Advances in the Study of Behavior Stress and Behavior
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Contents
Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix
Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xi
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...
Xlll
The Concept of Stress and Its Relevance for Animal Behavior
DIETRICH VON HOLST
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
I1. The Concept of Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
I11. Social Stress in Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . 42
IV . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
Stress and Immune Response
VICTOR APANIUS
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
I1. The Nature of Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
I11. The Nature of Immunocompetence . . . . . . . . . . . . . . . . . . 136
IV. Neurological Linking of Stress and Immunocompetence . . 140
V. Endocrine Linkage of Stress and Immunocompetence . . . . 142
Vl . Why Stress Alters Immunocompetence . . . . . . . . . . . . . . . 145
VII . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
Behavioral Variability and Limits to Evolutionary Adaptation
under Stress
P. A . PARSONS
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155
I1. Energy Limits to Adaptation . . . . . . . . . . . . . . . . . . . . . . . 158
I11. Variability and the Survival of Variants . . . . . . . . . . . . . . . 164
IV . Extending the Limits of Adaptation . . . . . . . . . . . . . . . . . . 165
V. From Stress-Resistance Genotypes to a
Connected Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
VI . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174
V
vi CONTENTS
Developmental Instability as a General Measure of Stress
ANDERS PAPE M@LLER
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
I1. Genetic and Environmental Determinants of
Developmental Instability . . . . . . . . . . . . . . . . . . . . . . . . . . 186
111. Directional Selection and Developmental Instability . . . . . 190
IV . Fitness Correlates of Developmental Instability . . . . . . . . . 192
V . Practical Uses of Developmental Instability . . . . . . . . . . . . 193
VI . Conclusions and Prospects for Future Studies . . . . . . . . . . 206
VII . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208
Stress and Decision-Making under the Risk of Predation:
Recent Developments from Behavioral. Reproductive. and
Ecological Perspectives
STEVEN L . LIMA
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
I1. Behavior of Feeding Animals: Classical Motivations . . . . . 217
111. Patterns of Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
IV . After an Encounter with a Predator . . . . . . . . . . . . . . . . . . 235
V . Social Situations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
VI . Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241
VII . Long-Term Consequences of Decision Making . . . . . . . . . 245
VIII . Ecological Influences and Implications . . . . . . . . . . . . . . . . 248
IX. Additional Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . 261
X . Conclusions and Summary . . . . . . . . . . . . . . . . . . . . . . . . . 264
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265
Parasitic Stress and Self-Medication in Wild Animals
G. A . LOZANO
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
I1. Self-Medication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
111. Prophylactic Se1f.Medication . . . . . . . . . . . . . . . . . . . . . . . . 294
IV. Therapeutic Self-Medication . . . . . . . . . . . . . . . . . . . . . . . . 298
V . Skepticism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
VI . Behavioral Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . 304
CONTENTS vii
VII . Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 308
VIII . Summary and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . 310
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311
Stress and Human Behavior: Attractiveness. Women’s Sexual
Development. Postpartum Depression. and Baby’s Cry
RANDY THORNHILL AND F. BRYANT FURLOW
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 319
I1. Human Attraction and Attractiveness . . . . . . . . . . . . . . . . 321
I11. Parent-Daughter Relations and Women’s Sexual
Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332
IV . Postpartum Depression . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341
V . Infant Crying as a Signal of Phenotypic Quality . . . . . . . . . 352
VI . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 359
Welfare. Stress. and the Evolution of Feelings
DONALD M . BROOM
I . Feelings. Their Role and Their Evolution . . . . . . . . . . . . . 371
I1. Welfare. Stress. and Feelings . . . . . . . . . . . . . . . . . . . . . . . . 394
I11. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 400
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 401
Biological Conservation and Stress
HERIBERT HOFER AND MARION L . EAST
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 405
I1. Stress in a Conservation Biology Context . . . . . . . . . . . . . . 407
I11. Designing a Conservation Study to Measure Stress and
Its Impact . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
IV. The Natural History of Stress . . . . . . . . . . . . . . . . . . . . . . . 428
V . Effects of Anthropogenic Stressors . . . . . . . . . . . . . . . . . . . 452
VI . Conservation Research and Management Activities as
Stressors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 473
VII . The Equivalence of Natural and Anthropogenic Stressors 486
...
