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Toxoplasmosis of Animals
and Humans
Toxoplasmosis of Animals
and Humans
J. P. Dubey
Third edition published 2022
by CRC Press
6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487-2742
and by CRC Press

2 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN
© 2022 Government of USA
First edition published by CRC Press 1988
Second edition published by CRC Press 2010
CRC Press is an imprint of Taylor & Francis Group, LLC
Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for
the validity of all materials or the consequences of their use. The authors and publishers have attempted to trace the copyright holders of all
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ISBN: 9780367543129 (hbk)

ISBN: 9781032058238 (pbk)
ISBN: 9781003199373 (ebk)
Typeset in Times
by codeMantra
Dedicated
This book is dedicated to my family without whose support I would not have
reached here. I was born in a family of priests in a remote village in India.
Our family profession for hundreds of years was preaching and spreading
“vedic” knowledge. My family name, Dubey, means the people who mastered
2 of 4 ancient vedas. Until recently,priesthood was an inherited profession.
My parents had no formal education and chose me to continue the family
profession of priesthood. The village had grade 4 school and I did not attend
it until 9-year-old. Considering that I was bright, my uncle, Pandit Girwar
Lal Dubey (elder brother of my father and head of family), took me to his
house in Delhi. He did not have children of his own and his house was like an
orphanage with meager resources. He had a lower level clerical job in Indian
Railways. I never had money to buy books or pay tution. I credit my success
and memory having to study from borrowed books. After obtaining 2-year
college degree, prospects for further education were zero (because my uncle
had retired with no pension) until my classmate (Avinash Arora) encouraged
me to apply to a newly opened veterinary school, Mhow, India because there
were no tuition or dormitory charges. I excelled in veterinary school and that
paved my way for free graduate studies, Ph.D., and yes marriage to my life
partner, Niti Dubey (see reference370). Nothing was planned in my life but God
has been watching over me. I am sure my parents and uncle have been watching
my achievements from heaven and happy that I have not forgotten the family
profession of spreading knowledge, albeit scientific. I appreciate the love and
support of both my sons, Ravi and Raj, who had to make sacrifices during
their growing up because I was either working in the laboratory or writing at
home. The smiling faces of my four granddaughters (Anjeli, Shalini, Ria, and
Mya and their mothers Meena and Ritu) provide incentive to keep working.
Finally, I am indebted to my wife, Niti Dubey, without whose support and love
I could not have succeeded in completing this book, and life in general.
J.P. Dubey
Contents
List of Abbreviations�� xvii
Preface to Third Edition�� xix
Author�� xxi
Chapter 1
Introduction and History of Toxoplasma gondii��1
1.1 Introduction and History1
1.2 Discovery of the Parasite1
1.3 Transmission1
1.3.1 Congenital Transmission��1
1.3.2 Carnivorism��4
1.3.3 Fecal–Oral, Sexual Cycle, and Discovery of the Oocyst��4
1.3.4 Discovery of the Full Life Cycle and Developmental Stages in the Intestine of Cats��5
1.4 Gratitude6
Chapter 2
Biology of Toxoplasma gondii��7
2.1 Taxonomic Classification 7
2.2 Structure and Life Cycle 7
2.2.1 Tachyzoite��7
2.2.1.1 Structure��7
2.2.1.2 Host Invasion��12
2.2.1.3 Multiplication by Endodyogeny��13
2.2.2 Bradyzoites and Tissue Cysts��16
2.2.2.1 Structure��16
2.2.2.2 Tissue Cyst Distribution in Host Tissues��18
2.2.2.3 Tissue Cyst Rupture and Reactivation��19
2.3 Life Cycle in the Definitive Host, the Cat 22
2.3.1 Bradyzoite-Induced Cycle��27
2.3.1.1 Enteroepithelial Cycle��27
2.3.2 Oocyst-Induced Cycle��36
2.3.3 Tachyzoite-Induced Cycle��36
2.4 Life Cycle in the Intermediate Hosts, Including Humans and Cats 38
2.4.1 Oocyst-Induced Infections��38
2.4.1.1 Mice��38
2.4.1.2 Rats��41
2.4.2 Bradyzoite-Induced Infections��44
2.5 Molecular Biology 44
2.6 Transmission 44
2.6.1 Transmission by Oocysts��44
2.6.1.1 Cats are Everywhere��44
2.6.1.2 Fatal Feline Attraction��55
2.6.1.3 Excretion of Oocysts by Naturally Infected Domestic Cats��55
2.6.1.4 Excretion of Oocysts by Naturally Infected Wild Felids��62
2.6.1.5 Dispersal of Oocysts in the Environment��63
2.6.1.6 Environmental Resistance of Oocysts��64
2.6.1.7 Detection of Oocysts in Environmental Samples��66
2.6.1.8 Infectiousness of the Oocyst for Humans��67
2.6.2 Transmission by Tissue Cysts��67
2.6.2.1 Effect of Freezing, Salting and Heat, Irradiation, High Pressure, and Vacuum Packing
on Tissue Cysts��67
vii
viii Contents
2.6.3 Transmission by Tachyzoites��68

2.7 Epidemiology 68
2.8 Host–Parasite Relationships 69
2.8.1 Pathogenesis in General��69
2.8.2 Ocular Toxoplasmosis��75
2.8.3 Pathogenesis of Abortion��75
2.9 Diagnosis 77
2.9.1 Serologic��78
2.9.1.1 Dye Test��80
2.9.1.2 IHA��81
2.9.1.3 MAT��81
2.9.1.4 IFA��82
2.9.1.5 ELISA��82
2.9.1.6 Western Blotting��85
2.9.1.7 Avidity Tests��85
2.9.1.8 Rapid Tests��85
2.9.2 Detection of T. gondii DNA��85
2.9.3 Immunohistochemical Staining��85
2.10 Validation of Serology by Isolation of Viable T. gondii86
2.11 Protective Immunity and Immunoprophylaxis 87
2.12 Treatment 88
2.13 Prevention and Control 88
2.13.1 Humans��88
2.13.2 Cats��89
2.13.3 Zoos��89
Chapter 3
Techniques for Studying Toxoplasma gondii��91
3.1 aboratory Maintenance of T. gondii
L 91
3.1.1 Cultivation��91
3.1.1.1 Tachyzoites��91
3.1.1.2 Tissue Cysts��92
3.1.1.3 Merozoites Enteroepithelial Stages��92
3.1.1.4 Oocysts��93
3.2 Isolation of T. gondii 95
3.2.1 Bioassays of Tissues in Mice��95
3.2.1.1 Body Fluids��95
3.2.1.2 Acutely Infected Tissues��95
3.2.1.3 Chronically Infected Tissues��95
3.2.1.4 Bioassays of T. gondii in Cats��96
3.2.1.5 Inoculation and Examination of Mice for T. gondii��97
3.3 Cryopreservation98
3.4 Diagnosis99
3.4.1 Cytology, Histopathologic, and Immunohistochemical Procedures��99
3.4.1.1 Diagnosis of Protozoal Abortion��99
3.5 Immunohistological Examinations100
3.6 Serologic Procedures100
3.6.1 Modified Agglutination Test��100
3.6.2 Indirect Fluorescent Antibody Test�� 101
3.6.3 ELISA�� 101
3.6.3.1 General Procedure: Antigen Source�� 101
3.6.4 Procedure for Avidity ELISA��102
3.7 Polymerase Chain Reaction103
3.7.1 Extraction of DNA from Feces��103
Contents ix
3.7.2 Protocol for the Extraction of DNA from Fresh or Fixed Materials��104
3.7.3 Detection of T. gondii in Soil Samples��104
3.7.4 Options for Transporting DNA Prior to Analysis��104
3.8 Safety Concerns and Precautions While Working with T. gondii 104
Chapter 4
Toxoplasma gondii Infections in Humans (Homo sapiens)��107
4.1 Serologic Prevalence107
4.2 Parasite Prevalence109
4.3 Clinical Infections109
4.3.1 Postnatally Acquired Toxoplasmosis��109
4.3.1.1 Toxoplasmosis Outbreaks and Lessons Learned�� 114
4.3.1.2 Brazil, Hotspot for Outbreaks�� 116
4.3.1.3 Meatborne Outbreaks�� 118
4.3.1.4 Multi-factorial Outbreaks in French Guiana and Suriname��120
4.3.1.5 Conclusions�� 121
4.3.2 Prenatally Transmitted (Congenital) Toxoplasmosis��122
4.4 Parasite Strain Genetics and Clinical Toxoplasmosis in General129
4.5 Diagnosis129
4.5.1 Lymphoglandular Toxoplasmosis��129
4.5.2 In the Immune-Deficient Patient��130
4.5.3 In Ocular Toxoplasmosis��130
4.5.4 In the Pregnant Woman��130
4.5.5 In the Fetus�� 131
4.5.6 In the Baby�� 131
4.6 Treatment131
4.7 Prevention132
4.7.1 Immunosuppressed Patients��132
4.7.2 Prophylactic Treatment during Pregnancy��132
Acknowledgments133
Chapter 5
Toxoplasma gondii Infections in Cats��135
5.1 Domestic Cats135
5.1.1 Prevalence��135
5.1.1.1 Serologic Investigations��135
5.1.1.2 Isolation of Viable T. gondii in Tissues of Cats�� 145
5.1.1.3 Detection of T. gondii DNA in Tissues of Cats�� 145
5.1.1.4 Prevalence of T. gondii Oocysts in Cats��150
5.1.2 Clinical Infections and Oocyst Excretion��150
5.1.3 Genetic Types of T. gondii in Domestic Cats��153
5.1.4 Experimental Infections in Cats��153
5.1.4.1 Immunization of Cats to Prevent Oocyst Excretion��153
5.1.4.2 Serological Responses of Experimentally Infected Cats��153
5.1.4.3 Pathogenesis of Congenital Infection��157
5.2 Other Felids157
5.2.1.2 Isolation and Genetic Characterization of Viable T. gondii from Wild Felids��164
5.2.1.3 Detection of T. gondii DNA from Wild Felids��164
5.2.1.4 Prevalence of T. gondii Oocysts in Wild Felids��164
5.3 Clinical Toxoplasmosis in Wild Felids165
Acknowledgments166
x Contents
Chapter 6
Toxoplasma gondii Infections in Dogs (Canis familiaris)�� 167
6.1 Natural Infections167
6.1.1 Serologic Investigations�� 167
6.1.2 Isolation of Viable T. gondii from Tissues of Apparently Healthy Adult Dogs�� 167
6.1.3 Detection of T. gondii DNA in Tissues of Dogs�� 176
6.1.4 Detection of T. gondii DNA in Feces of Asymptomatic Dogs�� 176
6.1.5 Clinical Infections�� 176
6.2 Experimental Infections178
6.3 Genetic Diversity of T. gondii in Dogs179
6.4 Conclusions180
Chapter 7
Toxoplasma gondii Infections in Pigs (Sus scrofa)�� 181
7.1 Domestic Pigs 181
7.1.1 Natural Infections in Domestic Pigs�� 181
7.1.1.1 Serologic Investigations�� 181
7.1.1.2 Serological Tests Comparison on Sera from Naturally Infected Pigs��193
7.1.1.3 Isolation of Viable T. gondii from Pig Tissues��195
7.1.1.4 Detection of T. gondii DNA in Pig Tissues��195
7.1.1.5 Clinical Toxoplasmosis��195
7.1.2 Experimental Infections��203
7.1.2.1 Clinical��203
7.1.2.2 Immunity��209
7.1.2.3 Congenital Toxoplasmosis��209
