Magnetite Biomineralization and Magnetoreception in Organisms A New Biomagnetism

TOPICS IN GEOBIOLOGY Series Editor: F. G. Stehli, University of Oklahoma

Volume 1 SKELETAL GROWTH OF AQUATIC ORGANISMS Biological Records of Environmental Change Edited by Donald C. Rhoads and Richard A. Lutz

Volume 2 ANIMAL-SEDIMENT RELATIONS The Biogenic Alteration of Sediments Edited by Peter L. McCall and Michael J. S. Tevesz

Volume 3 BIOTIC INTERACTIONS IN RECENT AND FOSSIL BENTHIC COMMUNITIES Edited by Michael j. S. Tevesz and Peter L. McCall

Volume 4 THE GREAT AMERICAN BIOTIC INTERCHANGE Edited by Francis G. Stehli and S. David Webb

Volume 5 MAGNETITE BIOMINERALIZATION AND MAGNETORECEPTION IN ORGANISMS A New Biomagnetism Edited by joseph L. Kirschvink, Douglas S. Jones, and Bruce j. MacFadden

Magnetite Biomineralization and Magnetoreception in Organisms A New Biomagnetism

Edited by Joseph L. Kirschvink California Institute of Technology Pasadena, California

Douglas S. Jones University of Florida Gainesville, Florida

and

BruceJ. ~acFadden Florida State Museum University of Florida Gainesville, Florida

Plenum Press • New York and London

Library of Congress Cataloging in Publication Data

Main entry under title:

Magnetite biomineralization and magneto reception in organisms.

(Topics in geobiology; v. 5) Bibliography: p. Includes index. 1. Biomagnetism. 2. Biomineralization. 3. Magnetite. I. Kirschvink, Joseph L. II.

Jones, Douglas S. III. MacFadden, Bruce J. IV. Series. QH504.M34 1985 591.19'214 85-17037 ISBN-13:978-1-4613-7992-8 e-ISBN-13 :978-1-4613-0313-8 DOl: 10.1007/978-1-4613-0313-8

©1985 Plenum Press, New York Softcover reprint of the hardcover 1st edition 1985

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All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

Contributors

Kenneth P. Able Department of Biology, State University of New York, Albany, New York 12222

Kraig Adler Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853

R. Robin Baker Department of Zoology, University of Manchester, Manchester M13 9PL, United Kingdom

Subir K. Banerjee Department of Geology and Geophysics, University of Minnesota, Min­neapolis, Minnesota 55455

Gordon B. Bauer Department of Psychology, University of Hawaii, Honolulu, Hawaii 96822

Richard P. Blakemore Department of Microbiology, University of New Hampshire, Dur-ham, New Hampshire 03824

Edward R. Buchler ORI, Inc., Silver Spring, Maryland 20910

Ruth E. Buskirk Institute for Geophysics, University of Texas, Austin, Texas 78712

Shih·Bin R. Chang Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125

Michael Chwe Division of Geological and Planetary Sciences, California Institute of Tech­nology, Pasadena, California 91125

Tom Dayton Department of Psychology, University of Oklahoma, Norman, Oklahoma 73019

Anne Demitrack Department of Geology, Stanford University, Stanford, California 94305

Andrew E. Dizon Southwest Fisheries Center La Jolla Laboratory, National Marine Fish­eries Service, National Oceanic and Atmospheric Administration, La Jolla, California 92038

J. Robert Dunn Department of Geological Sciences, University of California, Santa Bar­bara, California 93106

Darci Motta S. Esquivel Centro Brasileiro de Pesquisas Fisicas, CBPF/CNPq, Rio de Ja­neiro, Brazil

Paul Filmer Division of Geological and Planetary Sciences, California Institute of Tech­nology, Pasadena, California 91125

v

vi Contributors

Richard B. Frankel Francis Bitter National Magnet Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Cliff Frohlich Institute for Geophysics, University of Texas, Austin, Texas 78712

Michael Fuller Department of Geological Sciences, University of California, Santa Bar­bara, California 93106

William F. Gergits Department of Biology, State University of New York, Albany, New York 12222

W. 1. Goodman 2-G Enterprises, Mountain View, California 94043

W. S. Goree 2-G Enterprises, Mountain View, California 94043

James 1. Gould Department of Biology, Princeton University, Princeton, New Jersey 08544

