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- Herausgeber: John Wiley & Sons
- Kategorie: Wissenschaft und neue Technologien
- Sprache: Englisch
The Behavior of Animals
An updated view of animal behavior studies, featuring global experts
The Behavior of Animals, Second Edition provides a broad overview of the current state of animal behavior studies with contributions from international experts. This edition includes new chapters on hormones and behavior, individuality, and human evolution. All chapters have been thoroughly revised and updated, and are supported by color illustrations, informative callouts, and accessible presentation of technical information.
- Provides an introduction to the study of animal behavior
- Looks at an extensive scope of topics- from perception, motivation and emotion, biological rhythms, and animal learning to animal cognition, communication, mate choice, and individuality.
- Explores the evolution of animal behavior including a critical evaluation of the assumption that human beings can be studied as if they were any other animal species.
- Students will benefit from an updated textbook in which a variety of contributors provide their expertise and global perspective in specialized areas
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the behavior of animals
MECHANISMS, FUNCTION, AND EVOLUTION
SECOND EDITION
EDITED BY JOHAN J. BOLHUIS, LUC-ALAIN GIRALDEAU AND JERRY A. HOGAN
This edition first published 2022
©2022 John Wiley & Sons, Inc.
Edition History
John Wiley & Sons, Inc. (1e, 2004)
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Contents
Cover
Title page
Copyright
List of Contributors
Foreword
by Robert A. Hinde
Preface
1.
The Study of Animal Behavior
2.
Stimulus Perception
3.
Motivation and Emotion
4.
Biological Rhythms and Behavior
5.
Brain and Behavior
6.
Hormones and Behavior
7.
Development of Behavior
8.
Learning and Memory
9.
Animal Cognition
10.
Applied Animal Behavior and Animal Welfare
11.
The Function of Behavior
12.
Mate Choice, Mating Systems, and Sexual Selection
13.
Animal Personality, the Study of Individual Behavioral Differences
14.
Animal Communication
15.
Evolution of Behavior
16.
The Evolution of Hominin Behavior
17.
Evolutionary Approaches to Human Behavior
Name Index
Subject Index
End User License Agreement
List of Illustrations
Chapter 2
Figure 2.1 (A) The “reflection experiment.”...
Figure 2.2 Looking into a “black-box”:...
Figure 2.3 Configurational features in sign-stimuli....
Figure 2.4 The prey (a, c) vs. threat (b, d) configuration...
Figure 2.5 (a) Common toad displaying anti-predator behavior...
Figure 2.6 Male silk moth in alerted position, with combed...
Figure 2.7 Principles of scent detection in moths by...
Figure 2.8 Prey-feature analysis in common toads....
Figure 2.9 Neuroimaging toad’s visual system...
Figure 2.10 “Window hypothesis” of...
Figure 2.11 Visual processing streams in the...
Chapter 3
Figure 3.1 Conception of behavior systems. Stimuli from the...
Figure 3.2 Lorenz’ model of motivation. The tap (T)...
Figure 3.3 Results of an experiment on guppy courtship.,...
Figure 3.4 Courtship and mating behavior of the...
Figure 3.5 Genetically featherless chicks...
Figure 3.6 Upright postures of the herring gull:...
Figure 3.7 “Waltzing” in a male...
Figure 3.8 Facial expressions of fear and aggression...
Chapter 4
Figure 4.1 Rest-activity records from...
Figure 4.2 (A) Daily rhythm of core body...
Figure 4.3 Plasticity of rest–activity...
Figure 4.4 A phase-response curve (PRC)...
Figure 4.5 The rat brain and some areas...
Figure 4.6 The molecular basis of...
Chapter 5
Figure 5.1 The facial ruff of the barn owl...
Figure 5.2 Acoustic measurements taken from microphones...
Figure 5.3 (a) Auditory neurons and neurons in the...
Figure 5.4 Electron micrograph of the head...
Figure 5.5 (a) The brain of the honeybee...
Figure 5.6 (a) Schematic sagittal view of the...
Figure 5.7 Juvenile zebra finch males were injected at...
Chapter 6
Figure 6.1 Simplified metabolic pathway...
Figure 6.2 Schematic view of the endocrine...
Figure 6.3 Schematic model illustrating how a...
Figure 6.4 Reciprocal interactions between...
Figure 6.5 Schematic representation of the...
Chapter 7
Figure 7.1 “Epigenetic landscape”...
Figure 7.2 Schematic illustration of two...
Figure 7.3 Zebra finch (left) and...
Figure 7.4 Stages in song development in...
Figure 7.5 Three ways in which experience,...
Figure 7.6 Mean preference scores...
Figure 7.7 Schematic drawings of the...
Chapter 8
Figure 8.1 (a) Associative connections in...
Figure 8.2 (a) A typical color-based...
Figure 8.3 A serial position curve...
Figure 8.4 An experiment on chunking in...
Figure 8.5 A schematic of the experiment...
Figure 8.6 The effect of electroconvulsive...
Chapter 9
Figure 9.1 (a)
Ammophiia sabulosa
,...
Figure 9.2 Greylag goose retrieving an egg. (a)...
Figure 9.3 Supernormal stimulus. Herring gull...
Figure 9.4 (a) Computational framework for the...
Figure 9.5 The lifetime of an engram. The formation...
Figure 9.6 Observational learning in doves...
Figure 9.7 Bumblebee using a string to...
Figure 9.8 Young capuchin monkey using a stick to...
Figure 9.9 (a) Female
Portia fimbriata
...
Figure 9.10 Neural encoding of regret in...
Chapter 10
Figure 10.1 A dog in the Australian...
Figure 10.2 A moose (
Alces alces
)...
Figure 10.3 A serval (
Felis serval
)...