Vlll CONTENTS
VIII . Minimizing Occurrence and Impact of Stress in
Conservation Research and Management . . . . . . . . . . . . . . 488
IX . Conclusions: How Important Is Stress in Biological
Conservation? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 494
X . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 496
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 497
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527
Contents of Previous Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . 549
Contributors
Numbers in parentheses indicate the pages on which the authors’ contributions begin.
VICTOR APANIUS (133),Department of Biological Sciences, Florida International
University, University Park, Miami, Florida 33199
DONALD M. BROOM (371), Department of Clinical Veterinary Medicine, Univer-
sity of Cambridge, Madingley Road, Cambridge CB3 OES, United Kingdom
MARION L. EAST (405), Max -Planck -1nstitut f i r Verhaltensphysiologie, 0-82319
Seewiesen Post Starnberg, Germany
BRYANT FURLOW (319). Department of Biology, University of New Mexico,
Albuquerque, New Mexico 87131
HERIBERT HOFER (405). Max -P/anck -1nstitut far Verhaltensphysiologie, D -
82319 Seewiesen Post Starnberg, Germany
DIETRICH VON HOLST (1). Department of Animal Physiology, University of
Bayreuth, 95440 Bayreuth, Germany
STEVEN L. LIMA (215), Department of Life Sciences, Indiana State University,
Terre Haute, Indiana 47809
G. A. LOZANO (291), Department o,f Biology, University of California, Riverside,
Calljornia 92522
ANDERS PAPE M0LLER (181), Laboratoire d’Ecologie, UniversitP Pierre et
Marie Curie, Paris Cedex 5, France
P. A. PARSONS (155), School of Genetics and Human Variation, La Trobe Univer-
sity, Bundoora, Victoria 3083, Australia
RANDY THORNHILL (31Y), Department of Biology, University of New Mexico,
Albuquerque, New Mexico 87131
ix
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Preface
The aim of the Advances in the Study of Behavior series remains as it
has been since the series began: to serve the increasing number of scientists
who are engaged in the study of animal behavior by presenting their theoret-
ical ideas and research to their colleagues and to those in neighboring fields.
We hope that the series will continue its “contribution to the development
of cooperation and communication among scientists in our field,” as its
intended role was phrased in the preface to the first volume in 1965. Since
that time, traditional areas of animal behavior research have been given
new vigor through the links they have formed with related fields and by
the closer relationship that now exists between those studying animal and
human subjects.
Beginning with Volume 25, which was on the special topic of Parental
Care, we departed from the previous policy of publishing articles on varied
subjects in every volume. This volume, titled “Stress and Behavior,” is the
second thematic volume. The next volume will again be a broad-ranging
one, as was the last, and it is our intention to continue the series with this
mixture of wide-ranging volumes of eclectic interest and occasional volumes
focusing on particular themes that appear timely to us.
Although volumes such as this do represent a new initiative, they do not,
we believe, violate the basic principles underlying the series. The specific
theme of Stress and Behavior was chosen because it is an especially exciting
and active area of research at present, and one to which researchers with
a wide range of approaches and backgrounds are making important contri-
butions. We have invited as contributors leading experts across this range,
thus giving a truly multidisciplinary perspective on the topic.
For this volume we have been fortunate to be joined by Dr. Anders
Pape Mflller as guest editor, and his expertise in the area has been of
immense help to us. Sadly, this will also be the last volume for which Dr.