7.1.2.4 Tissue Cyst Formation and Persistence of T. gondii in Tissues��209
7.1.2.5 Viability of T. gondii in Cured Pork Products��209
7.1.2.6 Survival of T. gondii in Vacuum-Packed Pork��209
7.2 T. gondii Infections in Wild Swine (Boars)209
7.2.1 Seroprevalence��209
7.2.2 Isolation of Viable T. gondii from Tissues of Wild Swine��209
7.2.3 Detection of T. gondii DNA from Tissues of Wild Swine�� 216
7.2.4 Congenital Toxoplasmosis in Wild Swine�� 216
7.3 Genetic Types of T. gondii in Pigs216
Chapter 8
Toxoplasma gondii Infections in Sheep�� 217
8.1.1 Serologic Investigations�� 217
8.1.2 Isolation and Genetic Characterization of T. gondii from Tissues of Sheep��236
8.1.3 Tissue Cyst Burden��236
8.1.4 Detection of T. gondii DNA in Sheep��244
8.1.5 Abortion and Lamb Losses Due to Toxoplasmosis��244
8.1.6 Venereal Transmission��247
8.1.7 Genetic Variability of T. gondii in Sheep��247
8.2.1 Clinical Disease in Orally Inoculated Sheep��256
8.2.2 Pathogenesis of Abortion��256
8.2.3 Reducing Parasite Load by Immunization��256
8.2.4 Reducing Abortion by Immunization of Ewes��256
8.2.5 Chemoprophylaxis��256
8.3 Diagnosis and Pathogenesis of T. gondii-Induced Abortion257
8.4 Reducing Losses in Sheep Due to Toxoplasmosis through Prophylaxis258
Acknowledgments258
Contents xi
Chapter 9
Toxoplasma gondii Infections in Goats (Capra hircus)��259
9.1.1 Serologic Investigations��259
9.1.2 Isolation of Viable T. gondii from Tissues of Goats��270
9.1.3 Detection of T. gondii DNA in Blood, Milk, and Tissues of Goats��270
9.1.4 Clinical Infections��270
9.1.5 Clinical Toxoplasmosis in Adult Goats��270
9.1.6 Neonatal Toxoplasmosis��272
9.1.7 Genetic Diversity of T. gondii in Goats��274
9.2.1 Earlier (pre-1988) Observations��274
9.2.2 Post-1988 Observations on Abortion and Protection��275
9.2.3 Excretion of T. gondii in Milk of Experimentally Infected Goats��275
9.2.4 Venereal and Congenital Transmission of T. gondii��275
9.2.5 Tissue Parasitization at 30 and 90 Days and Survival of Tissue Cysts in Vacuum Packing in
Goats Fed T. gondii Oocysts��276
9.2.5.1 Clinical, Biochemical, Serological��276
9.2.5.2 Vacuum Packing Survival��277
9.2.6 T. gondii in Goat Milk and Public Health Significance��277
9.3 Treatment/Prophylaxis for Abortion277
Chapter 10
Toxoplasma gondii Infections in Cattle (Bos spp.)��279
10.1.2 Isolation of Viable T. gondii��288
10.1.3 Detection of T. gondii DNA from Cattle Tissues��288
10.1.4 Clinical Toxoplasmosis, Congenital Infections, and Abortion��290
10.2.1 Persistence of T. gondii in Tissues or Fluids��290
10.2.2 Congenital Transmission��290
10.3 Public Health Significance of Toxoplasmosis in Cattle291
10.3.1 Beef��291
10.3.2 Milk��291
10.4 Genetic Diversity of T. gondii in Cattle291
10.5 Conclusions292
Acknowledgments292
Chapter 11
Toxoplasma gondii Infections in Water Buffaloes (Bubalus bubalis)��293
11.2 Attempts at Isolating Viable T. gondii 294
11.3 Presence of Tissue Cysts in Tissues or Milk294
Chapter 12
Toxoplasma gondii Infections in Equids (Horse, Donkey, Mule)��295
12.1.1 Serologic Investigations in Horses��295
12.1.2 Serologic Prevalence in Donkeys��295
12.1.3 Serologic Prevalence in Mules��295
12.1.4 Serologic Prevalence in Wild Equids��295
12.2 Isolation of Viable T. gondii from Tissues of Horses and Donkey295
xii Contents
12.3 Prevalence of T. gondii DNA300

12.5 Genetic Diversity301
12.6 Public Health and Social Aspects of T. gondii Infections in Horses and Donkeys301
Chapter 13
Toxoplasma gondii Infections in Camels (Camelus spp.)��303
13.1.2 Isolation of Viable T. gondii from Tissues��303
13.1.3 Prevalence of T. gondii DNA in Camel Tissues��303
13.1.4 Presence of T. gondii in Camel Milk��303
Chapter 14
Toxoplasma gondii Infections in South American Camelids (Lama spp.)��305
14.1 Seroprevalence305
14.2 Isolation and Molecular Characterization305
14.3 Clinical Toxoplasmosis305
Chapter 15
Toxoplasma gondii Infections in Chickens (Gallus domesticus)��307
15.1.1.2 Isolation of Viable T. gondii��307
15.1.1.3 Detection of T. gondii DNA�� 319
15.1.1.4 Detection of T. gondii by Histopathology and Immunohistochemistry�� 321
15.1.1.5 Comparison of Serology, PCR Techniques, and Bioassay for the Detection of T. gondii�� 321
15.1.2 Clinical Infections�� 321
15.1.3 Epidemiology and Use of Sentinel Chickens�� 321
15.1.4 Genetic Diversity of Viable T. gondii Isolates��322
15.2.1 Clinical and Diagnosis��322
15.2.2 Effect of Breed/Strain of Chickens, T. gondii Genotype on Toxoplasmosis in Chickens��325
15.2.3 Effect of T. gondii Genotype, Seroconversion, Tissue Parasitization, and Chemoprophylaxis on
Toxoplasmosis in Chickens��325
15.2.4 Concurrent Infections��325
15.3 Conclusions325
Chapter 16
Toxoplasma gondii Infections in Other Avian Species (Excludes Gallus domesticus)��327
16.1 Turkeys (Meleagris gallopavo)327
16.2 Ducks (Anas spp.) and Geese332
16.3 Ostriches (Struthio camelus) and Other Ratites332
16.4 Other Wild Avian Species333
16.4.1 Carnivorous Birds��333
16.4.2 Herbivorous/Insectivorous Birds��338
16.4.3 Migratory Birds��350
16.5 Clinical Toxoplasmosis in Wild Birds351
16.6 Genetic Diversity of T. gondii Isolates352
16.7 Conclusions352
Contents xiii
Chapter 17
Toxoplasma gondii Infections in Non-human Primates��355
17.1 Natural Infections 355
17.1.2 Clinical Toxoplasmosis��355
17.1.3 Genetic Diversity��367
17.2 Experimental Infections 367
17.3 Conclusion 368
Chapter 18
Toxoplasma gondii Infections in Australasian Marsupials��369
18.1 Introduction369
18.2 Zoo Animals Outside of Australia and New Zealand369
18.3 Infections in Free-Range Marsupials in Australasia369
18.3.1 Koalas (Phascolarctos cinereus)��369
18.3.2 Kangaroos��369
18.3.3 Wombats (Vombatus ursinus)��371
18.3.4 Brush-tailed Rock Wallaby (Petrogale penicillata)��371
18.3.5 Eastern Quoll (Dasyurus viverrinus)��371
18.3.6 Congenital/Neonatal Transmission��371
18.3.7 Other Marsupials��371
18.4 Diagnosis371
18.5 Treatment372
18.6 Genetic Diversity of T. gondii from Marsupials372
18.6.1 Free-Range Marsupials��372
18.6.2 Captive Marsupials��372
18.7 Public Health Importance373
Chapter 19
Toxoplasma gondii Infections in Marine Mammals��375
19.1 Sea Otters (Enhydra lutris nereis, Enhydra lutris kenyoni)375
19.1.2 Isolation of Viable T. gondii or Parasite DNA��375
19.1.3 Clinical Toxoplasmosis in Sea Otters��384
19.1.4 Neonatal/Congenital Toxoplasmosis in Sea Otters��384
19.1.5 Genetic Types and Clinical Toxoplasmosis in Sea Otters��384
19.2 California Sea Lion (Zalophus californianus)385
19.3 Dolphins385
19.4 Hawaiian Monk Seal385
19.5 Miscellaneous Marine Mammals385
19.6 Genetic Typing of DNA from Marine Mammals Excluding Sea Otters388
19.7 Public Health Significance388
19.8 Conclusion388
Chapter 20
Toxoplasma gondii Infections in Deer and Other Cervids��389
20.1 Prevalence of T. gondii Infection389
20.1.1 White-Tailed Deer (Odocoileus virginianus)��389
20.1.2 Elk (Wapiti, Cervus canadensis)��389
20.1.3 Roe Deer (Capreolus capreolus)��389
20.1.4 Red Deer (Cervus elaphus)��389
20.1.5 Other Cervids��389
20.1.6 Detection of T. gondii DNA in Venison��390
xiv Contents
20.1.7 Isolation of Viable T. gondii�� 391

20.2 Genotypes of T. gondii from Cervids391
Chapter 21
Toxoplasma gondii Infections in Yak (Bos grunniens), Bison (Bison spp.), and Other Wild Ruminants��397
21.1 Toxoplasmosis in Yak (Bos grunniens)397
21.2 Toxoplasmosis in Other Wild Ruminants397
21.2.1 Seroprevalence��397
21.2.2 T. gondii DNA��397
21.2.3 Clinical��397
Chapter 22
Toxoplasma gondii Infections in Bears (Ursus spp.)��401
22.2 Subclinical T. gondii Infection in Bears (Ursus spp.)401
22.2.1 Black Bears (Ursus americanus)��401
22.2.1.1 Serological Investigations��401
22.2.1.2 Isolation of Viable T. gondii��403
22.2.1.3 Biology and Transmission��403
22.2.2 Brown Bears (Ursus arctos)��405
22.2.3 Polar Bears (Ursus maritimus)��405
22.3 Clinical Toxoplasmosis in Bears406
Chapter 23
Toxoplasma gondii Infections in Wild Canids��409
23.1 Prevalence409
23.1.1 Serological Investigations��409
23.1.2 Isolation of Viable T. gondii�� 417
23.1.3 Detection of T. gondii DNA�� 417
23.2 Clinical Toxoplasmosis421
23.4 Conclusions425
Acknowledgments425
Chapter 24
Toxoplasma gondii Infections in Rodents��427
24.1 Prevalence427
24.1.2 Isolation of Viable T. gondii from Rodent Tissues��437
24.1.3 Detection of T. gondii DNA��437
24.2 Clinical Toxoplasmosis in Rodents437
24.3 Genetic Diversity of T. gondii from Rodents437
24.4 Conclusions446
Acknowledgments446
Chapter 25
Toxoplasma gondii Infections in Rabbits (Oryctolagus spp.) and Hares (Lepus spp.)��447
25.2 Parasitologic Prevalence447
Contents xv

25.4 Genotypes of T. gondii from Rabbits and Hares447
Chapter 26
Toxoplasma gondii Infections in Bats�� 451
26.2 Seroprevalence451
26.3 Detection of T. gondii DNA451
26.4 Isolation of Viable T. gondii and Genetic Characterization455
26.5 Clinical Toxoplasmosis in Bats455
Chapter 27
Toxoplasma gondii Infections in Miscellaneous Animals��457
27.1 Pandas (Ailurus fulgens, Ailuropoda melanoleuca)457
27.2 Hibernating and Poikilothermic Animals457
27.3 Other Miscellaneous Animals458
27.3.1 Serologic Investigation��458
27.3.2 Isolation of Viable T. gondii��459
27.3.3 Clinical Toxoplasmosis��459
27.3.3.1 Slender-Tailed Meerkats (Suricata suricatta)��459
27.3.3.2 European Mole (Talpa europaea)��459
27.3.3.3 Rock hyrax (Procavia capensis)��459
27.3.3.4 Fossa (Cryptoprocta ferox)��459
References��461
Index��527
List of Abbreviations
Ab: Abomosal contents Ly: Lymph node
AS: Association Ma: Masseter muscle
B: Brain MAT: Modified agglutination test (Dubey and
Bf: Beef Desmonts, 1987)354
Bl: Blood 1MAT: (Toxo-Screen DA®, Biomerieux, Marcy
CAdv: Canine adenovirus l’Etiole, France). This is the same test as
CDV: Canine Distemper Virus MAT.