Figure 10.4 The price that caged American mink...
Figure 10.5 Calf demand for two types of...
Figure 10.6 Facial expressions of a newborn...
Figure 10.7 Cognitive bias in dairy calves...
Chapter 11
Figure 11.1 The power expressed as multiples...
Figure 11.2 The results of Krebs et...
Figure 11.3 Results of Giraldeau and Kramer...
Figure 11.4 Red knots (
Calidris canutus
)...
Figure 11.5 The payoff functions of the...
Figure 11.6 The value of two habitats...
Figure 11.7 The university ducks experiment...
Chapter 12
Figure 12.1 Mating system described as a...
Figure 12.2 Polygyny threshold model with...
Figure 12.3 Male mating success in...
Figure 12.4 Egg survival (%) in relation to...
Figure 12.5 Survival rate of male barn...
Figure 12.6 Sex ratio of zebra...
Chapter 13
Figure 13.1 Representation of personality...
Figure 13.2 Illustration of the distribution...
Figure 13.3 The broccoli model of...
Figure 13.4 A) Fitness increases with...
Figure 13.5 The relative importance...
Chapter 14
Figure 14.1 Non-informational and...
Figure 14.2 A taxonomy in which signals...
Figure 14.3 Representative flight paths...
Figure 14.4 A graphical version of the handicap mechanism...
Figure 14.5 A graphical version of a differential benefits model...
Figure 14.6 Spectrograms of three...
Chapter 15
Figure 15.1 (
left
) Darwin predicted that...
Figure 15.2 In the hypothetical phylogeny...
Figure 15.3 Mean body hue of males and...
Figure 15.4 (
top
) The dose-dependent...
Figure 15.5
(left)
(a) Several ecological (beak depth...
Figure 15.6 (A) The relationship between two...
Figure 15.7
(top)
Weber’s Law predicts...
Chapter 16
Figure 16.1 Graphic representation of encephalization...
Figure 16.2 Reconstruction by the paleoartist Jay...
Figure 16.3 Side views of the toothrows of (from top to bottom):...
Figure 16.4 Highly approximate tentative genealogical...
Figure 16.5 Diorama at the American Museum of...
Figure 16.6 The “Nariokotome Boy“...
Figure 16.7 Two Acheulean implements from the type...
Figure 16.8 Three-quarter view of the most...
Figure 16.9 Reconstruction of the largest of the...
Figure 16.10 Comparison between a reconstructed...
Figure 16.11 The best preserved of the small...
Figure 16.12 Monochrome rendering of a...
Chapter 17
Figure 17.1 Charles Darwin (from Wikimedia Commons)...
Figure 17.2 Frontispiece of Thomas...
Figure 17.3 John B. Watson (from Wikimedia Commons)...
Figure 17.4 Field studies have shown that...
Figure 17.5 Sarah Hrdy (courtesy of Dan Hrdy)...
Figure 17.6 The human archaeological record...
Figure 17.7 A) In most mammals, the individuals...
Figure 17.8 In an experimental study, the...
Figure 17.9 Capuchin monkeys...
List of Tables
Chapter 2
Table 2.1 Invariance in Gestalt perception...
Table 2.2 From heterogeneous summation...
Table 2.3 Feature discrimination causes dishabituation.
Table 2.4 Command neuron hypothesis.
Table 2.5 Constants α and β...
Table 2.6 Minimum number of cell types...
Chapter 8
Table 8.1 Experimental designs in classical conditioning
Chapter 10
Table 10.1 Three Conceptions of Animal...
Chapter 11
Table 11.1 Payoffs to the row player...
Guide
Cover
Title page
Copyright
Table of Contents
List of Contributors
Foreword
Preface
Begin Reading
Name Index
Subject Index
End User License Agreement
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contributors
Professor Gregory F. Ball
Department of Psychology
University of Maryland
2141 Tydings Hall
7343 Preinkert Drive
College Park, MD 20742
USA
Professor Jacques Balthazart
University of Liege
GIGA Neurosciences
Quartier Hôpital
15 Avenue Hippocrate
Tour Pharmacie (Bat. B36, 1er étage)
B-4000 Liège
Belgium
Professor Johan J. Bolhuis
Cognitive Neurobiology
Department of Psychology
Utrecht University
PO Box 80.086
Yalelaan 2
3584 CM Utrecht
The Netherlands
Professor Gillian R. Brown
School of Psychology & Neuroscience
University of St. Andrews
South Street
St. Andrews, Fife, KY16 9JP
United Kingdom
Dr Harald Burghagen†
Universität Kassel
Fachbereich Naturwissenschaften
Abteilung Zoologie/Physiologie, Neurobiologie
Heinrich-Plett-Str. 40
D-34132 Kassel
Germany
Dr Catharine P. Cross
School of Psychology & Neuroscience
University of St. Andrews
South Street
St. Andrews, Fife, KY16 9JP
United Kingdom
Professor Dr Jörg-Peter Ewert
Universität Kassel
Fachbereich Naturwissenschaften
Abteilung Zoologie/Physiologie, Neurobiologie
Heinrich-Plett-Str. 40
D-34132 Kassel
Germany
Professor David Fraser
Animal Welfare Program
Faculty of Land and Food Systems
University of British Columbia
2357 Main Mall
Vancouver, British Columbia
Canada V6T 1Z4
Professor Luc-Alain Giraldeau
Institut national de la recherche scientifique
490, rue de la Couronne
Québec QC
Canada G1K 9A9
Professor Geoffrey Hall
Department of Psychology
University of York
York YO10 5DD
United Kingdom
Professor Robert A. Hinde, FRS†
St. John’s College
Cambridge CB2 1TP
United Kingdom
Professor Jerry A. Hogan
Department of Psychology
University of Toronto
Toronto, Ontario
Canada M5S 3G3
Professor Kimberly Kirkpatrick
Director, Cognitive and Neurobiological Approaches to Plasticity Center
Department of Psychological Sciences
Kansas State University
496 Bluemont Hall
Manhattan, KS 66506
USA
Professor Kevin N. Laland
Centre for Biological Diversity
School of Biology
University of St. Andrews
Sir Harold Mitchell Building
St. Andrews
Fife KY16 9TF
United Kingdom
Professor Ralph E. Mistlberger
Department of Psychology
Simon Fraser University