Douglas S. Jones Department of Geology, University of Florida, Gainesville, Florida 32611

Timothy K. Judge Department of Biological Sciences, State University of New York, Al­bany, New York 12222

Roger 1. Jungerman Department of Physics, University of California, Santa Cruz, Cali­fornia 95064. Present address: Department of Applied Physics, Stanford University, Stanford, California 94305

Joseph 1. Kirschvink Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125

Henrique G. P. Lins de Barros Centro Brasileiro de Pesquisas Fisicas, CBPF/CNPq, Rio de Janeiro, Brazil

Laurent Longfellow Department of Physics, University of California, Santa Cruz, Cali­fornia 95064

Heinz A. Lowenstam Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125

Bruce J. MacFadden Florida State Museum, University of Florida, Gainesville, Florida 32611

Stephen Mann Inorganic Chemistry Laboratory, Oxford University, Oxford OX1 3QR, United Kingdom

Janice G. Mather Department of Zoology, University of Manchester, Manchester M13 9PL, United Kingdom; Current address: Zoological Laboratory, Institute of Zoology and Zoophysiology, University of Aarhus, DK-8000, Aarhus C, Denmark

Bruce M. Moskowitz Department of Geological and Geophysical Sciences, Princeton Uni­versity, Princeton, New Jersey 08544

Michael H. Nesson Department of Agricultural Chemistry, Oregon State University, Cor­vallis, Oregon 97331

William P. O'Brien, Jr. Institute for Geophysics, University of Texas, Austin, Texas 78712

Georgia C. Papaefthymiou Francis Bitter National Magnet Laboratory, Massachusetts In­stitute of Technology, Cambridge, Massachusetts 02139

Contributors vii

Chris R. Pelkie Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853

Anjanette Perry Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822

Karla A. Peterson Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125

David E. Presti Department of Biology, University of Oregon, Eugene, Oregon 97403

Brenda Roder Division of Geological and Planetary Sciences, California Institute of Tech­nology, Pasadena, California 91125

Bruce Rosenblum Department of Physics, University of California, Santa Cruz, California 95064

Gary R. Scott Lodestar Magnetics, Inc.,' Oakland. CaUfornia 94608

Durward D. Skiles Seismographic Station, University of California, Berkeley, California 94720

Kenneth M. Towe Department of Paleobiology, Smithsonian Institution, Washington, D.C. 20560

William F. Towne Department of Biology, Princeton University, Princeton, New Jersey 08544

Benjamin Walcott Department of Anatomical Sciences, School of Medicine, State Uni­versity of New York, Stony Brook, New York 11794

Michael M. Walker Southwest Fisheries Center La Jolla Laboratory, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, Cali­fornia 92038

Peter J. Wasilewski NASA Goddard Space Flight Center, Greenbelt, Maryland 20771

Ellen D. Yorke Department of Physics, University of Maryland Baltimore County, Ca­tonsville, Maryland 21228

John Zoeger Los Angeles County Museum of Natural History, Los Angeles, California 90007

Preface

The mystery of how migrating animals find their way over unfamiliar terrain has intrigued people for centuries, and has been the focus of productive research in the biological sci­ences for several decades. Whether or not the earth's magnetic field had anything to do with their navigational abilities has sufaced and been dismissed several times, beginning at least in the mid to late 1800s. This topic generally remained out of the mainstream of scientific research for two reasons: (1) The apparent irreproducibility of many of the be­havioral experiments which were supposed to demonstrate the existence of the magnetic sense; and (2) Perceived theoretical difficulties which were encountered when biophysi­cists tried to understand how such a sensory system might operate. However, during the mid to late 1960s as the science of ethology (animal behavior) grew, it became clear from studies on bees and birds that the geomagnetic field is used under a variety of conditions. As more and more organisms were found to have similar abilities, the problem shifted back to the question as to the basis of this perception. Of the various schemes for trans­ducing the geomagnetic field to the nervous system which have been proposed, the hy­pothesis of magnetite-based magnetoreception discussed at length in this volume has per­haps the best potential for explaining a wide range of these effects, even though this link is as yet clear only in the case of magnetotactic bacteria.

