the Olfactory Epithelium by Zinc Sulphate Nasal Anaesthesia Occlusion of Nostrils Insertion of Nasal Tubes Dependence on the Air the Pigeons Breathe Removal of Trace Gases by Filtration Air from Different Environments Olfactory Misguidance Spatial Separation of Sites of Air-Smelling and Release Outward-Journey Detours Natural Olfactory Misguidance Spatial Range and Variability of Olfaction-Based Homing Distance Range and Efficiency in Different Regions Temporal Variability

11 Contents XI 7.5 Varying Home Site Conditions in Aviary Experiments Shielding, Deflecting and Reversing Winds Applying Artificial Odours and Winds A Digression to the Preferred Compass Direction (PCD) Spatial Structures in the Chemical Atmosphere A Working Hypothesis Gradients in Ratios of Trace Gases Applicability of Atmospheric Gradients to Navigation Assumed Dependence on Geographical Peculiarities The Short Distance/Long Distance Problem Avian Olfactory Perception: A Suitable Tool for Navigation? The Problem of Sensitivity The Problem of Odour Discrimination The Problem of Compound Selection The Problem of Adaptation/Habituation Arguments Against Olfactory Navigation and Replies Intuitive Incredibility Potential Non-Specific Side Effects Inconsistent Results Conclusions and Perspectives Experimental Evidence of Olfactory Navigation How Does Olfactory Navigation Operate? Do Pigeons Have an Olfactory Map? Unsolved Problems Remaining Challenges TheRoleoftheVisualLandscape The Landscape as a Home-Guiding Factor Non-Olfactory Homing Downgrading of Visual Signals Homing with Olfaction and Vision Impaired Interrelations Between Landscape and Sun Compass The Landscape as a Disturbing Factor Conclusions and Perspectives The Neural Bases of Pigeon Homing The Hippocampus and the Familiar-Landscape Map The Hippocampus and the Olfactory Map The Piriform Cortex and the Olfactory Map Roles of Other Brain Regions and Hemispheric Lateralization Conclusions and Perspectives Homing in Other Birds Experimental Approaches Brief Overview

12 XII Contents Compass Orientation and Preferred Compass Directions Goal-Oriented Navigation Homing in Natural Life Non-Migratory Excursions Homing as a Constituent of Bird Migration Conclusions and Perspectives Research History: Blind Alleys and an Unexpected Passage Overall Synthesis and Perspective Environmental Cues Involved in Home-Finding Processes Two Homing Mechanisms Challenges for Future Research Unsettled Basics of Pigeon Homing Problems of Visual Landscape Orientation Problems of Olfactory Navigation Outlook Appendix: Notes on Selected Particulars References Subject Index

13 1 Introduction 1.1 Avian Migration and Navigation Among other aspects of bird migration, such as aerodynamics, energetics and associated migratory strategies, including remarkable ecological adaptations, the aspect of spatial orientation is certainly the most striking one. Consequently, migratory orientation has been investigated in great detail.it is known that birds can determine compass directions by means of the geomagnetic field, the stellar sky or the sun, which are globally available as directional references. Using their compasses, the birds can select genetically encoded directions which lead them to their winter quarters. An endogenous time programme gives the appropriate distance of flight in a temporal scale. Experimental data suggest that such bearing-and-distance programmes, which are roughly adapted to, and modified by, topographical and ecological conditions of the covered regions, and which in some species include even directional changes, are the general bases of many or most population-specific migratory routes. Applying in this way its endogenous intentions to the external world, even a young bird, leaving its birth place for the first time, eventually arrives in the far distant wintering range of its population. With larger birds,such as waterfowl or storks,which migrate in flocks during the daytime, also guidance of juveniles by adults along traditional routes is involved. Such guidance can be excluded in most of the smaller birds, particularly in the many passerine species migrating predominantly at night. Detailed reports on bird migration and migratory orientation can be found in other books (see Alerstam 1990; Berthold 1996, 2000, 2001; Berthold et al. 2003). In spring, the bearing-and-distance programme can be expected to operate analogously to its operation in autumn; only the directions need to be reversed. A bird may return thereby to its population-specific breeding range. It is hardly imaginable, however, that a redstart can reach, on this basis alone, the village and the garden in which it had bred the year before. Migrating at night and exposed to drift-causing winds, simply keeping the body axis on a genetically encoded compass course would be insufficient. In fact, the birds can perform better. It has been shown that birds of many species (e.g. starlings, cowbirds, blackbirds, swallows, swifts, terns, gulls, storks, shearwaters, petrels and albatrosses) are able to find a familiar home site by goal-related navigation from far distant unfamiliar areas to which they had been passively displaced (for lists of such experiments and for references see Matthews 1955; Wiltschko