8888 University Drive
Burnaby, British Columbia
Canada V5A 1S6
Dr Anders Pape Møller
Directeur de Recherche
Ecologie Systématique Evolution
Université Paris-Saclay
CNRS, AgroParisTech
F-91405 Orsay Cedex
France
Professor Pierre-Olivier Montiglio
Groupe de Recherche en Ecologie Comportementale et Animale
Département des Sciences Biologiques
Université du Québec à Montréal
CP 8888, succursale centre-ville
Montréal, Québec,
Canada H3C 3P8
Professor Stephen Nowicki
Department of Biology
Duke University
130 Science Drive
Durham, NC 27708
USA
Professor Denis Réale
Groupe de Recherche en Ecologie Comportementale et Animale
Département des Sciences Biologiques
Université du Québec à Montréal
CP 8888, succursale centre-ville
Montréal, Québec,
Canada H3C 3P8
Professor Benjamin Rusak
Departments of Psychiatry and Psychology & Neuroscience
Dalhousie University
5909 Veterans Memorial Lane
Halifax, Nova Scotia
Canada B3H 2E2
Professor Michael J. Ryan
Department of Integrative Biology
University of Texas
Austin, TX 78712
USA
Professor William A. Searcy
Department of Biology
University of Miami
Coral Gables, FL 33124
USA
Professor David F. Sherry
Advanced Facility for Avian Research
Departments of Psychology and Biology
Western University
1393 Western Road
London, ON
Canada N6G 1G9
Professor Ian Tattersall
Division of Anthropology
American Museum of Natural History
New York, NY 10024
USA
Professor Daniel M. Weary
Animal Welfare Program
Faculty of Land and Food Systems
University of British Columbia
2357 Main Mall
Vancouver, British Columbia, Canada V6T 1Z4
foreword
ROBERT A. HINDE
Writing a foreword for such a stimulating series of chapters, which represent the state of animal behavior studies at this time, is a considerable responsibility. Perhaps I can do best by looking not forward, as might seem appropriate, but backward, and thus attempt to provide a context for the chapters that follow. Of course it cannot be a fully objective backward view, because I am looking from where I am now, and what I see is biased by my own experience. It is bound also to involve simplification. But I hope that it will provide a useful perspective.
In the early decades of the twentieth century, most studies of animal behavior fell into two groups. In one were the naturalists, mostly amateurs, without scientific pretensions but with a long tradition stretching back beyond the nineteenth century. In the other were the psychologists, producing an increasing body of data and theory mostly concerned with learning processes. Of course this dichotomy is already unjust and simplistic. Darwin himself could be called a naturalist; and an originator of learning theory (J.B. Watson) started from naturalistic observation. However, the work of the learning theorists, impressive in its own right, was not to have much impact on the traditions that led to the chapters in this book until much later.
Those traditions can be said to stem from the emergence of ethology in the 1930s. This was due to Lorenz, an Austrian MD with a PhD in comparative anatomy, and Tinbergen, a Dutch zoologist who moved to England a few years after the end of World War 2. Both men had a passionate interest in animals, but this was expressed in very different ways. Lorenz kept a menagerie of diverse animals in his home, though also studying the local jackdaws and the semi-tame geese that he reared. Tinbergen, by contrast, was a dedicated field naturalist. Although he later worked with captive animals, it was always with problems that he had brought in from the field, and he liked best to be in the field himself. Tinbergen’s first pupil, Baerends, suggested that the contrast lay in their attitudes to their subjects: Tinbergen saw himself as a nonparticipant hidden observer of animals, Lorenz as an adopted alien member and protector. Lorenz was a thinker who tried to relate or contrast his observations with current biological and philosophical views, while Tinbergen was much more empirical, an experimenter as well as an observer.
But both rejected the vitalist view that the phenomena of “instinct” were unanalysable and the misuse of the Gestalt concept to imply that analysis is unnecessary because the whole is always more than the sum of its parts. They also rejected the focus of most learning theorists on the input/output relations of the whole organism, with neglect of the “physiological machinery,” and the sterility of the artificial environments used to study animals in many psychological laboratories.
The term “ethology” has been applied primarily to the work of students who, though differing widely in the problems they tackled, the methods they used, the level of analysis at which they worked, and the theoretical interpretations (if any) that they adopted, shared certain orienting attitudes. They insisted that the proper description of behavior is a necessary preliminary to its analysis; and that the behavior of an animal must be studied in relation to the environment to which it has become adapted in evolution. In addition they held that full understanding of behavior required knowledge not only of its development and causation but also of its biological function and its evolution. The result was a vast amount of data on the behavior of animals and a certain amount of model-building to elucidate the mechanisms underlying behavior. In 1973 Lorenz and Tinbergen (together with von Frisch) were awarded the Nobel Prize in Physiology and Medicine.