CNS: Central nervous system MATt: Modified agglutination test titer
CPV: Canine parvovirus MC-PCR: Magnetic-capture PCR
CSF: Cerebrospinal fluid Mk: Milk
D: Diaphragm N-PCR: Nested PCR
DT: Sabin–Feldman dye test Nc: Neospora caninum
ELISA: Enzyme linked immunosorbent assay ND: No data or not stated
F: Fetal NS: No association
FeLV: Feline Leukemia Virus P: Placenta
FIPV: Feline Infectious Peritonitis Virus p.i.: Post-inoculation
FIV: Feline Immunodeficiency Virus PAS: Periodic acid Schiff reaction
FR: Free range PCR: Polymerase chain reaction
G: Gizzard PD: Pepsin digest
H: Heart PV: Parasitophorous vacuole
HE: Hematoxylin and eosin stain PVM: Parasitophorous vacuolar membrane
HIV: Human Immunodeficiency Virus qPCR: Quantitative PCR
i.m.: Intramuscular RFLP: Restriction fragment length polymorphism
i.p.: Intraperitoneal RT-PCR: Real-time PCR
i.v.: Intravenous s.c.: Subcutaneous inoculation
IFA: Indirect fluorescent antibody test Sc: Spinal cord
IgG: Immunoglobin G St: Stomach
IgM: Immunoglobin M SEM: Scanning electron microscopy
IHA: Indirect hemagglutination test SW: Swiss Webster albino mouse
IHC: Immunohistochemistry Sk: Skeletal muscles
IMC: Inner membrane complex Sp: Spleen
IMHA: Immune-mediated hemolytic disease Tf: Thoracic fluid
IMTP: Immune-mediated thrombocytopenia T. gondii: Toxoplasma gondii
K: Kidney T: Tongue
KO: Interferon gamma gene knockout mice TCA: T. gondii circulating antigen
LAMP: Loop-mediated amplification TEM: Transmission electron microscopy
LAT: Latex agglutination test Tg: Toxoplasma gondii
Li: Liver WB: Western blot
Lu: Lung
xvii
Preface to Third Edition
In the last years since the second edition of this book based on viable isolates and DNA directly from infected
was published in 2010, there has been an explosion of host tissue) and prospective.
knowledge concerning the parasite T. gondii and toxoplas- During the last 55 years, I have had the privilege of
mosis. One reason for this is because T. gondii has been working with virtually all hosts of T. gondii, including
and continues to be used extensively as a model for the all livestock species, wildlife, and zoo animals. I feel
cell biology of apicomplexan parasites. Although several blessed to have collaborated with hundreds of scien-
books have been published on toxoplasmosis, the pres- tists. In the interest of brevity and economy, references
ent book provides unique information on all known host cited in the first 2 editions, although mentioned, are not
types for this parasite including humans and bats and is listed in the literature cited section in the present edi-
compiled by a single author. A separate chapter on history tion. Because the literature on toxoplasmosis is vast (over
(Chapter 1) is added. 30,000 references), I have extensively borrowed tables
I view Chapter 2 as the strength of this edition as it from literature (mostly from my papers) to reduce cita-
focuses in detail on the biology of the parasite. Many tions. In the present edition, there are more than 1,500
scientists use T. gondii to investigate problems in cell citations.
biology and genetics, and in support, I have provided All surveys concerning animals that I found in litera-
information on methods of cultivation and safety proce- ture are listed to help future researchers, irrespective of
dures detailed in Chapter 3. Chapter 4, which deals with the sample size, journal or language published. The refer-
toxoplasmosis in humans, was originally written by my ences are arranged chronologically and alphabetically by
former professor and coauthor of the first edition, C. P. the first author for the benefit of readers.
Beattie, who passed away in 1987 before the edition was I would like to acknowledge those who made this
even published. I have revised the content but kept the book possible; I feel guilty that I cannot possibly list all
original format and added worldwide estimates of rates of them. Oliver Kwok, Camila Cezar, Fernando Murata,
of congenital toxoplasmosis. Each of the remaining book and other colleagues and staff in my laboratory who have
chapters 5–27 deals with toxoplasmosis in known host helped with proofreading and preparations of tables. Dr.
types of T. gondii, including a chapter on marine mam- Chunlei Su’s help concerning data and interpretation of
mals that are dying from toxoplasmosis. In these chap- genetic types and Dr. Yurong Yang’s help with Chinese
ters, I have extensively reviewed literatures from 2009 to literature are gratefully acknowledged. I am also grate-
2021, provided factual data, and have avoided specula- ful to many scientists (some acknowledged individually
tion. For each of these hosts, a similar format is used that in Chapter 1), who have contributed to this book in more
includes prevalence (serological, detection of DNA, and than one way.
isolation of viable parasite), epidemiology, clinical dis-
ease, diagnosis, genetic characterization (data separated J.P. Dubey
xix
Author
J. P. Dubey, MVSc, PhD, 1,600 research papers in international journals, about

Dsc, was born in India. He half of them on toxoplasmosis. In 1985, he was chosen
earned his veterinary degree to be the first recipient of the Distinguished Veterinary
in 1960 and master’s in vet- Parasitologist Award by the American Association of
erinary parasitology in 1963 Veterinary Parasitologists. Dr. Dubey is the recipi-
from India. He earned a Ph.D. ent of the 1995 WAAVP Pfizer Award for outstanding
in medical microbiology in contributions to research in veterinary parasitology and
1966 from the University has also received the 2005 Eminent Parasitologists Award
of Sheffield, England. Dr. by the American Society of Parasitologists. The Thomas
Dubey received postdoc- Institute for Scientific Information identified him as one of
toral training from 1968 to the world’s most cited authors in plant and animal s ciences
1973 with Dr. J.K. Frenkel, for the last decade.
Department of Pathology and In 2003, Dr. Dubey was named to the newly c reated
Oncology, University of Kansas Medical Center, Kansas Senior Science and Technology Service (SSTS), the
City, Kansas. From 1973 to 1978, he was an associ- selection for which is by invitation only, on approval of
ate professor of veterinary parasitology, Department of the Secretary of Agriculture, and is one of the few such
Pathobiology, Ohio State University, Columbus, Ohio, scientists and executives within the USDA’s Agricultural
and from 1978 to 1982 he was a professor of veteri- Research Service (USDA-ARS). In 2010, he was elected
nary parasitology, Department of Veterinary Science, to the U.S. National Academy of Sciences, Washington,
Montana State University, Bozeman, Montana. He is DC, and inducted in the USDA-ARS Hall of Fame. In
presently a senior scientist, Animal Parasitic Diseases 2018, he was the first recipient of the William C. Campbell
Laboratory, Beltsville Agricultural Research Center, One-Health Award by the American Association of
Agricultural Research Service, United States Department Veterinary Parasitologists. In the same year, he received
of Agriculture (USDA), Beltsville, Maryland. the honorary Doctor of Science degree from McGill
Dr. Dubey has spent more than 55 years research- University, Montréal, Québec, Canada. Recently, he was
ing Toxoplasma and related cyst-forming coccidian recognized as the one the topmost cited among 20,926
parasites of humans and animals. He has published over parasitologists worldwide.
xxi
Chapter 1
Introduction and History of Toxoplasma gondii
1.1 INTRODUCTION AND HISTORY Splendore1168 discovered the same parasite in a rabbit in
Brazil, also erroneously identifying it as Leishmania, but
Toxoplasma gondii is one of the most well-studied he did not name it.
parasites because of its medical and veterinary impor- It is a remarkable coincidence that this disease was
tance. It is used extensively as a model for cell biology of first recognized in laboratory animals and was first
apicomplexan organisms. Two recently published books thought to be Leishmania by both groups of investiga-
provide an update of its cell biology, molecular biology, tors. Both Nicolle and Splendore were medical doctors.
and methods to study it.1228,1311 Some of the advantages Charles Jules Henri Nicolle was a well-known French sci-
of using this parasite for cell biology are as follows: entist and eventually received the Nobel Prize in 1928 for
T. gondii is large enough to be easily seen under the his work on typhus. Manceaux, also French, was an assis-
light microscope, can be grown in virtually any warm- tant to Nicolle. Alfonso Splendore had emigrated from
blooded cell line, can be maintained indefinitely in mice Italy to Brazil, where he made numerous contributions in
and cell culture, and there is only one species that infects microbiology; he was to become the Chief Scientist at the
all hosts. Additionally, this parasite is readily amenable Bacteriological Laboratory at Portuguese Hospital, São
to genetic manipulation, with refined protocols for clas- Paulo, Brazil. It is noteworthy that although they were on
sic and reverse genetics, high transfection efficiency, different continents, they communicated with each other
and expression of epitope tags. Recently a book was regarding their discoveries.435
published that detailed methods to study its cell biology
and genetic manipulation.1228 The third edition of the
book “Toxoplasma gondii”: The Model Apicomplexan- 1.3 TRANSMISSION
Perspective and Methods has 1,184 pages contributed by
numerous expert in the field.1311 Transmission of T. gondii was at first a mystery. Soon
It has been more than a century since the discovery of the after its discovery, it was found that gundis, native to the
parasite in 1908 and the event was celebrated with publication of foothills and mountains of southern Tunisia, were not
historical accounts of the parasite and its biology.394,399,491,911,1310 infected naturally, but acquired infection in captivity. T.