The question then arises as to what is the proper term for this new field of research. According to the definition of Williamson and Kauffman (1980), biomagnetism is supposed to include the study of the magnetic fields produced by an organism, whereas magneto­biology should include the study of responses or the detection of such fields by organisms. In a strict sense, the fallacy of this term splitting is clear in the case of the magnetotactic bacteria, where the magnetite is responsible both for the strong local magnetic fields (up to 0.4 tesla at the end of a magnetosome) and for their magnetotactic behavior. In general, however, we prefer to use the term biomagnetism (or biogenic ferromagnetism) for studies which focus on the presence of magnetite for the simple reason that it is far easier to detect the presence of minute concentrations of ferromagnetic material in tissues than it is to determine what, if anything, they are used for.

We organized a special symposium on magnetite biomineralization at the 1981 meeting of the American Geophysical Union in San Francisco, principally because much of the active research in this branch of biomagnetism was being conducted in laboratories nor­mally devoted to the study of rock- and paleomagnetism. The goal of this session was to bring together scientists working on various aspects of the magnetite biomineralization problem, and it attracted a large number of participants from the physical, geological, and biological sciences. During this meeting, the point was raised that literature of direct im­portance to this branch of biomagnetism was scattered in journals ranging from bacteriology to geophysics, and that there was no common source to which one could turn for in-depth discussions or guidance. This work was organized in response to that need. It seems clear from the diversity of papers in this volume that we have been reasonably successful in covering a wide spectrum of the subject matter involved, and we hope that it will be of use as a basic reference source in years to come. Included in this compilation are papers

ix

x Preface

which deal with most aspects of magnetite biomineralization, including in-depth discus­sions focused on the biomineralization process (e.g., the Lowenstam and Kirschvink, Nes­son and Lowenstam, Frankel et 01., and Mann chapters), the physical properties of mag­netite which make it more than just another biogenic iron oxide mineral (Banerjee and Moskowitz, Chapter 2), the information content of the geomagnetic field which might be of use to magnetically sensitive organisms (Skiles, Chapter 3), and the expanding number of organisms which are known to have both a geomagnetic sensitivity and the ability to precipitate magnetite biochemically (Chapters 13 through 25). Although the ferromagnetic hypothesis for magnetoreception appears to have been first suggested and experimentally tested by Gustav Ising (1945), the theoretical development of this model is quite recent and is extended further in this volume by Yorke (Chapter 10), Kirschvink and Walker (Chapter 11), and discussed in relation to the possible use of an induction-based electrical sensitivity by Rosenblum et 01. (Chapter 9). During the past few years, significant advances have also been made in laboratory techniques which allow the detection and identification of subnanogram quantities of ferromagnetic materials. These include the ultrasensitive superconducting (SQUID) magnetometers discussed by Fuller et 01. (Chapter 4), the in­expensive magnetic shielding techniques developed by Scott and Frohlich (Chapter 8), the magnetite extraction procedure of Walker et 01. (Chapter 5), Mossbauer spectroscopy as used by Frankel et 01. (Chapter 13), and the ever-improving techniques of electron mi­croscopy (reviewed here in separate chapters by Towe, Mann, and Walcott). A final ques­tion is whether or not magnetite crystals formed by the magnetotactic bacteria can be found and traced in the fossil record; differing views are expressed here by Demitrack (Chapter 35) and by Chang and Kirschvink (Chapter 36). Such "magnetofossils," if they exist, would provide a much needed explanation for the great magnetic stability of many deep-sea sediments and might eventually place constraints on the oxygen concentration in the bot­tom waters of ancient seas.

Also included in this volume is a chapter which deals with the question of whether or not primates possess the ability to biochemically precipitate magnetite, and whether or not humans have a magnetic sensitivity similar to that of other organisms. As explained in the editorial introduction to that chapter, this latter topic has generated far more con­troversy than any other section in this volume, and as such we have expanded it to include discussions and replies from scientists on both sides of the question. We encourage the reader to examine this material closely and formulate a balanced opinion based on as much of the raw behavioral evidence as possible, but in particular we hope that this discussion will attract and encourage additional work on this difficult problem.