Although ethology was primarily a European phenomenon in the early postwar years, two research workers in the USA were to have a considerable influence on its development, though in very different ways. Beach, a behavioral endocrinologist interested primarily in the hormonal control of sexual behavior, met Tinbergen in the USA and became a powerful supporter of ethology. Schneirla, a comparative psychologist working at the American Museum of Natural History, was intensely critical. One of his students, Lehrman, published a hard-hitting critique of ethology in 1953. There were three main issues. Lehrman and Schneirla took exception to Lorenz’s distinction between “innate” and “acquired” behavior as neither empirically valid nor heuristically valuable. They objected to the energy model of motivation that Lorenz used, though this also came in for criticism from within ethology. And both were unhappy about the ethologists’ tendency to apply concepts across a wide range of species differing in their levels of cognitive capacity. On their side, the ethologists felt that the adjective in “comparative psychology” was a sham, for contrasting distantly related species did not constitute comparison in a biological sense. They were also unhappy about the manner in which many comparative psychologists (though not so much those influenced by Schneirla) generalized on the basis of studies of a few mammalian species, predominantly the laboratory rat. For a while the differences between the two groups seemed irreconcilable. However, soon after his critique was published, Lehrman came to Europe and met a number of European ethologists. Tinbergen, Lorenz, and Lehrman were all bird watchers, with a passionate enthusiasm for natural history. Lehrman had an infectious geniality, and friendships were soon made. This brought about a rapprochement between ethology and many of the members of Schneirla’s group, a rapprochement that came not so much from academic discussion, but from the compatibility of personalities. On the issue of ontogeny, both sides changed their emphasis, the comparative psychologists withdrawing from their extreme emphasis on experience, and the differences in approach to the “comparative” issue were recognized.
It seems to happen not infrequently in the history of science that those regarded as originating a branch of science are subsequently seen to have been wrong in many of their generalizations. For instance, Freud (psychoanalysis) used a misleading model of motivation, Piaget (developmental psychology) based generalizations on a tiny sample of subjects, and Jeffreys (geophysics) refused to accept the evidence for continental drift. This was also the case with ethology. Many of the concepts that had been invaluable tools in the early days of ethology—the “innate releasing mechanism” and “fixed action pattern” for instance—were subsequently seen to involve oversimplification, and now seldom figure in the literature. But not surprisingly the change in outlook was not adopted simultaneously by all ethologists, and this led to some divisions within ethology. Lorenz, whose influence was particularly strong in Germany and the USA (through two research workers who had worked with him, Hess and Barlow), was slower to relinquish the innate/acquired dichotomy and energy model of motivation than Tinbergen and workers in the Netherlands and the UK.
An issue important for the nature/nurture debate became prominent in the 1960s. Both Tinbergen and Lorenz had long argued on the basis of empirical evidence that species were specially equipped for particular learning tasks that were biologically important for them. Thorpe’s book on birdsong, published in 1961, showed that the chaffinch was predisposed to learn the species-characteristic song pattern. A few years later, Rozin, Garcia, and others demonstrated a predisposition to avoid toxins in mammals. Such findings were directly contrary to the orientation of the learning theorists, who were searching for laws of learning valid for all species and all situations. It thus became apparent that, in many cases, what was “innate” was a predisposition to learn some things in particular contexts. This was to be of special importance for the study of human behavior.
Lorenz, originally a comparative anatomist, had used species differences and similarities as a taxonomic tool, and Tinbergen had always had an interest in the function of behavior. But, of the four problems of causation, development, function, and evolution, the main (though by no means the only) emphasis in ethology had been on the first two. In the 1970s this changed with the publication of Wilson’s Sociobiology. The orienting attitudes of ethology continued but the motivational models disappeared and many of the old concepts fell into disuse. Behavioral ecology came to the fore, and new theoretical approaches made possible the study of function in a quantitative fashion. Data on foraging behavior were compared with the behavior to be expected (on certain assumptions that were not always made fully explicit) from an organism foraging with maximal efficiency. Later, attention turned to such issues as sperm competition and the role of fluctuating asymmetry. Hamilton’s work on kin selection, first published in 1964 but neglected for much of the next decade, made possible a new approach to social behavior. Game theory was recruited, and mathematical modeling came to be a much used tool in studies of behavior.
At the same time, the influence of ethology started to penetrate into a number of other disciplines. Lehrman and Rosenblatt, as well as Beach and his many students, adopted the orienting attitudes of ethology in their work on behavioral endocrinology. Von Holst had already studied the elicitation of fixed action patterns by brain stimulation through implanted electrodes, and the importance of using unconfined animals where possible was recognized by neurophysiologists. Bowlby, a psychoanalyst concerned with the effects of maternal deprivation in children, realized that what had been called the “irrational fears of childhood” (fear of falling, being alone, etc.) would have been highly adaptive in the environments in which early hominids lived, and an ethological element was incorporated in the “attachment theory” which he elaborated, an approach that was to become central in studies of child development. The study of human nonverbal communication profited from the input of ethologists, such as Eibl Eibesfeldt. The techniques of the behavioral ecologists were applied in studies of preindustrial human groups. An ethological influence is to be seen in studies of human personal relationships, and even in studies of religion and morality. Thus, while ethology as a set of concepts or as a theory of animal behavior has been largely superseded, the influence of its orienting attitudes has increased and is potent in other disciplines.
While behavioral ecology took center stage in the study of animal behavior, many felt it to be impoverished by the neglect of problems of development and causation. This book will go a long way toward setting the balance straight. Each of the four problems is covered, and the chapters introduce the growing points in the study of animal behavior at the start of the twenty-first century.
preface
The idea for this book arose out of a need that we (and many of our colleagues) felt for a comprehensive textbook on animal behavior. There is no shortage of animal behavior textbooks, so why did we want to produce a new one? First, animal behavior is a dynamic field of research, and we believe that a modern textbook should incorporate all the contemporary subdisciplines of behavioral biology, such as animal welfare, evolutionary psychology, animal cognition, and behavioral neuroscience. In some ways, the science of animal behavior has become a victim of its own success, as it covers a much wider field than it did initially. Gone are the days when one author could write a textbook both comprehensive and authoritative: Robert Hinde’s classic Animal Behaviour: A Synthesis of Ethology and Comparative Psychology (1970) is an outstanding example of such a book, and it continues to inspire many of us. Given the breadth of contemporary animal behavior research, we felt that it was important to invite experts in the respective subdisciplines to write a chapter about their specialist topic.
