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Food and Feed Safety Systems
and Analysis
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Food and Feed Safety Systems
and Analysis
Edited by

Steven C. Ricke
Griffiths G. Atungulu
Chase E. Rainwater
Si Hong Park
Academic Press is an imprint of Elsevier
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Contents
List of Contributors��������������������������������������������������������������������������������������������xv
Preface������������������������������������������������������������������������������������������������������������xvii
Section 1: Animal and Pet Feed Safety����������������������������������������1
Chapter 1: Changes in the Food Safety Landscape of Pet Foods in the United States���� 3
Brittany L. White, Billie L. Johnson, Russell Morgan and Richard G. Shields Jr.
History of Pet Food Types and Formats������������������������������������������������������������������3
Pet Food Safety Issues Associated With Raw Materials�����������������������������������������5
Base Ingredient Selection�������������������������������������������������������������������������������������5
Humanization of Pet Food������������������������������������������������������������������������������������6
Nutrient Deficiencies and Excesses����������������������������������������������������������������������7
Antinutritional Factors������������������������������������������������������������������������������������������8
Prion Diseases�����������������������������������������������������������������������������������������������������10
Selection of Food Additives��������������������������������������������������������������������������������10
Cross-Contamination Risks��������������������������������������������������������������������������������11
Mycotoxins���������������������������������������������������������������������������������������������������������11
Globalization������������������������������������������������������������������������������������������������������14
Achieving Commercial Sterility in Pet Food Production
and Potential Recontamination������������������������������������������������������������������������������14
A History of Recalls in Pet Food���������������������������������������������������������������������������16
Changes in the Regulatory Landscape for Pet Food����������������������������������������������18
References�������������������������������������������������������������������������������������������������������������20
Chapter 2: Mycotoxin Issues in Pet Food�������������������������������������������������������������25
Griffiths G. Atungulu, Zeinab Mohammadi-Shad and Shantae Wilson
Introduction�����������������������������������������������������������������������������������������������������������25
Aflatoxin�������������������������������������������������������������������������������������������������������������25
Deoxynivalenol���������������������������������������������������������������������������������������������������26
Fumonisin�����������������������������������������������������������������������������������������������������������26
Ochratoxins���������������������������������������������������������������������������������������������������������26
Tremorgens���������������������������������������������������������������������������������������������������������27
Mycotoxin Prevalence�������������������������������������������������������������������������������������������27
Pet Food–Related Mycotoxicoses Outbreaks and Recalls������������������������������������30

v
vi Contents

Mycotoxin Analyses and Related Challenges�������������������������������������������������������30


Sampling Issues��������������������������������������������������������������������������������������������������30
Detection Issues��������������������������������������������������������������������������������������������������33
Mycotoxin Management in Pet Food��������������������������������������������������������������������34
Conclusions�����������������������������������������������������������������������������������������������������������38
References�������������������������������������������������������������������������������������������������������������39
Chapter 3: Emerging Pet Food Drying and Storage Strategies to
Maintain Safety�������������������������������������������������������������������������������45
Gbenga A. Olatunde and Griffiths G. Atungulu
Introduction�����������������������������������������������������������������������������������������������������������45
Classification of Pet Food and Main Nutritional Elements�����������������������������������45
Main Composition of Pet Food and Primary Sources����������������������������������������47
Storage Strategies to Minimize Nutritional Composition Loss�����������������������������47
Vitamin Potency�������������������������������������������������������������������������������������������������47
Lipid or Fat Rancidity�����������������������������������������������������������������������������������������48
Protein Denaturation�������������������������������������������������������������������������������������������49
Carbohydrate Loss����������������������������������������������������������������������������������������������50
Moisture Content������������������������������������������������������������������������������������������������51
Emerging Drying Techniques��������������������������������������������������������������������������������51
Convective Heated Air Drying����������������������������������������������������������������������������51
Microwave Drying����������������������������������������������������������������������������������������������53
Infrared Drying���������������������������������������������������������������������������������������������������55
Fluidized Bed Drying�����������������������������������������������������������������������������������������57
Conclusions�����������������������������������������������������������������������������������������������������������58
References�������������������������������������������������������������������������������������������������������������58
Chapter 4: Animal Feed Mill Biosecurity: Prevention of Biological Hazards�������������63
Anne Huss, Roger Cochrane, Mary Muckey and Cassie Jones
Introduction�����������������������������������������������������������������������������������������������������������63
Animal Food�������������������������������������������������������������������������������������������������������64
Manufacture of Animal Feeds����������������������������������������������������������������������������68
Biological Hazards���������������������������������������������������������������������������������������������69
Food Safety Modernization Act��������������������������������������������������������������������������71
Feed Mill Biosecurity��������������������������������������������������������������������������������������������72
Hazard Analysis��������������������������������������������������������������������������������������������������74
Hazard Mitigation�����������������������������������������������������������������������������������������������75
Conclusions�����������������������������������������������������������������������������������������������������������78
References�������������������������������������������������������������������������������������������������������������78
Further Reading�����������������������������������������������������������������������������������������������������81
Chapter 5: Physical and Chemical Methods for the Reduction of Biological
Hazards in Animal Feeds������������������������������������������������������������������83
Anne Huss, Roger Cochrane, Cassie Jones and Griffiths G. Atungulu
Introduction�����������������������������������������������������������������������������������������������������������83
Feed Manufacturing�����������������������������������������������������������������������������������������������85
Contents vii

Physical Methods������������������������������������������������������������������������������������������������85
Chemical Methods����������������������������������������������������������������������������������������������90
Conclusions�����������������������������������������������������������������������������������������������������������92
References�������������������������������������������������������������������������������������������������������������92
Section 2: Preharvest Food Safety Systems - Incidence and
Control of Foodborne Pathogens��������������������������������97
Chapter 6: Antimicrobial Resistance in Foodborne
Pathogens���������������������������������������������������������������������������������������99
Corliss A. O’Bryan, Philip G. Crandall and Steven C. Ricke
Introduction�����������������������������������������������������������������������������������������������������������99
Foodborne Illness and Antimicrobial Resistance������������������������������������������������101
Acquired Antimicrobial Resistance������������������������������������������������������������������101
Mechanisms of Bacterial Antimicrobial Resistance��������������������������������������������103
Antibiotic Inactivation or Modification������������������������������������������������������������103
Efflux Pumps����������������������������������������������������������������������������������������������������104
Altered Target���������������������������������������������������������������������������������������������������104
Reservoirs of Multidrug-Resistant Bacteria and Genes��������������������������������������105
Food Animals����������������������������������������������������������������������������������������������������105
Companion Animals�����������������������������������������������������������������������������������������105
Wild Animals and Insects���������������������������������������������������������������������������������106
Environment�����������������������������������������������������������������������������������������������������106
Intervention Methods to Reduce Antibiotic Resistance��������������������������������������107
Curtail Antibiotic Use in Agriculture����������������������������������������������������������������107
Proper Usage of Antibiotics in Human Medicine���������������������������������������������108
Develop New Drugs������������������������������������������������������������������������������������������108
Conclusions���������������������������������������������������������������������������������������������������������109
References�����������������������������������������������������������������������������������������������������������109
Chapter 7: The First 30 Years of Shiga Toxin–Producing Escherichia coli
in Cattle Production: Incidence, Preharvest Ecology,
and Management������������������������������������������������������������������������������ 117
Christina L. Swaggerty, Nicolae Corcionivoschi, Steven C. Ricke
and Todd R. Callaway
Background����������������������������������������������������������������������������������������������������������117
Ecology of Shiga Toxin–Producing Escherichia coli and Gastrointestinal
Colonization��������������������������������������������������������������������������������������������������������119
Management Practices and Transportation����������������������������������������������������������121
Biosecurity��������������������������������������������������������������������������������������������������������122
Cattle Grouping������������������������������������������������������������������������������������������������122
Bedding and Pen Surfaces��������������������������������������������������������������������������������123
Manure Management����������������������������������������������������������������������������������������123
Transportation and Lairage�������������������������������������������������������������������������������123
Stress�����������������������������������������������������������������������������������������������������������������124
viii Contents

Conclusions���������������������������������������������������������������������������������������������������������124
References�����������������������������������������������������������������������������������������������������������125
Chapter 8: The First 30 Years of Shiga Toxin–Producing Escherichia coli in
Cattle Production: Preharvest Intervention Strategies������������������������133
Christina L. Swaggerty, Ester Grilli, Andrea Piva, Nicolae Corcionivoschi,
Steven C. Ricke and Todd R. Callaway
Background����������������������������������������������������������������������������������������������������������133
Water and Feed Management������������������������������������������������������������������������������134
Probiotic Approaches to Influence Microbial Ecology in the
Gastrointestinal Tract of Cattle�������������������������������������������������������������������������134
Probiotics����������������������������������������������������������������������������������������������������������134
Direct-Fed Microbials���������������������������������������������������������������������������������������135
Competitive Exclusion��������������������������������������������������������������������������������������136
Prebiotics����������������������������������������������������������������������������������������������������������136
Colicins�������������������������������������������������������������������������������������������������������������137
Direct Antipathogen Strategies����������������������������������������������������������������������������137
Antibiotics��������������������������������������������������������������������������������������������������������138
Sodium Chlorate�����������������������������������������������������������������������������������������������138
Bacteriophages��������������������������������������������������������������������������������������������������138
Cattle Hide Washing�����������������������������������������������������������������������������������������139
Vaccination�������������������������������������������������������������������������������������������������������139
Organic Acids and Botanicals���������������������������������������������������������������������������142
Conclusions���������������������������������������������������������������������������������������������������������144
References�����������������������������������������������������������������������������������������������������������144
Chapter 9: Foodborne Salmonella in Laying Hens and Egg Production�����������������153
Steven C. Ricke, Turki M. Dawoud, Zhaohao Shi, Pravin Kaldhone and
Young M. Kwon
Introduction���������������������������������������������������������������������������������������������������������153
Salmonella Infections and Poultry�����������������������������������������������������������������������154
Salmonella and the Laying Hen Reproductive Tract�������������������������������������������155
Incidence of Salmonella and Management of Laying Hens��������������������������������157
Control Programs for Salmonella in Laying Hen Flocks—General Concepts������ 158
Interventions for Preharvest Egg Production�������������������������������������������������������159
Interventions for Postharvest Egg Processing�����������������������������������������������������161
Conclusions���������������������������������������������������������������������������������������������������������162
References�����������������������������������������������������������������������������������������������������������163
Chapter 10: Cereal Grain Fractions as Potential Sources of Prebiotics: Current
Status, Opportunities, and Potential Applications���������������������������173
Xuhui Zhuang, Chen Zhao, Keshun Liu, Peter M. Rubinelli, Steven C. Ricke
and Griffiths G. Atungulu
Introduction���������������������������������������������������������������������������������������������������������173
Contents ix