Historic landmarks are summarized in Table 1.1. gondii was suspected to be transmitted by arthropods
because it was found in the blood of the host and transmis-
sion of Plasmodium and Leishmania by arthropods was
1.2 DISCOVERY OF THE PARASITE on the minds of researchers at the time. Many scientists
investigated possible transmission by several species of
Nicolle and Manceaux928 found a protozoan in tissues arthropods with completely unsuccessful results.522
of a hamster-like rodent, the gundi, Ctenodactylus gundi,
which was being used for leishmaniasis research in the 1.3.1 Congenital Transmission
laboratory of Charles Nicolle at the Pasteur Institute in
Tunis. Nicolle initially believed the parasite to be a piro- It is ironic that the congenital mode of transmission
plasm, then Leishmania, but soon realized that he had dis- was recognized first, because it is not the most common
covered a new organism and named it T. gondii based on mode of transmission of T. gondii. In 1939, 3 pathologists
the morphology (mod. L. toxo = arc or bow, plasma = life) working in New York City conclusively identified T. gondii
and the host.929 Thus, its complete designation is T. gondii in an infant girl who was delivered full-term by Caesarean
(Nicolle and Manceaux, 1908) Nicolle and Manceaux section on 23 May 1938 at Babies Hospital, New York.1318
1909. In retrospect, the correct name for the parasite The girl developed convulsive seizures at 3 days of age and
should have been T. gundii; Nicolle and Manceaux had lesions were noted via an ophthalmoscope in the maculae
incorrectly identified the host as Ctenodactylus gondi. of both eyes. She died when she was only 1-month-old and
1
2 TOXOPLASMOSIS OF ANIMALS AND HUMANS
Table 1.1
Summary of Landmarks in the History of T. gondiia
Finding Reference
Etiologic Agent
Protozoa found in the rodent, Ctenodactylus gundi in Tunisia Nicolle and Manceaux (1908)
Protozoa found in a rabbit in Brazil Splendore (1908)
Name T. gondii proposed (taxon = bow, plasma = form, in Greek) Nicolle and Manceaux (1909)
First viable T. gondii isolate obtained from an animal Sabin and Olitsky (1937)
First isolate of T. gondii from human Wolf et al. (1939)
Human and animal T. gondii proven identical Sabin (1941)
Pathogenesis of toxoplasmosis, including hydrocephalus Frenkel and Friedlander (1951); Frenkel (1953, 1956)
Parasite Morphology and Life Cycle
Tachyzoite (trophozoite, feeding form, proliferative form, endodyozoite)
Term tachyzoite proposed (tachy = fast, zoite = life) Frenkel (1973)
Endodyogeny described Goldman et al. (1958)
Ultrastructure described Gustafson et al. (1954); Sheffield and Melton (1968)
Tissue cyst, bradyzoite, cystozoite
Cyst recognized Levaditi et al. (1928)
Cyst described cytologically Frenkel and Friedlander (1951); Frenkel (1956)
Ultrastructure described Wanko et al. (1962); Ferguson and Hutchison (1987)
Term bradyzoite proposed (bradys = slow, zoon = animal) Frenkel (1973)
Term tissue cyst proposed Dubey and Beattie (1988)
Bradyzoite resistance to digestive enzymes recognized Jacobs et al. (1960a)
Development of tissue cysts and bradyzoites described Dubey and Frenkel (1976)
Complete biology of bradyzoites and tissue cysts reviewed Dubey et al. (1998)
Feline enteroepithelial stages
Coccidian phases described Frenkel et al. (1970); Hutchison et al. (1970); Sheffield and
Melton (1970); Dubey and Frenkel (1972)
Oocyst morphology described Dubey et al. (1970b)
Five asexual T. gondii types (A–E) described Dubey and Frenkel (1972)
Ultrastructure of coccidian stages described Sheffield (1970); Piekarski et al. (1971); Ferguson et al.
(1974, 1975, 1979a, 1979b); Christie et al. (1978); Speer,
Clark, and Dubey (1998); Speer and Dubey (2005)
Lipid metabolism determines host specificity of T. gondii oocyst excretion 310
in cats
Transmission
Congenital
Transmission demonstrated in human Wolf et al. (1939)
Repeated transmission found in house mouse Beverley (1959)
Congenital transmission found in a large wild animal species, white-tailed Dubey et al. (2008)
deer
Carnivorism, transmission by meat of intermediate hosts
Suggested carnivorous transmission Weinman and Chandler (1954)
Transmission by meat found in humans Desmonts et al. (1965)
Fecal-oral
Transmission by a resistant fecal form of T. gondii demonstrated Hutchison (1965)
Coccidian phase recognized Hutchison et al. (1970, 1971); Frenkel et al. (1970); Dubey
et al. (1970a, 1970b); Sheffield and Melton (1970);
Overdulve (1970)
Definitive and intermediate hosts defined, including excretion of oocysts Frenkel et al. (1970); Miller et al. (1972); Jewell et al.
only by felids (1972)
First oocyst-inhaled/ingested human toxoplasmosis outbreak described Teutsch et al. (1979)
Genetics and Different Genetic T. gondii Strains
Recombinants and genetic crosses produced Pfefferkorn and Pfefferkorn (1980)
Isoenzyme differences used to distinguish T. gondii strains Dardé et al. (1987); Tibayrene et al. (1991)
Restriction fragment length polymorphism used to group T. gondii strains Sibley et al. (1992); Howe and Sibley (1995)
into 3 Types (I–III)
(Continued)
INTRODUCTION AND HISTORY OF T. GONDII 3
Table 1.1 (Continued)

Finding Reference
National, continental, intercontinental, and pandemic T. gondii strains Lehmann et al. (2006)
distinguished
T. gondii genome annotated Khan et al. (2005)
Immunity and Protection
T. gondii neutralizing antibody recognized Sabin and Ruchman (1942)
Antibodies found to kill extracellular but not intracellular T. gondii Sabin and Feldman (1948)
Protection transferred by immune lymphoid cells but not by antibodies Frenkel (1967)
Interferon gamma found to be main cytokine for protection Suzuki et al. (1988)
Role of CD4+ and CD8+ cells in protection defined Gazzinelli et al. (1991)
Toxoplasmosis in Humans
Congenital
First proven case of congenital toxoplasmosis described Wolf et al. (1939)
Typical tetrad clinical signs described (hydrocephalus or microcephalus, Sabin (1942)
chorioretinitis, intracerebral calcification)
Acquired
First case in a child Sabin (1941)
Fatal toxoplasmosis in adults found Pinkerton and Weinman (1940)
Lymphadenopathy recognized as the most frequent symptom Siim (1956); Beverley and Beattie (1958)
Susceptibility to toxoplasmosis in AIDS patient recognized Luft et al. (1983)
Chronic infection
Cysts found in autopsy slides, indicating chronic asymptomatic infection Plout (1946); Kean and Grocott (1947)
Toxoplasmosis in Other Animals
Toxoplasmosis found in a domestic animal, dog Mello (1910)
Immunosuppressive Canine Distemper Virus influenced clinical Campbell et al. (1955)
toxoplasmosis outcome in dogs
Epidemic toxoplasmosis abortions in sheep recognized Hartley and Marshall (1957)
Toxoplasmosis in animals reviewed critically Dubey and Beattie (1988)
Toxoplasmosis found a common infection in a marine mammal species, Cole et al. (2000)
sea otter
Diagnosis
Novel Sabin–Feldman dye test described Sabin and Feldman (1948)
Toxoplasma skin test as a survey tool Frenkel (1948)
Tests developed to detect IgM antibodies in cord blood Remington et al. (1968); Desmonts et al. (1981)
Simple direct agglutination test developed (DAT, MAT) Desmonts and Remington (1980); Dubey and Desmonts
(1987)
First validation of a serologic test using isolation of the parasite as standard Dubey et al. (1995a); Dubey (1997)
PCR test developed to detect T. gondii DNA using B1 gene Burg et al. (1989)
Treatment
Sulfonamides found effective against T. gondii Sabin and Warren (1942)
Pyrimethamine found synergistic with sulfonamides against dividing Eyles and Coleman (1953)
tachyzoites
Folic acid and yeast improve activity of sulfadiazine and pyrimethamine Frenkel and Hitchings (1957)
Spiramycin found to have antitoxoplasmic activity Garin and Eyles (1958)
Clindamycin found to be antitoxoplasmic McMaster et al. (1973); Araujo and Remington (1974)
Prevention and Control
Prophylactic treatment, and screening of pregnant women initiated in Thalhammer (1973, 1978); Desmonts and Couvreur
Austria and France to reduce congenital toxoplasmosis (1974a, 1974b)
Hygienic measures advocated to prevent human exposure to oocysts Frenkel and Dubey (1972)
Thermal curves to kill T. gondii in meat by cooking, freezing, and Dubey et al. (1986); Dubey et al. (1990); Kotula et al.
irradiation constructed (1991)
Animal production practices developed to reduce T. gondii infection in Dubey et al. (1995b); Weigel et al (1995)
farm animals
Low prevalence of T. gondii in pigs correlated with reduction of Dubey et al. (2005); Jones et al. (2007)
seroprevalence of T. gondii in humans
(Continued)
Table 1.1 (Continued)

Finding Reference
Vaccination
A vaccine to reduce fetal losses in sheep commercialized Wilkins and O’Connell (1983); Buxton and Innes (1995)
Ts-4 vaccine for intermediate host Waldeland and Frenkel (1983)
T-263 vaccine to prevent oocyst excretion by cats Frenkel et al. (1991)
a Source: Dubey, J. P., 2008, J. Eukaroyt. Microbiol., 55, 467–475.394 For citations, see this reference. Additional reference is in bold.
an autopsy was performed. The brain, spinal cord, and the lamb chops). Since the prevalence of T. gondii is much
right eye were removed for examination. Free and intra- higher in sheep than in horses or cattle, this illustrated
cellular T. gondii were found in lesions of encephalomyeli- the importance of carnivorism in the transmission of
tis and retinitis of the girl. Portions of cerebral cortex and T. gondii. Although beef is rarely infected with T. gondii,
spinal cord were homogenized in saline and inoculated viable T. gondii has been isolated from horsemeat destined
intracerebrally into rabbits and mice, producing encepha- for human consumption and severe toxoplasmosis has
litis. T. gondii was demonstrated in the neural lesions and been reported in humans in France after eating imported
T. gondii from these animals was successfully passaged horsemeat (see Chapter 4). This experiment in Paris was
into other mice. Congenital transmission was later found justified ethically because of the prevailing belief at that
to occur in many species of animals, particularly sheep617 time the feeding of uncooked meat was beneficial in
and rodents.403 recovery from tuberculosis (pers. comm., G. Desmonts); it
is detailed here to indicate how valuable information can
1.3.2 Carnivorism be obtained from simple experiments.
Weinman and Chandler1309 suggested that transmis- 1.3.3 Fecal–Oral, Sexual Cycle, and
sion might occur through the ingestion of undercooked Discovery of the Oocyst
meat. This hypothesis for transmission via the ingestion
of infected meat was tested by Desmonts et al.305 in an While congenital transmission and carnivorism can
experiment with children in a Paris sanatorium. They explain some of the transmission of T. gondii, it does not
compared the acquisition rates of T. gondii infection in explain the widespread infection in vegetarians and herbi-
children before and after admission to the sanatorium. Of vores. The real breakthrough in the discovery of the life
the 1,125 children admitted to the Children’s Tuberculosis cycle of the parasite came when Hutchison667 first discov-
Department of the Hospital of Brévannes, 641 (56.9%) ered T. gondii infectivity was associated with cat feces.
had no antibodies to T. gondii at the time of admission, Dr. William McPhee Hutchison was a parasitologist
whereas 204 of 641 children became seropositive during in the Department of Biology, Strathclyde University,
their hospital stay. The mean duration of hospitalization Glasgow, Scotland. He had a Ph.D. in parasitology, but
of these children was 9 months (from 3 months to > 1 year). had never researched protozoans before. In a preliminary
Children were serologically tested at admission and then experiment, he fed the Beverley strain of T. gondii tissue
every 4 months until the end of hospitalization (although cysts to a cat experimentally infected 2 months previously
some children given just one test). All the children were with Toxocara cati.667 Feces containing nematode ova
given beef meat juice (1 teaspoon/day) and raw horsemeat were collected starting 2 weeks after feeding T. gondii.
