Nonhuman Primate Welfare: From History, Science, and Ethics to Practice

Preface
Contents
Part I: History of Nonhuman Primates in Captivity and Primate Welfare in Different Settings
The History of Primates in Zoos
1 Introduction
2 Development of the Modern Zoo
3 Species Kept by Zoos
4 Iconic Apes
5 Human Primates on Exhibition in the Zoo
6 Changes in Housing
7 Changes in Husbandry
8 Human-Animal Interaction
9 Zoos and Primate Research
10 Primates in Zoos, Then and Now
References
The History of Chimpanzees in Biomedical Research
1 Introduction
2 Early Chimpanzee Use in Research and the Road to the Yerkes Primate Research Center
3 Use and Care of Captive Chimpanzees in Research
3.1 Chimpanzees in Aerospace Studies
3.2 Chimpanzees in Linguistic Studies
3.3 Chimpanzee Use in Experimental Medicine and Biology
3.4 Large-scale Sourcing of Chimpanzees for Experimental Studies
3.5 Captive Research Chimpanzee Housing and Care
4 Ethical Concerns Regarding Captive Chimpanzee Welfare and the Development of a Research Chimpanzee Sanctuary
5 Research Chimpanzees Under the Microscope: Reports of the Institute of Medicine (IOM) and the NIH Council of Councils Workin...