Advances in fields other than ethology have contributed a great deal to the devel­opment of the hypothesis of magnetite-based magnetoreception. One example involves the experimental and theoretical determination of the single-do~ain size for magnetite (e.g., Neel, 1955; Evans and McElhinny, 1969; Butler and Banerjee, 1975). However, it is clear that the single most important discovery was the identification of magnetite in chiton teeth by Heinz Lowenstam (1962a). The continuing work on biomineralization by Lowenstam and his students (Lowenstam, 1963, 1967, 1974, 1980, 1981; Towe and Lowenstam, 1967; Kirschvink and Lowenstam, 1979; Lowenstam and Weiner, 1983) ushered in the modern era of the systematic study of biomineralization processes. Although it was not recognized at the time, the magnetic properties of the chiton radulae also constituted the first bio­magnetic effect to be discovered. The commonly accepted "founding" of biomagnetism, the measurement of the magnetic field produced by the heart, was not reported until the next year (Baule and McFee, 1963).

The story of how Lowenstam was led to the discovery of magnetite in chiton teeth has never been told in print before, yet is one of the most interesting examples of a superb naturalist at work. After the Nazis twice prevented him from receiving his Ph.D. from the University of Munich for being Jewish, he fled from Germany in 1937 and came to the United States. Heinz worked for several years during World War II as a paleontologist with

Preface xi

the Illinois Geological Survey and afterwards at the University of Chicago. As travel funds for fieldwork were scarce, he studied the complexes of Silurian reefs in the Chicago area which were within easy reach of the public transportation system. As a result of these efforts, Heinz deduced the pattern of ecological communities in the reef and surrounding sediments, and based on the assemblage of fossils present could determine their distance from the main wave-resistant structures (Lowenstam, 1950). Mundane as this may seem, it was an essential step which made it possible to locate subsurface petroleum reservoirs in fossil reefs based on exploratory drilling, a technique many oil companies were quick to exploit.

After his move to the California Institute of Technology in 1952, Heinz expanded his studies of fossil reef communities to include the Tertiary deposits found on tropical islands in the Central Pacific, with a particular focus on Palau. Due to sea level changes during the past few million years, many of these reefs are now exposed on land and offer easy access for study. Heinz noticed that when these limestone masses were exposed close to the intertidal zone, they often eroded into peculiar mushroom-shaped features. These "nip" islands were capped with vegetation and often had waves splashing around the base (Low­enstam, 1974), one of which is shown on the jacket of this book. Geomorphologists at that time thought that the action of the surf was responsible for the erosion in the intertidal zone, but this did not seem to fit the pattern which Lowenstam observed. He noticed that the depth that the nips cut into the limestone increased as one moved away from the active surf area toward the more quiet waters of the lagoons, an observation which clearly ruled out wave action as their source. Upon closer examination, Heinz discovered that the lime­stone within the actively eroding portion of the nips was heavily striated with subparallel chisel marks produced by the grazing action of polyplacophoran molluscs (chitons). This was strange, as limestone is much harder than the protein, chitin, which was thought to be the main structural component in the radular teeth of all molluscs. Yet the teeth were clearly eroding the rock, and there had to be a simple explanation. Visual examination of the radula (the tongue plate) revealed that the pairs of major lateral teeth contained a hard, somewhat shiny black substance which upon further analysis was identified as magnetite. For many years, petrologists and biologists alike were skeptical that the material in the teeth could have been a true biochemical precipitate, rather than inorganic sand grains which were merely assimilated from the local environment. Geologically, magnetite was only known to form at high temperatures and pressures in igneous and metamorphic rocks, and it came as quite a surprise to find it as a biochemical precipitate in the teeth of a mollusc.

Heinz Lowenstam was finally awarded his Ph.D. by the University of Munich in 1981, in recognition of the excellence of his work and in partial reparation for past injustices.

References

Baule, G. M., and McFee, R., 1963, Detection of the magnetic field of the heart, Am. Heart J. 66:95-96.

Butler, R. F., and Banerjee, S. K., 1975, Theoretical single-domain grain size range in magnetite and titanomagnetite, J. Geophys. Res. 80:4049-4058.

Evans, M. E., and McElhinny, M. W. 1969, An investigation of the origin of stable remanence in magnetite bearing igneous rocks, J. Geomagn. Geoelectr. 21:757-773.

Ising, G. 1945, Die physicalische Molichkeit eines tierischen Orientierungssines auf Basics der Er­drotation, Ark. Mat. Astron. Fys. 32A(18):1-23.

Kirschvink, J. 1., and Lowenstam, H. A., 1979, Mineralization and magnetization of chiton teeth: Paleomagnetic, sedimentologic, and biologic implications of organic magnetite, Earth Planet. Sci. Lett. 44:193-204.