Brief Overview of Cereal Grain Production and Processing�������������������������������174


Global Cereal Grain Production�����������������������������������������������������������������������174
The Processing of Cereal Grains����������������������������������������������������������������������176
Components From Cereal Grains for Potential Prebiotic Use:
Extraction and Fractionation�������������������������������������������������������������������������������177
Animal Studies Involving Fractions for Prebiotics Application��������������������������182
Human Health Responses���������������������������������������������������������������������������������182
Animal Feeding������������������������������������������������������������������������������������������������182
Foodborne Pathogen Reduction������������������������������������������������������������������������183
Gut Microbiome�����������������������������������������������������������������������������������������������184
Economics for Application—Human and Animal Health Markets���������������������184
Future Directions�������������������������������������������������������������������������������������������������185
Mycotoxin Removal�����������������������������������������������������������������������������������������185
Grain Processing and By-product Utilization���������������������������������������������������186
Genetic Modifications���������������������������������������������������������������������������������������187
Conclusions���������������������������������������������������������������������������������������������������������187
References�����������������������������������������������������������������������������������������������������������187
Section 3: Postharvest Food Safety Systems – Incidence and
Control of Foodborne Pathogens������������������������������193
Chapter 11: Interventions to Reduce Shiga Toxin–Producing Escherichia coli
on Beef Carcasses at Slaughter������������������������������������������������������195
Corliss A. O’Bryan, Sean J. Pendleton, Steven C. Ricke and
Philip G. Crandall
Introduction���������������������������������������������������������������������������������������������������������195
Risk Categorization of Incoming Cattle��������������������������������������������������������������196
Hide-on Interventions������������������������������������������������������������������������������������������197
Chemical Dehairing������������������������������������������������������������������������������������������197
Chemical Washes����������������������������������������������������������������������������������������������198
Steam Treatments���������������������������������������������������������������������������������������������199
Biological Treatments���������������������������������������������������������������������������������������199
Shellac��������������������������������������������������������������������������������������������������������������199
Summary of Hide Treatments���������������������������������������������������������������������������200
Carcass Interventions�������������������������������������������������������������������������������������������200
Physical Interventions���������������������������������������������������������������������������������������200
Chemical Interventions�������������������������������������������������������������������������������������202
Spray Chilling���������������������������������������������������������������������������������������������������204
Emerging Technologies���������������������������������������������������������������������������������������205
Electron Beam Irradiation��������������������������������������������������������������������������������205
Essential Oils����������������������������������������������������������������������������������������������������206
Conclusions���������������������������������������������������������������������������������������������������������206
Acknowledgments�����������������������������������������������������������������������������������������������207
References�����������������������������������������������������������������������������������������������������������207
x Contents

Chapter 12: Microbiological Safety of Unpasteurized Fruit and


Vegetable Juices Sold in Juice Bars and Small Retail Outlets�������������213
Armitra Jackson-Davis, Aubrey Mendonca, Shakaree Hale, Jealae Jackson,
Alescia King and Joy Jackson
Introduction���������������������������������������������������������������������������������������������������������213
Raw Juice Characteristics: Influence on Pathogen Survival��������������������������������217
Nonthermal Technologies to Control Pathogens in Juice������������������������������������218
Regulatory Perspective of Raw Juice������������������������������������������������������������������220
Conclusions���������������������������������������������������������������������������������������������������������221
References�����������������������������������������������������������������������������������������������������������221
Chapter 13: Listeria monocytogenes Adaptation and Growth at
Low Temperatures: Mechanisms and Implications
for Foodborne Disease������������������������������������������������������������������227
Joshua C. Saldivar, Morgan L. Davis, Michael G. Johnson and Steven C. Ricke
Introduction���������������������������������������������������������������������������������������������������������227
Listeriosis Epidemiology�������������������������������������������������������������������������������������228
Listeria monocytogenes Pathogenesis Mechanisms��������������������������������������������229
Listeria and Food Sources�����������������������������������������������������������������������������������232
Listeria monocytogenes and Cold Stress�������������������������������������������������������������234
Cellular Metabolism During Cold Stress������������������������������������������������������������236
Potential for Cross-Protection and Cold Stress���������������������������������������������������237
Cold Stress and Virulence������������������������������������������������������������������������������������238
Genomic Approaches for Identifying Cold Stress Function��������������������������������239
Conclusions���������������������������������������������������������������������������������������������������������240
References�����������������������������������������������������������������������������������������������������������241
Chapter 14: Use of Natural Antimicrobials of Plant Origin to Improve the
Microbiological Safety of Foods�����������������������������������������������������249
Aubrey Mendonca, Armitra Jackson–Davis, Rkia Moutiq and Emalie Thomas-Popo
Introduction���������������������������������������������������������������������������������������������������������249
Food Applications for Pathogen Control�������������������������������������������������������������250
Fruit and Vegetable Juices��������������������������������������������������������������������������������250
Meat Products���������������������������������������������������������������������������������������������������253
Fish Products����������������������������������������������������������������������������������������������������255
Dairy Products��������������������������������������������������������������������������������������������������256
Limitations in Food Applications������������������������������������������������������������������������257
Sensory Changes�����������������������������������������������������������������������������������������������257
Miscibility Problems�����������������������������������������������������������������������������������������258
Interactions With Food Matrix Components����������������������������������������������������258
pH Dependency������������������������������������������������������������������������������������������������258
Temperature Dependency���������������������������������������������������������������������������������259
Microbial Contamination and Type of Microbe�����������������������������������������������259
Contents xi

Techniques for Delivery of Essential Oils and Their Components���������������������259


Incorporation in Food Packaging����������������������������������������������������������������������260
Encapsulation����������������������������������������������������������������������������������������������������260
Incorporation in Biodegradable Edible Coating�����������������������������������������������261
Exploiting Synergistic Actions of Essential Oils and Their Components�����������261
Interactive Outcomes and Intra–Essential Oil Interactions������������������������������261
Analysis of Combined Effects��������������������������������������������������������������������������263
Theoretical Mechanisms�����������������������������������������������������������������������������������263
Regulations for Food Applications����������������������������������������������������������������������264
U.S. Food and Drug Administration�����������������������������������������������������������������264
European Food Safety Authority����������������������������������������������������������������������264
China Food Additives Association��������������������������������������������������������������������265
Conclusions and Future Prospects�����������������������������������������������������������������������265
References�����������������������������������������������������������������������������������������������������������266
Chapter 15: Characteristics of Bacteriocins and Use as Food Antimicrobials
in the United States���������������������������������������������������������������������273
Corliss A. O’Bryan, Ok Kyung Koo, Michael L. Sostrin, Steven C. Ricke,
Philip G. Crandall and Michael G. Johnson
Food Antimicrobials��������������������������������������������������������������������������������������������273
Bacteriocins���������������������������������������������������������������������������������������������������������274
Classification and Nomenclature of Bacteriocins���������������������������������������������274
Mode of Action of Bacteriocins������������������������������������������������������������������������275
Nisin��������������������������������������������������������������������������������������������������������������������276
Pediocins��������������������������������������������������������������������������������������������������������������278
Bacteriocins in Food Systems������������������������������������������������������������������������������279
Regulatory Environment in the United States��������������������������������������������������279
Methods to Use Bacteriocins in Food Products������������������������������������������������279
Factors Affecting Use of Bacteriocins in Food�������������������������������������������������281
Food Applications������������������������������������������������������������������������������������������������281
Conclusions���������������������������������������������������������������������������������������������������������282
References�����������������������������������������������������������������������������������������������������������282
Section 4: Emerging Food Safety Systems��������������������������������287
Chapter 16: Detection Strategies for Foodborne Salmonella and Prospects
for Utilization of Whole Genome Sequencing Approaches�����������������289
Si Hong Park, Mushin Aydin, Peixin Fan, Shinyoung Lee, Lin Teng, Sun Ae Kim,
Soohyoun Ahn, Steven C. Ricke, Zhaohao Shi and Kwangcheol C. Jeong
Salmonella as a Foodborne Pathogen—Food Safety Perspectives����������������������289
Poultry as a Major Vehicle for Transmission of Salmonella�������������������������������291
Detection Technology������������������������������������������������������������������������������������������291
Detection Methods for Salmonella in Poultry: General Concepts�������������������291
Culture-Based Methods������������������������������������������������������������������������������������292
xii Contents