6 NIH Decision and Post-Decision Impact
7 Conclusion
References
Using Primates in Captivity: Research, Conservation, and Education
1 Why Study Primates?
2 Primate Research Settings
3 Disciplines, Species, Origins, and Numbers
4 Welfare, Ethics, and Legislation
5 Good Research Practice
6 Conclusions
References
The Welfare of Primates in Zoos
1 Introduction
2 Presence of Familiar Humans
3 Presence of Unfamiliar Humans
3.1 Assessing Human-Animal Relationships
3.2 Reducing the Impact of Visitors on Welfare
3.3 Direct Human-Animal Contact
4 Social Management
4.1 Single-Sex Groups
4.2 Contraceptive Methods
5 Conclusions
References
Welfare of Primates in Laboratories: Opportunities for Refinement
1 Introduction
2 Differences Between Laboratories and Other Captive Settings
3 Primate Use in Laboratories
4 Ethical Framework of 3Rs and Welfare
5 Importance of Welfare for Quality of Scientific Output
6 Welfare Assessment
7 The Role of Human Behavior Change in Refinement
8 Conclusions
References
The Welfare of Primates Kept as Pets and Entertainers
1 Introduction
2 Definitions
3 History
4 Domesticated or Wild
5 Public Understanding of Primate Behavior
6 Legislation, Regulation, and Numbers
7 Trade
8 Housing
9 Temperature, Humidity, Light
10 Noise
11 Inbreeding
12 Diet and Nutrition
13 Diabetes
14 Skeletal Disease
15 Pregnancy and Weaning
16 Social Issues
17 `Undesirable´ Behaviors and Interventions
18 Transfer of Disease Between Humans and Primates
19 Rehabilitation Issues
20 Conclusion
References
Primates Under Human Care in Developing Countries: Examples From Latin America
1 Introduction
2 History
3 Captive Nonhuman Primates in Numbers
3.1 Brazil
3.2 Mexico
3.3 Uruguay
4 Endangered New World Monkeys in Captivity
5 Legal Protection for Primates in Latin American and Caribbean Countries
6 Human Care for Primates in Latin America, Where to Go from Here?
Appendix: Laws and Documents Consulted
References
Part II: Assessing Nonhuman Primate Welfare
Using Behavior to Assess Primate Welfare
1 Introduction
2 Abnormal Behavior
2.1 Stereotypies
2.2 Pathological Behavior
2.3 The Prevalence of Abnormal Behavior
2.4 Risk Factors/Causes of Abnormal Behavior
2.4.1 Extrinsic Effects
2.4.2 Rearing
2.4.3 Later Environmental Restriction
2.4.4 Stress Due to Clinical Procedures, Human Activity, and Husbandry
2.5 Intrinsic Effects
2.6 Species
2.7 Temperament
2.8 Age
2.9 Sex
3 The Function of Abnormal Behavior
3.1 Maladaptive
3.2 Coping Hypothesis
4 Using Abnormal Behaviors to Measure Welfare
5 Interventions for Abnormal Behavior
5.1 Social Housing
5.2 Inanimate Enrichment
5.3 Increased Cage Size
5.4 Outdoor Housing
5.5 Positive Reinforcement Training
5.6 Drug Therapy
6 Anxiety-Related Behavior
6.1 Behavioral Measures of Anxiety
6.2 Testing Anxiety and Identifying the Anxious Phenotype
6.3 Using Anxiety Behaviors to Measure Welfare
6.4 Anxiety Behaviors and Welfare-Related Studies
7 Measures of Good Welfare
8 Species-Appropriate Behaviors as Benchmarks for Welfare
9 Conclusions
References
Cognitive Bias Tasks: A New Set of Approaches to Assess Welfare in Nonhuman Primates
1 The Potential of Cognitive Bias Tasks for Assessing Nonhuman Primate Welfare
2 Cognitive Bias Tasks Explained: Design and Application
3 Judgment Bias
3.1 What Is It?
3.2 Method: The Basics
3.3 Examples of Application for Measuring Primate Welfare
3.4 Advantages and Limitations
4 Attention Bias
4.1 What Is It?
4.2 Method: The Basics
4.3 Examples of Application for Measuring Primate Welfare
4.4 Advantages and Limitations
5 Take Home and Considerations for Study Design
References
Physiological Measures of Welfare
1 Introduction
2 Hypothalamic-Pituitary-Adrenal Axis
2.1 Measuring Cortisol Levels
2.1.1 Short Time Scale (i.e., Point Samples): Blood and Saliva
2.1.2 Medium Time Scale: Urine and Feces
2.1.3 Long Time Scale: Hair
2.2 Measuring Regulation of the HPA Axis
3 Sympathetic-Adrenal-Medullary System
4 Cardiovascular System
5 Immune System
6 Conclusion
References
Questionnaires and Their Use in Primate Welfare
1 Introduction
2 Design and Analysis
3 The Need for Reliable Methodology in Studying Welfare
4 Different Types of Questionnaires for Studying Primate Welfare
References
Part III: Nonhuman Primate Housing and Husbandry
Meeting Cognitive, Behavioral, and Social Needs of Primates in Captivity
1 Introduction
2 The Influence of Ecology and Evolution on the Needs of Captive Primates
2.1 Cognitive Needs
2.1.1 Physical Cognition
2.1.1.1 Delay of Gratification and Self-Control
2.1.1.2 Memory and Planning
2.1.1.3 Tool Use and Causal Understanding
2.1.2 Social Cognition
2.1.2.1 Social Interaction
2.1.2.2 Social Learning
2.1.2.3 Mirror Self-Recognition and Theory of Mind
2.1.2.4 Behavioral Testing as Cognitive Enrichment
3 Behavioral Needs