Manfred Milinski will act as an associate editor: he has made a valuable
contribution to the series, for which we are very grateful. His place will be
taken by Dr. Tim Roper, of the University of Sussex, and we look forward
to benefiting from his broad interests and well-honed editorial skills in
future volumes.
P. J. B. Slater
xi
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Stress & Behavior
Introduction
All organisms suffer from a deficiency of one or more resources during
their lifetime, and conditions for development, growth, survival, and repro-
duction are rarely, if ever, optimal. This was realized by Charles Darwin,
who used competition among conspecifics for limiting resources as a corner-
stone of his theory of natural selection. Although suboptimal living condi-
tions are widespread, the relationship between environmental conditions
and behavior has not attracted much attention from scientists (for excep-
tions, see Hoffmann and Parsons, 1989; Maller and Swaddle, 1997).
The conditions under which organisms live are frequently suboptimal,
and the difference between suboptimal and optimal conditions is often
perceived by individuals as causing a change in their state. Stress is an
appealing but illusive concept in biology, with definitions being almost as
numerous as the different fields of research. Although stress can be defined
explicitly in terms of concentrations of biochemicals involved in metabolism
(Ivanovics and Wiebe, 1982), a general but still operational definition is
that provided by Hoffmann and Parsons (1989): the state caused by any
agent that results in suboptimal performance and potentially causes perma-
nent damage to an individual.
Life has evolved under stressful conditions, although exceptions exist,
such as the relatively constant environments experienced by organisms
living in caves and hot springs. The fact that organisms generally live
and reproduce under adverse environmental conditions has not been well
appreciated by the majority of the community of biologists. Theoretical
evolutionary biology has not considered stress to be of overriding impor-
tance. For example, Sewall Wright’s famous shifting balance theory is based
on the concept of a fitness landscape with multiple valleys and peaks. The
unappreciated fact that different phenotypes may be expressed under poor
and optimal conditions may have enormous effects on the ability of species
to evolve from one peak to another. Empirical evolutionary biologists have
performed most of their studies on fruit flies, mice, and rats under benign
laboratory conditions where stress is much reduced compared to natural
situations. Interestingly, phenotypic and genetic parameters are not congru-
ent or even comparable in such situations, as revealed by recent studies
of animals reared under more and less benign conditions (Bijlsma and
Loeschcke, 1997; Maller and Swaddle, 1997).
This discrepancy between conditions under which animals are studied
and conditions under which they live also applies to behavioral research.
...
Xlll
xiv INTRODUCTION
Laboratory studies are generally performed under benign conditions with
ad libitum availability of food and a virtual absence of predators and para-
sites. Field studies are predominantly conducted in optimal habitats with
high population densities, whereas much less is known about behavior of
animals in low-quality, marginal habitats where stress is predominant.
Behavior under adverse environmental conditions is a topic of general
interest for two reasons. First, such studies may provide us with a better
understanding of the conditions under which most evolution has taken
place. Second, studies of behavior under stressful conditions may give us
a better understanding of the consequences of global change, as well as
provide us with important information on conservation biology.