(20–60 g, 2 or 3 times/week); these children represented The feces, after floatation in 33.0% zinc sulfate solution
the control group. The monthly rate of acquisition of and storage in tap water in an open beaker for 12 months
T. gondii infection was 4.8%, which was 5 times higher to embryonate T. cati eggs, induced toxoplasmosis in
than for the general population (deduced from data in mice. This discovery was a breakthrough because, until
children at the time of admission). For the experimental then, both known forms of T. gondii, i.e., tachyzoites and
group (66 children), barely cooked lamb chops were added bradyzoites, were killed by water. Microscopic exami-
twice a week to the usual diet of beef meat juice and raw nation of feces revealed only T. cati eggs and Isospora
horsemeat. The monthly rate of acquisition of T. gondii oocysts. In Hutchison’s667 published report, T. gondii
infection was 9.2%, which was nearly twice that of the infectivity was not attributed to either oocysts or T. cati
other hospitalized children. They estimated that the time eggs. He suspected transmission of T. gondii via the eggs
required to infect 50.0% of the hospital population has of T. cati, similar to the transmission of the fragile flag-
to be 5 years for a general population, a little more than ellate Histomonas meleagridis via Heterakis gallinae
1 year for the hospitalized children (usual diet), but a little eggs. He initially wanted to test the nematode hypoth-
more than 6 months for the experimental group (those fed esis using Toxocara canis and T. gondii transmission in
INTRODUCTION AND HISTORY OF T. GONDII 5
a dog. However, he decided on the cat and T. cati model earthworms, flies, and cockroaches could act as transport
because there was no place to house dogs.394 Transmission hosts and further disseminate oocysts in the environment.
of T. gondii by T. canis eggs made more sense because of Like other coccidian oocysts, T. gondii oocysts were
the known zoonotic potential of T. canis; T. cati was not, found to be highly resistant to environmental influences,
at that time, known to infect humans, but T. canis was. It including commonly used disinfectants (see Tables 2.22,
is probable that the discovery of the life cycle of T. gondii 2.23—Chapter 2). I am still searching for a chemical that
would have been delayed if Hutchison had worked with will kill T. gondii oocysts without harming humans.
dogs instead of cats. One of the most intriguing recent findings related
Hutchison668 proposed transmission of T. gondii via to oocyst biology concerns widespread T. gondii infec-
T. cati eggs. He used 2 cats (#5, #8) in the second experi- tions in marine mammals (Chapter 19). Who would have
ment whose serological status for T. gondii had not been thought that noncaptive marine mammals would die of
determined.668 Cat #5 had previously been experimentally toxoplasmosis acquired from freshwater runoff from land
infected with T. cati and was excreting nematode ova in contaminated with oocysts? We are indeed surrounded by
the feces. Cat #8 had not been infected with T. cati. He fed seas contaminated with T. gondii oocysts.
T. gondii–infected mice to each cat for 5 days and floated
feces in zinc sulfate to collect ova. After incubating the 1.3.4 Discovery of the Full Life Cycle
ova in water to embryonate them, he orally inoculated and Developmental Stages
fecal floats to groups of 6 mice. T. gondii infection was in the Intestine of Cats
achieved from the feces of cat #5 from day 13 through
day 30, when the experiment was terminated; fecal floats As stated earlier, it became clear in 1970 that there
from cat #8 were all negative. He then reversed the role was profuse multiplication of T. gondii in the intestine
of cat #5 and cat #8. He gave an anthelmintic to cat #5, to of cats after eating tissue cysts. The challenge was to
remove worms, and experimentally infected cat #8 with sort out different asexual stages in enterocytes because
T. cati—and repeated T. gondii feeding and fecal infec- the entire asexual and sexual cycle could be completed
tivity testing. As he expected, no fecal infectivity was in 60 hours.334 We have found 5 morphologically distinct
detected in the feces of cat #5, but cat #8 was excreting types of T. gondii that could develop in enterocytes before
T. gondii in feces from days 17–30 when the experiment gametogony. These stages are designated types A–E
was terminated. Thus, T. gondii was transmitted only in (instead of generations because there are several genera-
association with T. cati infection. Hutchison had a precon- tions within each T. gondii type). These asexual stages in
ceived hypothesis of nematode transmission of T. gondii. the feline intestine are structurally distinct from tachyzo-
In hindsight, we now know that the chance of success of ites that also develop in the lamina propria. The entero-
Hutchison’s second experiment was remote (perhaps 1 in epithelial stages (Types A–E, gamonts) are formed in the
1,000, or more) because cats usually excrete oocysts only intestinal epithelium and the development of types B–E
upon primary exposure; once they become immune, they schizonts in enterocytes has been confirmed ultrastruc-
usually do not excrete oocysts upon re-exposure to the turally.1167 Occasionally, type B and C schizonts develop
parasite.403 within enterocytes that are displaced beneath the epithe-
Hutchison’s experiment is described here again, for lium into the lamina propria.
the benefit of future graduate students, to underscore that I should emphasize that the asexual types A–C are
even a brilliantly planned experiment requires repetition time-dependent stages, few in number, and difficult to
to support a hypothesis. It also illustrates that seminal find.403
discoveries can be made in small laboratories with lim- To locate these early stages, I examined hundreds of
ited resources. The nematode theory of the transmission sections from the small intestines of cats fed tissue cysts.
of this parasite was discarded in 1969, and the T. gondii To find the earliest stage, type A, I had sectioned at 5 μm
oocyst was discovered in 1970 (Table 1.1). the entire duodenum of a kitten fed tissue cysts and micro-
Seroepidemiological studies on isolated islands in scopically examined all sections at 1,000× magnification.
the Pacific,1276 Australia,912 and the USA377 have shown The success in finding enteroepithelial stages was in
an absence of T. gondii on islands without cats, confirm- part due to the use of newborn kittens still nursed by their
ing the important role of the cat in the natural transmis- dam. This procedure allowed me to infect part of the litter
sion of T. gondii. Wallace’s study on Pacific Islands was with T. gondii tissue stages and to keep 1–2 littermates
remarkable and full of challenges. These islands are really as controls. The litter was killed as soon as oocysts were
remote and their main contact with the outside world is excreted, and before oocysts were sporulated, thus avoid-
via USA Coast Guard cutter ships. Wallace was allowed ing contamination of the environment. Until then, new-
only 2 days to work on each island. He was also one of born animals were not used for coccidiosis research.
the first to find T. gondii oocysts in the feces of naturally The mystery why only cats can excrete T. gondii
infected cats (Chapter 5). Additional studies revealed that oocysts was resolved recently.310 Felines are the only
mammals that lack delta-6-desaturase activity in their toxoplasmosis (see Table 1.1). Elmer Pfefferkorn, with his
intestines, which is required for linoleic acid metabolism, wife Lorraine Cassidy Pfefferkorn (see Table 1.1), made
resulting in systemic excess of linoleic acid. T. gondii the first genetic cross of T. gondii and laid the foundation
sexual development occurs when cultured feline intesti- for genetic research on T. gondii.
nal epithelial cells are supplemented with linoleic acid. I am grateful for collaborations, friendship, and
Inhibition of murine delta-6-desaturase and supplemen- guidance from Drs. Ajzenberg, D., Almería, S., Alvarado-
tation of their diet with linoleic acid allowed T. gondii Esquivel, C., Beattie, C.P*., Beverley, J. K.A*, Boothroyd,
sexual development in mice. This mechanism of species J.C., Boyle, J.P., Desmonts, G*., Dardé, M.L., Dumetre,
specificity is the first defined for a parasite sexual cycle.310 A., Fayer, R., Feldman, H. A.*, Ferguson, D. J. P., Frenkel,
Personal experiences leading to the discovery of the J. K.*, Gamble, H.R., Gennari, S.M., Gómez-Marin, J.E.,
oocyst and full life cycle of T. gondii were reviewed.370,435 Grigg, M. E., Hartley, W.M.*, Hill, D, E., Jacobs, L.*,
Jones, J. L., Lehmann, T., Lindsay, D.S., Lopes, A.P.A.,
Lunney, J.K., McLeod, R., Montoya, J. G., Munday,
1.4 GRATITUDE B.L*., Murrell, K.D., Pande, B.P.*, Pena, H.F.J., Pradhan,
A.B., Remington, J. S*., Rosenthal, B.M., Schares, G.,
This account will not be complete without mention- Sibley, L.D., Speer, C.A., Su, C., Thulliez, Ph, Urban,
ing contributions of 2 virologists, Albert Bruce Sabin, and J.F., Venturini, L.*, Venturini, M.C., Villegas, E., Villena,
Elmer Roy Pfefferkorn who made profound contributions I., Weiss, L. M., and many others during the 60 years of
to T. gondii biology. Dr. Sabin, who is best known for devel- research on toxoplasmosis that made this book possible
oping the polio virus vaccine, also isolated and distributed (*now deceased). I am grateful to all those who made it
worldwide the famous R.H. strain of T. gondii, developed possible for me to be part of it or observer for half the his-
the Sabin–Feldman dye test, and developed treatment for tory (1908–2020) of T. gondii.
Chapter 2
Biology of Toxoplasma gondii
2.1 TAXONOMIC CLASSIFICATION was known of the complete life cycle of most Isospora
species until 1970, when the life cycle of T. gondii was
T. gondii is a coccidian parasite with cats as the defini- discovered. Until then, Isospora species were consid-
tive host and warm-blooded animals as intermediate ered parasites of carnivores (dogs, cats) and birds were
hosts. It belongs to not thought to be host-specific. In 1970, the oocyst of
T. gondii was discovered (see Chapter 1). This finding
Phylum: Apicomplexa; Levine, 1970 was a breakthrough in medical and veterinary sciences
Class: Sporozoasida; Leukart, 1879 and eventually led to the recognition of several new taxa
Subclass: Coccidiasina; Leukart, 1879 of economically important Toxoplasma-like parasites
Order: Eimeriorina; Leger, 1911
(e.g., Hammondia, Neospora, Sarcocystis) and discov-
Family: Toxoplasmatidae, Biocca, 1956
Genus: Toxoplasma Nicolle and Manceaux, 1909
ery of their life cycles.
Historically, T. gondii originated probably as a coccid-
There is only one species of Toxoplasma, T. gondii. ian parasite of cats with a fecal-oral cycle. With domestica-
Coccidia are among the most important parasites of tion, it adapted transmission by several modes, including
animals, and they were the first protozoa discovered.446 transmission by fecal-oral cycle, by carnivorism, and
The oocyst is the key stage of all coccidians, and their transplacentally. Although T. gondii can be transmitted in
classification was based on the number of sporozoites many ways, cats are essential for its natural propagation.
and structure of the oocyst. Oocysts with 4 sporocysts, There are 3 infectious stages of T. gondii: the tachyzoites,
each with 2 sporozoites (total 8 sporozoites), are clas- the bradyzoites, and oocysts. These stages are linked in a
sified as Eimeria. Coccidiosis due to Eimeria species complex life cycle (Figure 2.1).
is one of the most economically important diseases of
poultry, cattle, sheep, goats, and many other herbivores;
it is difficult to raise livestock coccidia-free. Oocysts 2.2 STRUCTURE AND LIFE CYCLE
with 2 sporocysts, each with 2 sporozoites, were origi-
nally classified as Isospora (now Cystoisospora). In 2.2.1 Tachyzoite
the last 2 decades Cyclospora (2 sporocysts each with
2 sporozoites) and Cryptosporidium (4 naked sporozo- 2.2.1.1 Structure
ites) have become prominent because of public health
concern. Tachyzoite (táchos = speed in Greek) is the rapidly mul-
Before the discovery of the life cycle of T. gondii, tiplying stage. The tachyzoite is crescent-shaped, approxi-
coccidians were considered host-specific with a simple mately 2 × 6 μm (Figures 2.2a and 2.3a), with a pointed
1-host life cycle. Infection was confined to the intestines anterior (conoidal) end and a rounded posterior end. In
and usually to enterocytes. With few exceptions, Eimeria histological sections, tachyzoites are often round, 2–4 μm
species still follow this life cycle. The host becomes in diameter with a central vesicular nucleus (Figure 2.3d).