3.1 Space
3.2 Activity
3.3 Social Needs
4 Conclusions and Future Directions
Bibliography
Primate Breeding Colonies: Colony Management and Welfare
1 Introduction
2 Basic Requirements of Colony Management
3 Specialized Aspects of a Primate Breeding Colony Management Program
3.1 Veterinary Care
3.2 Housing
3.3 Social Behavior
3.4 Welfare and Environment Enrichment
4 Record Keeping and Pedigree Management
4.1 Population Genetics and Demography
4.2 Demographic Management
4.3 Genetic Management
4.4 Integrating Demographics and Genetics into Breeding Plans
5 Closing
References
Common Husbandry, Housing, and Animal Care Practices
1 Introduction
2 Animal Husbandry
2.1 Husbandry Components in a Research Setting
2.2 Regulations
2.3 Understanding the Behavioral Biology
3 Health Monitoring/Disease Prevention
3.1 Daily Health Checks
3.2 Routine Health Monitoring
3.3 Disease Prevention
3.3.1 Personal Protective Equipment
3.3.2 Disease Surveillance
3.3.3 Vaccination
3.4 Quarantine
3.5 Sedation/Anesthesia
3.6 Identification
4 Nutrition
4.1 Standard Diet
4.2 Food Presentation
4.3 Developmental Needs
5 Shelter
5.1 Microenvironment (Enclosure)
5.1.1 Caging
5.1.2 Other Enclosure Types
5.1.3 Cage Complexity
5.1.4 Flooring and Substrates
5.2 Macroenvironment
5.2.1 Temperature
5.2.2 Lighting
5.2.3 Noise
5.3 Cleaning
6 Humane Handling
6.1 Animal Management
6.1.1 Appropriate Rearing
6.1.2 Reducing Relocations
6.1.3 Make Handling Predictable and Consistent
6.2 Human-Animal Interactions
6.2.1 Positive Relationship with Care Staff
6.2.2 Positive Reinforcement Training
7 Conclusions
References
Housing and Husbandry for Primates in Zoos
1 Overview and Introduction
2 Regulations, Guidelines, and Accreditation
3 Balancing Housing and Husbandry Requirements with Zoo Mission
3.1 Behavioral Needs of Zoo-Housed Primates
3.2 Accommodating Zoos´ Exhibition Needs
3.3 Accommodating Zoo´s Research Needs
4 Specific Enclosure Design and Husbandry Considerations
4.1 Space
4.2 Retreat Areas
4.3 Indoor Versus Outdoor Facilities
4.4 Indoor Enclosures
4.5 Three-Dimensional Structures
4.6 Enclosure Materials and Substrates
4.7 Mixed-Species Exhibits
4.8 Environmental Enrichment
4.9 Diet and Nutrition
5 Summary
References
Humane Endpoints and End of Life in Primates Used in Laboratories
1 Introduction
2 An Overview of the Use of Nonhuman Primates in Science
3 European Regulations and the Ethical Perspective
4 What Is a Humane Endpoint?
5 Setting the Humane Endpoint: Objective Assessments of Welfare
6 The Outcome of Welfare Assessment
7 Considerations Around End of Life of Primates
8 Incorporation of Humane Endpoints in Management
References
Part IV: Individual Differences, Application, and Improvement of Nonhuman Primate Welfare
Primate Personality and Welfare
1 Primate Personality and Welfare
2 Personality
3 Measuring Personality
3.1 Reliability
3.2 Validity
3.3 Structure
4 Personality and Welfare
4.1 Ratings
4.2 Behavior
4.3 Health and Physiology
5 Applications
6 Future Improvements
7 Conclusions
References
Sociality, Health, and Welfare in Nonhuman Primates
1 Introduction
2 Social Status, Dominance Relationships, and Welfare
2.1 Potential Costs of Being Subordinate
2.2 Resource Competition, Aggressive Interactions, and Welfare
2.2.1 Addressing Welfare Concerns Related to Aggression and Trauma
2.3 Psychosocial Stress and Welfare
2.4 Potential Costs of High Rank
2.5 Rank Stability and Certainty
2.5.1 Group-Level Aspects of the Status-Welfare Relationship
3 Social Bonds and Welfare
3.1 Affiliative Interactions and Stress Physiology
3.2 Strong Social Bonds
3.3 Social Network Position and Structure and Welfare
3.4 Welfare Implications of Affiliative Interactions and Social Bonds
4 Conclusions/Summary
References
Research Benefits of Improving Welfare in Captive Primates
1 Introduction
2 Welfare, Behavioral Management, and Scientific Data
2.1 Socialization and Data
2.2 Enrichment and Data
2.3 Positive Reinforcement Training and Data
3 Nonhuman Primate Subject Characteristics and Their Effects on Data
3.1 Pathogens and Data
3.2 Temperament and Data
4 Acclimation and Data Quality
5 Animal Handling and Data Quality
6 Multiple Protocols, Re-Use, and Data Quality
7 Conclusions
References
Enrichment
1 Introduction
2 Aims of Enrichment
3 Enrichment Program
3.1 Designing an Enrichment Program
4 Safety Considerations
5 Types of Enrichment
5.1 Social Enrichment
5.2 Physical Enrichment
5.3 Food-Based Enrichment
5.4 Sensory Enrichment
5.4.1 Visual Enrichment
5.4.2 Tactile Enrichment
5.4.3 Auditory Enrichment
5.4.4 Olfactory Enrichment
5.5 Cognitive Enrichment
6 Assessment
7 Conclusion
References
Challenging Cognitive Enrichment: Examples from Caring for the Chimpanzees in the Kumamoto Sanctuary, Japan and Bossou, Guinea
