HANDBOOK OF

APPLIED DOG BEHAVIOR AND TRAINING

Volume One

Adaptationand

Learning

Steven R. Lindsay

FOREWORD BY Victoria Lea VoithCharter Diplomate, American College of Veterinary BehavioristsPresident, American Veterinary Society of Animal Behavior

HANDBOOK OF APPLIED DOG BEHAVIOR AND TRAINING

Volume One

Adaptationand

Learning

HANDBOOK OF

APPLIED DOG BEHAVIOR AND TRAINING

Volume One

Adaptationand

Learning

Steven R. Lindsay

FOREWORD BY Victoria Lea VoithCharter Diplomate, American College of Veterinary BehavioristsPresident, American Veterinary Society of Animal Behavior

STEVEN R. LINDSAY, MA, is a dog behavior consultant and trainer who lives in Philadelphia, Pennsyl-vania, where he provides a variety of behavioral training and counseling services. In addition to his longcareer in working with companion dogs, he previously evaluated and trained highly skilled military work-ing dogs as a member of the U.S. Army Biosensor Research Team (Superdog Program). Mr. Lindsay alsoconducts workshops and is the author of numerous publications on dog behavior and training.

Cover design by Justin EcclesText design by Dennis Anderson

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Printed on acid-free paper in the United States of AmericaFirst edition, 2000

Library of Congress Cataloging-in-Publication Data

Lindsay, Steven R.Handbook of applied dog behavior and training / Steven R. Lindsay; foreword by Victoria LeaVoith.—1st ed.

p. cm.Contents: v. 1. Adaptation and learning.ISBN-13: 978-0-8138-0754-6ISBN-10: 0-8138-0754-91. Dogs—Behavior. 2. Dogs—Training. I. Title.

SF433.L56 1999636.7′0887—dc21 99-052013

The last digit is the print number: 9 8 7 6

Dedicated with affection

and respect to my dog,

Yuki,whose gentle and sincere

ways have revealed the virtues

of the human-dog bond in

ways that words alone will

forever fail to express.

Contents

1 Foreword xi

1 Acknowledgments xiii

1 Introduction xv

1 Origins and Domestication 3

Archeological Record 4Domestication: Processes and Definitions 4Biological and Behavioral Evidence 11Effects of Domestication 12The Silver Fox: A Possible Model of Domestication 22Selective Breeding, the Dog Fancy, and the Future 23References 28

2 Development of Behavior 31

The Critical or Sensitive Period Hypothesis 33Early Development and Reflexive Behavior 35Socialization: Learning to Relate and Communicate 43Learning to Compete and Cope 50Learning to Adjust and Control 58Preventing Behavior Problems 67References 68

3 Neurobiology of Behavior and Learning 73

Cellular Composition of the Brain 75Hindbrain and Midbrain Structures 76Diencephalon 78Limbic System 82Learning and the Septohippocampal System 87Cerebral Cortex 90Neurotransmitters and Behavior 93Neural Substrates of Motivation (Hypothalamus) 102Neurobiology of Aggression (Hypothalamus) 103Neurobiology of Fear 105Autonomic Nervous System–mediated Concomitants of Fear 108Neurobiology of Compulsive Behavior and Stereotypies 113Neurobiology of Attachment and Separation Distress 115

Psychomotor Epilepsy, Catalepsy, and Narcolepsy 119References 121

4 Sensory Abilities 127

Vision 127Audition 133Olfaction 136Vomeronasal Organ 145Gustation 146Somatosensory System 149Reflexive Organization 154Extrasensory Perception 156References 161

5 Biological and Dispositional Constraints on Learning 167

Nature Versus Nurture 167Instincts, “Fixed” Action Patterns, and Functional Systems 169Instinctual Learning 171Preparedness and Selective Association 174Instinctive Drift and Appetitive Learning 182Contrafreeloading 183Genetic Predisposition and Temperament 184Breed Variations 187Inheritance of Fear 190Heredity and Intelligence 193References 195

6 Classical Conditioning 201

Pavlov’s Discovery 202Basic Conditioning Arrangements Between Conditioned Stimulus and

Unconditioned Stimulus 203Common Examples of Classical Conditioning 204Konorski’s Conceptualization of Reflexive Behavior 205Rescorla’s Contingency Model of Classical Conditioning 207Stimulus Factors Affecting Conditioned-Stimulus Acquisition

and Maintenance 211Conditioned Compound Stimuli 215Higher-Order Conditioning 215Generalization and Discrimination 216Extinction of Classical Conditioning 218Spontaneous Recovery and Other Sources of Relapse 218Habituation and Sensitization 219Special Phenomena of Classical Conditioning 219Classically Generated Opponent Processes and Emotions 222Counterconditioning 225Classical Conditioning and Fear 226References 231

viii CONTENTS

7 Instrumental Learning 233

Differences Between Classical and Instrumental Conditioning 234Theoretical Perspectives 236Thorndike’s Connectionism 236Guthrie’s Learning Theory and Behavior Modification 237Tolman’s Expectancy Theory 240B. F. Skinner and the Analysis of Behavior 243Basic Concepts and Principles of Instrumental Learning 245Motivation, Learning, and Performance 249Antecedent Control: Establishing Operations and

Discriminative Stimuli 250Premack Principle: The Relativity of Reinforcement 251Learning and the Control of the Environment 252Schedules of Positive Reinforcement 254Everyday Examples of Reinforcement Schedules 255Hope, Disappointment, and Other Emotions Associated

with Learning 256Matching Law 257Extinction of Instrumental Learning 259Differential Reinforcement 260Attention Control 262Training and Stimulus Control 263Shaping: Training Through Successive Approximations 263Adduction 265Chaining: Ordering Complex Performances 265Prompting, Fading, and Shadowing 266Rehearsal and Staging 267Transfer of Learning 267Behavioral Contrast and Momentum 268Social Learning 269Higher-Order Classes of Behavior 272Attention and Learning 273A Brief Critique of Traditional Learning Theory 276Prediction-Control Expectancies and Adaptation 282Conclusion 285References 286

8 Aversive Control of Behavior 289

Fear and Pain 290Negative Reinforcement and Avoidance Learning 290Mowrer’s Two-Process Theory of Avoidance Learning 292A Cognitive Theory of Avoidance Learning 294Safety Signal Hypothesis 295Species-Specific Defensive Reactions and Avoidance Training 297Punishment 298P+ and P−: A Shared Emotional and Cognitive Substrate? 305Punishers, Rewards, and Verifiers 306