14 2 1 Introduction 1992; Åkesson 2003). To achieve this performance, the animals must have more than a compass. Only if a bird is aware that it is north (and not south, east or west) of home, can it usefully apply a compass in order to steer a southward course guiding it home. The process of birds finding their way back from a position in a distant unfamiliar area (where the animals have never been before) to a familiar geographical position (which has been established, during longer-lasting previous presence, as a home site ) has often been called navigation in a narrow sense (Sect. 1.3). There is hardly any doubt that birds commonly apply goal-related navigation in the course of their migrations (Sect ) and that,without this capability, bird migration patterns would never have achieved their present overall character. Nevertheless, as substantial parts of migratory orientation, homing mechanisms are usually not closely inspected in books and articles dealing with bird migration. In fact, these mechanisms have not been closely investigated in migratory species. However, they have been intensely investigated in a non-migratory domesticated bird. I feel confident that the knowledge gained from pigeon homing can largely be considered as knowledge about avian homing in general and hence also of goal-finding in the course of bird migration. 1.2 Why Investigate Domestic Homing Pigeons? In research on avian navigation, the homing pigeon acts as a kind of laboratory rat. Without the experiments conducted with this domestic animal, only a small fraction of our present knowledge about the mechanisms used by birds to find their way home from remote areas would have been achieved. The advantages of homing pigeons, as compared to any wild species, are obvious. Hundreds or even thousands of pigeons can be kept in man-made lofts at man-selected locations. Over the whole year the birds are easily available for experimental use without laborious and stressful trapping procedures. Individual returns from releases can be precisely recorded, usually by only one observer. Homing pigeons are always motivated to return to their loft, not only during the short breeding season. Due to their strong homing drive,they fly off mostly immediately after release, thus giving opportunity to observe their initially selected courses, whereas most other birds tend to land on nearby trees or in meadows etc. before starting homeward movements some time later. Over short and median distances, many pigeons return in a non-stop flight, so that the time they need for homing reflects,by and large,the length of the route they have flown. Even many of the pigeons that fail to home provide information about their orientation: Due to their social impulses, they tend to enter one or another of the pigeon lofts which are, in some countries, quite densely scattered over the land. Reports by pigeon fanciers contribute instructive spatial distributions of recovery sites. Finally, pigeons are very handy, their size is neither too small nor too large. They are large enough to be observed with bin-

15 1.2 Why Investigate Domestic Homing Pigeons? 3 oculars over approximately 2 km and large enough to carry the weight of a small transmitter for telemetry or some other apparatus apt to record their flight paths. They are small and tame enough to be confined in large numbers together in manageable crates for transport. These outstanding advantages resulted in in-depth investigations on homing capabilities of birds being almost exclusively conducted with homing pigeons. Thus, the question arises whether pigeon homing can be seen as a model case of bird homing in general. At least there are good reasons to assume that it can. It appears extremely unlikely that, in the course of domestication from the rock pigeon (Columba livia) and selective breeding, an entirely novel navigation mechanism that did not exist before in the genus Columba, has been implanted into the strains of homing pigeons. The fact that the rock pigeon is usually sedentary implies no argument against the assumption that navigation mechanisms detected in homing pigeons can indicate mechanisms used by other birds during migration. Closely related species (e.g. Columba palumbus) do migrate, and Berthold et al. (1990) have shown that offspring of partially migratory birds of a given species can be genetically transformed, by means of selective breeding, to either full migrants or non-migrants within only a few generations. It is uncertain whether selection performed by man noteworthily affected the navigational capabilities of pigeons. Much more obvious is improvement of the homing drive, which appears less highly developed in the rock pigeon (Alleva et al. 1975; Visalberghi et al. 1978) and in other wild birds (e.g. Able et al. 1984). In pigeon races, the breeder is concerned with getting a maximum number of pigeons homed at maximum speed. The fastest homers are then preferentially selected for breeding. Homing speed in such races, however, is not primarily a result of outstanding navigation but rather of motivation, physical strength and persistence. The birds are usually trained to return in large flocks from always the same direction. Thus, the ability to find their way home from novel directions and sites by making individual decisions is not a criterion for selection. Of course, there may be differences among pigeons and other species in many details of homing behaviour, for instance in the motivation to fly home at all,in the hierarchy in which different navigational cues are used or in the effectiveness with which such cues are exploited. It seems most likely, however, that once we understand pigeon homing we are able to understand the principles of avian goal-oriented navigation in general. Nevertheless, this assumption remains merely an assumption unless it can be actually shown that at least the most substantial conclusions drawn from experiments with homing pigeons can in fact be generalized and are valid for other bird species as well. Some supporting evidence is already available (Chap. 10). Although the carrier pigeon is a unique subject for research on animal homing, the huge amount of data obtainable from millions of homing flights performed in the course of pigeon races has only a minor value as a source of information in the context of this research. As mentioned above, races take place in large flocks, usually comprising thousands of birds, so that, in a statistical