Animals are widely used as research subjects, yet it is only recently that we have acknowledged the bond that frequently develops between subject and researcher. An increasing body of evidence suggests that it may result in profound behavioral and physiological changes in the animal subject in turn having marked effects on what is being studied. It may simply not be possible to avoid aversive encounters in certain species. This being the case, "resting" metabolic baselines may be seen in a new light as being elevated from truly normal levels or behavioral observations may include an inordinate number of undiagnosed defensive reactions. Over the course of 24 chapters, THE INEVITABLE BOND sends a clear message: To ignore the existence of experimenter effects on animals or to minimize the bond that created them reflects considerable scientific myopia. It reveals insensitivity to the complexity of the animal subject and may distort our understanding of the very processes we intend to study.
2. Contact between scientists and animals often follows regular patterns and sets the stage for anticipation of hedonic events in the animal's life. Such anticipation may be viewed in terms of complex cognitive processes or in simple Pavlovian terms. Regardless of one's level of analysis, there are undeniable effects to be reckoned with. The results of such experience are apparent in behavioral studies conducted in both laboratory and field settings. They also appear in physiological studies, ranging from biomedical (e.g. heart rate, blood pressure, immunological changes) to animal science (e.g. growth, production). Although we acknowledge that the behavioral and physiological effects of the scientist-animal relationship may be reciprocal, we have chosen to focus on the animal. To date, this half of the equation has been virtually ignored.
3. A number of chapters in THE INEVITABLE BOND (see full Table of Contents after this Precis) detail the discovery of how the the scientist-animal bond has affected the animal. Others take these effects as a given and describe attempts that have been made to accommodate them within a research setting. In either case, what we are describing seems analogous to the Heisenberg Principle, according to which the act of observation may itself alter the subject matter. The book surveys the effects of repeated interactions with the scientist on an unexpected variety of animal subjects. An introductory chapter by Estep & Hetts examines the range of possible relationships scientists can have with animal subjects (e.g., dominance-submission; predator-prey). Estep & Hetts argue that each of these possibilities, whether intentionally or unintentionally developed, can have important consequences for research.
4. The range of animals on which effects have been detected includes intuitively obvious examples involving canid subjects (chapters by Scott; Ginsburg & Hiestand; Fentress; and Kostarczyk). Other relatively unsurprising cases involve interactions between human researchers and nonhuman primates (chapters by Oden & Thompson; Boysen; and Boccia et al.). In addition, the most ubiquitous group of research animals, rodents, is no stranger to the effects of the scientist-animal relationship, as surveyed in the chapter by Dewsbury.
5. There are, however, less obvious instances of contact between scientists and animal subjects. Ian Duncan describes such effects in research with poultry. He notes that, despite domestication, poultry continue to display a surprising degree of fearful behavior toward human investigators. Hemsworth et al. survey the wide ranging negative interactions that occur between human handlers and pigs, and how these situations result in frequently undetected behavioral and physiological evidence of stress in the animals. Crowell-Davis notes that despite the ubiquity of horses in human culture, there is scant knowledge of the effect humans have on horse behavior and physiology. Like canid subjects, horses are remarkably sensitive detectors of minimal social cues, including those emitted by humans. Although the Clever Hans effect was named for precisely such an instance (i.e., a horse's behavior being affected by contact with a scientist), there has been little subsequent attention paid to this possibility. Crowell-Davis surveys the literature, including the results of her own research program, and indicates how ethological protocols might benefit from a greater understanding of the effects of humans on horse behavior. Lyons describes the role of early socialization in establishing a pattern of interactions between scientists and goats, and how physiological data can be used to assess these responses. Summerlee offers the same possibility for detecting experimenter-generated arousal in rabbits. Finally, Schusterman et al. offer similar evidence that early social interactions between California sea lions and human researcher result in major changes in the animals' behavior. These changes may be measured directly and used to considerable advantage, whether in routine handling or in specific experimental work to explore the cognitive and perceptual capabilities of the animals.
6. We document examples of THE INEVITABLE BOND involving even less orthodox subjects. Bowers & Burghardt examine the interactions that occur between scientists and various species of reptile. Although the nature of the "bond" that develops between human and snake, for example, may not conform to expectations established by our experience with domestic mammals, there are unmistakable sign that familiarity breeds measurable forms of behavioral and physiological change in these cold blooded animals. Burghardt also contributes a chapter describing the profound and often moving impact of the bond between human observers and captive black bears. Using both historical material and examples from his own research, Burghardt paints a vivid picture of how such bonding alters ursine behavior.
7. The effects of THE INEVITABLE BOND are not confined to "higher animals." This point is nowhere clearer than in the chapter by Mather. In perhaps the most surprising contribution, this chapter extends the book's principle to invertebrates, surveying evidence of the effects of human contact on several species of octopus.
8. The abiding question raised by such reports is "How can a human record the behavior or physiology of an animal subject that has not been altered in some way by contact with the human?" The issue is not whether humans can be an objective observer because of their familiarity with the animal. Human bias and "Rosenthal effects" are well documented within the experimental literature. It is patently obvious that once we name our subjects "devil" or "angel," it is hard to claim objectivity in recording their behavioral repertoires. However, these issues are not the topic of our book. Rather, we are concerned with whether the animal can remain unaffected by such contact. Can a subject remain "natural" when a human is somehow in the picture? Is there such a thing as an "unobtrusive observer"? Several chapters, e.g. those by Fentress and Caine, suggest a negative answer to these questions. This is a startling conclusion, with very strong implications for animal research. Indeed, were such reports and their implications taken at face value, it is unimaginable that research with animals could simply carry on in a "business as usual" fashion.