Contents ix

Direct and Remote Punishment 308Using Time-out to Modify Behavior 309How to Use Time-out 310Types of Time-out 312Time-out and Social Excesses 313Negative Practice, Negative Training, and Overcorrection

(Positive Practice) Techniques 314Remote-Activated Electronic Collars 315Misuse and Abuse of Punishment 316Abusive Punishment: The Need for Universal Condemnation 320General Guidelines for the Use of Punishment 320References 322

9 Learning and Behavioral Disturbances 325

Experimental Neurosis 326Gantt: Schizokinesis, Autokinesis, and Effect of Person 329Liddell: The Cornell Experiments 332Masserman: Motivational Conflict Theory of Neurosis 335Frustration and Neurosis: The Theories of Maier and Amsel 340Learned Helplessness 342Post-Traumatic Stress Disorder 344Conflict and Neurosis 346Neurosis and the Family Dog 356References 357

10 Human-Dog Companionship: Cultural and Psychological Significance 361

Theories of Pet Keeping 361Forming the Ancient Bond 364Affection and Friendship 366The Effect of Person 367When the Bond Fails 368Psychoanalysis and the Human-Dog Bond: Conflicts and Contradictions 371Communicating, Relating, and Attachment 374The Question of Animal Awareness 381Mysticism 385Dog Devotion: Legends 388Cynopraxis: Training and the Human-Dog Relationship 389References 392

10 Index 397

x CONTENTS

Foreword

VICTORIA LEA VOITH, DVM, PHD

Charter Diplomate of the American College of Veterinary Behaviorists

President, American Veterinary Society of Animal Behavior

but others will be compelled to obtain theoriginal works and read them.

Very practical and important aspects ofthis book are Steve Lindsay’s training, treat-ment, and management strategies regardingdog behavior. Steve’s broad experiences in thedog world have enabled him to integratevaluable components of a variety of trainingand management procedures. The techniquesare explained very thoroughly and in suffi-cient detail that an educated person shouldbe able to understand and implement them.His approaches are designed to achieve a sat-isfying human-dog relationship from the per-spective of both species.

This handbook will help dog owners andmany, many canine behavior consultants/counselors and trainers. It will also stimulatefurther discussion, observation, research, andanalyses, ultimately leading to more knowl-edge about dog behavior and human-dog in-teractions. I consider it the most valuablepublication about dogs since Scott andFuller’s classic text Genetics and the Social Be-havior of the Dog, published in 1965.

THIS IS A monumental work arising from the love of dogs and the pursuit of

knowledge. Cynophiles, academics, animalbehaviorists (with and without institutionaldegrees), literate dog owners, and anyonewho has ever wanted to know something spe-cific or just plain more about dogs are in-debted to Steve Lindsay for this labor of love.

This treatise is an encyclopedia aboutdogs: in-depth reviews and interpretations ofthe literature pertaining to the dog’s history,physiology, behavior, and interactions withpeople, and explanations and evaluations oftraining procedures, management strategies,and problem-solving techniques. This book isnot limited to a review of the literature aboutdogs but also discusses basic scientific disci-plines and discoveries with other species thatpertain to understanding dogs. It is obviousthat Steve Lindsay has thoroughly read andanalyzed every publication he has refer-enced—an increasing rarity in today’s press.The summaries of research papers or theoreti-cal discussions will suffice for some readers,

xi

Acknowledgments

MANY PEOPLE deserve acknowledgmentfor their contributions, but none more

so than the dog owners who have given methe privilege and responsibility of helpingthem to train their dogs or to assist them inresolving a behavior problem. I feel a specialdebt of gratitude to William Carr, Scott Line,and Victoria Voith. Dr. Carr graciously gavefreely of his time to read and discuss the en-tire manuscript. His knowledge and expertisehelped to clarify a number of important areasof relevant research, especially developmentsin comparative psychology and the study of

olfaction. Dr. Line reviewed the entire textand provided useful suggestions for its im-provement. Dr. Voith has been a source ofsustained encouragement for the project sinceits inception, giving me valuable guidance andadvice. A special thank you is due to ChristinaCole for her unselfish help and support. I amgrateful to John Flukas, whose editorial advicehas been consistently constructive and helpful.Finally, I thank Gretchen Van Houten and thegreat staff at Iowa State University Press fortheir assistance and patience in preparing themanuscript for publication.

xiii

THE DOG has occupied an enduring placein our cultural heritage as an icon of in-

terspecies cooperation and faithfulness. Spec-ulation about the origins of this unique rela-tionship continues to inspire lively debateand discussion, but nothing definitive can yetbe said about the motivations guiding thefirst dog keepers to capture and tame wild orsemidomesticated canids as companions andhelpers. Even less can be said about the vari-ous functions these protodogs served or themethods used by our ancestors to train them.What is known suggests that the dog’s do-mestication was not the result of a consciouseffort or stroke of genius, but rather the out-come of a slow evolutionary process overmany thousands of years. The gradual biolog-ical transformation of the wolf into the do-mestic dog appears to have culminated in thedevelopment of close social interaction be-tween humans and dogs sometime during theStone Age. What form this relationship took14,000 years ago is not known, but it is likelythat some practical implications of dogs wererecognized and exploited by ancient hunter-gatherers. Most of the potential utilitarianbenefits arising from domestication wouldhave been of little use, though, if it had notbeen for the simultaneous development ofthe methods needed for managing and con-trolling dog behavior. The obvious necessityof behavioral control for early humans intheir various dealings with dogs led the natu-ralist G. L. Buffon to write in the 18th cen-tury, “The training of the dog seems to havebeen the first art invented by man, and thefruit of that art was the conquest and peace-able possession of the earth” (quoted in Jack-son, 1997).