Second, a large proportion of extant textbooks are single-author volumes that approach animal behavior from a particular perspective, for example from an evolutionary point of view or with the emphasis on mechanisms. We believe that a modern science of animal behavior should encompass both functional and causal approaches. For such a comprehensive approach, we found the classic formulation of the aims and methods of ethology (the study of animal behavior) by Niko Tinbergen, one of its founding fathers, most useful. Tinbergen suggested that there are four basic questions in animal behavior, namely about causation, development, survival value (function), and evolution. We agree with Tinbergen that all these four questions are equally important. Hence all of them are represented in this book. Like Tinbergen, we also find it important to distinguish among the four questions. In particular, it is important to realize which of the four questions is addressed, and to use a research approach appropriate for that question. Most chapters in the book focus on one of the four questions, with cause and development being the main subjects of the first ten chapters, and survival value (function) and evolution being the main subjects of the last seven chapters. But most chapters are also concerned with more than one question, noted separately of course, supporting Tinbergen’s claim that all questions should be answered.
We are very pleased with the enthusiastic response we received from the authors invited to contribute to this book. They are all leaders in their respective fields, and we feel privileged that they participated in this project. Robert Hinde has passed away since his foreword was written, but his words are just as relevant to the second edition of this book as they were to the first. His influence remains.
1 the study of animal behavior
JOHAN J. BOLHUIS, LUC-ALAIN GIRALDEAU AND JERRY A. HOGAN
INTRODUCTION
The scientific study of animal behavior is often called ethology, a term used first by the nineteenth century French zoologist Isidore Geoffroy Saint Hilaire, but then used with its modern meaning by the American zoologist Wheeler (1902). Ethology is derived from the Greek ethos, meaning “character.” The word “ethics” is also derived from the same Greek word, which makes sense, because ethics is basically about how humans ought to behave. Unfortunately, the word “ethology” is also often confused with the word “ethnology” (the study of human peoples), with which it has nothing in common. In fact, the very word processor with which we are writing this chapter keeps prompting us to replace “ethology” by “ethnology”! For whatever the reason, the word “ethology” is not used as much as it used to be, although there is still an active animal behavior journal bearing this name. Instead of “ethology,” many authors now use the words “animal behavior” or “behavioral biology” when they refer to the scientific study of animal behavior.
A Brief History of Behavioral Biology
Early days
Scientists (and amateurs) have studied animal behavior long before the word “ethology” was introduced. For instance, Aristotle had many interesting observations concerning animal behavior. The study of animal behavior was taken up more systematically, however, mainly by German and British zoologists around the turn of the nineteenth century. The great British naturalist Charles Darwin (1809–1882), in his classic book on the theory of evolution by natural selection (1859), devoted a whole chapter to what he called “instinct.” As early as 1873, a British amateur investigator, Douglas Spalding, recorded some very interesting observations on the instinctive behavior of young domestic chicks, including a phenomenon that was later called “imprinting” (Chapter 7). At the beginning of the twentieth century, the behavior of animals was also studied in the context of learning by the Russian physiologist Ivan P. Pavlov (1927) and the American psychologist Edward L. Thorndike (1911; Chapter 8).
Lorenz and Tinbergen
In the middle of the twentieth century, the study of animal behavior became an independent scientific discipline, called ethology, mainly through the efforts of two biologists, the Austrian Konrad Lorenz (1903–1989) and the Dutchman Niko Tinbergen (1907–1988). It can be said that Lorenz was the more philosophical and theoretical of the two. He put forward a number of theoretical models on different aspects of animal behavior such as evolution and motivation. He was also the more outspoken of the two men, and some of his publications met with considerable controversy. Tinbergen was very much an experimentalist, who together with his students and collaborators conducted an extensive series of field and laboratory experiments on the behavior of animals of many different species. In 1973, Lorenz and Tinbergen were awarded the Nobel Prize for Physiology and Medicine. They shared their prize with Karl von Frisch (1886–1982), an Austrian comparative physiologist and ethologist who had pioneered research into the dance “language” of bees (Chapter 14).
Ethology and comparative psychology
During the early days of ethology there was a certain amount of scientific rivalry between mainly European ethologists and North American experimental psychologists, who also studied animal behavior in what was usually called comparative psychology. The European ethologists emphasized that animal behavior is a biological phenomenon, and as such a product of evolution. This is exemplified by the use of the word “instinct” (e.g., in the title of Tinbergen’s 1951 classic book The Study of Instinct), which referred to the “innate” components of behavior that are subject to natural selection. A prominent critique of this way of thinking came from the American psychologist Daniel Lehrman, in his 1953 paper “A critique of Konrad Lorenz’ theory of instinctive behavior.” In this paper he argued against Lorenz’ theory in which behavior can be dissected into “innate” and “acquired” (learned) components (see Chapter 7 for a more detailed discussion of these issues). In general, American psychologists emphasized the effects of learning on behavior. Pavlov had already demonstrated the importance of what we now call Pavlovian (or classical) conditioning, and Thorndike studied learning processes that are now known as instrumental conditioning (Chapter 8). Another difference between the ethologists and experimental psychologists was that the former often observed animals of many different species in their natural environment, while the latter, despite the name comparative psychology, often concentrated on one species, such as the rat or the pigeon, that was studied exclusively in the laboratory.