Immunological-Based Methods������������������������������������������������������������������������292
Molecular-Based Methods��������������������������������������������������������������������������������293
Salmonella Identification Using Whole Genome Sequencing��������������������������295
Conclusions and Future Prospects�����������������������������������������������������������������������301
References�����������������������������������������������������������������������������������������������������������302
Chapter 17: Use and Impacts of Whole Genome Sequencing in
Retail Food Safety�����������������������������������������������������������������������309
Clara Assisi, Andrea J. Etter and Haley F. Oliver
History of Whole Genome Sequencing���������������������������������������������������������������309
Current and Future Platforms������������������������������������������������������������������������������310
Single-Molecule, Real-Time Sequencing������������������������������������������������������������310
Oxford Nanopore (MinION)�������������������������������������������������������������������������������311
Illumina Platforms�����������������������������������������������������������������������������������������������311
Whole Genome Sequencing Has Changed the Epidemic Curve for
Food Safety����������������������������������������������������������������������������������������������������������313
Whole Genome Sequencing Projects������������������������������������������������������������������315
The 100,000 Pathogen Genome Project�����������������������������������������������������������315
GenomeTrakr����������������������������������������������������������������������������������������������������316
Current Applications of Whole Genome Sequencing in the
Retail Food System����������������������������������������������������������������������������������������������316
Future Applications of Whole Genome Sequencing in Retail�����������������������������317
References�����������������������������������������������������������������������������������������������������������317
Chapter 18: Historical, Current, and Future Prospects for Food Safety in
Poultry Product Processing Systems�����������������������������������������������323
Rachael E. Blevins, Sun Ae Kim, Si Hong Park, Rafael Rivera and
Steven C. Ricke
Introduction���������������������������������������������������������������������������������������������������������323
Salmonella and Campylobacter as Major Pathogens in Poultry�������������������������324
Poultry Product Shelf-Life and Spoilage Microbiota������������������������������������������325
Bacterial Contamination/Reduction During Poultry Processing Steps���������������325
Before Scalder��������������������������������������������������������������������������������������������������325
Scalder��������������������������������������������������������������������������������������������������������������326
Picker����������������������������������������������������������������������������������������������������������������327
Evisceration������������������������������������������������������������������������������������������������������329
Inside/Outside Bird Wash and On-Line Reprocessing�������������������������������������330
Chiller���������������������������������������������������������������������������������������������������������������331
Food Safety Regulations Regarding Pathogen Reduction�����������������������������������332
Methods of Monitoring Sanitation Effectiveness in the Poultry
Slaughter Facility�������������������������������������������������������������������������������������������������335
Contents xiii

 urrent and Future Prospects for Microbial Profiling in the


C
Poultry Slaughter Facility������������������������������������������������������������������������������������336
Conclusions���������������������������������������������������������������������������������������������������������339
References�����������������������������������������������������������������������������������������������������������340
Chapter 19: Unraveling Food Production Microbiomes: Concepts and
Future Directions�������������������������������������������������������������������������347
Steven C. Ricke, Jessica C. Hacker, Kristin L. Yearkey, Zhaohao Shi,
Si Hong Park and Chase E. Rainwater
Introduction���������������������������������������������������������������������������������������������������������347
Whole Genome Sequencing and the Food Industry��������������������������������������������348
Characterizing Food System Microbiota�������������������������������������������������������������351
Sequencing Food System Microbiomes��������������������������������������������������������������352
Molecular-Based Microbial Diversity Profiling��������������������������������������������������355
Current Sequencing Strategies and Bioinformatics
Software Programs����������������������������������������������������������������������������������������������357
Microbiome Sequencing Strategies������������������������������������������������������������������357
Mothur��������������������������������������������������������������������������������������������������������������359
QIIME���������������������������������������������������������������������������������������������������������������360
QIIME Versus Mothur��������������������������������������������������������������������������������������360
Machine Learning and Potential Applications for Bioinformatics����������������������362
General Concepts����������������������������������������������������������������������������������������������362
Supervised Learning�����������������������������������������������������������������������������������������364
Unsupervised Learning�������������������������������������������������������������������������������������365
Reinforcement Learning�����������������������������������������������������������������������������������365
Conclusions and Future Directions����������������������������������������������������������������������366
Acknowledgments�����������������������������������������������������������������������������������������������367
References�����������������������������������������������������������������������������������������������������������367
Chapter 20: Student Cross-Training Opportunities for Combining Food,
Transportation, and Critical Infrastructure Cybersecurity
Into an Academic Food Systems Education Program������������������������375
Dale R. Thompson, Chase E. Rainwater, Jia Di and Steven C. Ricke
Introduction���������������������������������������������������������������������������������������������������������375
Security Challenges in the United States����������������������������������������������������������375
Food Security—General Concepts�������������������������������������������������������������������376
An Example of Data Generation and Food Security—The Integrated
Poultry Industry���������������������������������������������������������������������������������������������������378
The Need for Graduate-Level Students���������������������������������������������������������������381
Education Strategies��������������������������������������������������������������������������������������������382
Interdisciplinary Education�������������������������������������������������������������������������������382
xiv Contents

Proposed Curriculum����������������������������������������������������������������������������������������383
Mapping to a Standard Cybersecurity Framework�������������������������������������������386
Recruitment���������������������������������������������������������������������������������������������������������386
Placement�������������������������������������������������������������������������������������������������������������387
Conclusions���������������������������������������������������������������������������������������������������������387
References�����������������������������������������������������������������������������������������������������������388
Index��������������������������������������������������������������������������������������������������������������393
List of Contributors
Soohyoun Ahn University of Florida, Gainesville, FL, United States
Clara Assisi Purdue University, West Lafayette, IN, United States
Griffiths G. Atungulu University of Arkansas Division of Agriculture, Fayetteville, AR, United States
Mushin Aydin Arkansas State University, Jonesboro, AR, United States
Rachael E. Blevins University of Arkansas, Fayetteville, AR, United States
Todd R. Callaway University of Georgia, Athens, GA, United States
Roger Cochrane Kansas State University, Manhattan, KS, United States
Nicolae Corcionivoschi Agri-Food and Biosciences Institute, Northern Ireland, United Kingdom
Philip G. Crandall University of Arkansas, Fayetteville, AR, United States
Morgan L. Davis University of Arkansas, Fayetteville, AR, United States
Turki M. Dawoud University of Arkansas, Fayetteville, AR, United States; King Saud University,
Riyadh, Saudi Arabia
Jia Di University of Arkansas, Fayetteville, AR, United States
Andrea J. Etter Purdue University, West Lafayette, IN, United States
Peixin Fan University of Florida, Gainesville, FL, United States
Ester Grilli University of Bologna, Ozzano Emilia, Italy
Jessica C. Hacker University of Arkansas, Fayetteville, AR, United States
Shakaree Hale Alabama Agricultural and Mechanical University, Huntsville, AL, United States
Anne Huss BioMatrix International, Princeton, MN, United States
Armitra Jackson-Davis Alabama Agricultural and Mechanical University, Huntsville, AL,
United States
Jealae Jackson Alabama Agricultural and Mechanical University, Huntsville, AL, United States
Joy Jackson University of Texas-Arlington, Arlington, TX, United States
Kwangcheol C. Jeong University of Florida, Gainesville, FL, United States
Billie L. Johnson Simmons Pet Food, Emporia, KS, United States
Michael G. Johnson University of Arkansas, Fayetteville, AR, United States
Cassie Jones Kansas State University, Manhattan, KS, United States
Pravin Kaldhone University of Arkansas, Fayetteville, AR, United States
Sun Ae Kim University of Arkansas, Fayetteville, AR, United States
Alescia King Alabama Agricultural and Mechanical University, Huntsville, AL, United States
Ok Kyung Koo Gyeongsang National University, Jinju, Republic of Korea
Young M. Kwon University of Arkansas, Fayetteville, AR, United States

xv
xvi List of Contributors

Shinyoung Lee University of Florida, Gainesville, FL, United States


Keshun Liu United States Department of Agriculture, Agricultural Research Service, Aberdeen, ID,
United States
Aubrey Mendonca Iowa State University, Ames, IA, United States
Zeinab Mohammadi-Shad University of Arkansas Division of Agriculture, Fayetteville, AR,
United States; Nestlé Iran P.J.S. Co., Mohammadiyeh City, Iran
Russell Morgan Simmons Pet Food, Siloam Springs, AR, United States
Rkia Moutiq Iowa State University, Ames, IA, United States
Mary Muckey Kansas State University, Manhattan, KS, United States
Corliss A. O’Bryan University of Arkansas, Fayetteville, AR, United States
Gbenga A. Olatunde University of Arkansas, Fayetteville, AR, United States
Haley F. Oliver Purdue University, West Lafayette, IN, United States
Si Hong Park University of Arkansas, Fayetteville, AR, United States; Oregon State University,
Corvallis, OR, United States
Sean J. Pendleton University of Arkansas, Fayetteville, AR, United States
Andrea Piva University of Bologna, Ozzano Emilia, Italy
Chase E. Rainwater University of Arkansas, Fayetteville, AR, United States
Steven C. Ricke University of Arkansas, Fayetteville, AR, United States
Rafael Rivera U.S. Poultry & Egg Association, Tucker, GA, United States
Peter M. Rubinelli University of Arkansas, Fayetteville, AR, United States
Joshua C. Saldivar Stanford University School of Medicine, Stanford, CA, United States
Richard G. Shields Jr. Simmons Pet Food, Siloam Springs, AR, United States
Zhaohao Shi University of Arkansas, Fayetteville, AR, United States
Michael L. Sostrin University of Arkansas, Fayetteville, AR, United States; Walmart Stores, Inc.,
Bentonville, AR, United States
Christina L. Swaggerty United States Department of Agriculture/Agricultural Research Service,
College Station, TX, United States
Lin Teng University of Florida, Gainesville, FL, United States
Emalie Thomas-Popo Iowa State University, Ames, IA, United States
Dale R. Thompson University of Arkansas, Fayetteville, AR, United States
Brittany L. White Simmons Pet Food, Siloam Springs, AR, United States
Shantae Wilson University of Arkansas Division of Agriculture, Fayetteville, AR, United States
Kristin L. Yearkey University of Arkansas, Fayetteville, AR, United States
Chen Zhao Academy of State Administration of Grain, Beijing, People’s Republic of China
Xuhui Zhuang Academy of State Administration of Grain, Beijing, People’s Republic of China
Preface