Buffon’s suggestion that dog training was“the first art invented by man” suffers from alack of empirical evidence. Nonetheless, it isreasonable to believe that the practice of con-trolling and modifying dog behavior to servehuman purposes springs from very ancientroots that antedate the rise of civilization.Early human association with animals as nat-ural competitors and beasts of prey offeredample opportunity born of strife and neces-sity to develop an appreciation of animalhabits and various methods for controllinganimal behavior. Such information transmit-ted from generation to generation wouldhave provided a viable cultural tradition ofanimal lore for the development of dog train-ing as an art of considerable sophistication.From an early date, dogs have performedmany services, such as assisting humanhunters in the pursuit of game, giving alarmto the presence of intruders, pulling sledge ortravois, providing warmth and comfort, aswell as offering playful distraction for chil-dren. Practical uses aside, even the most ca-sual interaction between humans and dogswould have demanded a rudimentary under-standing of dog behavior and the ability tocontrol it. Both biological changes (nature)and cultural transmission (nurture) combinedto forge the primal human-dog bond—anepigenetic process that is reenacted in the lifeof every companion dog.

Despite the ubiquitous distribution ofdogs throughout the ancient world, historicalrecords describing their early use, breeding,and training are relatively rare and incom-plete. A few ancient authors wrote at lengthon the subject of dog behavior, training, andmanagement, but, for the most part, many

Introduction

Before you can study an animal, you must first love it.

KONRAD LORENZ (Fox, 1998)

xv

important details about the specific methodsused by ancient trainers to modify dog be-havior are left to the reader’s imagination.The writings of Xenophon are of particularvalue in this respect, but even the patronphilosopher of dog and horse training pro-vides only scant and scattered informationabout how dogs were trained in the distantpast. Although occasional departures fromthis pattern can be found, very few authorstook up the subject of dog behavior andtraining as a serious area of study, at least un-til fairly recent times. A turning point awayfrom this general neglect occurred with theappearance of Darwin’s The Expression of theEmotions in Man and Animals. Darwin’s evo-lutionary theories and careful descriptions ofdog behavior exerted a profound influence onnaturalists sympathetic to his ideas, encour-aging them to pay attention to dog behavioras a way to understand better the origins ofhuman conduct. These developments playedan instrumental role in the advancement ofpsychology and paved the way for a widerscientific and popular interest in dog behav-ior.

The scientific study of dog behavior andpsychology was placed on an experimentalfoundation by the Russian physiologist IvanPavlov. Pavlov and his many associates craftedvarious experimental methods for studyingassociative learning processes in dogs. The re-sult of this revolutionary research was a col-lection of detailed and exhaustive analyses ofthe functional relations controlling the acqui-sition and extinction of conditioned reflexivebehavior. Following in the wake of Pavlov’sdiscoveries, subsequent developments in thescience of behavior and learning theory wereextremely energetic and enthusiastic, withmany thousands of studies being carried outand their findings published over the ensuingdecades. In America, around the same timethat Pavlov was making his mark on the his-tory of psychology in Russia, EdwardThorndike was conducting a systematic studyof voluntary or instrumental behavior at Co-lumbia University. His detailed observationson how animals learn to escape from variouspuzzle boxes through trial and error (or, as hemight prefer, “trial and success”) establishedthe study of instrumental behavior. Together,

Pavlov and Thorndike formed the intellectualand methodological foundations for the ex-perimental study of animal behavior andlearning. Most behavioral research in the20th century can be traced back to the pio-neering work of these two experimentalists.

Darwin’s evolutionary approach to the in-vestigation of animal behavior was embracedby another group of scientists, mainly com-posed of Europeans, who emphasized the im-portance of direct observation of species-typi-cal behavior occurring under naturalconditions. Their efforts set the foundationsfor the development of ethology. In America,comparative (animal) psychologists, who, liketheir European counterparts, were also inter-ested in the evolutionary continuity of behav-ior across species, also took up the Darwinianbanner. Unlike the early ethologists, however,comparative psychologists stressed the needfor experimental methodology, thus limitingtheir research to a few species (mainly pri-mates, rodents, and birds) housed under lab-oratory conditions.

These combined scientific efforts haveproduced an authoritative body of knowledgeabout animal behavior. Much of this infor-mation is highly specialized, sometimes diffi-cult to access, and often only available as iso-lated research reports. Consequently, animportant purpose for writing this book hasbeen to draw upon these various trends in or-der to establish a foundation of principlesand methods for understanding and manag-ing dog behavior. The material reviewed forthis purpose has been selected based on twogeneral criteria: scientific validity and rele-vance for the practical management of dogbehavior. In surveying the literature, I havemade a conscientious effort to review theoriginal materials. It became apparent earlyon that many reports and secondary texts hadbeen either inappropriately interpreted orgeneralized beyond what is justifiable by theavailable data. I have done my best to avoidsuch pitfalls and to correct errors of the pastwhere appropriate. The topics covered inVolume One include origins and evolution,ontogeny, neurobiology, senses, biologicalconstraints, classical conditioning, instrumen-tal learning, aversive control, and behavioralpathology. A concluding chapter examines

xvi INTRODUCTION

the human-dog relationship, including itscultural and psychological significance.Volume 2 (in press) covers the etiology andassessment of behavior problems, aggression,fear and phobias, separation distress, hyperac-tivity, compulsive behavior, destructive be-havior, and social excesses.

Many of the experiments described in thefollowing chapters were performed at a hugecost of suffering for scores of laboratory ani-mals, including thousands of dogs, experi-mented upon for the sake of scientific curios-ity and the advancement of our collectiveknowledge. It is heartening to know that,over the past decade or so, many reforms (of-ten led by experimental scientists themselves)have taken place with respect to the way ex-perimental animals are treated and housed.These regulatory changes would make manyhistorically important studies very difficult orimpossible to perform under the currentstandards of laboratory animal care and wel-fare. However, to ignore this significant bodyof scientific literature because of the sufferingit has brought to laboratory animals wouldbe tantamount to a double injury. It seemsfitting that such knowledge should be appliedwhenever possible for the benefit of those an-imals whose sacrifice made it possible.Morally speaking, there are no good or badscientific facts, but there are good and badways in which experiments are performedand scientific knowledge applied for practicalpurposes.