Behaviorism
The emphasis of the North American psychologists on learning was epitomized by the rise of behaviorism in the 1930s. Behaviorism was a very influential school of thought initiated by the American psychologist John B. Watson (1878–1958), with his book Behaviorism (1924). Essentially, Watson considered psychological phenomena to be physical activity rather than some kind of mental event. He proposed that we cannot make any scientific statements about what might be going on in our minds, and that introspection was unreliable. Rather, for behaviorists, psychology is the study of observable behavior and of the external physical factors that influence it. At the time, behaviorism was extremely influential in science and beyond. Within North American psychology it was the dominant school of thought for several decades. Behaviorist theory also affected education practice, particularly with Watson’s book Psychological Care of Infant and Child (1928). Watson once made the famous statement:
Give me a dozen healthy infants, well-formed, and my own specified world to bring them up in and I’ll guarantee to take any one at random and train him to become any type of specialist I might select—doctor, lawyer, artist, merchant-chief, and, yes, even beggarman and thief, regardless of his talents, penchants, tendencies, abilities, vocations, and race of his ancestors.
This epitomizes behaviorist ideas about child rearing. Watson considered the upbringing of children to be an objective, almost scientific exercise, without the need for affection or sentimentality.
Watson’s most famous student was Burrhus Frederic Skinner (1904–1990), who applied behaviorist ideas to the study of learning. For Skinner (1938) and his behaviorist colleagues, learning had to do with changing relationships between visible entities, not with what might be going on inside the animal’s head. In particular, behaviorist learning theorists suggest that learning refers to changes in the frequency of responding due to its consequences. Most of their experiments involve operant conditioning (see Chapter 8), in which a certain response by the animal (e.g., pressing a lever) is rewarded (“reinforced”) with food.
Cognitive psychology
Within experimental psychology there came a reaction to behaviorism in what we now call cognitive psychology. In contrast to behaviorism, cognitive psychologists start with the assumption that individuals (humans and other animals) have a mental life that can be investigated (Chapter 9). For instance, Skinner (1957) maintained that language development in children was a learning process, in which responses (i.e., uttering certain sounds) were reinforced. The American linguist Noam Chomsky (1959) wrote a highly critical review of Skinner’s book on language development, suggesting that language acquisition is not a case of instrumental conditioning, but a much more complex interaction between experience and internal cognitive mechanisms (Chapter 7). At birth the child is already endowed with essential knowledge of language, the theory of which is known as Universal Grammar. Clearly, learning is involved in the development of language, but it is not the only factor. Chomsky and colleagues have recently described the growth of language in the child as “the interplay of three factors: domain-specific principles of language (Universal Grammar), external experience, and properties of non-linguistic domains of cognition including general learning mechanisms and principles of efficient computation” (Yang et al. 2017). Another important publication that signaled the beginning of the cognitive revolution is a book by the British psychologist Donald Broadbent (1958) who, in contrast to Skinner, analyzed learning and memory in terms of cognitive mechanisms rather than stimulus–response relations. Hogan (1988, 2017) has noted that what cognitive psychologists call “cognitive structures” are in fact the same as the causal mechanisms that were proposed by ethologists such as Lorenz and Tinbergen (Chapters 3 and 9).
Four Questions in the Study of Animal Behavior
Niko Tinbergen published a very important paper in 1963, in which he outlined four major questions in the study of animal behavior, namely causation,development, survival value, and evolution. As he readily admitted, Tinbergen wasn’t original, because three of these questions (causation, survival value, and evolution) had already been put forward by the British biologist Julian Huxley (1887–1975) as the major questions in biology, but Tinbergen added a fourth question, development. Many authors, including ourselves, use the word function as a substitute word for survival value, but the term function is used in many different ways in biology (Wouters 2003), and care is necessary when using it. It should also be mentioned that the evolutionary biologist Ernst Mayr (1904–2005) in 1961 popularized a different categorization of problems in biology: proximate and ultimate causation. Proximate causation is similar to Tinbergen’s causal question, but ultimate causation is a controversial term that deals with evolutionary issues somewhat differently from Tinbergen’s questions of survival value and evolution. However, no matter how these questions are broken up, it is crucially important that students of animal behavior be quite clear about the type of question they are addressing when they study or speak of animal behavior.
We find Tinbergen’s analysis so important that we would say you cannot really understand animal behavior if you do not also understand the meaning of his four questions. Some of the more heated contemporary debates in the field of animal behavior can often be traced to misunderstandings about the meaning of these questions (e.g., Hogan 1994, 2017; Bolhuis & Macphail 2002). It is essential, therefore, that any productive discussion about animal behavior involves participants that are capable of clearly stating which of the four questions they are addressing. This view of animal behavior has also served as the framework for the organization of the present book, with the first half covering mostly causal and developmental topics while the second half deals with questions of survival value (or function) and evolution.
Tinbergen’s four questions are sometimes also called the four whys, because they represent four ways of asking “why does this animal behave in this way?” Let’s consider a bird singing at dawn, say a male song sparrow (Melospiza melodia). The question is: why is this bird singing? This seems a perfectly straightforward question, but in fact it is not, because answers can take any of four different forms. These different forms—you’ve guessed it—have to do with Tinbergen’s four questions. The first question concerns causation: what causes the bird to sing? The answers include the stimuli or triggers of behavior whether they be internal or external, the way in which behavioral output is guided, factors that stop behavior, and the like. These are questions concerning the causation of behavior. Sometimes this is called motivation, a topic discussed at length in Chapter 3. Tinbergen’s question of causation also concerns the mechanisms or structure of behavior. These mechanisms involve the “machinery” that operates within the animal and which are responsible for the production of behavioral output (Chapters 5 and 9).