1 Introduction
2 Kumamoto Sanctuary: The First Sanctuary for Retired Laboratory Chimpanzees in Japan
3 Behavior that Is Typical in Captivity Can Be Atypical in the Wild
4 The Agency of Chimpanzees Living in Captivity
5 Sharing Resources in Captive Conditions
6 The Wild Model: Sharing Resources in a Natural Habitat
7 The Behavioral Freedom of Chimpanzees: Cognitive Enrichment as a Bridge Between Welfare and Conservation
8 Conclusion
References
Training Research Primates
1 Introduction
2 Regulatory Support for the Use of PRT Methods
3 Basic Training Concepts
4 First Steps in Positive Reinforcement Training
5 How Positive Reinforcement Training Is Used in the Research Environment
5.1 Training for Movement
5.2 Positive Reinforcement Training and Social Housing
5.3 Training for Biological Sample Collection
5.4 Training for Other Research Procedures
5.5 Training for Restraint
5.6 Moving Away from the Need for Restraint
5.7 Training Cooperation with Veterinary Care
6 Is There a Role for Negative Reinforcement?
7 Training to Improve Animal Welfare
8 Positive Reinforcement Training Helps People Working in Research Settings
9 Positive Reinforcement Training Improves Science
10 Advancing Animal Training Through Behavior Analysis
10.1 Functional Analysis
10.2 Preference Assessment
11 Developing Animal Training Programs
11.1 Program Structure
11.2 Project-Based Approach
11.3 Section-Wide Approach
11.4 Facility-Wide Approach
11.5 Personnel Considerations
12 Moving Forward
References
Part V: Biomedical Research, Ethics, and Legislation Surrounding Nonhuman Primate Welfare
Arguments Against Using Nonhuman Primates in Research
1 Introduction
2 Uses of Nonhuman Primates in Research
2.1 Drug/Product Testing
2.2 Disease Modeling/Basic Research
3 Scientific Argument: Empirical Evidence of Benefits
3.1 Drug Testing
3.2 Disease Models/Basic Research
3.2.1 HIV/AIDS
3.2.2 Alzheimer´s Disease
3.2.3 Stroke
3.2.4 Parkinson´s Disease
4 Reasons for Failure
4.1 Genetic Differences Between Humans and Nonhuman Primates
4.2 Consequences of Genetic Differences for Nonhuman Primate Use in Drug Tests
4.3 Consequences of Genetic Differences for Nonhuman Primate Use in Neuroscience
4.4 Stress Associated with Laboratory Environment and Experimentation
4.5 The Ethical Argument
4.5.1 Capacity to Suffer, and Direct Harms
4.5.2 Indirect Harms
4.6 What Can Be Done? Alternative Methods
4.7 Summary and Conclusion
References
The Indispensable Contribution of Nonhuman Primates to Biomedical Research
1 The Role of Nonhuman Primates in Biomedical Research
2 Categorical Challenges to the Scientific Value of Research on Nonhuman Primates
3 A Nuanced Approach to Nonhuman Primate Research
4 The Need for Transparent Science Communication About Responsible Nonhuman Primate Research
References
An Unexpected Symbiosis of Animal Welfare and Clinical Relevance in a Refined Nonhuman Primate Model of Human Autoimmune Disea...
1 Introduction
2 Concise Phylogeny of Animal Models Used in Preclinical Immunology Research
3 Multiple Sclerosis (MS)
4 Translational Relevance of the Marmoset EAE Model
5 Mechanistic Basis of MS Risk Factors: Lessons from the Marmoset EAE Model
5.1 Predisposing Genes
5.2 Infections
6 Welfare Aspects
7 Perspectives and Concluding Remarks
References
Animal Welfare, Animal Rights, and a Sanctuary Ethos
1 Ethics Beyond the Human
2 Nonhuman Primates and Their Exploitation
2.1 Laboratory Research
2.2 Entertainment
2.3 Zoos
2.4 The Pet Trade
3 Animal Welfare Concerns
4 Animal Rights
5 A Sanctuary Ethos
6 Conclusion
References
The Welfare Impact of Regulations, Policies, Guidelines, and Directives and Nonhuman Primate Welfare
1 Introduction
2 European Framework
3 United States
3.1 U.S. Department of Agriculture
3.2 Office of Laboratory Animal Welfare
3.3 Specific Controls on the Use of Chimpanzees
4 Other Countries
4.1 Australia
4.2 Canada
4.3 China
4.4 India
4.5 Japan
4.6 Singapore
4.7 South America and Africa
5 Professional Society Guidelines
6 National Primate Societies
6.1 Other National Primate Societies
7 Networks
8 Conclusion
References
Index