Finally, dog behavior problems represent aserious welfare concern. Currently, the vastmajority of dog behavior services are per-formed by dog trainers, with a handful ofveterinary and applied animal behavior con-sultants providing regional counseling ser-vices through veterinary schools and privateanimal behavior practices spread out thinlyacross the country. It is difficult to pin downexactly how professional services are dividedbetween these groups, but a recent survey bythe American Veterinary Medical Association(1997) suggests that a relatively small numberof companion animals are referred for behav-ioral counseling. The report estimates thatless than one-half of 1% of dog owners in the

United States utilized veterinary behavioralcounseling services in 1996. This is a some-what surprising and puzzling statistic, consid-ering that some authorities suggest that be-havior problems represent a leading cause ofeuthanasia, causing the death of more dogseach year than die as the result of infectiousdisease, metabolic conditions, and cancercombined. Although this estimate appears tobe inflated (see When the Bond Fails in Chap-ter 10), dog behavior problems do, undoubt-edly, represent a significant source of distressand death for dogs. Obviously, cooperationbetween all applied animal behavior profes-sionals is required in order to service the be-havioral needs of the dog-owning publicmost efficiently and effectively. Animal be-havior counseling, dog training, and veteri-nary behavioral medicine bring a variety ofspecific contributions and unique strengths tothe practical control of dog behavior and themanagement of dog behavior problems. Re-cently, leadership from these various profes-sional groups made the first tentative stepstoward constructive collaboration by estab-lishing various educational programs, spon-soring interdisciplinary forums, and organiz-ing other mutually beneficial ventures.Unfortunately, however, practitioners fromthese various disciplines are not always famil-iar with the specialized knowledge and skillsutilized by others working outside of theirimmediate domain or not sharing their aca-demic and practical background. It is my sin-cere hope that this book will play a construc-tive role in ameliorating this situation bybridging some of these gaps and contributingto the process of professional and educationalreform of dog training and behavioral coun-seling.

REFERENCES

American Veterinary Medical Association (1997).U.S. Pet Ownership and Demographic Source-book. Schaumberg, IL: AVMA, Center for In-formation Management.

Fox MW (1998). Concepts in Ethology: AnimalBehavior and Bioethics. Malabar, FL: Krieger.

Jackson F (1997). Faithful Friends: Dogs in Lifeand Literature. New York: Carrol and Graf.

INTRODUCTION xvii

3

Archeological RecordDomestication: Processes and Definitions

Interspecific Cooperation: MutualismTerms and Definitions: Wild, Domestic,

and FeralThe Dingo: A Prototypical DogThe Carolina Dog: An Indigenous Dog?

Biological and Behavioral EvidenceBiological EvidenceBehavioral Evidence

Effects of DomesticationMorphological Effects of DomesticationBehavioral Effects of DomesticationPaedomorphosis

The Silver Fox: A Possible Model ofDomestication

Selective Breeding, the Dog Fancy, and theFuture

Origins of Selective BreedingProspects for the Future

References

UNDERSTANDING THE dog’s behaviorand appreciating its unique status as

“man’s best friend” is not possible withoutstudying its evolution and domestication.From ancient times onward, numerousspecies have undergone pronounced biologi-cal and behavioral changes as the result ofdomestication. The purposes guiding theseefforts are as diverse as the species involved.

Utilitarian interests such as the procurementof food, security, and other valuable resourcesor services derived from the animal weresurely important incentives, but utilitarianmotives alone are not enough to explain thewhole picture, especially when consideringthe domestication of the dog.

Many theories have been advanced to ex-plain how the progenitor of the dog was orig-inally tamed and brought under the yoke ofcaptivity and domestication. These theoriesoften include colorful portraits of primitivelife, motives, and purposes that rely on anumber of questionable and unprovable as-sumptions about prehistoric existence(Morey, 1994). For example, one popularview suggests that humans may possess anageless and universal (innate?) urge to keepanimals as pets. Although this theory hassome attractive features, it is difficult to de-fend scientifically. Certainly, dogs share an in-timate place in Western society and are oftentreated with affectionate care in many mod-ern primitive cultures as well (Serpell,1986/1996); nonetheless, one cannot excludethe possibility that this so-called “affection-ate” motive is a rather late cultural develop-ment. Further, although it is true that keep-ing pets as attachment objects is commonaround the world today, one cannot jumpfrom this observation to the conclusion that asimilar set of motives guided ancient people

1

Origins and Domestication

For thousands of years man has been virtually, though unconsciously, performingwhat evolutionists may regard as a gigantic experiment upon the potency of individ-ual experience accumulated by heredity; and now there stands before us this mostwonderful monument of his labours—the culmination of his experiment in the trans-formed psychology of the dog.

GEORGE ROMANES, Animal Intelligence (1888)

to capture and domesticate wild animals. At-titudes about animals and, in particular, dogsappear to be guided by beliefs and customsthat are to a considerable extent conditionedand dependent on cultural, economic, andgeographical circumstances (see Chapter 10).

Undoubtedly, a dog’s life during the earlystages of domestication was very differentthan it is today. Over the centuries, the dog’sfunctions have evolved and changed, some-times dramatically, depending on the asser-tion or absence of relevant cultural and sur-vival pressures. In times of scarcity and need,the defining motive for keeping dogs wasprobably dominated by utilitarian interests;whereas, during times of abundance andwell-being, dogs could be readily transformedinto convenient objects for affection, com-fort, or entertainment.

ARCHEOLOGICAL RECORD

Despite the difficulties, discovering when andhow this enduring relationship first appearedare questions of tremendous scientific interestand importance. Authorities differ with re-spect to the exact historical moment or timeframe, but many prehistoric sites show that aclose association between humans and dogshas existed continuously for many thousandsof years. Although a loose symbiotic mutual-ism probably existed long beforehand, theearliest archeological evidence of a “true” do-mestic dog is dated to 14,000 years beforethe present (BP). The artifact (a mandible)was unearthed from a Paleolithic grave site atOberkassel in Germany (Nobis, 1979, inClutton-Brock and Jewell, 1993). Protschand Berger (1973) have collected and carbondated canine skeletal remains taken at varioussites around the world, showing great antiq-uity and geographical dispersion: Star Carr(Yorkshire, England), 9500 BP; Argissa-Mag-ula (Thessaly), 9000 BP; Hacilar (Turkey),9000 BP; Sarab (Iran), 8900 BP; and Jericho,8800 BP. One of the most famous of thesearcheological finds is a Natufian skeleton ofan old human (sex unknown) and a puppyburied together some 12,000 years ago at EinMallaha in Israel (Davis and Valla, 1978).The human’s hand is positioned over thechest of the 4- or 5-month-old puppy (Fig.

1.1). One is moved by the ostensible inti-macy of the two species buried together, andeven tempted to ascribe a feeling of “tender-ness” to the embrace binding the person andpuppy together over the centuries.