Lowenstam, H. A., 1950, Niagaran reefs in Illinois and their relation to oil accumulation, Oil Gas J. 48:49-77.

xii Preface

Lowenstam, H. A., 1962a, Magnetite in denticle capping in recent chitons (Polyplacophora), Bull. Geol. Soc. Am. 73:435-438.

Lowenstam, H. A., 1962b, Goethite in radular teeth of recent marine gastropods, Science 137:279-280.

Lowenstam, H. A., 1963, Biologic problems relating to the composition and diagenesis of sediments, in: The Earth Sciences: Problems and Progress in Current Research (T. W. Donnelly, ed.), Uni­versity of Chicago Press, Chicago, pp. 137-195.

Lowenstam, H. A., 1967, Lepidocrocite, an apatite mineral, and magnetite in teeth of chitons (Poly­placophora), Science 156:1373-1375.

Lowenstam, H. A., 1968, Weddellite in a Marine Gastropod and in Antarctic Sediments, Science 162:1129-1130.

Lowenstam, H. A., 1972, Phosphate hard tissues of marine invertebrates: their nature and mechanical function, and some fossil implications. Chem. Geol. 9:153-166.

Lowenstam, H. A., 1974, Impact of life on chemical and physical processes, in: The Sea, Volume 5 (E. D. Goldberg, ed.), Wiley, New York, pp. 715-796.

Lowenstam, H. A., 1980, Bioinorganic constituents of hard parts, in: Biogeochemistry of Amino Acids (P. E. Hare, T. D. Hoering, and K. King, Jr., eds.), Wiley, New York, pp. 3-16.

Lowenstam, H. A., 1981, Minerals formed by organisms, Science 211:1126-1131. Lowenstam, H. A., 1984, Biomineralization processes and products and the evolution of biominer­

alization, 27th lnt. Geol. Congr. Sect. Paleontol. Theme C.02.1.5. Lowenstam, H. A., and Weiner, S., 1983, Mineralization by organisms, and the evolution of biomi­

neralization, in: Biomineralization and Biological Metal Accumulation (P. Westbroek and E. W. de Jong, eds.), Reidel, Dordrecht, pp. 191-203.

Neel, L., 1955, Some theoretical aspects of rock magnetism, Philos. Mag. Suppl. Adv. Phys. 4:191-243.

Towe, K. M., and Lowenstam, H. A., 1967, Ulstrastructure and development of iron mineralization in the radular teeth of Cryptochiton stelleri (Mollusca), J. Ulstrastruct. Res. 17:1-13.

Williamson, S. J., and Kaufman, 1., 1980, Biomagnetism, J. Magn. & Magn. Mater. 22:129-201.

Contents

I. Introduction and Background

Chapter 1 • Iron Biomineralization: A Geobiological Perspective

Heinz A. Lowenstam and Joseph L. Kirschvink

1. Introduction.......................................... 3 2. Biological Aspects of Iron Mineralization ................... 6 3. Biological Functions of Iron Biomineralization ............... 10 4. Geological Aspects of Biogenic Fe Oxides and Sulfides . . . . . . . . . 10

References ........................................... 13

Chapter 2 • Ferrimagnetic Properties of Magnetite

Subir K. Banerjee and Bruce M. Moskowitz

1. Introduction.......................................... 17 2. Basic Data ........................................... 18 3. Bulk Properties ....................................... 21 4. Magnetic Domain States ................................ 23 5. Remanent Magnetizations ............................... 31 6. Magnetic Granulometry ................................. 36

References ........................................... 38

Chapter 3 • The Geomagnetic Field: Its Nature, History, and Biological Relevance

Durward D. Skiles

1. Introduction.......................................... 43 2. The Main Geomagnetic Field. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47 3. The Field of External Origin ............................. 87

References ........................................... 98

II. Experimental Techniques and Instrumentation

Chapter 4 • An Introduction to the Use of SQUID Magnetometers in Biomagnetism

M. Fuller, W. S. Goree, and W. 1. Goodman

1. Introduction.......................................... 103 2. Operating Principles of SQUIDs. . . . . . . . . . . . . . . . . . . . . . . . . . . 104

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3. Cryogenics........................................... 121 4. Instrument Configurations ............................... 129 5. Applications of SQUID Magnetometers in Biomagnetism ....... 136 6. Conclusions.......................................... 148