Food safety is comprised of several rapidly changing research fields and public forums
(including microbiology, ecology, education, epidemiology, bioinformatics, economics,
globalization, among others) with numerous influences at both the scientific and the
economic level driving the directions it takes as these fields progress. In addition, the issues
associated with food safety that are considered of greatest concern continue to evolve as
food production systems become more complicated. Accordingly, food systems have
become more interconnected, resulting in many more potential sites for foodborne patho-
gen contamination that can impact other steps in food production, processing, and retail.
Foodborne pathogens possess the ability to intrude into any phase of food production and
contaminate the food products that they come in contact with. This includes animal feeds
consumed by food animals, resulting in colonization of the gastrointestinal tract and
potentially systemic infection of the host animal. Infected animals can become contami-
nated meat products that in turn can cross-contaminate processing equipment and other
meat products that are in contact with this equipment. As technologies such as whole
genome sequencing have become more common place, the ability for specifically identify-
ing and subsequently tracking a particular foodborne pathogen has vastly improved the
epidemiology and opportunity for a more complete resolution of foodborne disease
outbreaks. However, as the data sets grow, issues such as training the next generation of
food safety professionals to be proficient in data analytics and cybersecurity management
remain challenges for designing academic educational programs to efficiently accomplish
this training.
In this book, chapters have been generated to merge the concept of food safety being highly
integrated with the more recent developments in scientific research on foodborne pathogens
and the new methods developed to study them. Topics are designed to cover food systems and
foodborne ecology and how these approaches can be used to not only conduct research on
food safety and foodborne pathogens but also implement some of the emerging diagnostic
tools. This book will explore and discuss cutting edge research about emerging issues associ-
ated with foodborne pathogens and food safety systems at all levels from pet food to live
animal production, and finally food processing. Topics are designed to cover food systems
and foodborne pathogen ecology and how these approaches can be used to not only conduct

xvii
xviii Preface

research on food safety and foodborne pathogens but also develop educational materials for
training incoming professionals in the field on subjects, such as food systems data analytics
and cybersecurity.
More specifically, topics in this book will not only cover and update current food safety
thinking, but subsections of the book will also explore how to integrate food systems concepts
into pet food manufacturing and preharvest food safety practices and potential dietary amend-
ments to restrict foodborne pathogen colonization. This is followed by chapters on posthar-
vest food safety practices, current issues associated with certain foodborne pathogens, and
recent developments in interventions to limit their contamination in meat products and food
products such as juices. The last section includes chapters on application of emerging tech-
nologies such as whole genome sequencing for detection and microbial community profiling.
Finally, a chapter on the data analyses aspects of food systems as well as discussion on
cross-training education strategies to convey this knowledge to graduate students in food
science and computer engineering programs for preparing them to not only understand the
biological aspects of foodborne pathogens and food production systems but also develop their
ability to integrate these subjects into data analyses and cyberprotection programs. In sum-
mary, this book presents food safety as an integrative science among food production sys-
tems, the biology of pathogens defined by large data sets, their subsequent analyses, and
ultimately the overall interpretation and application in commercial food production.

Steven C. Ricke
University of Arkansas
Fayetteville, AR, United States
SECTION 1

Animal and Pet Feed Safety


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CHAPTE R 1

Changes in the Food Safety Landscape of


Pet Foods in the United States
Brittany L. White1, Billie L. Johnson2, Russell Morgan1, Richard G. Shields Jr.1
1Simmons Pet Food, Siloam Springs, AR, United States; 2Simmons Pet Food, Emporia, KS,
United States

History of Pet Food Types and Formats


In the United States, prepared food for pets actually began as table scraps, and it remains this
way in developing countries today. Feeding table scraps potentially presents food safety risks
associated with the lack of preservation, especially if the scraps are not fed immediately after
preparation. In the 1860s, James Spratt developed Spratt’s Dog Cakes which were biscuits for
pets, and initial commercial production in the United States began in 1895. This was shortly
followed by the introduction of Milk Bone in 1908. Clarence Gaines founded Gaines Food
Co. in the mid-1920s with 100-pound bags of dog meal and later introduced a pelleted
version called Gaines Krunchons. Gaines is also credited with the first food claiming com-
plete and balanced nutrition, which added nutritional adequacy to the food safety concerns
associated with pet food. Meals and pelleted diets tended to mirror processing options avail-
able for livestock feeds; however, the development of complete and balanced foods transi-
tioned the formulation to a blend of meat, milk, and cereal grains. The first canned food
emerged in the early 1920s with the launch of Ken-L-Ration by the Chappel Brothers as an
effort to find a market for horsemeat. This brand was the first to recommend mixed feeding of
dry and wet pet food in the 1930s. The canned food ultimately began to dominate the pet food
market, using coproducts of numerous meat and fish packers including Wilson Meat Packing,
Swift & Company, Armour & Company, and John Morrell & Company. In 1941, canned pet
food represented 91% of lbs sold. However, a can shortage during World War II resulted in a
transition from cans to glass containers. By 1946 the pet food market had shifted back to dry
foods, with wet pet food representing only 15% of the business volume. The initial canned
wet pet foods were primarily hermetically sealed in steel cans which were soldered, but the
can style ultimately transitioned to drawn and ironed cans of steel and more recently to
aluminum and plastic components. Today retortable pouches and semirigid tubs and trays
with heat seals compared with conventional metal seams have become quite popular and
therefore present new sealing and cooking challenges as overpressure is required to maintain
seal integrity.
Food and Feed Safety Systems and Analysis. http://dx.doi.org/10.1016/B978-0-12-811835-1.00001-4
Copyright © 2018 Elsevier Inc. All rights reserved. 3
4 Chapter 1

The industry changed dramatically in the 1950s with the launch of the extruded pet food
Purina Dog Chow, which almost instantly became the #1 brand nationally. Even in the
presence of this shift, wet pet food represented 60% of the volume in 1960, and today
represents closer to 25%. The 1980s brought about the addition of chunk-in-gravy style
canned food, whereas the loaf format formerly predominated. This required some formula-
tion changes to allow for chunk binding and also gravy viscosity. In the 1990s came the
introduction of Purina ONE which was the first product to have actual meat as the #1
ingredient in a dry, extruded formula. As the use of extruders in pet food application
expanded, product offerings extended beyond traditional dry kibble to shelf stable, soft
moist foods with Gaines-Burgers being the first soft moist offering in the 1960s. Soft moist
food formulation actually was an outgrowth of mink diet feeding and required extensive
use of hurdle technologies to ensure food safety at higher moistures. In 1981, Kibbles N’
Bits was introduced, which represented a new pet food format termed soft dry, which
contained dry and soft moist components mixed together in a single offering. This repre-
sented new challenges, namely how to prevent moisture migration from the soft moist
piece to the dry component. In 1996, product design changes were again required for soft
moist cat foods as the Food and Drug Administration (FDA) prohibited use of propylene
glycol in cat foods (21 CFR 589.1001) because it had been shown to cause abnormalities
in red blood cells (Christopher et al., 1989). Propylene glycol had been the most common
humectant used in soft moist formulations as it had an added benefit of being a miticide
(EPA, 2004).
There are several other emerging pet food formats that currently represent a much smaller
share of the pet food market, including pet treats. Freeze drying is a processing technique that
has been growing steadily at 45.5% per year since 2011 (Phillips-Donaldson, 2016). One pet
food processing category that has primarily been used for treats products is injection molding,
which has origins in the plastics industry. Of interest from a food safety standpoint is
Greenies, an injection molded treat that was launched in 1998 by S&M NuTec, LLC. By 2003
Greenies became the #1 treat by value sales, surpassing the long-standing top seller, Milk
Bone (http://www.petfoodindustry.com/articles/637-success-and-more). The brand was sold
in 2006 amid numerous complaints of choking and digestibility hazards associated with the
treat. Another category of pet treats that has emerged in recent years that represents unique
food safety challenges is dehydrated jerky treats. In the early 2000s, dehydrated chicken jerky
treats for dogs were primarily being produced in China. Between 2007 and 2013, the FDA
received 4500 reports of pet illness and 580 reported pet deaths due to consuming jerky treats
made in China. After extensive investigation, no specific cause was ever identified. However,
in 2013, the state of New York found traces of an antibiotic in the jerky treats made in China,
which was not allowed for consumption, so many major brands voluntarily recalled their
products being made in China, leaving shelf vacancy that was ultimately filled by jerky treats
made in the United States.
Changes in the Food Safety Landscape of Pet Foods in the United States 5

Pet Food Safety Issues Associated With Raw Materials


Alongside changes in product format, the ingredients used in pet food formulations have
changed over the years as well. Some of these changes have come either from the need to add
“good” ingredients or eliminate “bad” ingredients, when in fact many have both strengths and
weaknesses. Some ingredient components that have been traditionally considered as “antinutri-
tional” in animal agriculture because of adverse impacts on growth or food utilization, such as
tannins and phytates, may actually have some health-promoting activities (Thompson, 1993).
For the majority of pet food history, ingredients used were familiar, consistent with those used
in the animal feed industry, which were derived from domestic grains, rendered meals, or
from chemicals synthesized in countries with well-developed feed safety systems. Food safety
recalls in pet food were typically the result of lack of research on cumulative toxicity of
common feed compounds or mold toxins for pets. Ingredients with a long history of use, such
as corn, soy, and wheat, have fallen into disfavor with some pet parents and manufacturers
resulting in the need to replace their nutrient or functional contribution with other ingredients
that may have long-term effects that are not completely understood. Understanding toxicity of
nutrients and ingredient components in both pets and humans is quite challenging as chronic
effects of exposure during the lifetime of the pet must be considered. In addition, as with all
animals, researchers must also consider ingredient interactions that may either ameliorate or
exacerbate the effects of a single compound. The difficulty in understanding the long-term
safety of an ingredient is exacerbated by differences in the way in which different species
may react that may compound the effects, and utilization of pets in research, especially when
there is a risk of causing harm to the pet, has fallen into disfavor.
Use of new and different ingredients in pet foods may be driven by an effort by a brand to gain
market share. Brands have often capitalized on “free-from” claims in human and pet foods or
have focused highlighted ingredient quality or safety attributes to differentiate themselves from
ingredients used in other brands. The individualization of products for pets with special needs has
also resulted in a proliferation in the use of unique ingredients. Globalization has caused changes
in raw material sourcing as relocation of the ingredient further processing industry and a desire
for novel ingredients has required manufacturers to import many ingredients, forcing utilization
of unfamiliar materials from unfamiliar suppliers. The humanization of pets has also resulted in
use of unique and more expensive ingredients that tend to be more susceptible to economically
motivated adulteration (EMA). Because of the species dependence in food safety risks associated
with different compounds, the impact of such adulteration can have unintended effects.