The earliest remains of a domestic dog inNorth America were found at the JaguarCave site in the Beaverhead Mountains ofIdaho. These bones had been previouslydated from 10,400 to 11,500 BP, but radio-carbon dating of some of the artifacts re-vealed that they are “intrusions” of a muchmore recent origin, with a probable age notexceeding 3000 years (Clutton-Brock andJewell, 1993).

DOMESTICATION: PROCESSES ANDDEFINITIONS

Robert Wayne and his associates at UCLAhave performed a molecular genetic analysisof the evolution of dogs and wolves, suggest-

4 CHAPTER ONE

FIG. 1.1. A Natufian burial site at Ein Mallaha innorthern Israel shows a human skeleton in what ap-pears to be an “eternal embrace” with the skeletal re-mains of a puppy located in the upper right-handcorner. From Davis and Valla (1978), reprinted withpermission.

ing that efforts to domesticate dogs may havetaken place much earlier than indicated bythe archeological record, putting the dog’sorigins back 100,000 years or more (Vila etal., 1997). The researchers argue that thesemore ancient efforts to domesticate dogs mayhave occurred without producing significantmorphological change in the protodog, thusexplaining the absence of dog skeletal arti-facts appearing before 14,000 years ago:

To explain the discrepancy in dates, we hy-pothesize that early domestic dogs may nothave been morphologically distinct from theirwild relatives. Conceivably, the change around10,000 to 15,000 years ago from nomadichunter-gather societies to more sedentary agri-cultural population centers may have imposednew selective regimes on dogs that resulted inmarked phenotypic divergence from wildwolves. (1997:1689)

Although no physical evidence of domesticdogs living with humans before 15,000 yearsago exists, skeletal remains of wolves havebeen found in association with hominid en-campments in China (the Zhoukoudian site)from 200,000 to 500,000 years ago (Olsen,1985).

Although contested in the past, the bio-logical ancestry of the dog is now certain. Onthe basis of both genetic and behavioral stud-ies the dog is a domestic wolf. However, con-siderable debate still surrounds the identity ofthe closest relative among wolf subspecies.Zeuner (1963) has argued that the mostlikely lupine progenitor is Canis lupus pallipes(the Indian wolf ), a small Eastern variety. Hebases this assumption on both behavioral andmorphological considerations. The smallerIndian wolf would have been less of a threatto human encampments and would havebeen more readily tolerated than the largerand more aggressive northern varieties.

Olsen and Olsen (1977) have selected theChinese wolf (Canis lupus chanco) as the mostlikely canid progenitor. They base theirchoice on this wolf ’s small size and mandiblemorphology, noting that the apex of thecoronoid process (the uppermost part of thejaw) turns back in both the Chinese wolf andthe domestic dog but not in the jaw bone ofother wolf species (Fig. 1.2). Clutton-Brock

(1984) has identified Canis lupus arabs (awestern Asiatic wolf ) and the European wolfas the most likely ancestors of most modernEuropean breeds, with Canis lupus lupus hav-ing a greater representation in the genome ofArctic and European spitz-type breeds. It is conceivable that the proliferation of domestic dogs has been genetically in-fluenced by several wolf subspecies at differ-ent times and places, or owes its genetic pastto a wolf species that is no longer existent(Fig. 1.3).

Interspecific Cooperation: Mutualism

By the end of the last glacial period, early hu-mans’ migratory activities overlapped thehunting range of competing predators, espe-cially wolves. As nomadic people came intocontact with wolves, some members of the

Origins and Domestication 5

FIG. 1.2. Note how the apex of the coronoid process(see arrow) tends to turn back. This feature is notapparent in other subspecies of wolves, coyotes, orjackals. It is a common anatomical feature found indogs, however, suggesting that the Chinese wolf mayhave played an important role in the ancient domesti-cation of the dog. From Olsen and Olsen (1977),The Chinese wolf, ancestor of New World dogs, Sci-ence 197: 533–535, reprinted with permission.

Chinese Wolf(Canis lupus chanco)

North American Wolf(Canis lupus lycaon)

wolf population may have been confidentenough to follow closely behind these mi-grant hunting and gathering groups. By stay-ing nearby, the ever-opportunistic wolvescould have easily tracked animals woundedby hunters, thus securing an easy meal forthemselves at least until the advancing hunt-ing party arrived at the scene. Also, by re-treating and lingering at a safe distance,wolves could scavenge on the slaughtered re-mains left behind (Zeuner, 1963). JulietClutton-Brock (1984, 1996) has speculatedthat such a hunting partnership may haveplayed an important role in the developmentand spread of the bow and arrow as a hunt-ing tool during the Mesolithic period, argu-ing that wolves or protodogs may have pro-vided a significant advantage to early huntersby tracking and subduing large animalswounded by arrows fitted with sharp stoneheads called microliths. Besides forming aneffective hunting partnership, wolf-pack terri-tories may have formed around humancamps, thus providing a natural protectiveshield against the threat of predation by other

less friendly wolves and competing humangroups. Possibly, from this mutually benefi-cial situation, an ecological niche was formedfrom which the protodog underwent novelmorphological and genetic changes graduallyleading to domestic dogs.

Close social contact of this kind requiresthat the animal in question possess a highfear threshold and a reduced tendency to flee,essential behavioral characteristics of domesti-cation (Hediger, 1955/1968). Scientific evi-dence for a genetically divergent distributionof temperament traits based on relative tame-ness and confidence among canids has beendemonstrated in the fox (Belyaev, 1979).Among farm-bred foxes, a small percentageexhibit a reduced tendency to act fearfully oraggressively in the presence of people. Bybreeding these less fearful individuals to-gether over several generations, Belyaev hasdeveloped a strain of tame, human-friendlyfoxes (see below). Although a similar geneticbasis for social tolerance has not beendemonstrated in wolves, it is reasonable to as-sume that a certain percentage of the Pleis-