infected by ingesting sporulated oocysts of Eimeria. Ultrastructurally, it has complex structure with several
After excystation, the sporozoites penetrate intestinal organelles.68,135,150,492,910,955,1089 The tachyzoite consists of
epithelial cells and multiply asexually before forming various organelles and inclusion bodies including a pel-
male and female gamonts. Oocysts are produced after licle (outer covering), cytoskeleton (inner membrane
fertilization and are passed in feces in a noninfective complex (IMC), subpellicular microtubules, apical rings,
unsporulated stage. Sporulation occurs outside the host polar rings, a conoid), secretory (rhoptries, micronemes,
and oocyst become infectious. Unlike Eimeria, the life dense granules) micropore, a mitochondrion, endoplas-
cycle of which has been known for many years, little mic reticulum, a Golgi complex, ribosomes, rough and
7
Figure 2.1
Life cycle of T. gondii.
smooth endoplasmic reticula, nucleus, acidocalcisomes, originate from the apical cap, above the 22 subpellicular
amylopectin granules, Golgi apparatus, and an apicoplast microtubules. One or more cytostome-like-structures,
(Figures 2.3–2.5). The pellicle consists of 3 membranes: 1 termed micropores, are present at the apical half of the
plasmalemma and 2 closely applied membranes that form parasite. Micropore is a 150-nm diameter in-foldings of
an IMC. The IMC is formed from a patchwork of flattened the plasma membrane with a thickened collar. The func-
vesicles derived from endoplasmic reticulin and Golgi tion of micropore is not clear but thought to be uptake of
system. The inner membrane is discontinuous at the ante- materials.
rior tip above the polar rings, at the micropore and at the There are 2 apical and 2 polar rings (outer and inner).
basal complex posterior pore at the extreme posterior tip The apical rings are located at the anterior tip of the para-
of the zoite. Additionally, a network of filamentous intra- site and consist of electron dense material (Figure 2.2d).
membranous particles (IMPs) with a mean diameter of The outer ring encircles the top of the resting conoid. The
8–10 nm and composed of a group of proteins (alveolins) outer polar ring is an electron-dense thickening of the
that are located below the IMC. These 22 rows of IMPs IMC at the anterior end of the tachyzoite. The inner
BIOLOGY OF T. GONDII 9
Figure 2.2 Schematic drawings of T. gondii stages. (a) Tachyzoite. (b) Bradyzoite. (c) Sporozoite. 1. Pellicle. 2. Conoidal (ante-
rior) end. 3. Posterior end. 4. Micropore. 5. Rhoptry. 6. Microneme. 7. Apicoplast. 8. Amylopectin granules. 9. Dense
granules. 10. Golgi body. 11. Mitochondrion. 12. Endoplasmic reticulin. 13. Nucleus. (d) Apical complex. 14. Internal
microtubules. 15. Microtubules of conoid. 16. IMC. 17. Plasmalemma. 18. Apical ring 1. 19. Apical ring 2. 20. Polar ring
1. 21. Polar ring 2. 22. Subpellicular tubules. (e) Macrogamont. 23. Veil forming bodies. 24. Wall forming bodies (WFB)
1. 25. WFB 2. 26. Lipid body. 27. Mitochondrion. 28. Endoplasmic reticulum. 29. Nucleus. 30. Amylopectin granules.
(f) Microgamete. 31. Perforatorium. 32. Basal body. 33. Flagellum 1. 34. Flagellum 2. 35. Flagellum 3. 36. Microtubule.
37. Mitochondrion. 38. Nucleus.
ring anchors the subpellicular microtubules. The conoid originate from the inner polar ring and run longitudi-
(0.3 × 0.4 µm) is a truncated hollow cone and consists nally approximately two-thirds of length of the cell, just
of tubulin structures wound like compressed springs beneath the IMC (Figure 2.4). They are evenly spaced,
(Figure 2.2d). Twenty-two subpellicular microtubules and their distal ends are not capped. In addition, there
Figure 2.3 Tachyzoites (a–d) and tissue cysts (e–i) of T. gondii. (a) Tachyzoites (arrow) are crescent-shaped compared with red blood
cells (arrowhead), impression smear, mouse lung (Giemsa). (b) Fluorescent image of 2 dividing tachyzoites, expressing
YFP ± tubulin (cyan) and RFP-TgMORN1 (yellow). The apical ends (arrowhead) of the parasites are oriented toward the top
of the image. The 2 dome-like structures in each parasite are daughter cortical cytoskeletons highlighted by YFP ± tubulin
(cyan) and RFP-TgMORN1 (yellow). Arrow points to nonconoidal end. (Courtesy of Drs. K. Hu and John Murra, University
of Pennsylvania, Philadelphia, USA.) (c) Group of tachyzoites showing Golgi (Grasp-mRFP; red, arrow) and apicoplast
(anti-acyl carrier protein with Alexa 488; green, arrowhead) with DAPI staining. (Courtesy of Dr. Boris Striepen, University
of Georgia, Athens, USA.) (d) Group of tachyzoites (arrow) in a PV in the lamina propria of small intestine of cat. Dividing
tachyzoites (arrow) are bigger in size and plump. Arrowhead points to a host cell nucleus. Histologic section (H&E). (e)
Small tissue cyst. Note thin silver-positive cyst wall (arrowhead) and bradyzoites with terminal nuclei (arrow). Impression
smear, mouse brain. Wilder’s silver stain plus Giemsa. (f) Tissue cyst with a thin PAS-negative (or faintly stained) cyst wall
(arrowhead) intensely PAS-positive bradyzoites (arrow). Histologic section of the brain. PAS reaction counter-stained with
hematoxylin. (g) Tissue cyst from the mouse brain, demonstrating green fluorescent protein (GFP) expressing bradyzoites
(green, arrowhead). The cyst wall stained with antibody to cyst wall protein 1 (CST1) followed by a rhodamine labeled sec-
ondary antibody (red, arrow). (Courtesy of Drs. Joshua Mayoral and Louis M. Weiss, Albert Einstein College of Medicine,
Bronx, New York, USA.) (h) Tissue cyst freed from mouse brain. Note hundreds of bradyzoites (arrowhead) enclosed in a
thin cyst wall (arrow). Unstained. (i) Tissue cyst in histological section of mouse brain, 14 months p.i. Note only nuclei of
bradyzoites (arrowhead) are visible and the cyst wall is very thin (arrow). H&E.
Figure 2.4
T. gondii tachyzoites as seen by helium ion scanning microscopy. (a, b) Rosettes of tachyzoites attached to residual
body by posterior end. Note profuse intravacuolar network (arrowhead). The tachyzoites are partially covered by host
cell (double arrowheads). (c, d) Apical end of extracellular T. gondii tachyzoites. Note subpellicular microtubules (arrow-
heads) arising from polar ring (arrow) of the conoid (c). The subpellicular microtubules are covered by the pellicle
simulating a tear-drop appearance. (Courtesy of Wanderley de Souza and Marcia Attias, Universidade Federal do Rio
de Janeiro, Brazil.)
are two 400-nm long intraconoidal tightly bound micro- Another organelle that has been identified is called plant-
tubules. The subpellicular microtubules are like a rib like vacuole; it is enclosed in a single membrane.
cage and are arranged in a gentle counterclockwise spiral. The nucleus is usually situated toward the central area
Individual microtubules have prominent transverse stria- of the tachyzoite. It is nearly spherical with an anterior
tions. Between the anterior tip and the nucleus there are up concavity. It consists of a nuclear envelope with pores,
to 10 club-shaped organelles called rhoptries (Figure 2.5). clumps of chromatin, and a centrally located nucleolus.
A rhoptry consists of an anterior narrow electron dense The mitochondrion is branched, nearly as long as the
neck up to 2.5 µm long that extends into the interior of the whole tachyzoite, and has bulbous cristae. It is thought
conoid, and a sac-like, often labyrinthine posterior end (up to be an endosymbiont. Considerable biological curiosity
to 0.25 × 1 µm). Micronemes are electron-dense rod-like has been focused on a nonphotosynthetic organelle called
structures (250 × 50 nm) that are at the anterior end of the the plastid (Figure 2.2a). It is a 4-membrane bound, alga-
parasite around the polar ring (Figure 2.5). Dense gran- derived obligatory endosymbiont structure. It has an extra
ules are electron dense, approximately 200 nm in diam- chromosomal 35 kb DNA. It is approximately 500 nm in
eter and scattered throughout the tachyzoite but mostly in diameter and filled with granular filamentous material. At
the posterior end. Acidocalcisomes, approximately 10, are the posterior (nonconoidal) end of the tachyzoite, there is
acidic organelles that are involved in calcium regulation. a basal complex structure.
Figure 2.5
TEM of T. gondii tachyzoites. (a) Longitudinal section of an intracellular tachyzoite in cell culture. Am, amylopectin gran-
ule; Co, conoid; Dg, electron-dense granule; Go, Golgi complex; Mn, microneme; No, nucleolus, Nu, nucleus; Pv, parasi-
tophorous vacuole; Rh, rhoptry; Lb, lipid. (b) A tachyzoite penetrating a neutrophil in mouse peritoneum; note the moving
junction (Mj) at the site of penetration into the neutrophil and the extraordinary early development of the tubulovesicular
membranes (Tv) in the space between the neutrophil and the tip of the tachyzoite. (Dubey, J.P., Lindsay, D.S., Speer,
C.A., 1998, Clin. Microbiol. Rev., 11, 267–299.381)
2.2.1.2 Host Invasion their contents through the plasmalemma just above the
conoid to the exerior. The mechanical events involved in
Although tachyzoites can move by gliding, flexing, zoite attachment and penetration include (i) gliding of the
undulating, and rotating, they have no visible means of zoite; (ii) probing of the host cell with the zoite’s conoidal
locomotion such as cilia, flagella, or pseudopodia. Instead, tip; (iii) indenting the host cell plasmalemma; (iv) form-
their motility is powered by the actin-myosin motor com- ing a moving junction (Figure 2.5b) that moves posteriorly
plex anchored to the IMC. The intracellular components along the zoite as it penetrates into the host cell; and (v)
and the extracellular milieu have been called the glideo- partially exocytosing micronemes, rhoptries, and dense
some.529,614 The outermost IMC membrane is studded with granules. T. gondii can penetrate a variety of nucleated
myosin complexes, like a conveyor-belt system. T. gondii cell types from a wide range of hosts, indicating that the
is nonmotile at room temperature. The gliding occurs biochemical receptors involved in attachment and penetra-
counterclockwise and tachyzoite can move up to 10 µm tion are probably common to most animal cells. T. gondii
in 1 second.1138 can penetrate the host plasmalemma in 26 seconds. The
Functions of the conoid, rhoptries, and micronemes are invasion involves 2 Ca2+-dependent events of protrusion of
not fully known but are probably associated with host-cell the conoid and secretion of microneme and rhoptry con-
penetration and creating an intracellular environment suit- tents forming a moving junction. The tachyzoite is tem-
able for parasite growth and development and exit from the porarily deformed as it penetrates and squeezes through
host cell. The conoid can rotate, tilt, extend, and retract the host plasmalemma. Recent studies have shown that the
as the parasite probes the host-cell plasmalemma imme- tachyzoite can gain entry in host by endocytosis as well as
diately before penetration. Rhoptries have a secretory active penetration.1010 The parasite is quickly surrounded
function associated with host cell penetration, secreting by a membrane that is evidently derived from the host-cell
plasmalemma minus host proteins. This membrane is des- and underwent endodyogeny to form tachyzoites. Even
tined to become the parasitophorous vacuole (PV) mem- though the sporozoites were just passing through ileal
brane (PVM); and a number of parasite proteins associate enterocytes, they still formed PVs that contained exocy-
with it including rhoptry proteins, ROP2, 3, 4, and 7. ROP2 tosed dense granule material and well-developed TMNs
is located on the host-cell cytoplasmic side of the PVM (Figures 2.6 and 2.7). Exocytosed material and TMNs
suggesting a role in host/parasite biochemical communica- associated with the PVs of sporozoites in transit across
tion. Within a few minutes after penetration, tachyzoites the intestinal epithelium indicate that parasite replica-
modify the newly formed PV and the PVM with parasite tion does not always follow the formation of a parasite-
proteins and a tubular membranous network (TMN) forms modified PV. After entering cells in the lamina propria,
within the PV within first hour of invasion. The TMNs are sporozoites presumably formed a second PV multiplied
antigenically and structurally different from PVM but have by endodyogeny.