The second question is about development: How did the singing behavior of the bird come about in the lifetime of an animal? A male song sparrow does not sing immediately after it has hatched from the egg, and it takes quite some time before it has developed a song, a process that involves learning. Such questions that concern development of behavior, sometimes also called ontogeny, will be discussed explicitly in Chapter 7. The third question has to do with the consequences of singing for the singer’s fitness: What is the function of the bird singing; what is it singing for? Does singing help the bird keep intruding males away from his nest? Or does it serve to attract females? Or does it do both? The topic of function (survival value), its methods of enquiry, and main findings will be discussed explicitly in Chapter 11. The fourth question concerns evolution: how did this behavior come about in the course of evolution? Behavior does not leave fossils behind and so the study of its evolutionary history requires the development of special methods. These methods, based on taxonomy and comparisons among species, will be discussed in detail in Chapter 15.
The previous paragraph illustrates that the question “why does this bird sing?” is not very useful, as it can have four different meanings. It can be very confusing if a biologist studying birdsong does not make it clear which of the four “why questions” he/she is asking, and it could lead to futile arguments concerning whether the bird is singing to attract mates or because it learned its song. The same problem arises in all other areas of animal behavior, so it is very important to make clear which question is being addressed in any study. Of course, it is possible that a particular investigator wants to address more than one question at a time. This is perfectly legitimate, as long as it is made explicit which of the questions are addressed at what time. A famous example of this is an experimental paper by Tinbergen and his associates (Tinbergen et al. 1962) on the behavior of blackheaded gulls (Larus ridibundus). After the chicks have hatched, the adult birds remove the empty eggshells from the nest. Tinbergen and his students investigated both the causation and the function (survival value) of this behavior using elegantly designed simple field experiments. They discovered the stimulus characteristics of items removed from the nest and, in the same paper, also reported results relevant to nest predation.
There is also considerable overlap among the four questions. For instance, the development of behavior is essentially a causal problem but may also involve functional aspects (Chapter 7). The evolution of behavior often depends on mechanism. For instance, emergent properties of an animal’s sensory and perceptual capabilities (mechanisms) may create opportunities for sexual selection to operate in the evolution of extravagant traits (Chapters 12 and 14). Finally, questions in one domain (e.g., function) can provide clues for questions in another domain (e.g., causation). For instance, a number of bird species cache food, some for a few hours, others for months (Vander Wall 1990). It is plausible that the ecological circumstances that have given rise to these different forms of food caching may have also influenced the birds’ ability to memorize spatial locations. In fact, a large number of studies are concerned with investigating the spatial memory of food caching versus nonfood-caching birds (Chapter 8).
Trends in the Study of Animal Behavior
Behavioral ecology: from mechanism to function
Much of the research and theorizing of early ethologists such as Lorenz and Tinbergen was concerned with the causation of behavior. When Tinbergen was invited to move from the Dutch University of Leiden to the University of Oxford, he established the Animal Behaviour Research Group, while at the same time the ecological ornithologist David Lack was taking over the newly founded Edward Grey Institute of Ornithology. The coincidence of having both these scientists and their followers in the same department in Oxford sowed the seeds of a discipline that was to blossom much later in the mid-1970s under the name of behavioral ecology.
Behavioral ecology arose out of the fusion of evolutionary ecology, population ecology, and ethology. A number of conditions were ripe in the mid-seventies for such an event. In 1975 the Harvard entomologist Edward O. Wilson published Sociobiology, The New Synthesis (1975). Wilson’s book was firmly grounded in population genetics and evolutionary biology. Its clear presentation of William D. Hamilton’s concepts of inclusive fitness, kin selection, the evolution of altruism and social groups among others, provided the essential foundations for a successful evolutionary approach to social behavior. Not long after that, in 1978, John R. Krebs at Oxford University and Nicholas B. Davies at Cambridge co-edited a book they called BehaviouralEcology: An Evolutionary Approach, which applies a similar evolutionary approach but this time to all, not just social, behavior. The publication of that book marks the official birth of behavioral ecology, which now includes sociobiology (see Chapter 17).
Behavioral ecology today is more of an approach than a body of accumulated fact. Its initial success grew out of a combination of optimality theory and evolutionary thinking that pictures the expression of behavioral traits as constrained trade-offs between their evolutionary benefits and costs (Chapter 11). The development of the concept of the evolutionarily stable strategy (ESS) by the British evolutionary biologist John Maynard Smith (1982) allowed this cost–benefit approach to be applied to a wide range of behavioral interactions. Evolutionary thinking and the cost–benefit approach cast a new light on behavioral systems such as foraging, fighting, and habitat selection (Chapter 11). When applied to communication it raised an important number of questions concerning the design of signals and their functions (Chapter 14). While early ethologists tended to picture sexual reproduction as a cooperative venture between males and females, the evolutionary approach has somewhat subverted this idyllic view. Mating systems and mate choice (Chapter 12) as well as conflicts of interests between mates (Chapter 14) have become exciting and rapidly developing areas of the discipline. Darwin himself pictured behavior as a character that was modified over generations by selection. Behavior, hence, has a history that can be and is studied with contemporary organisms (Chapters 15 and 16).