6 CHAPTER ONE

C A N I S L U P I S

EuropeanWolf

IndianWolf

North AmericanWolf

ChineseWolf

Mastiffs

Scent Hounds

Sight Hounds

Feral Dogs

Herding DogsTerriersEuropean Toy

Dogs

Great DaneSt. BernardNewfoundlandBulldogPug

Gun DogsSpaniels

BorzoiSalukiAfghanDeerHounds

DingoPariah

Dogs

Spitz DogsNative American

Dogs

Oriental SpanielsOriental Toy DogsChow

FIG. 1.3. Various subspecies of the wolf are believed to have contributed to the genome of the domestic dog.According to one theory, the dog was independently domesticated in various parts of the world, with no singlesite of origin. Although grouped as though from discrete origins, the breeds included here have probably un-dergone considerable crossbreeding over their long history of development. After Clutton-Brock and Jewell(1993).

tocene wolf population was probably lessfearful and aggressive toward humans thanaverage wolves. The adaptive value of behav-ioral polymorphism in wolves and its rele-vance to domestication have been discussedin detail by Fox (1971) and by Scott, the lat-ter writing,

As a dominant predator the wolf is protectedfrom certain kinds of selection pressure, thuspermitting the survival of individuals with aconsiderable variation from the mean. As ahighly social species, wolves should be subjectto selection favoring variation useful in cooper-ative enterprises, as a greater degree of variationpermits a greater degree of division of labor.For example, a wolf pack might benefit bothby the presence of individuals that were highlytimid and reacted to danger quickly and effec-tively, and also by the presence of other morestolid individuals who did not run away butstayed to investigate the perhaps nonexistentdanger. (1967:257)

Similarly, Young and Goldman reported that“wolves held in captivity have shown that ineach litter there are two or three whelps thatshow tameness early; the remainder are ab-solutely intractable and often die if one at-tempts to train them” (1944/1964:208–209).This prosocial population would have dis-played a greater tolerance for human contactor may have even been “preadapted” for do-mestication—especially if they were not be-ing actively hunted or persecuted.

Mutual tolerance offered many benefitsfor both species. Early people who toleratedscavenging and the proximate presence ofdogs enjoyed a hygienic benefit (resulting inthe control of garbage and pestilence) and aprotected perimeter of barking dogs, provid-ing valuable early warning of approaching en-emies. After a propitious length of time, per-haps hundreds or thousands of years, suchloose symbiotic contact may have resulted inthe development of a specialized ecologicalniche in which the most tame individualwolves began to breed in close associationwith people. This transitional step wouldhave taken place gradually, requiring little orno purposeful intervention on the part ofearly humans. Such a pattern of scavengingaround human encampments by feral and

semiferal dogs is evident in many parts of theworld today (Fiennes and Fiennes, 1968).Even in large American cities, semiferal dogssatisfy the majority of their nutritional needsby scavenging (Fox, 1971; Beck, 1973). AlanBeck (1973) has observed that stray dogs sat-isfy most of their nutritional needs by raidinggarbage cans and relying on handouts whengarbage is not available. Handouts may havebeen an important source of food for earlydogs as well. Domestic dogs exhibit a uniqueproclivity and skill for food begging—a be-havioral attribute that would have been veryuseful for underfed primitive canines depend-ing on human generosity for their survival.As the result of a growing familiarity betweengenetically “tame” scavengers and beggingdogs, early people had many opportunitiesfor close interaction, thereby making othersocial exchanges possible, including the adop-tion of pups.

John P. Scott (1968) has imagined that aprimitive mother, having lost her own childand enduring the discomfort of lactation,may have saved a wolf puppy from the campsoup pot by adopting and nursing it as herown. If, in addition, the wolf happened to bea female, it might have chosen the camp as asuitable place to give birth, resulting in a newgeneration of even closer interaction and so-cial affiliation. Although such a scenario can-not be proven, it is statistically possible, evenplausible. Many examples of the suckling ofdomestic animals by women have been foundamong existing tribal cultures (e.g., thePapuan of New Guinea).

Although primitive humans’ intentionsand purposes for keeping dogs in close prox-imity are not known, a certain degree of so-cial tolerance and mutual acceptance wasclearly present in both species. In addition tovarious utilitarian or symbiotic benefits, earlyinteraction between humans and dogs surelydepended on a high degree of respectful def-erence shown by early canids toward humans.Dogs exhibiting threatening tendencieswould have been quickly expelled or killed,and eliminated from the gene pool early inthe domestication process. Those animals ex-hibiting submission behaviors and social sub-ordination—that is, a readiness to respond tohuman directives—would have been more

Origins and Domestication 7

likely to survive and to reproduce under theprotection of domestic conditions. Early do-mestic dogs that also exhibited a high degreeof affection toward their captors would havebeen brought into even closer intimacy, en-joying added protection, better food, andother survival advantages not extended to lessaffectionate counterparts. As time went on,various specialized functions could have beenelaborated out of this basic foundation, in-cluding all the familiar roles served by thedog today—for example, alarm barking andprotection, hunting activities, herding, draftwork, and companionship. Undoubtedly, atsome point in the natural history of humansand dogs, interspecies tolerance and coopera-tive interaction became mutually advanta-geous, thus forging the foundation for a last-ing relationship.

Terms and Definitions: Wild, Domestic, and Feral

Reports following a recent fatal wolf-dog at-tack exemplify some of the confused ways inwhich terms like domestic, wild, and tameare used. The victim, a 39-year-old mother oftwo, was mauled and killed as her childrenlooked on near their Colorado home. Severalauthorities were asked to comment on theunusual attack. It was the first documentedcase in which a wolf hybrid had killed anadult person. A police detective investigatingthe incident said, “They [wolf hybrids] maybe domesticated, but they’re still wild animalssubject to unpredictable behavior.” Anotherauthority, speaking for a local Humane Soci-ety, commented, “Animals like that are nottame. You can pet them but they are wild.”The words tamed and domesticated are usedhere interchangeably, as though they meanabout the same thing, roughly synonyms forpet. But this habit of usage is misleading.Taming is a necessary prerequisite for domes-tication, but taming alone is not sufficient.Many wild animals can be readily “tamed” bypatient handling and socialization, but theycannot be classified as domestic animals untilthey have also undergone extensive behavioraland biological change resulting from selectivebreeding over the course of many genera-tions. Such breeding is designed (consciously

or unconsciously) to enhance various behav-ioral and physical characteristics conducive todomestic harmony and utility.