connections to it.292 The PVM acquires pore structures that As stated earlier, most studies on host parasite interac-
freely allow charged molecules up to 1,200 kDals to dif- tions were performed with tachyzoites.1138 Recently, host
fuse bidirectionally between the PV and host-cell cyto- cell-sporozoite interaction in vitro was studied ultrastrc-
plasm. Dense granule associated proteins are secreted turally and by immunofluorescence.1207 Within 1–5 min-
into the PV. Collectively, these modifications establish a utes of incubation of human foreskin fibroblasts cultures
parasite-friendly environment within the host-cell cyto- with sporozoites, a moving junction was formed, as shown
plasm conducive to parasite replication. The PVM is not by the presence of a rhoptry neck protein (RON4)-positive
a homogenous structure of uniform thickness. The vol- ring around the invading parasite or the accumulation of
ume of PV may increase many folds within 24 hours of its RON4 at the sporozoite rear end, considered typical of
formation. The organelles in progeny are synthesized de invading or just invaded zoites. An unusual feature was
novo; however, a recent study proposed recycling of micro- the presence of sporozoite-specific trails (ssts) at the non-
neme protein MIC2 from mother to daughter tachyzo- conoidal (rear) end of the sporozoite (Figure 2.8). These
ites.991 Tachyzoites continue to divide by endodyogeny. In ssts were 10–100 μm long, generally formed a straight
vivo, most groups of tachyzoites are arranged randomly line, and consisted of tubulo-vesicular structures associ-
due to asynchronous cycles of endodyogeny. However, ated with dense granule proteins, including GRA1. PVM-
occasionally rosettes are formed due to synchronous divi- enclosed sporozoites could traverse host cells, exit intact,
sion (Figure 2.4a and b). In rapidly dividing tissue culture and infect new cells.1207 At any stage of the host-parasite
adapted strains, T. gondii within a vacuole may divide interaction, sporozoites were surrounded by only 1 PVM;
synchronously, but this is not the norm. Rarely, tachyzo- the secondary large vacuole observed in a previously is
ites of certain strains may divide by binary fission. The now considered an artifact.1165
host-cell ruptures when it can no longer support the growth
of tachyzoites. Exit from the host cell is mediated by a pro- 2.2.1.3 Multiplication by Endodyogeny
tein (TgPLP1) secreted by the parasite. A highly dynamic
F-actin network connects individual tachyzoites support- Tachyzoites multiply asexually within the host
ing multidirectional vesicular transport.991 One interesting cell by repeated endodyogeny, a specialized form of
and elusive phenomenon is association of host mitochon- reproduction in which 2 progeny form within the par-
dria and endoplasmic reticulum (ER) to the PV.11 Within ent parasite (Figure 2.9), consuming it. In endodyog-
minutes of tachyzoite invasion into the host cell, host mito- eny, the Golgi complex and the apicoplast divide, first
chondria and ER are tightly associated with PVM and the becoming 2 at the anterior end of the nucleus, along
extent of this juxtaposed association does not change with with the formation of 2 centrosomes from the nucleus.
enlargement of the PV. The T. gondii vacuole does not fuse Next, the conoid, the anterior portions of the IMCs,
with host lysosomes. After exit from the host cell, parasite and the subpellicular microtubules of the progeny cells
can leave long trails.1138 These trails include SAG1, MIC2, appear as 2 dome-shaped structures anteriorly. The
and actin but not myosin.991 parasite nucleus becomes horseshoe-shaped and the
Most of the available information concerning the ends of the nucleus move into the dome-shaped ante-
interaction of T. gondii zoites with host cells has been rior ends of the developing progeny. The IMC and
derived from in vitro cultivation with tachyzoites. Limited subpellicular microtubules continue to extend posteri-
information is available on initial host-cell interaction orly and surround one half of the nucleus, which even-
with bradyzoites and sporozoites. In 1 study, host ER, but tually pinches into 2. Partitioning of the ER and the
not mitochondria, surrounded the initial phases of PV for- mitochondrion continue. Rhoptries and micronemes
mation.601 In mice orally inoculated with oocysts, spo- are synthesized de novo in the progeny. The progeny
rozoites excysted and passed through enterocytes and continues to grow until they reach the surface of the
goblet cells of the mouse ileal epithelium and entered the parent. The IMC of the parent disappears, and its outer
lamina propria where they infected all cells of the host, membrane becomes the plasmalemma of the progeny
Figure 2.6
TEM of T. gondii sporozoites in mouse ileum at 2 hours after oocyst oral inoculation. (a) Two intracellular sporozoites
located above the host nucleus (Hn) in an ileal enterocyte; note the electron-dense material (Ed) in the PV surrounding
the sporozoite cut in cross-section and the tubulovesicular membranous network (Tm) in the other sporozoite. Am, amy-
lopectin granule; Dg, dense granule; Mn, microneme; Nu, nucleus of sporozoite; Rh, rhoptry. (b) Sporozoite located at the
base of an ileal enterocyte. BI, basal lamina of the intestinal epithelium; Hn, host cell nucleus; Mv, microvilli of enterocyte;
Lp, lamina propria. (Speer, C.A., Clark, S., Dubey, J.P., 1998, J. Parasitol., 84, 505–512.1166)
cells. The organelles in progeny are synthesized de endodyogeny. In vivo, most groups of tachyzoites
novo; however, a recent study proposed recycling of are arranged randomly due to asynchronous cycles
the microneme protein MIC2 from mother to daugh- of endodyogeny. However, occasionally rosettes are
ter tachyzoites.991 Tachyzoites continue to divide by formed due to synchronous division (Figure 2.10). In
Figure 2.7
TEM of T. gondii sporozoites in ileal lamina propria of a mouse at 6 hours after feeding irradiated sporulated oocysts.
(a) Two sporozoites in a macrophage (Mo); Ec, enterocyte; En, endothelial cell of blood vessel. (b) Sporozoite within
a macrophage; Dg, dense granule; Go, Golgi complex; Mn, microneme; Nu, nucleus; Pv, parasitophorous vacuole;
Rh, rhoptry; Tn, tubulovesicular membrane network. (Dubey, J.P., Thayer, D.W., Speer, C.A., Shen, A.K., 1998, Int. J.
Parasitol., 28, 369–375.380)
rapidly dividing tissue culture adapted strains, T. gondii The rate of invasion and growth varies depending on
within a vacuole may divide synchronously, but this is the strain of T. gondii and the host cells. After entry of
not the norm. Rarely, tachyzoites of certain strains may tachyzoites into a host cell, there is a variable period of
divide by binary fission. The host cell ruptures when it lag phase before the parasite divides, and this lag phase is
can no longer support the growth of tachyzoites. Exit partly parasite-dependent. Mouse virulent strains of T. gon-
from the host cell is mediated by a protein (TgPLP1) dii grow faster in cell culture than “avirulent” strains, and
secreted by the parasite. some strains of T. gondii form more rosettes than others.
Figure 2.8
TEM of T. gondii sst arising from the posterior end of a sporozoite (arrowheads). (a, b) An intracellular sporozoite point-
ing with its conoidal end toward the extremity of a human foreskin fibroblast protrusion, arising from the posterior pole
of the PVM. Note: posteriorly located nucleus (nu), clumps of amylopectin granules (am), and a dense granule (dg) in
sporozoite. (Tartarelli, I., Tinari, A., Possenti, A., Cherchi, S., Falchi, M., Dubey, J.P. and Spano, F., 2020, Int. J. Parasitol.,
50, 1099–1115.1207)
2.2.2 Bradyzoites and Tissue Cysts cysts are elongated and may be 100 μm long. Although
tissue cysts may develop in visceral organs, including the
2.2.2.1 Structure lungs, liver, and kidneys, they are more prevalent in the
neural and muscular tissues, including the brain, eyes, and
After a few rounds of multiplication, tachyzoite con- skeletal and cardiac muscles.
verts into a slowly replicating stage, bradyzoite, and The tissue cyst wall is elastic, argyrophilic, <0.5 μm
becomes enclosed in cyst wall (see Chapter 3 for stage thick (Figure 2.3), and it encloses hundreds of crescent-
conversion).865 The bradyzoite is the encysted stage of the shaped bradyzoites, 5–8.5 × 1–3 μm in size. The tissue
parasite in tissues. Bradyzoites are also called cystozo- cyst wall is only faintly periodic acid-Schiff (PAS) posi-
ites. To avoid confusion between the term cyst (also called tive compared to the enclosed bradyzoites (Figure 2.3f).
pseudocyst) in tissues versus oocyst in feces, we proposed The cyst wall contains chitin-like polysaccharides and
the term tissue cyst for the encysted stage of the parasite.355 glycoproteins that are detectable by fluorescently labelled
Tissue cysts grow and remain intracellular as the brady- lectins (Figure 2.3g).200,678 The tissue cyst develops within
zoites divide by endodyogeny. Tissue cysts vary in size; the PV in the host cell cytoplasm. The PV is rarely vis-
young tissue cysts may be as small as 5 μm in diameter ible in older tissue cysts. The thickness and the charac-
and contain only 2 bradyzoites (Figure 2.11), while older ter of the cyst wall may vary depending on the age of the
ones may contain thousands of organisms (Figure 2.3h). parasite and the host cell parasitized (Figure 2.12). The
Occurrence of odd numbers of bradyzoites in young tis- tissue cyst wall is uneven in thickness and appears rough.
sue cysts indicates asynchronous division. In histological The outer limiting membrane, probably derived both from
sections tissue cysts in the brain are often spheroidal and the host and the parasite, is lined with granular mate-
rarely reach a diameter of 70 μm, whereas intramuscular rial (hereon termed granular layer, GL) which also fills
Figure 2.9
TEM of an in vivo T. gondii tachyzoite undergoing endodyogeny. Note Cd, conoid of developing tachyzoite; Co, conoid
of mother tachyzoite; Dg, electron-dense granule; Ga, Golgi adjunct; Hm, host cell mitochondrion; Hn, host cell nucleus;
Id, inner membrane complex of developing tachyzoite; Im, inner membrane complex of mother tachyzoite; Mi, mitochon-
drion; Mn, microneme; Nu, nuclei of daughter tachyzoites; Pl, plasmalemma of mother tachyzoite; Pm, parasitophorous
vacuolar membrane; Pv, parasitophorous vacuole; Rh, rhoptries of daughter tachyzoites. (Dubey, J.P., Lindsay, D.S.,
Speer, C.A., 1998, Clin. Microbiol. Rev., 11, 267–299.381)
the space between the bradyzoites. In fixed material, the surrounded by host mitochondria, depending on the host-
GL consists of granules or particulate material with few cell parasitized or unknown factors. Mitochondria were
vesicles. In older tissue cysts, the GL has deep invagina- not surrounded in the tissue cyst in Figure 2.11b, but many
tions of the outer limiting membrane with interconnecting were present in the tissue cyst in Figure 2.12; both tissue
branches or channels extending up to half width of the GL. cysts were in mouse brain. The accumulation of micro-
Bradyzoites are juxtaposed against the GL (Figure 2.13). tubules and intermediate filaments around the tissue cyst
Some bradyzoites degenerate, especially in older tissue wall apparently provide rigidity to the tissue cyst wall.969
cysts. In younger tissue cysts, the bradyzoites are often Tissue cysts are metabolically active and small molecules
plump and contain relatively fewer organelles than in older (10 kDa) can diffuse through the tissue cyst wall.
tissue cysts (Figure 2.13). Factors regulating the formation Bradyzoites differ structurally only slightly from
of tissue cysts in vivo are not fully understood. The PV in tachyzoites (Table 2.1). They have a nucleus situated
tissue cysts lacks typical TMN found in tachyzoites. The toward the posterior end, whereas the nucleus in tachyzo-
matrix between bradyzoites has vesicles, lipid-like bodies, ites is more centrally located. The contents of rhoptries
and tubular structures. The tissue cyst may or may not be in bradyzoites are usually electron dense, whereas those
Figure 2.10
TEM of 4 T. gondii tachyzoites in final stages of endodyogeny that are still attached by their posterior ends to a common
residual body (Rb); note that several host cell mitochondria (*) are situated in close proximity to the PV, which con-
tains extensively developed tubulovesicular membranes (Tv); Am, amylopectin granule; Co, conoid; Dg, electron-dense
granule; Hn, host cell nucleus; Mn, microneme; Mp, micropore; Nu, nucleus; Rh, rhoptry. (Dubey, J.P., Lindsay, D.S.,
Speer, C.A., 1998, Clin. Microbiol. Rev., 11, 267–299.381)
in tachyzoites are labyrinthine. However, the contents of 2.2.2.2 Tissue Cyst Distribution in Host Tissues
rhoptries in bradyzoites vary with the age of the tissue cyst.