Base Ingredient Selection

With increased recognition of food sensitivities in pets, there has also been increased use of
alternative meat and vegetable proteins and carbohydrate sources. In addition, the proliferation
6 Chapter 1

of clean label, simple diets with shorter history of use present an increased risk due to increased
predominance of a single ingredient in the food compared with formulas that rely on nutrient
contributions of a variety of ingredients. This issue has been exacerbated by current trends of
“wild” and “paleo” diets for pets, which are based on foods that are eaten by animals in the wild
and consist primarily of meats, fish, fruits, and vegetables and excludes grains.
The growing consumer trends of grain free foods and limited ingredient diets tend to use
alternative starch sources to replace conventional cereal grains. The risk this presents is
two-fold. First, it leads to the sourcing new raw materials outside of the United States and
also demands incorporation of ingredients that have a much less comprehensive food safety
evaluation. Even some of these ingredients that are familiar, such as potatoes, carry food
safety risks such as the presence of glycoalkaloids in coproducts derived from skins
(Nicholson et al., 1988; Smith et al., 1996). Alkaloids are also found in tomatoes and egg-
plant, which have emerged in recent pet food formulations (Friedman et al., 1996).

Humanization of Pet Food

The trend toward humanization of pet foods has also exposed pets to increased quality and/or food
safety risks. Following human food trends, there has recently been an interest in utilization of
organic, genetically modified (GM)-free, and sustainable ingredients. Meeting these needs
requires the use of a more-restricted raw material stream, which also increases susceptibility to
EMA. Furthermore, although the intent may not be an impact to food safety, negative conse-
quences can occur if harmful diluents or replacements are used. This was demonstrated by the
melamine contamination of wheat gluten and milk in 2007. In a publication by GMA (2010), it
was estimated that economic adulteration and counterfeiting of global food costs the food industry
10–15 billion dollars each year. Moore et al. (2012) reported that olive oil, milk, honey, and saffron
were the most common adulteration targets in a review of incidents occurring between 1980 and
2010. Fruit juices, especially those of superfruits, have also been known to be subject to dilution
with less costly juices. In a Congressional Research Service Report by Renee Johnson (2014), it
was also reported that fish and seafood fraud may be widespread in some markets. Even common
meats like beef were found in 2013 to be adulterated with horsemeat (Walker et al., 2013).
There has been increased recognition of the presence of several human metabolic defects in
pets such as copper storage disease and gluten intolerance in dog breeds and urinary crystals
in dogs and cats which in turn results in special dietary needs and restrictions. Many special-
ized diets with respect to nutrient content are best distributed under the direction of a veteri-
narian as, although they may be helpful to target animals, they may be inadequate for the
general pet population.
Consumption of what would be considered quality human foods by pets can cause a food
safety risk. In some cases, it results from species differences in metabolism, whereas in
others, it is from the fact that food products intended for humans are not meant to be sole
Changes in the Food Safety Landscape of Pet Foods in the United States 7

diets, so presence of high levels of some compounds may be well tolerated by humans but not
by pets. The toxicity of theobromine in dark chocolates, particularly baking chocolate, is well
recognized (Gans et al., 1980). Onions have historically been used in several pet rations;
however, it was found that in 1998 that cats fed baby food with onion powder developed
Heinz body anemia (Robertson et al., 1998) from the organosulfur compounds present in the
onions. In cats this occurred because of the susceptibility of hemoglobin to oxidation
(Christopher et al., 1995). Dogs also have reduced tolerance to organosulfur compounds
relative to humans because of lower erythrocyte catalase activity. In addition, although the
mechanism is not clearly understood, grapes and raisins are also thought to contain harmful
compounds, reportedly causing vomiting, diarrhea, and renal disorders. Furthermore, xylitol,
a sugar alcohol commonly used in food industry as a nonnutritive sweetener, can cause
hepatic failure in dogs (Dunayer and Gwaltney-Brant, 2006). These examples, among others,
demonstrate that care must be taken when developing pet foods intended to mimic human
food trends, as the consequences can be detrimental to the pet.

Nutrient Deficiencies and Excesses

An area that is often not considered when designing food safety systems is primary or second-
ary nutrient deficiency and toxicity; however, this has been the cause of several recalls in
recent history. Nutrient deficiencies can result from the lack of primary nutrients in the diet or
insufficient bioavailability of the nutrients present in the diet. Insufficient bioavailability can
occur both because of the form of the nutrient in the diet or from nutrient interactions, and
these are addressed in only very limited scope in AAFCO nutrient profiles (Official
Publication, 2016). This is clearly demonstrated by the history of dietary taurine recommen-
dations for cats. In spite of a long history of nutrition research, the fact that taurine was
required by the cat to prevent feline central retinal degeneration was not established until
1975 (Hayes et al., 1975). Further research established that taurine status was influenced by
dietary potassium level and dietary acidification for urine pH control (Dow et al., 1992). In
addition, requirements were higher for canned than for dry diets (Douglass et al., 1991).
Inconsistencies remained in taurine status resulting from food consumption which could not
be answered by total dietary taurine and it was found that bioavailability in raw materials
differed from that of synthetic taurine (Odle et al., 1993). Similarly, copper recommendations
in dry and canned pet foods differ (higher in dry diets) and status can be influenced by
nutrient balance and raw material bioavailability (Shields, 1998). Copper status is also
adversely affected by excess zinc intake (NRC, 2006). Based on some pet research (Morris
and Rogers, 1995), copper oxide was ultimately removed as a nutritional source of copper in
pet food due to lack of bioavailability. Assurance of nutritional adequacy therefore requires
understanding of ingredient nutrient content and bioavailability as well as interactions with
other dietary components. When new nutrient requirements are added which require addition
of unfamiliar ingredients, there remains a risk of nutrient deficiencies in spite of apparently
adequate analyzed dietary content.
8 Chapter 1

In contrast to the aforementioned situation, some sources of nutrients can improve bioavail-
ability relative to standard sources. Shurson et al. (1996) found that stability of vitamins in
premixes containing minerals was greater when the latter were provided as organic com-
plexes. Similarly, nutrient retention and reproductive performance have been reported to be
higher when dogs were fed mineral complexes compared with inorganic sources (Kuhlman
and Rompala, 1998; Lowe and Wiseman, 1998).
Besides nutrient deficiencies, excesses can also be of concern. Thyroid hormones are orally
active, and therefore, care must be taken to remove thyroid glands from food and feed ingre-
dients. Hamburger thyrotoxicosis has been found in humans fed ground beef contaminated
with bovine thyroid gland (Hedberg et al., 1987). Similarly, Stengel and Neiger (2012)
identified hyperthyroidism in dogs fed raw meat or fresh or dried gullets. Hyperthyroidism
has also been identified in cats, and Johnson et al. (1992) concluded that thyroid disorders
may result from wide swings in dietary iodine levels present in commercial cat diets.
Fat soluble vitamin excesses are also of concern because of the fact that they can accumulate
over time. With respect to vitamin D, there is some familiarity with toxicity because of expo-
sure of pets to rodenticides containing high levels of vitamin D. Morris and Rogers (1995)
expressed concerns regarding high levels of vitamin D in some cat foods. Subsequent analyti-
cal research by this same author, specifically with tuna, suggested that fish viscera and espe-
cially liver contain extremely high levels of vitamin D. The concern regarding excess vitamin
D has also expanded to dog foods with the reduction in allowed dietary maximums in the 2016
AAFCO Official Publication, likely resulting from the most recent research summary by NRC
(2006). Fortunately, some tissues contain high levels of vitamin A, which is known to help
ameliorate vitamin D toxicity in some animal species, including dogs (Aburto et al., 1998).
A portion of the vitamin D concern relates to impairment of calcium metabolism. An addi-
tional concern for canine diets is excess calcium, for which the maximum allowed levels for
large breed puppies was significantly lowered in the most recent AAFCO Official Publication
as a result of several articles in peer-reviewed publications. This research demonstrated that
large breed puppies may be unable to protect themselves against excessive calcium intake
(Hazewinkel et al., 1991).

Antinutritional Factors

Another food safety concern related to nutrient composition of foods is the potential presence
of antinutritional factors. Fish and some meat products are known potentially to contain
biogenic amines which arise from bacterial fermentation of amino acids. Although histamine
(from histidine) has received the most attention, especially with tuna, several others can arise
from other amino acids. The term “biogenic amines” refers to the nonvolatile amines, such as
cadaverine, putrescine, spermidine, spermine, tyramine, tryptamine, and histamine, produced
in fish and shellfish products harvested and not kept at ideal temperature conditions to prevent
Changes in the Food Safety Landscape of Pet Foods in the United States 9

spoilage. Spoilage microorganisms break down the amino acids and the toxic compounds
originate from the decarboxylation of specific free amino acids in fish or shellfish tissue
(Rawles et al., 1996). The most well-known health impact of biogenic amines is histamine
poisoning, which occurs a few minutes to several hours after the ingestion of foods containing
high levels of histamine. Primary symptoms in humans are skin rash, nausea, vomiting,
diarrhea, and so forth, which are mimicked in the companion animals symptoms as well. The
toxicity of histamine is potentiated by the other biogenic amines present such as putrescine,
cadaverine, and spermidine (Radosevich, 2016). A review of biogenic amines in fish species
was authored by Shalaby (1996). These biogenic amines appear to be stable to processing
(Veciana-Nogues et al., 1997a), and canned cat foods have been found to have measurable
levels of histamine (Guraya and Koehler, 1991). There is a multitude of biogenic amines that
can be present in these products, so Veciana-Nogues et al. (1997b) recommended using the
sum of biogenic amines as a quality attribute.
Some species of fish such as herring, alewives, anchovies, mackerel, and clams also contain
thiaminase which degrades thiamine (vitamin B1) and increases the dietary requirement of
thiamine, particularly if raw fish sources are used (Smith and Proutt, 1944). This antithiamine
effect in the diet can be exacerbated by the preservation of meats using sulfur dioxide as a
preservative as it also degrades the vitamin (Studdert and Labuc, 1991). Sodium metabisulfite
is another sulfur-containing preservative which has been recognized by FDA in 21 CFR
182.3766 as an antithiamine compound. Many vegetables are treated with sulfites to prevent
browning and this must be monitored as well.
Dioxin contamination has affected animal feeds globally on numerous occasions. Dioxins are
a group of chemically related compounds that are persistent environmental pollutants. The
World Health Organization reports that dioxins are highly toxic and can cause reproductive
and developmental problems, damage the immune system, interfere with hormones, and also
cause cancer (WHO, 2016). Although not specifically affecting pet foods, the use of ball clay,
which contains dioxins, as a conditioning and flow agent in soybean meal did impact ingredi-
ents which could have impacted the pet food supply. An instance of dioxin contamination in
soybean meal in Mississippi impacted the poultry feed supply in 1997. As a result, ball clay
was eliminated by FDA as an allowed conditioning agent in feed ingredients (FDA, 1999).
Numerous dioxin contamination cases have also occurred in the European Union (EU) feed
supply from contamination of fat sources with industrial oils not designed for food use. An
isolated contamination of zinc oxide in some mineral premixes designed for livestock
occurred in 2003. With many premix manufacturers preparing products for multiple species,
this represented an additional risk to the pet food industry at the time. There was also an
incident in 2007 where dioxin contamination was detected in guar gum used in the human
food supply in the EU. With the globalization of the raw material supply chain, this presented
a true risk to the US supply as this material is a commonly used thickener for both pet and
human foods, and, as a result, close monitoring of the supply was initiated.
10 Chapter 1