The words wild and feral are also fre-quently used interchangeably in popular dis-cussions. The feral dog is not simply wild,but is a previously domesticated animal thathas been released or has escaped back intonature to reproduce and fend for itself. As isdiscussed below, dingoes exemplify manycharacteristic features of feral dogs, havingevolved from early Asiatic dogs that escapeddomestic captivity on reaching Australia sev-eral millennia ago. Since that time, dingoeshave reverted to a feral existence with onlytemporary symbiotic affiliations with hu-mans. Dingoes have existed under such con-ditions of quasi domestication for many gen-erations without actually returning to a truedomestic state.

The Dingo: A Prototypical Dog

An excellent source of ethnographic evidenceoutlining the general course of early domesti-cation can be found in the enduring relation-ship between the Aborigines of Australia anddingoes. This symbiotic dyad provides a valu-able anthropological picture of what life be-tween primitive humans and early canidsmay have been like during the earliest incipi-ent stages of domestication. In most details,dingoes differ only slightly from Asian wolves(Canis lupus pallipes), except for modest be-havioral and morphological changes associ-ated with quasi domestication—for example,variable tail carriage (sometimes carried inthe sickle-like form of dogs), some evidenceof piebald marking (especially on the feet andchest), and occasionally lop-eared examplesare observed but are probably the result ofEuropean hybridization. Like wolves, dingoesdo very poorly as domestic animals—even af-ter they have been crossed with domesticdogs (Trumler, 1973). The pelage of dingoescomes in a wide variety of colors, includingblack, white, black and tan, brindle, and gin-ger tan—the most common color observed(Corbett, 1995).

Meggitt (1965) has reviewed the relevantrecorded literature regarding dingoes andtheir varied role in aboriginal culture. He has

8 CHAPTER ONE

expressed skepticism regarding the usefulnessof dingoes in hunting. Some evidence sug-gests, however, that a cooperative hunting re-lationship may have existed at various timesand in ecologically specialized niches liketropical rain forests. Aboriginal hunters havebeen known to track free-ranging dingoes onthe trail of prey and taking it as their ownonce the quarry was caught, leaving the din-goes with scraps and offal for their efforts.Corbett (1995) reports that the Garawa tribeof northern Australia uses dingoes to trackand worry wounded prey, allowing thehunters to catch up and dispatch the weak-ened and distracted animal. However, inother localities like the desert, camp dingoesare driven back at the outset of a hunting ex-pedition because they are considered a hin-drance rather than an aid to a hunter’sprospects of finding game (Gould, 1970).Nomadic Aborigines hunt by concealmentand stealth, making dingoes of limited valueto such efforts. As an independent predator,dingoes sometimes hunt cooperatively insmall pack units, especially when huntinglarge prey (e.g., kangaroos). However, theyare seldom observed to congregate in suchpacking groups. Of 1000 dingoes sighted byCorbett and Newsome (1975), 73% weresolitary hunters, 16.2% were in pairs, andonly 5.1% were observed in trios.

Aborigines routinely collect puppies dur-ing the winter months from remote denningsites and rear the captured progeny to pu-berty. Upon reaching sexual maturity, thecaptive dingoes usually escape into the bushto reproduce and never return. This patternof adoption and escape prevents the develop-ment of a true domesticated dingo, since itsbreeding is not actively controlled and di-rected by human design. It should be noted,however, that deformed or otherwise unsuit-able puppies are culled and eaten, thus pro-viding some degree of active selection. Fur-ther, it is likely that those dingoes notperforming well under domestic conditionsare either expelled or killed. Although Abo-rigines find dingo meat somewhat unpalat-able, they will eat it if hungry enough. Invarious parts of Southeast Asia and the PacificIslands, dogs are preferred over pigs and fowlas meat. Corbett (1995) speculates that the

first dingoes reached Australia as cargo—asource of fresh food—but, once havingreached shore, some may have fled into thebush to give birth and to fend for themselves.

Apparently, some puppies belonging toAboriginal women are purposely crippled bybreaking their front legs to prevent themfrom wandering off. A similarly pragmatic ra-tionale may inform the constant pampering(sometimes involving suckling) and attentionthat dingoes are given by their Aboriginalcaptors. Such caregiving interaction may es-tablish a strong psychological “leash” of aug-mented affectional bonding and heighteneddependency. In 1828, the explorer MajorLockyer noted the strong emotional attach-ment between the Aborigines and their dingopuppies. He had taken a liking for a blackpuppy in the possession of a native, offeringhim an ax in exchange for the dingo. Urgedby his companions to accept the offer, theAborigine nearly conceded to the trade“when he looked down at the dog and theanimal licked his face, which settled the busi-ness. He shook his head and determined tokeep him” (in Bueler, 1973:102). These senti-ments were later echoed by Lumholtz (1884,in Corbett, 1995), reporting that the Aborig-ines treated their dingo puppies with greaterattention and care than given to their chil-dren. He describes the character of this rela-tionship and interaction in highly affection-ate terms: “The dingo is an importantmember of the family; it sleeps in the hutsand gets plenty to eat, not only of meat butalso of fruit. Its master never strikes, butmerely threatens it. He caresses it like a child,eats the fleas off it, and then kisses it on thesnout” (1995:16). The treatment observed byLumholtz appears to represent an exceptionrather than a general rule. While treated withgreat fondness, the camp dingoes are oftenmaintained in poor health and fed the poor-est scraps or nothing at all—forced to fendfor themselves on what they can find. Meg-gitt (1965) points out that domestic dingoescan be distinguished from free-ranging coun-terparts by their starved appearance. AmongAborigines, dingoes are kept mainly as pets,as warm sleeping companions, as scavengersof garbage and excrement, and as watch-dogs.

Origins and Domestication 9

Richard Gould (1970), an anthropologist,made several interesting observations of theinteraction and bonding between Aboriginesand dingoes during a brief study involving aremote group who had limited or no previ-ous contact with Europeans. The group ofAborigines in question lived in a remote andbarren area of the Gibson Desert called Pu-lykara located in Western Australia. They ex-isted on the meager bounty of desert faunaand flora, mainly consisting of vegetablefood, although meat was preferred wheneveravailable. Among the 10 Aborigines formingthe group were 19 dingoes, 12 of which be-longed to a single woman, whom Gouldchristened the “Dog Lady.” Although thedingoes were frequently petted and fussedover, the people rarely fed them. He notedthat the dingoes were not only “the skinniestdogs I have ever seen, but they were alsocompulsive cringers and skulkers” (1970:65),surviving on what they could find around thecamp or by stealing. Paradoxically, the peopleexpressed great sensitivity for their dingoes’plight. One woman, upon receiving a pieceof candy from the researcher, covered herdingo’s eyes so that the dingo could notwatch her eating it.