9. The message of THE INEVITABLE BOND is not relentlessly pessimistic. Although we are plainly proposing a caveat to researchers, there is an optimistic side to this principle. The scientist-animal bond is not simply a confound looming over all animal research. It may also be used as an adjunct to "good science." In related chapters dealing with the study of animal cognition, Boysen and Pepperberg, working with chimpanzees and parrots, respectively, document how sustained positive interactions with their subjects have not only facilitated data collection but also allowed these investigators to report forms of cognitive abilities (conceptual and numerical behavior) rarely observed in nonhuman subjects.
10. Another positive aspect of THE INEVITABLE BOND is its implications for animal welfare. Veterinarian Viktor Reinhardt describes how improving the relationship between technicians and rhesus monkeys may not only be put to good use in the arduous task of collecting biological samples, but how it may also enhance the psychological well being of subjects living in a large facility. In a final chapter, Lehman explores the philosophical/ethical implications of bonding between researcher and subject, raising a number of questions such as whether the scientist has a special obligation to the animal by virtue of a measurable bond which has developed over the course of research.
11. There is an irony in the fact that the fundamental point of THE INEVITABLE BOND is viewed as troublesome or contentious in many quarters. Were the book concerned with research on human behavior, virtually none of its points would be viewed as heretical or disturbing. In fact, the message would be so widely accepted as to render it unworthy of publication. It is generally accepted that human subjects are not passive sources of data. The message of THE INEVITABLE BOND is only newsworthy because it deals with animals, i.e. with interspecies situations.
12. Is it not reasonable to suppose a continuum of so-called experimenter effects? Just as human subjects are known to have needs and motives that may have an impact on data collection, so may animal subjects. The design of experiments with human subjects routinely takes experimenter-subject interactions into account. THE INEVITABLE BOND proposes that we give no less consideration when working with animal subjects.
13. What are the implications of claiming that experimenter effects on research animals are inevitable? For one thing, continued myopia about their existence is not without risk. As chapters by Duncan and Caine independently warn, it may simply not be possible to avoid aversive encounters in certain species. In short, the ubiquitous claim that "animals were adapted to the presence of the researcher prior to testing or observation" may be self-deluding fiction. This being the case, "resting" metabolic baselines may be seen in a new light as being elevated from truly normal levels. Similarly, behavioral observations may include an inordinate number of undiagnosed defensive reactions.
14. Over the course of 24 chapters, THE INEVITABLE BOND sends a clear message: To ignore the existence of experimenter effects on animals or to minimize the bond that created them reflects considerable scientific myopia. At the least, it reveals insensitivity to the complexity of the animal subject. At the most, it may distort our understanding of the very processes we intend to study.
1. The inevitable bond. Hank Davis and Dianne Balfour
2. Interactions, relationships, and bonds: the conceptual basis for
scientist-animal interactions. Daniel Q. Estep and Suzanne Hetts
3. Studies of rodent-human interactions in animal psychology.
Donald A. Dewsbury
4. The covalent animal: on bonds and their boundaries in behavioral
research. John C. Fentress
5. The phenomenon of attachment in human-nonhuman relationships.
John Paul Scott
6. Humanity's "best friend": origins of our inevitable bond with dogs.
Benson E. Ginsburg and Laurie Hiestand
7. The use of dog-human interaction as a reward in instrumental conditioning
and its impact on dogs' cardiac regulation. Ewa Kostarczyk
8. Behavioral arousal and its effect on the experimental animal and the
experimenter. Alastair J.S. Summerlee
9. Practice makes predictable: the differential effect of repeated
sampling on behavioral and physiological responses in monkeys.
Maria L. Boccia, Christy Broussard, James Scanlan, and Mark L.
Laudenslager
10. Improved handling of experimental rhesus monkeys. Viktor Reinhardt
11. Social interactions as a condition for learning in avian species:
a synthesis of the disciplines of ethology and psyhcology.
Irene M. Pepperberg
12. Pongid pedagogy: the contribution of human-chimpanzee interactions
to the study of ape cognition. Sarah T. Boysen
13. The role of social bonds in motivating chimpanzee cognition.
David L. Oden and Roger K.R. Thompson
14. Minimizing an inevitable bond: the study of automated avoidance in rats.
Morrie Baum and Laurie Hiestand
15. Underestimating the octopus. Jennifer Mather
16. The scientist and the snake: relationships with reptiles.
Bonnie B. Bowers and Gordon M. Burghardt
17. Fear of humans and its consequences for the domestic pig.
P.H. Hemsworth, J.L. Barnett, and G.J. Coleman
18. The effect of the researcher on the behavior of poultry.
Ian J.H. Duncan
19. Early human-animal relationships and temperament differences among
domestic dairy goats. David M. Lyons
20. The effect of the researcher on the behavior of horses.
Sharon L. Crowell-Davis
21. Imprinting and other aspects of pinniped-human interactions.
Ronald J. Schusterman, Robert Gisiner, and Evelyn B. Hanggi
22. Humans as predators: observational studies and the risk of
pseudohabitutation. Nancy G. Caine
23. Human-bear bonding in research on black bear behavior.
Gordon M. Burghardt
24. Scientist-animal bonding: some philosophical reflections.
Hugh Lehman
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