Prion Diseases

Prion diseases, also known as transmissible spongiform encephalopathies (TSEs), are neuro-
degenerative diseases that affect humans and animals and represent another significant food
safety concern in pet foods. Even sourcing from countries with effective food safety systems
was shaken with the discovery of TSEs including those of bovine origin (bovine spongiform
encephalopathy) where the infective agent was not of traditional microbial origin and was not
destroyed even with traditional rendering processes. Although no TSE has been identified in
dogs, a cat form has been identified (Gruffydd-Jones et al., 1991). This occurrence which
started in Western Europe and was later identified in Canada and then in the United States
caused trade disruptions and changes in the sources of meat materials used for pet food,
including discontinuation of the use of mechanically deboned ruminant materials. FDA
published research (Adam and Reeves, 1998; Heller et al., 2001) relating to the presence of
pentobarbital in dog foods. The presumption was that this resulted from rendering of eutha-
nized pets as a component of rendered meals and fat. This was not confirmed on species
identification and may have in fact resulted from formation of heterocyclic amines or other
compounds during processing which were identified as pentobarbital in the assay procedure.
With the concerns about TSEs at the time, recycling of animal species components being
placed into the food supply of the same species understandably caused concerns.

Selection of Food Additives

A key aspect of many pet food safety systems is the use of additives as hurdles to slow or
inhibit the potential for negative chemical or biochemical reactions. Some additives are used
to lower water activity, whereas others may lessen redox potential, lower acidity, control
oxidation, or reduce bacterial load (Leistner, 2000). Alternatively, some hurdles such as
microbial cultures and prebiotics are added to impart indirect health benefits for the animal.
One such additive is propylene glycol, which was once a commonly used humectant in soft
moist food formulations. After a long history of use, research results of Bauer et al. (1991)
found that consumption of this ingredient by cats resulted in Heinz body anemia. The “no
effect” level was found to be well below that required for humectants action; therefore, the
FDA banned it from use in cat food formulations. Earlier research with dogs did not result in
such effects (Weil et al., 1971), likely because of differences in the susceptibility of cats’ and
dogs’ erythrocytes to oxidative damage.
Besides humectants, the type of antioxidants has also shifted throughout pet food history.
Although antioxidants are generally thought to provide protection both in the food and in the
animal if absorbed, high levels or specific cellular conditions can result in these same com-
pounds acting as prooxidants (Palozza, 1998). At one time, ethoxyquin was the most commonly
used antioxidant in feed and pet food products as it was extremely effective. This compound
remains approved today at a maximum usage level of 150 parts per million (ppm) (21 CFR
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quills on their upper surface. There are also a few slight lanceolate
dark spots on the sides of the body, and on the tibial feathers.
Length to end of tail 23 1/2 inches, to end of wings 21 1/2, to end of
claws 18 3/4, to carpal joint 5 1/2; extent of wings 51 1/4; breadth of
gape 1 1/8; wing from flexure 17; tail 9 3/4; bill along the ridge 1 5/12;
tarsus 2 4/12; hind toe 1 1/12, its claw 1 5/12; middle toe 2 1/12, its claw
(worn) 11/12. Weight 2 lb., it being much emaciated.

The tongue, a, is 10 1/2 twelfths long, fleshy, deeply emarginate at


the base, having on its upper surface numerous orifices of mucous
crypts, towards the end narrowed, deeply concave, horny, with the
extremity rounded and very slightly emarginate. The œsophagus, b c
d e, is 7 1/2 inches long, wide, dilated into a large crop, c d, lying on
the right side; the proventriculus, f, is 1/2 inch in diameter, with a belt
of oblong glandules, arranged into four very prominent longitudinal
ridges, with deep grooves between them. The stomach, f g h, is
round, compressed, 1 1/2 inch in length, 1 inch 5 twelfths in breadth;
its muscular coat thin, composed of large fasciculi, not arranged into
distinct muscles; its inner coat soft, without horny epithelium, but
irregularly rugous, especially towards the pylorus, which has three
knobs or valves. The intestine, h i j k, is 36 1/2 inches long, 5 twelfths
in diameter at its anterior part, gradually contracting to 4 twelfths.
The rectum is 3 1/2 inches long, 1/2 inch in diameter at the
commencement; the cœca 2 twelfths long, 1 1/2 twelfth in diameter;
the cloaca, l m, globular. The right lobe of the liver is 2 inches 4
twelfths long, the left 2 inches 1 twelfth; the gall-bladder large.
The crop or dilatation of the œsophagus was nearly filled by two
excrescences from its inner surface, of a soft spongy texture, but not
ulcerated, or in any part scirrhous. The inner surface of the stomach
was similarly affected, but in a much less degree, and the pyloric
region was indurated. The intestines quite sound.

The trachea, m n o, is 6 inches long, considerably flattened, 5 1/2


twelfths, in breadth at the upper part, gradually diminishing to 4
twelfths. Its rings, about 78 in number, are ossified, the last large,
divided, arched, and with a broad membrane, o, intervening between
them and the first bronchial ring. The lateral or contractor muscles, p,
are very strong, as are the sterno-tracheal, q r, and there is a single
pair of inferior laryngeal muscles, s, inserted into the membrane
between the last ring of the trachea and the first of the bronchi. The
bronchial half rings 15, slender and cartilaginous.
BAND-TAILED PIGEON.

Columba fasciata, Say.


PLATE CCCLXVII. Male and Female.

In the course of Colonel Say’s expedition to the Rocky Mountains, a


single specimen of this large and handsome Pigeon was procured.
This individual was afterwards figured in the continuation of
Wilson’s American Ornithology. Many specimens however have
more recently been obtained by Dr Townsend, from whom I have
procured three pairs of adult and some young birds. Comparing
them with the figure above alluded to, I should consider it as having
been taken from a young male. In my plate are represented two
adult birds, placed on the branch of a superb species of Dogwood,
discovered by my learned friend, Thomas Nuttall, Esq., when on
his march toward the shores of the Pacific Ocean, and which I have
graced with his name! The beautiful drawing of this branch was
executed by Miss Martin, the amiable and accomplished sister of
my friend Dr Bachman. Seeds of this new species of Cornus were
sent by me to Lord Ravensworth, and have germinated, so that this
beautiful production of the rich valley of the Columbia River may now
be seen in the vicinity of London, and in the grounds of the
nobleman just mentioned, near Newcastle-upon-Tyne. Dr
Townsend’s notice respecting the bird here spoken of is as follows:

“The Band-tailed Pigeon is called by the Chinook Indians ‘akoigh
homin.’ It ranges from the eastern spurs of the Rocky Mountains
across to the Columbia River, where it is abundant. It arrived in 1836
in very great numbers, on the 17th of April, and continued in large
flocks while breeding. Their breeding places are on the banks of the
river. The eggs are placed on the ground, under small bushes,
without a nest, where numbers congregate together. The eggs are
two, of a yellowish-white colour, inclining to bluish-white, with minute
spots at the great end. These Pigeons feed upon the berries of the
black elder and the buds of the balsam poplar. When sitting in the
trees, they huddle very close together in the manner of the Carolina
Parrot, and many may be killed at a single discharge of the fowling-
piece. The flesh is tender and juicy, and therefore fine eating.”
Mr Nuttall has favoured me with an equally interesting notice. “This
large and fine Pigeon, always moving about in flocks, keeps in
Oregon only in the thick forests of the Columbia and the Wahlamet,
and during the summer is more particularly abundant in the alluvial
groves of the latter river, where throughout that season we
constantly heard their cooing, or witnessed the swarming flocks
feeding on the berries of the elder tree, those of the Great Cornel
(Cornus Nuttalli), or, before the ripening of berries, on the seed-
germs or the young pods of the Balsam poplar. The call of this
species is somewhat similar to that of the Carolina Dove, but is
readily distinguishable, sounding like a double suppressed syllable,
as h ’koo, h ’koo, h ’koo, h ’koo, uttered at the usual intervals, and
repeated an hour or two at a time, chiefly in the morning and
evening. They are said to breed on the ground, or in the low bushes,
but I did not find the nest, although I saw the birds feeding around
every day near Watpatoo Island. During the whole of this time they
keep in flocks, either in the poplars or elder bushes, and on being
started, sweep about like flocks of domestic pigeons, soon returning
to their fare, when they feed in silence, keeping a strict watch for
intruders. They remain on the lower part of the Columbia nearly the
whole year, late in the season (October and November) feeding
mostly on the berries of the Tree Cornel, but still they seem to
migrate some distance to the south, as the severity of the winter
approaches.”

Columba fasciata, Say, in Long’s Exped. to Rocky Mountains, vol. ii. p. 10.
Band-tailed Pigeon, Columba fasciata, Ch. Bonaparte, Amer. Ornith. pl.
viii, fig. 3, vol. i. p. 77.
Columba fasciata, Bonap. Synops. p. 119.
Band-tailed Pigeon, Nuttall, Manual, vol. i. p. 64.

Adult Male. Plate CCCLXVII. Fig. 1.