The Dog Lady is particularly interestingbecause of the manner in which she pam-pered and cared for her dingo companions.While she rarely fed the animals, she tookgreat pains to make them comfortable. Dur-ing the day, they slept under “shade shelters”constructed out of branches and twigs thatshe would periodically adjust in order to keepthem maximally protected from the sun.While the desert days are hot, the nights arefreezing cold. The custom of the Aboriginesis to sleep around a small campfire, huddledamong dogs. The Dog Lady, as one mightguess, had most of the pack wrapped aroundher, suggesting that a large motivation forkeeping so many dogs was comfort againstthe cold desert nights. One night Gould at-tempted to take a photograph of the groupwhile they slept with their dogs. The flash ofthe camera startled the dingoes, causing themto run away into the night. The people wereleft shivering without their “doggy blankets.”It appears from Gould’s observations that themost important utilitarian function of the

camp dingoes for this particular group wasthat of a living blanket.

The Carolina Dog: An Indigenous Dog?

Research led by I. L. Brisbin at the SavannahRiver Ecology Laboratory is under way to de-termine whether a dingolike dog that hasbeen discovered living in the Savannah RiverReserve and other remote areas of South Car-olina is an indigenous dog with an ancientlineage or a more modern counterpart thathas become feral (Brisbin and Risch, 1997;Weidensaul, 1999). In either case, the Car-olina dog portends to reveal important infor-mation about the nature of domesticationand its reversal. Carolina dogs present a num-ber of behavioral and ecological adaptationsthat are not observed in other domestic dogs,suggesting a unique evolutionary course ofdevelopment. For example, females exhibit anunusual pattern of multiple estrous cycles(3/year) as young dogs, with longer periodsbetween estrous cycles occurring as they growolder. Brisbin and Risch speculate that thispattern of reproduction is particularly adap-tive under conditions where a high risk ofearly death exists. A young Carolina dogquickly produces one or more litters as soonas possible after reaching sexual maturity. Thethreat of diseases such as heart worm—amosquito-born condition that is rampant inthe South—may exert selection pressures thatfavor dogs who exhibit a more frequent pat-tern of estrous cycles. Another unusual fea-ture exhibited by female Carolina dogs istheir tendency to dig dens in which to whelptheir young. Domestic dogs typically do notdig dens before whelping their young. Whenin estrus or after giving birth, females also ex-hibit the rather unusual habit of buryingtheir feces by covering it with sand that ispushed about by their nose. Another unusualbehavioral oddity found in these dogs is theiravidity for digging “snout pits”—small holesdug in the shape of their muzzle. The func-tion of such behavior has not been deter-mined, but Brisbin speculates that the dogsmay be deriving some nutritional value fromeating the soil (geophagia). In addition, un-like most domestic dogs, Carolina dogs ex-hibit effective predatory behavior that enables

10 CHAPTER ONE

them to survive independently of humanprotection and care. A central hypothesis thatBrisbin is testing concerns the possibility thatthe Carolina dogs may be a vestige of primi-tive dogs that accompanied human migra-tions across the Bering land bridge. Whetherthe Carolina dogs possess a true dingolike ge-netic ancestry is a question that is being cur-rently evaluated through behavioral and mi-tochondrial DNA studies.

BIOLOGICAL AND BEHAVIORALEVIDENCE

Biological Evidence

Domestic dogs interbreed with three wildcanid species: coyotes, jackals, and wolves.Charles Darwin (1875/1988) discusses atlength in The Variation of Animals and PlantsUnder Domestication that the variability anddiversity of the dog could only be adequatelyexplained by postulating an admixture of sev-eral wild species represented in the caninegenome. Following in the tradition of Dar-win, Konrad Lorenz (1954) also argued thatdomestic dogs owe their genetic endowmentto a combination of canid bloodlines. He be-lieved that the dog was first domesticatedfrom the jackal (Canis aureus) and only latercrossed with the wolf. However, upon subse-quent reexamination of the behavioral evi-dence, Lorenz (1975) reassessed and re-formed his theory by substituting Canis lupuspallipes in place of the jackal. An importantfactor affecting his change of opinion was the

finding that jackals are much less sociableand exhibit a distinctive howling pattern notshared by dogs.

“The wolf, disarmed of ferocity, is nowpillowed in the lady’s lap.” This speculationwritten by Edward Jenner in 1798 has turnedout to be true. The genetic and behavioralevidence to date points uniformly to the wolfas the exclusive wild progenitor of the dog.Supporting this view is the fact that bothdogs and wolves share a very similar genotypeand readily interbreed. Testifying to the easewith which wolves and dogs interbreed is thegrowing population of wolf-dog hybrids. Ithas been roughly estimated that approxi-mately 300,000 wolf-dog hybrids are cur-rently kept as companion animals in theUnited States (Clifford and Green, 1991), al-though these numbers have been disputedand remain controversial.

Robert Wayne (1993) has confirmed theclose genetic relationship between dogs andwolves by comparing the mitochondrialDNA sequences of wild canids and dogs. Ac-cording to this line of research, dogs are do-mesticated wolves with only slight genetic al-terations affecting developmental timing andgrowth rates: “Dogs are gray wolves, despitetheir diversity in size and proportion; thewide variation in their adult morphologyprobably results from simple changes in de-velopmental rate and timing” (1993:220).Both wolves and dogs possess 78 chromo-somes (Table 1.1). Comparisons of canidDNA sequences reveal that dogs are moreclosely related to wolves than to coyotes. Al-

Origins and Domestication 11

TABLE 1.1. The diploid chromosome numbers for canids showing a close relationship between the dog,wolf, coyote, jackal, and other canids

Species Common name Range Chromosomes

Canis aureus Golden jackal Old World 78Canis lupus Gray wolf Holarctic 78Canis iatrans Coyote North America 78Cuon alpinus Dhole Asia 78Lycaon pictus African wild dog Sub-Sahara Africa 78Speothos venaticus Bush dog South America 74Chrysocyon brachyurus Maned wolf South America 76Vulpes vulpes Red fox Old and New World 36Alopex lagopus Arctic fox Holarctic 50

Source: After Wayne (1993:219).