Neuroethology and cognitive neuroscience
The mechanisms underlying behavior are also represented in the workings of the central nervous system. In fact, Tinbergen often used neural analogies and metaphors in his models of behavior. We shall see in Chapters 2 and 5 how the central nervous system obtains and processes information about its external world. As knowledge about the brain, both its gross and fine-level morphology as well as the way its neurons are connected, led to increased interface between brain and behavior a new subdiscipline arose that is called neuroethology (Ewert 1980; Chapter 2). In the early days of this new discipline, researchers concentrated on the study of the neural mechanisms of perception and movement, often in insects or simple vertebrates. More recently the study of the brain mechanisms of behavior is also directed at higher cognitive processes such as learning and memory or spatial orientation. Often, the terms behavioral neuroscience or cognitive neuroscience are used to describe these disciplines. Now, the combination of an extraordinary array of powerful techniques from electrophysiological recording to molecular analyses of RNA sequences allows researchers to delve deeper into the connection between behavior and its neural substrate (Chapters 5 and 9).
Cognitive ecology and neuroecology
Perhaps as a result of the success of behavioral ecology, the mechanisms of brain and cognition have also been studied more recently from a functional and/or an evolutionary perspective, in new fields known as cognitive ecology (Healy & Braithwaite 2000; Macphail & Bolhuis 2001) and neuroecology (Bolhuis & Macphail 2001). According to the former, an animal’s ability to collect and process information should be heavily influenced by its ecology. Neuroecology refers to the study of the neural mechanisms of behavior guided by functional and evolutionary principles. How do the evolutionary pressures for complex birdsong affect the evolution of the underlying neural substrate? How does having a large home range affect one’s ability to navigate? Does having to store food place selective pressure on spatial memory and its underlying brain regions? These functional and evolutionary approaches to the study of brain and cognition have come under considerable criticism from authors who claim that they are flawed, because Tinbergen’s four whys are being confounded (Bolhuis & Macphail 2001; Macphail & Bolhuis 2001; Bolhuis & Wynne 2009; Bolhuis 2015). For example, food storing in certain species of titmice and corvids has been interpreted as a case of adaptive specialization (Healy & Braithwaite 2000; Shettleworth 2010). According to this hypothesis, food-storing birds would have evolved superior spatial memory as well as a larger hippocampus (thought to be its neural substrate) compared to their nonstoring counterparts. Both parts of this hypothesis have not been confirmed by the data (see Chapter 8 for further discussion).
Animal welfare and human nature
Many people are interested in animal behavior out of mere curiosity, the need to know more about something. This is all very fine but there always comes a time when someone will ask “what is the purpose of studying animal behavior?” This question, whether from a research colleague, a friend, or a granting agency requires an answer expressed in terms of benefits to society. We see two areas in which animal behavior research can contribute to human society: animal welfare and understanding human nature.
Animals are important contributors to wealth and quality of life. They provide us with nourishment, the means to find cures and treatments for our illnesses, as well as invaluable companionship. Almost all of the information contained in this book relies on experiments and research conducted with animals. There is a growing concern that animals used for human benefit, however, be exposed to as little unpleasantness as necessary. Are housing cages too small, or densities of individuals too high? Is the knowledge acquired from experiments sufficiently important to authorize animal experimentation? The answer to such, often difficult, questions depends in many ways on knowing something about an animal’s behavior (Chapter 10).
People are endlessly curious about people and the sheer number of disciplines devoted uniquely to the study of human beings is eloquent testimony to this fact (e.g., medicine, anthropology, psychology, sociology, criminology). Animal behavior can provide insight into human behavior in two ways. More conventionally, phenomena observed in animals can be generalized, although often in some modified way, to humans. For example, just as a new antibiotic drug that cures an infection in some nonhuman primate can also be used, perhaps in a slightly modified way, to cure infections in humans, so can knowledge about how an animal learns be extended and applied to human learning. The second way, however, involves generalizing an approach rather than a result. For instance, can we learn anything new about human behavior by applying an evolutionary cost–benefit analysis to the things we do? This is what an area known as evolutionary psychology does (Chapter 17).
SUMMARY AND CONCLUSIONS
The study of the behavior of animals has grown into a highly diverse set of approaches and disciplines. Its subject area ranges from molecules and neurons to individuals and populations. One of Tinbergen’s major contributions to the study of animal behavior has been to make its goals explicit and clarify four types of questions that can be asked of behavior: causation, development, survival value, and evolution. In this book we strongly advocate Tinbergen’s position that behavior can only be understood through research on all four questions. In addition, we suggest that it should be made clear which of Tinbergen’s questions is addressed when a behavioral problem is investigated: a problem in one domain should not be investigated with concepts from another. The early chapters in this book examine primarily causal, mechanistic, and developmental questions, while the latter chapters examine survival value and evolution issues. But examples in many chapters also illustrate that multiple approaches are necessary for understanding a problem, affirming Tinbergen’s view.
FURTHER READING
Tinbergen’s (1963) paper on the four whys is essential reading for any serious student of animal behavior. It was reprinted in Houck and Drickamer (1996), which is a collection of classic papers on all aspects of animal behavior, and in Tinbergen’s Legacy (Bolhuis & Verhulst 2009), which is a collection of contemporary essays reflecting on Tinbergen’s classic paper. The four-part reader by Bolhuis and Giraldeau (2010) is organized on the basis of Tinbergen’s four whys and has a collection of classic and contemporary papers on the evolution, function, development, and causation of animal behavior. Tinbergen’s (1951) classic book is still very much worthwhile. It was reprinted in 1992 and is still available. The British ethologist William Thorpe (1979) has written a brief history of ethology, viewed from the inside, while Dewsbury (1989) provides a more recent account from the North American perspective. Boakes (1984) is an excellent review of the history of the study of animal behavior by psychologists, while Laland and Brown (2011) provide a very clear account of the different ways in which the behavior of animals (including humans) can be studied from an evolutionary perspective. Functional and evolutionary aspects of behavior are also discussed in Davies et al. (2012). Hogan’s (2017) book provides an exposition and critique of behavioral concepts and of historical and contemporary studies of behavior.
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