References ........................................... 149

Chapter 5 • Detection, Extraction, and Characterization of Biogenic Magnetite

Michael M. Walker, Joseph 1. Kirschvink, Anjanette Perry, and Andrew E. Dizon

1. Introduction.......................................... 155 2. Magnetometry Studies ...... . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156 3. Extraction and Characterization of Biogenic Magnetite ......... 160 4. Discussion........................................... 163 5. Summary............................................ 164

References ........................................... 165

Chapter 6 • Studying Mineral Particulates of Biogenic Origin by Transmission Electron Microscopy and Electron Diffraction: Some Guidelines and Suggestions

Kenneth M. Towe

1. Introduction.......................................... 167 2. Sample Preparation for Electron Microscopy . . . . . . . . . . . . . . . . . 168 3. Studying the Sample in the Microscope .................... 173 4. Analysis of Electron Diffraction Powder Patterns. . . . . . . . . . . . . . 178 5. Conclusions.......................................... 179

Selected References .................................... 180

Chapter 7 • The Cellular Localization of Particulate Iron

Benjamin Walcott

1. Introduction.......................................... 183 2. Anatomical Techniques ................................. 184 3. An Example: The Bumblebee. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188 4. Conclusions.......................................... 193

References ........................................... 195

Chapter 8 • Large-Volume, Magnetically Shielded Room: A New Design and Material

Gary R. Scott and Cliff Frohlich

1. Introduction.......................................... 197 2. General Principles of Electric and Magnetic Shielding ......... 199

Contents xv

3. Practical Techniques for Building Magnetically Shielded Rooms 208 4. Three Specific Examples ................................ 214 5. Summary............................................ 219

References ........................................... 220

III. Magnetoreception: Theoretical Considerations

Chapter 9 • Limits to Induction-Based Magnetoreception

Bruce Rosenblum, Roger 1. Jungerman, and Laurent Longfellow

1. Introduction.......................................... 223 2. Noise and General Considerations . . . . . . . . . . . . . . . . . . . . . . . . . 224 3. The Induction Magnetoreception Organ. . . . . . . . . . . . . . . . . . . . . 225 4. Conclusion........................................... 231 5. Addendum: A Comment on Navigation . . . . . . . . . . . . . . . . . . . . . 231

References ........................................... 231

Chapter 10 • Energetics and Sensitivity Considerations of Ferromagnetic Magnetoreceptors

Ellen D. Yorke

1. Introduction.......................................... 233 2. Energy Considerations .................................. 234 3. Response Times . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235 4. Sensitivity to Field Changes ............................. 238 5. Other Types of Receptors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 6. Tests of the Hypothesis ................................. 239

References ........................................... 241

Chapter 11 • Particle-Size Considerations for Magnetite-Based Magnetoreceptors

Joseph 1. Kirschvink and Michael M. Walker

1. Introduction.......................................... 243 2. The Thermally Driven Variance Model of Magnetic Intensity

Reception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248 3. Discussion........................................... 251 4. Summary............................................ 253

References ........................................... 253

Chapter 12 • Are Animal Maps Magnetic?

James 1. Gould

1. Introduction.......................................... 257 2. The Compass Sense ....... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258

xvi Contents

3. The Map Sense ....................................... 259 4. Problems with Magnetic Maps . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 5. Future Research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265

References ........................................... 266

IV. Magnetoreception and Magnetic Minerals in Living Organisms

Chapter 13 • Mossbauer Spectroscopy of Iron Biomineralization Products in Magnetotactic Bacteria

Richard B. Frankel, Georgia C. Papaefthymiou, and Richard P. Blakemore

1. Introduction to Mossbauer Spectroscopy . . . . . . . . . . . . . . . . . . . . 269 2. Application of Mossbauer Spectroscopy to Magnetotactic Bacteria 279

References ........................................... 285

Chapter 14 • Magnetotactic Microorganisms Found in Muds from Rio de Janeiro: A General View

Henrique G. P. Lins de Barros and Darci Motta S. Esquivel

1. Introduction.......................................... 289 2. The Geomagnetic Field ................................. 290 3. Results.............................................. 291 4. Conclusions.......................................... 305