Bill straight, rather short, slender, compressed; upper mandible with
a tumid fleshy covering at the base, where it is straight in its dorsal
outline, convex towards the end, with a sharp-edged, declinate,
rather obtuse tip; lower mandible with the angle long and pointed,
the sides erect at the base, sloping outwards toward the end, the
edges sharp, the tip narrow but blunt. Nostrils medial, oblique, linear.
Head small, oblong, compressed; neck of moderate length; body full.
Feet short, strong; tarsus very short, rounded, with two anterior rows
of large hexagonal scales; the hind part fleshy with very small
scales; toes broad and flat beneath, marginate, with large scutella
above; the hind toe smallest, the lateral nearly equal, the middle toe
much longer. Claws of moderate size, arched, compressed, grooved
beneath, rather acute.
Plumage rather compact above, blended beneath, on the hind neck
strong, with metallic gloss. Wings long, the second quill longest, the
third only a twelfth of an inch shorter, the first six-twelfths shorter,
and a little longer than the fourth, the rest rather quickly graduated;
secondaries of moderate breadth and rounded. First quill with the
outer web narrower at the base than toward the end, the second and
third quills with their outer webs having a slight sinus and attenuated
toward the end. Tail of moderate length, rounded, of twelve broad
abruptly rounded feathers, of which the lateral is half an inch shorter
than the longest.
Bill yellow, with the tips black. Feet yellow, claws greyish-black. Bare
space around the eyes carmine. The head, fore neck, and breast are
of a light reddish-purple or wine-colour, which on the abdomen and
lower tail-coverts fades into whitish; a narrow half-ring of white on
the hind neck, the lower part of which is of a metallic brownish-green
tint. The upper parts are greyish-blue, darker, and tinged with brown
on the fore part of the back and scapulars; sides of the body and
rump greyish-blue. Alula, primary coverts, primary quills, and outer
secondaries brownish-black, very narrowly margined with brownish-
white. Tail greyish-blue at the base, much paler and tinged with
yellow toward the end, these colours being separated at the distance
of two inches from the tip by a band of black.
Length to end of tail 16 inches, to end of wings 13 3/4; wing from
flexure 9; tail 6 1/4; bill along the ridge 10/12, along the edge of lower
mandible 1 1/12; tarsus 1 1/12; hind toe 8/12, its claw 5 1/2/12; middle toe
1/2
14 /12, its claw 7/12.
Adult Female. Plate CCCLXVII. Fig. 2.
The female differs from the male only in having the tints a little duller,
and on the upper parts somewhat darker, with the black band on the
tail less decided, the middle feathers being but faintly marked with it.
Length to end of tail 15 1/2 inches.

It was omitted to mention that the minute spots on the eggs are
white.
Nuttall’s Dog-wood.

Cornus Nuttalli, Audubon.


This very beautiful tree, which was discovered by Mr Nuttall, on
the Columbia River, attains a height of fifty feet or more, and is
characterized by its smooth reddish-brown bark; large, ovate,
acuminate leaves, and conspicuous flowers, with six obovate, acute,
involucral bracteas, which are rose-coloured at the base, white
towards the end, veined and reticulated with light purple. The berries
are oblong, and of a bright carmine.
ROCK GROUS.

Tetrao rupestris, Gmel.


PLATE CCCLXVIII. Male and Female.

Whilst at Labrador, I was informed by Mr Jones, of whom I have


made mention on several occasions, that a smaller species of
Ptarmigan than that called the Willow Grous, Tetrao Saliceti, was
abundant on all the hills around Bras d’Or, during the winter, when
he and his son usually killed a great number, which they salted and
otherwise preserved; and that in the beginning of summer they
removed from the coast into the interior of the country, where they
bred in open grounds, never, like the Willow Grous, retreating to the
wooded parts. They seldom appear at Bras d’Or until the last of the
Wild Geese have passed over, or before the cold has become
intense, and the plains deeply covered with snow. While about his
house, they repair to the most elevated hilltops, from which the
violence of the winds has removed the snow. There they feed on the
mosses and lichens attached to the rocks, as well as on the twigs
and grasses scantily found in such places at that season. They keep
in great packs, and when disturbed are apt to fly to a considerable
distance, shifting from one hill to another often half a mile off.
Not having seen this species alive, and my drawing having been
taken from specimens kindly presented to me by my friend Captain
James Ross, R. N., I cannot do better than present you here with
the observations of Dr Richardson, as recorded in the Fauna
Boreali-Americana. “Hutchins reports that the Rock Grous is
numerous at the two extremities of Hudson’s Bay, but does not
appear at the middle settlements (York and Severn Factories),
except in very severe seasons, when the Willow Grous are scarce,
and Captain Sabine informs us that they abound on Melville
Peninsula, Lat. 74° to 75°, in the summer. It arrived there in its snow-
white dress, on the 12th of May 1820; at the end of that month the
females began to assume their coloured plumage, which was
complete by the first week in June, the change at the latter period
being only in its commencement with the males. Some of the males
were killed as late as the middle of June in their unaltered winter
plumage. In this respect the species differs from the Willow Grous
whose males first assume the summer colour. The Rock Grous is
found also on Melville Peninsula and the Barren Grounds, seldom
going farther south in winter than latitude 63° in the interior, but
descending along the coast of Hudson’s Bay to latitude 58°, and in
severe seasons still farther to the southward. It also occurs on the
Rocky Mountains as far south as latitude 55°. It exists in Greenland,
is common in Norway, is known in Sweden by the name of Sno
Rissa, and is the species most frequent in the Museums of France
and Italy under the name of Tetrao Lagopus. It is not a native of
Scotland. The Rock Grous in its manners and mode of living
resembles the Willow Grous, except that it does not retire so far into
the woody country in winter. Contrary, however, to what Hearne
says, it is frequent in open woods on the borders of lakes in that
season, particularly in the 65th parallel of latitude, though perhaps
the bulk of the species remains on the skirts of the Barren Grounds.
It hatches in June. The ground colour of the egg is, according to
Captain Sabine, a pale reddish-brown, and is irregularly spotted and
blotched with darker brown.” Specimens in my possession, coloured
as here described, average one inch and five-eighths in length, by
an inch and an eighth in breadth.
Tetrao rupestris, Gmel. Syst. Nat. vol. i. p. 751.—Lath. Ind. Ornith. vol. ii.
p. 640.
Tetrao (Lagopus) rupestris, Richards. and Swains. Fauna Bor.-Amer. vol.
ii. p. 354.
Rock Grous, Nuttall, Manual, vol. ii. p. 610.

Adult Male in Winter. Plate CCCLXVIII. Fig. 1.


Bill short, robust; upper mandible with the dorsal outline curved, the
ridge and sides convex, the edges overlapping, the tip declinate, thin
edged, but rounded; lower mandible with the angle short and wide,
the dorsal line convex, the back broadly convex, the sides rounded,
the edges inflected, the tip blunt. Nostrils basal, roundish, concealed
by feathers.
Head small, ovate; neck of moderate length; body bulky. Feet of
ordinary length, robust; tarsus feathered, as are the toes, the first toe
very small, the middle toe much longer than the lateral, which are
nearly equal, the inner being a little longer. Claws slightly arched,
depressed, broad, with thin edges and rounded at the tip.
Plumage compact, the feathers generally ovate and rounded; those
on the tarsi, toes, and soles oblong, with loose stiffish barbs. Wings
rather short, concave; the primaries strong, narrow, tapering,
pointed; the first an inch and seven-twelfths shorter than the second,
which is four-twelfths shorter than the third, this being the longest,
but only exceeding the fourth by a twelfth and a half. Tail rather
short, nearly even, of sixteen broad feathers, of which two are
incumbent, less strong, and longer than the rest by two-twelfths of an
inch.
Bill black; superciliary membrane scarlet; claws dusky, towards the
end yellowish. The plumage is pure white, with the exception of a
broad band of black from the upper mandible to the eye, and for a
short space behind it; the shafts of the six outer quills, which are
brownish-black, and all the tail-feathers, the two middle excepted,
they being of a deep greyish-black colour, with a terminal narrow
band of white.
Length to end of tail 13 1/2 inches, to end of wings 12; wing from
flexure 8; tail 4 1/2; tarsus 1 2/12; hind toe 2/12, its claw 5/12; middle
toe 11/12, its claw 8/12.
Male in Summer. Plate CCCLXVIII. Fig. 2.
In summer, the plumage differs little in texture, with the exception of
that on the feet, which is short and thin on the tarsi, worn on the
base of the toes, of which the soles and half of the upper surface are
denuded. The bill and claws are of the same colour as in winter; but
the plumage is variegated with black, reddish-yellow, and white. The
upper parts may be described as black, transversely and irregularly
banded and spotted with yellowish-red, the feather terminally
margined with white, there being on each feather several bars of
yellowish-red running from the margin inwards, but leaving a black
space in the centre. The lower parts are lighter, more broadly and
regularly barred with brownish-black and light reddish-yellow. The
feathers along the edge of the wing, the alula, primary coverts,
nearly all the secondary coverts, primaries and outer secondaries,
white; as are the lower surface of the wing, the axillar feathers, and
some of the feathers on the abdomen, as well as those on the feet,
the latter being soiled or tinged with yellowish or grey. The shafts of
the primaries are brownish-black, and the tail is black as in winter,
tipped with white, and with the lateral feathers having part of their
outer web white; the two middle feathers barred like the back. The
dimensions of an individual are as follows:

Length to end of tail 13 1/2 inches, to end of wings 11 1/2; wing from
flexure 7 10/12; tail 4 1/2; bill along the ridge 7/12; tarsus 1 2/12; middle
toe 1 1/2/12, its claw 6/12.

Female in Summer. Plate CCCLXVIII. Fig. 3.


The female does not differ materially from the male, the yellow
bands being only broader and lighter.
Very great differences are observed in the length and form of the
claws, they being in some individuals very long, thin-edged, and
tapering, to a rounded point; in others very short, being worn down to
the stump. This species is considerably smaller than the Ptarmigan
of Scotland, which it precisely resembles in its winter plumage. In its
summer plumage, however, it differs in having the markings larger;
and as yet no specimens have been obtained marked with undulated
slender, ash-grey, and dusky lines, in any degree approaching those
characteristic of the British bird in its autumnal plumage. The bill of
the Rock Grous is shorter and thicker than that of the Ptarmigan,
although the reverse has been alleged.
MOUNTAIN MOCKING BIRD.

Turdus montanus.
PLATE CCCLXIX. Male.