In the first chapter, von Holst describes how social relationships, espe-
cially aggressive ones, can influence the physiological state of individuals
in many positive and negative ways. This chapter introduces the neuroendo-
crinology of the stress response. Stressed organisms are easy targets of
infectious diseases. The complex strategic use of the immune system some-
times affords suppression of immune defenses under stress as discussed by
Apanius in the second chapter. In the third chapter, Parsons presents an
energetic approach to the fitness of organisms that are challenged by biotic
and abiotic stress. Under stressed free-living conditions, his environmental
model suggests that favored “good genotypes” are likely to be stress resis-
tant and heterozygous. In the fourth chapter, Mgller discusses develop-
mental stability as a reflection of the ability of organisms to buffer their
developmental trajectories against disturbance. The inability to fulfill this
goal can be assessed in terms of fluctuating asymmetry, i.e., random devia-
tions from perfect symmetry, and used for studies of, for example, environ-
mental monitoring, animal welfare, and human medicine. In the fifth chap-
ter, Lima discusses the many ways in which behavioral decision-making
alters the nature of predator-induced stress. In the sixth chapter, Lozano
discusses the growing evidence that wild animals use self-medication in
response to parasitic stress. In chapter 7, Thornhill and Furlow examine
how stress interacts with human behavior in relation to physical attractive-
ness, the development of women’s sexuality, and parental investment in
babies. The biological function of feelings such as pain and fear may be to
affect an organism’s behavior in such a way that it maximizes the chances
that good things will happen and minimizes the chances that bad things
will happen. Broom discusses welfare, stress, and the evolution of feelings
in chapter 8. The last chapter, by Hofer and East, reviews why stress has
important implications for biological conservation and considers practical
ways in which conservationists can identify and tackle problems due to
stress.
INTRODUCTION xv
We believe that a concerted research effort concerning behavior of ani-
mals living under adverse environmental conditions will add considerably
to our understanding not only of the role that behavior plays in the general
coping strategies of animals, but also of the flexibility of behavioral strate-
gies under variable environmental conditions. The authors of the chapters
of this thematic volume of Advances in the Study of Behavior have shown
some ways in which this may be achieved.
A. P. M@ller
M. Milinski
References
Biljsma, R. and Loeschcke, V. (eds.) (1997). “Stress. Adaptation. and Evolution.” Birk-
hauser. Basle.
Hoffmann, A. A. and Parsons, P. A. (1989). “Evolutionary Genetics and Environmental
Stress.” Oxford University Press, Oxford.
Ivanovics, A. M. and Wiebe, W. J. (1982). Toward a working definition of stress: A review
and critique. In “Stress Effects on Natural Ecosystems” (G. W. Barrett and R. Rosenberg,
eds.), pp. 13-27. Wiley, New York.
M@ller,A. P. and Swaddle, J . P. (1997). “Asymmetry, Developmental Stability and Evolution.”
Oxford University Press, Oxford.
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ADVANCES IN THE STUDY OF BEHAVIOR. VOL 21
The Concept of Stress and Its Relevance for
Animal Behavior
VON HOLST
DIETRICH
DEPARTMENT OF ANIMAL PHYSIOLOGY
UNIVERSITY OF BAYREUTH
95440 BAYREUTH, GERMANY
1. INTRODUCTION
Mammals live in social systems, which differ from species to species but
are relatively constant for any species, although some variation as a function
of the ecological situation is possible. These social systems are maintained
by constant contact between the animals, which not only affects the behavior
of the individuals, but may also positively or negatively influence their
fertility and health. The negative consequences of social interactions are
usually explained by the stress concept as shown in a particularly impressive
way in the Australian dasyurid marsupials of the genus Antechinus.
This genus is widely distributed in Australia and feeds mainly on insects
and small vertebrates. All species examined so far exhibit an extremely
synchronous life cycle: At the end of September-during the Australian
spring-the females give birth to their young, which are weaned in January,
but continue to live in harmony with their mothers for a few more months.
At the end of May, the young leave their birthplace and spread out within
their habitat. The short reproductive season commences in August, during
the Australian winter. During the search for females, the males roam their
territory and are continually involved in vehement fights with other males.
Following the 2- to 3-week reproductive season and before the end of the
first year of their life, virtually all the males “die off.” The females survive
and after a 1-month gestation period they give birth to their young. A new
cycle ensues (Woolley, 1966). The death of the males is due to typical stress
reactions characterized by a tenfold increase in the plasma levels of free
glucocorticosteroids and a simultaneous breakdown of the immune and
inflammatory responses. As a consequence, gastrointestinal hemorrhaging
associated with gastroduodenal ulcers, bacterially induced hepatic necrosis,
heavy parasitic diseases, and other infections cause the death of all males
1
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