References ........................................... 308

Chapter 15 • Structure, Morphology, and Crystal Growth of Bacterial Magnetite

Stephen Mann

1. Introduction.......................................... 311 2. Instrumentation: High-Resolution Transmission Electron

Microscopy .......................................... 312 3. Materials and Methods ................................. 312 4. Results.............................................. 315 5. Discussion: Bioprecipitation of Bacterial Magnetite . . . . . . . . . . . . 323 6. Conclusions.......................................... 330

References ........................................... 331

Contents

Chapter 16 • Biomineralization Processes of the Radula Teeth of Chitons

Michael H. Nesson and Heinz A. Lowenstam

xvii

1. Introduction.......................................... 333 2. Materials and Methods ................................. 334 3. Anatomy and Operation of the Radula Apparatus ....... . . . . . . 335 4. Anatomy of the Radula Sac .............................. 337 5. Blood Chemistry ...................................... 341 6. The Ultrastructure of the Mineralization Zone . . . . . . . . . . . . . . . . 342 7. Concluding Remarks ................................... 361

References ........................................... 361

Chapter 17 • Magnetic Remanence and Response to Magnetic Fields in Crustacea

Ruth E. Buskirk and William P. O'Brien, Jr.

1. Introduction.......................................... 365 2. Experimental Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 368 3. Discussion........................................... 377 4. Summary............................................ 380

References ........................................... 381

Chapter 18 • Magnetic Field Sensitivity in Honeybees

William F. Towne and James 1. Gould

1. Introduction.......................................... 385 2. Magnetic Fields Cause Misdirection in the Waggle Dance. . . . . . . 386 3. Magnetically Oriented Horizontal Dances ................... 392 4. Magnetic Orientation of Comb-Building. . . . . . . . . . . . . . . . . . . . . 393 5. Magnetic Fields and Orientation in Time ................... 395 6. The Magnetic Receptor System ........................... 398 7. Summary and Conclusions .............................. 403

References ........................................... 404

Chapter 19 • Magnetic Butterflies: A Case Study of the Monarch (Lepidoptera, Danaidae)

Bruce J. MacFadden and Douglas S. Jones

1. Introduction.......................................... 407 2. Natural History of the Monarch Butterfly ................... 408 3. Materials and Methods ................................. 408 4. Induced Magnetization ................................. 410 5. Ontogeny of Magnetic Mineralization ...................... 411 6. Intraspecific and Interspecific Variation .................... 412 7. Attempts to Characterize the Magnetic Mineralogy ............ 413

xviii Contents

8. Summary and Conclusions .............................. 414 References ........................................... 415

Chapter 20 • Magnetoreception and Biomineralization of Magnetite: Fish

Michael M. Walker, Joseph 1. Kirschvink, and Andrew E. Dizon

1. Introduction.......................................... 417 2. Magnetic Sensitivity in Yellowfin Tuna .................... 419 3. Detection of Magnetic Material in Fish ..................... 422 4. Characterization of the Magnetic Material ................... 426 5. Identification and Analysis of the Magnetic Material. . . . . . . . . . . 429 6. Discussion........................................... 431

References ............................................ 434

Chapter 21 • Magnetoreception and Biomineralization of Magnetite in Amphibians and Reptiles

Anjanette Perry, Gordon B. Bauer, and Andrew E. Dizon

1. Introduction.......................................... 439 2. Amphibians.......................................... 440 3. Reptiles ............................................. 443 4. Conclusion........................................... 452

References ........................................... 452

Chapter 22 • Avian Navigation, Geomagnetic Field Sensitivity, and Biogenic Magnetite

David E. Presti

1. The Sensory Basis of Bird Navigation ...................... 455 2. Orientation Experiments with Homing Pigeons ............... 459 3. Orientation Experiments with Migratory Birds ............... 464 4. Effects of Small Magnetic Field Changes on Navigation: The

Possibility of a Geomagnetic Map ......................... 469 5. Laboratory Attempts to Measure Avian Magnetic Field Sensitivity

472 6. Magnetite in Birds and Possible Mechanisms of Magnetic Field

Sensitivity ........................................... 474 References ........................................... 477

Chapter 23 • Magnetic Remanence in Bats

Edward R. Buchler and Peter J. Wasilewski

1. Introduction.......................................... 483 2. Methods............................................. 483

Contents xix

3. Results 484 4. Discussion........................................... 485

References ........................................... 486

Chapter 24 • Magnetoreception and Biomineralization of Magnetite in Cetaceans

Gordon B. Bauer, Michael Fuller, AnjaneUe Perry, J. Robert Dunn, and John Zoeger

1. Introduction.......................................... 489 2. Behavioral Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 490 3. Anatomical Studies .................................... 495 4. Conclusion........................................... 503