This interesting and hitherto unfigured species was procured on the


Rocky Mountains by Dr Townsend, who forwarded a single
specimen to Philadelphia, where I made a drawing of it. The
following notice by Mr Nuttall shews that it is nearly allied in its
habits to the Mocking Bird:—
“On the arid plains of the central table-land, betwixt the northern
sources of the Platte and the Colorado of the West, in the month of
June, we frequently heard the cheering song of this delightful
species, whose notes considerably resemble those of the Brown
Thrush, with some of the imitative powers of the Mocking Bird. For a
great part of the day, and especially early and late, its song resounds
through the desert plains, as it warbles to its mate from some tall
weed or bush of wormwood, and continues with little interruption
nearly for an hour at a time. We met with it in the plains exclusively,
till our arrival at Wallah Wallah, but we are not certain of having seen
it in any part of California, it being apparently entirely confined to the
cooler and open regions of the Rocky Mountains. Just before arriving
at Sandy Creek of the Colorado, while resting for refreshment at
noon, I had the good fortune to find the nest in a wormwood bush, on
the margin of a ravine, from whence the male was singing with its
unusual energy. It contained four almost emerald green eggs,
spotted with dark olive of two shades, more numerous towards the
greater end, the spots large and roundish. The nest itself was made
of small twigs and rough stalks, lined with stripes of bark and bison
wool. The female flew off to a little distance, and looked on her
unwelcome and unexpected visitor, without uttering either call or
complaint.”

Orpheus montanus, Mountain Mocking Bird, Townsend, Journal of Acad.


of Nat. Sciences of Philadelphia, vol. vii. p. 192.

Adult Male. Plate CCCLXIX. Fig. 1.


Bill of moderate length, rather slender, compressed, straightish,
pointed; upper mandible with the dorsal line slightly declinato-
arcuate, the sides convex toward the end, the edges sharp, with a
slight sinus close to the narrow declinate tip; lower mandible with the
angle short and narrow, the dorsal line straight, the edges sharp and
a little declinate at the end, the tip narrow; the gape-line very slightly
arched.
Head oblong, of ordinary size; neck rather short, but somewhat
slender. Feet longish, rather strong; tarsus compressed, anteriorly
covered with seven large scutella, sharp-edged behind; toes of
moderate length, slender, the hind toe stout, the lateral nearly equal,
the anterior united for a short space at the base. Claws slender,
arched, compressed, acute.
Plumage soft and blended. Wings of moderate length, rounded, the
first quill short, the third and fourth longest, the second and fifth
equal, and about a quarter of an inch shorter than the fourth. Tail
long, rounded, of twelve rather narrow rounded feathers.
Bill dark-brown, the base of the lower mandible paler. Feet yellowish-
brown, claws dusky. The general colour of the upper parts is greyish-
brown, the tips of the secondary coverts, the edges of the primary
quills, and a large spot at the end of the three lateral tail-feathers,
white; the lower parts whitish, marked with triangular dusky spots, of
which there is a distinct line from the base of the bill; the throat, the
middle of the breast, the abdomen, and lower tail-coverts unspotted.
Length to end of tail 8 inches, to end of wings 5 3/4; wing from flexure
1/2
3 9/12; tail 3 1/2; bill along the ridge 7 /12; tarsus 1 2/12; hind toe 4/12,
1/
its claw 4/12; middle toe 8/12, its claw 3 4 /12.
VARIED THRUSH.

Turdus nævius, Gmel.


PLATE CCCLXIX. Adult Male.

Of this beautiful Thrush, of which a figure not having the black band
running quite across the breast, as is the case in the adult male, is
given by Mr Swainson, in the Fauna Boreali-Americana, Dr
Richardson speaks as follows:—“This species was discovered at
Nootka Sound, in Captain COOK’S third voyage, and male and
female specimens, in the possession of Sir Joseph Banks, were
described by Latham: Pennant has also described and figured the
same male. The specimen represented in this work was procured at
Fort Franklin, lat. 65 1/4°, in the spring of 1826. We did not hear its
song, nor acquire any information respecting its habits, except that it
built its nest in a bush, similar to that of the Merula migratoria. It was
not seen by us on the banks of the Saskatchewan; and, as it has not
appeared in the list of the Birds of the United States, it most probably
does not go far to the eastward of the Rocky Mountains in its
migrations north and south. It may perhaps be more common to the
westward of that ridge.”
Dr Richardson’s conjecture as to the line of march followed by it
has proved to be correct, Dr Townsend and Mr Nuttall having
found it abundant on the western sides of the Rocky Mountains. The
former of these zealous naturalists informs me that he “first found
this Thrush on the Columbia River in the month of October, and that
it becomes more numerous in winter, which it spends in that region,
though some remove farther south. It there associates with the
Common Robin, Turdus migratorius, but possesses a very different
note, it being louder, sharper, and quicker than those of the latter,
and in the spring, before it sets out for its yet unascertained
breeding-place, it warbles very sweetly. It is called Ammeskuk by the
Chinooks.”
Mr Nuttall’s notice respecting it is as follows:—“Of this bird, whose
manners so entirely resemble those of the Common Robin, we know
almost nothing. They probably breed as far north as Nootka, where
they were first seen by the naturalists of Cook’s expedition. On the
Columbia they are only winter birds of passage, arriving about
October, and continuing more or less frequently throughout the
winter. At this time they flit through the forest in small flocks,
frequenting usually low trees, on which they perch in perfect silence,
and are at times very timorous and difficult of approach, having all
the shy sagacity of the Robin, and appearing at all times in a very
desultory manner.”
The numerous specimens of this Thrush in my possession have
enabled me to compare it with Turdus migratorius, and another new
Thrush from Chili. On examining the tail, from the shape of which Mr
Swainson considers this species allied to our Mocking Bird, I found
its form, length, and extent beyond the wings, to correspond almost
exactly with those of the tail of our Robin; and, if it proves true that
the Varied Thrush forms a nest bedded with mud, it will strengthen
my opinion that both these and the Chilian species are as nearly
allied as possible, and therefore ought to be considered as true
Thrushes, of which, to assume the language of systematic writers,
Turdus migratorius is the type in America, whilst Turdus Merula is
that of Europe.
The two figures in my plate were taken from adult males shot in
spring. You will find a figure of the female in Plate CCCCXXXIII.
Turdus nævius, Gmel. Syst. Nat. vol. i. p. 817.—Lath. Ind. Ornith. vol. i. p.
331.
Orpheus meruloides, Thrush-like Mock-bird, Richards. and Swains.
Fauna Bor.-Amer. vol. ii. p. 187.

Adult Male, Plate CCCLXIX. Figs. 2, 3.


Bill of moderate length, rather strong, compressed, acute; upper
mandible with its dorsal outline slightly arched, the ridge narrow, the
sides convex toward the end, the edges sharp, overlapping, destitute
of notch, there being in its place an extremely slight sinus, the tip a
little declinate; lower mandible with the angle rather long and narrow,
the dorsal line very slightly convex, the ridge narrow, the sides erect
and convex, the edges sharp and slightly decurved towards the
narrow, rather obtuse, tip. Nostrils basal, oblong, half closed by a
horny operculum. Head of moderate size, ovate, convex anteriorly;
neck rather short, body moderately full. Feet of ordinary length,
rather stout; tarsus compressed, anteriorly covered with a long plate
and four inferior scutella, posteriorly with two long plates meeting at
a very acute angle. Toes rather large, the first strongest, the lateral
nearly equal, the third and fourth united as far as the second joint of
the latter. Claws rather large, moderately arched, much compressed,
acute.
Plumage soft and rather blended. Wings of moderate length, broad,
rounded; the first primary extremely short, being about a fifth of the
length of the third, which is longest, but scarcely exceeds the fourth;
the second four-twelfths shorter than the third. Tail large, rather long,
nearly even, of twelve broad rounded feathers.
Bill black, with the basal half of the lower mandible yellow; iris hazel;
feet and claws flesh-coloured. The general colour of the upper parts
is a deep leaden-grey, darker on the head, the feathers very
narrowly margined with brown; the quills and tail-feathers dusky, the
outer webs of the latter tinged with grey, and their tips white; the lore
dusky; a band of reddish-orange passes from over the fore part of
the eye down the side of the neck, and almost meets its fellow on the
hind part; two conspicuous bands of the same cross, the wing
obliquely being formed of the tips of the first row of small coverts,
and those of the secondary coverts; the outer webs of the primary
coverts about the middle, a band on the primaries near the base,
part of the outer webs towards the end, and the tips of the
secondaries, also pale reddish-orange. The lower parts in general
are reddish-orange, paler behind; a band of greyish-black passes
down the side, and crosses the lower part of the neck, where it is
almost pure black; the feathers of the sides are tipped with light grey;
those of the middle of the abdomen are white; and the lower tail-
coverts are tipped with the latter colour. The axillary feathers are
white, tipped with grey; the smaller coverts grey, tipped with reddish-
white, the primary coverts grey, the secondary nearly white, of which
also there is a bar formed by part of the inner webs of the quills.
Length to end of tail 10 1/4 inches; wing from flexure 5 1/4; tail 3 10/12;
1/2
bill along the ridge 10/12, along the edge of lower mandible 1 1 /12;
tarsus 1 1/4; hind toe 5 1/2/12, its claw 5 1/2/12; middle toe 10 1/2/12, its
claw 4/12.
Adult Female. Plate CCCCXXXIII. Fig. 6.
The female, which is scarcely smaller than the male, is coloured in
the same manner; but the upper parts are strongly tinged with olive-
brown; the reddish-orange bands are much paler, the tail-feathers
are margined with dull reddish-brown; the band on the lore, down the
sides of the neck, and across it, is light greyish-brown; the orange
tint of the lower parts is much paler; the lower wing-coverts have no
tinge of red, and part of the breast and abdomen is nearly pure
white.
Length to end of tail 10 inches; wing from flexure 5 2/12; tail 3 8/12; bill
along the ridge 10/12; tarsus 1 1/4; middle toe and claw 1 3/12.

The plant represented on the plate is the American Mistletoe,


Viscum verticillatum, on the berries of which several of our Thrushes
occasionally feed, as the Mistle thrush, Turdus viscivorus, is said to
do on those of Viscum album. It is found in almost every part of the
United States, growing chiefly on oaks and apple-trees.

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