References ........................................... 505

Chapter 25 • Magnetoreception and the Search for Magnetic Material in Rodents

Janice G. Mather

1. Introduction.......................................... 509 2. Influence of Magnetic Fields on Physiology. . . . . . . . . . . . . . . . . . 510 3. Magnetoreception ..................................... 510 4. The Search for the Magnetoreceptor ....................... 522 5. Summary............................................ 531

References ........................................... 532

V. Human Magnetoreception: An Editorial Introduction

Chapter 26 • Magnetoreception by Man and Other Primates

R. Robin Baker

1. Introduction.......................................... 537 2. Physiological Responses to Changes in the Ambient Magnetic

Field ............................................... 538 3. Magnetoreception ..................................... 539 4. Magnetoreceptors?.................................... 550 5. Discussion........................................... 556 6. Summary............................................ 559

References ........................................... 559

Chapter 27 • Statistical and Methodological Critique of Baker's Chapter

Tom Dayton

1. Statistics in General . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 563 2. "Chair" Experiments Results Section. . . . . . . . . . . . . . . . . . . . . . . 565

xx Contents

3. Princeton Data Do Not Support Baker ...................... 565 4. Magnets vs. Controls for Baker's Experiments ................ 567 5. Magnets vs. Controls for K-6 ............................. 567 6. Physiology of Magnetoreceptors . . . . . . . . . . . . . . . . . . . . . . . . . . . 568 7. Summary............................................ 568

References ........................................... 568

Chapter 28 • Human Navigation: Attempts to Replicate Baker's Displacement Experiment ........................ 569

Kenneth P. Able and William F. Gergits

Chapter 29 • Human Homing Orientation: Critique and Alternative Hypotheses

Kraig Adler and Chris R. Pelkie

1. Introduction.......................................... 573 2. Bus Tests Conducted at Ithaca, New York . . . . . . . . . . . . . . . . . . . 574 3. Oriented Distributions from "Random" Data . . . . . . . . . . . . . . . . . 584

References ........................................... 587 Notes ............................................... 587 Reply to Baker . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 591

Chapter 30 • Absence of Human Homing Ability as Measured by Displacement Experiments ....................... 595

James L. Gould

Chapter 31 • A Study of the Homeward Orientation of Visually Handicapped Humans

Timothy K. Judge

1. Introduction.......................................... 601 2. Methods............................................. 601 3. Results.............................................. 601 4. Discussion........................................... 602

References ........................................... 603

Chapter 32 • An Attempt to Replicate the Spinning Chair Experiment 605

Joseph 1. Kirschvink, Karla A. Peterson, Michael Chwe, Paul Filmer, and Brenda Roder

Contents xxi

Chapter 33 • A Cautionary Note on Magnetoreception in Dowsers. . . . 609

Joseph L. Kirschvink

Chapter 34 • Human Navigation: A Summary of American Data and Interpretation

1. 2. 3.

R. Robin Baker

The American Data The American Criticisms ............................... . Concluding Remarks .................................. . References ...................... .................... .

VI. Biogenic Magnetite in the Fossil Record

Chapter 35 • A Search for Bacterial Magnetite in the Sediments of Eel Marsh, Woods Hole, Massachusetts

Anne Demitrack

611 614 621 621

1. Introduction.......................................... 625 2. Bacterial Magnetite .................................... 626 3. Methods............................................. 627 4. Results.............................................. 630 5. Discussion........................................... 639

Appendix 1: Eel Marsh NRM and Saturation Magnetization Data

Appendix 2: Description of Computer Procedure Used to Make Stability Field Diagram 8a ................... .

References ........................................ .. .

Chapter 36 • Possible Biogenic Magnetite Fossils from the Late Miocene Potamida Clays of Crete

Shih-Bin R. Chang and Joseph Kirschvink

643

644 644

1. Introduction.......................................... 647 2. Samples............................................. 648 3. Laboratory Extraction of Magnetite ........................ 650 4. Magnetic Studies ...................................... 653 5. Size and Shape Distribution of Magnetite ................... 654 6. Origin of Magnetite .................................... 655 7. Conclusion and Applications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 666

References ........................................... 667

Index ................................................... 671