Bradyzoites in younger tissue cysts may have labyrinthine Tissue cyst distribution is in part controlled by the
rhoptries, whereas those in older tissue cysts are electron host, as shown with studies in rodents and cats.376,378
dense. Also, most bradyzoites have 1–3 rhoptries that are Knowledge on distribution of tissue cysts and the num-
looped back on themselves (Figure 2.13a). Bradyzoites ber present per gram of tissue are of epidemiologic sig-
contain several amylopectin granules which stain red with nificance. In food animals, more tissue cysts are present
PAS reagent; such material is either in discrete particles in muscles than in the brain. Distribution of tissue cysts
or is absent in tachyzoites. Bradyzoites are thinner than in different organs of animals fed oocysts of the GT-1
tachyzoites. There are more micronemes in bradyzoites, strain of T. gondii is shown in Table 2.2. In all hosts,
reaching posterior to the nucleus (Figure 2.13b). Even in muscular tissues were more parasitized than the brain,
the youngest tissue cyst containing only 2 bradyzoites, the and tissue cysts were also present in visceral tissues.
nucleus can be terminally located (Figure 2.11a). Tissue Similar observations were made with naturally infected
cysts are an integral part of the life cycle of T. gondii and animals (Table 2.3). Heart was the most consistently
are formed as early as 3 days p.i. In my opinion, there are infected organ. In a comparative study, pepsin digests of
no cyst-less strains of T. gondii in nature. the brains, heart, and leg muscles of chickens and cats
Figure 2.11
T. gondii tissue cysts in mouse brain. (a) Impression smear. Five small tissue cysts with silver positive cyst wall. Silver
stain and Giemsa. (b) TEM of a tissue cyst with only 4 bradyzoites. This is the youngest tissue cyst that I have examined
by TEM. Note well defined cyst wall clearly within a PV. The enclosed organisms have only a few organelles (amylopec-
tin granules-Am, rhoptries-Ro, micronemes-Mn, dense granules-Dg, and a conoid-Co), but the nucleus (Nu) is terminal.
(c) TEM of a small intracellular cyst with well-developed cyst wall. Note cyst wall (arrowheads) and amylopectin (Am) in
bradyzoites. The host cell nucleus (Hcn) is closely applied to the cyst wall. The PV is no longer visible. (From Dubey,
J.P., 2010, Toxoplasmosis of Animals and Humans, 2nd ed., CRC Press, Boca Raton.403)
were bioassayed in mice, 5 mice per digest (Table 2.4). 2.2.2.3 Tissue Cyst Rupture and Reactivation
Hearts were more positive than brains. Additionally,
the proportion of mice infected versus inoculated was Unlike food animals, murine brain has more tissue
also higher for the heart than the brain, indicating that cysts than other organs. Although more tissue cysts are
more T. gondii were present in the infected hearts than found per gram of tissue in mice than other hosts, the fate
brains (Table 2.4). The amount of tissue bioassayed was of tissue cysts is difficult to study in mice because mice
not the issue as in case of chickens; the entire brain was are never completely immune to T. gondii, and new tissue
bioassayed. cysts are formed even in chronic infections (Figure 2.14).
Estimates of T. gondii per gram of muscle in lambs In a quantitative study, tissue cyst rupture was found in
and goats naturally infected with T. gondii were low only 2 (0.27%) of 750 tissue cysts examined in the brains of
(Table 2.5). For this, 5, 10, and 50 g samples from natu- experimentally infected mice, although T. gondii-positive
rally infected lambs and goats from a local grocery were debris was found in 8 (1.4%) glial nodules.489,490 Another
bioassayed in mice for T. gondii. Not all 5 and 10 g sam- paper quantitatively studied the dynamics of tissue cysts in
ples were infected, indicating uneven distribution of tissue CBA/J mice infected with the ME 49 strain. Tissue cysts
cysts (Table 2.5). were separated by Percoll gradient fractionation from the
Bioassays of different tissues of naturally infected brains of mice euthanized at 3, 4, 5, 6, and 8 weeks p.i. The
pigs, goats, and lambs indicated that T. gondii was pres- number of tissue cysts and their sizes was remarkably simi-
ent in virtually all edible tissues (Table 2.6). T. gondii lar 3–8 weeks p.i.; both small (<40 μm) and large (>70 μm)
was widely distributed in the tissue of infected food tissue cysts were found at all time points.1304 There was no
animals. evidence for cyclic rupture of tissue cysts and formation of
Figure 2.12
TEM of a T. gondii tissue cyst in the heart of a naturally infected brushtail possum (Trichosurus vulpecula) from
Australia. The cyst wall (Cw) is butted against the cytoplasm of the cardiac myocyte. Note 1 plump bradyzoite with an
anterior conoid (Co), subterminal nucleus (Nu), amylopectin (Am), and numerous micronemes (Mn). (From Dubey, J.P.,
2010, Toxoplasmosis of Animals and Humans, 2nd ed., CRC Press, Boca Raton.403)
many new tissue cysts. Evidence indicated that the loss of because serological negativity does not equate with para-
tissue cysts (if any) is balanced by emergence of an equal site ‘‘cure”. When and how tissue cysts rupture is largely
number of tissue cysts destroyed. 1304 Whether this phe- unknown. Treatment with corticosteroids, antilympho-
nomenon is peculiar to the strain of mouse and the ME 49 cyte serum, and anti-interferon antibody is known to
strain requires further study.1304 induce immunosuppression and relapse due to toxoplas-
Factors affecting tissue cyst rupture are largely mosis. The animal model, route of inoculation, stage of
unknown. Tissue cyst rupture has rarely been documented T. gondii used for primary infection, and criteria used for
in naturally infected immunocompetent hosts. I have evaluation of relapses are all important considerations.
examined tissues of many naturally infected animals, For example, hamsters are more corticosteroid-sensitive
found ruptured tissue cysts only rarely.403 than mice or rats, and oral administration of cortico-
In a more recent study in experimentally infected rats, steroids is less effective than parenterally administered
tissue cyst rupture was frequent (Figures 2.15 and 2.16).434 corticosteroids.
However, there was no evidence for reactivation and the The genesis of new generations of tissue cysts in chroni-
presence of tachyzoites. Although observations were lim- cally infected mice is unknown. Clusters of tissue cysts are
ited to rats infected for 2 months, there was no evidence found in mice infected with certain strains of T. gondii, and
for the formation of new tissue cysts.434 sometimes in clinically normal mice. Whether bradyzoites
Little information is available concerning the mecha- leak out from intact tissue cysts is uncertain but unlikely.
nisms of relapse. Intact tissue cysts probably do not cause The rupture of tissue cysts and subsequent multiplication
any harm and persist for the life of the host, but this con- of tachyzoites can lead to fulminating toxoplasmosis even
cept has been questioned.1070 There are no definitive data in chronically infected mice. Tachyzoites may persist in
concerning the persistence of tissue cysts or lack of it chronic infection in certain hosts.
Figure 2.13
TEM of a T. gondii tissue cyst in mouse brain, 6 months p.i. (a) Note numerous bradyzoites are enclosed in cyst wall
(arrowheads). Several bradyzoites (marked 1-4) have looped rhoptries; 1 rhoptry is almost as long as the bradyzoite and
the blunt end of the rhoptry is pointed towards conoid (arrows). (b) Longitudinal section of a bradyzoite with an anterior
conoid (Co), few rhoptries (Ro), amylopectin granules (Am), dense granules (Dg), nucleus (Nu), cyst wall (Cw), numer-
ous haphazardly arranged micronemes (Mn), a mitochondrion (Mt); the posterior end is thickened (double arrows). The
cyst wall membrane is invaginated and the branches extend half-way into the interior of the cyst wall (arrowheads). Host
mitochondria (arrows) surround the cyst wall. (From Dubey, J.P., 2010, Toxoplasmosis of Animals and Humans, 2nd ed.,
CRC Press, Boca Raton.403)
Table 2.1 Relative Numbers (Mean, Range) of Organelles and Inclusion Bodies in Sporozoites, Tachyzoites, and Bradyzoites
of the VEG Strain of T. gondii as Determined Ultrastructurallya
Stage Rhoptries Micronemes Dense Granules Amylopectin Lipid
Sporozoite 5.9 (2–11) 55 (40–78) 9.4 (5–15) 7.8 (3–13) 1.25 (1–3)
Tachyzoite 6.7 (2–11) 25 (19–38) 9.1 (5–17) 2.4 (1–6) 0.6 (0–2)
Bradyzoite 5.5 (2–8) 75.5 (36–112) 2.7 (1–5) 21.8 (7–38) 0
a Source: Dubey, J.P., Lindsay, D.S., Speer, C.A., 1998, Clinic. Microbiol. Rev., 11, 267–299.381
Table 2.2 Persistence of T. gondii in Tissues of Animals Fed Oocysts the GT-1 Straina
Species Days p.i. Liver Kidneys Brain Skeletal Muscles Heart Diaphragm Reference
Sheep 97–173 6/8b 5/8 4/8 6/8 7/8 6/8 Dubey (1984)
Goats 335–441 6/6 3/6 5/6 6/6 6/6 6/6 Dubey (1982)
Horses 33–476 0/13 1/13 2/13 2/13 3/13 ND Dubey (1985)
Cattle 256, 267 2/2 1/2 0/2 1/2 0/2 0/2 Dubey (1983)
Pigs 38–171 2/8 2/8 8/8 5/8 8/8 4/8 Dubey et al. (1984, 1986); Dubey (1988)
Elk 73 1/2 0/2 2/2 1/2 1/2 2/2 Dubey et al. (1980)
Bison 28 1/1 0/1 0/1 0/1 0/1 ND Dubey (1983)
Coyotes 49–84 ND 1/4 3/4 4/4 2/4 2/4 Dubey (1982)
Foxes 36 2/2 ND 2/2 2/2 2/2 ND Dubey et al. (1983)
Dogs 166, 167 1/4 0/4 0/4 4/4 3/4 ND Dubey (1985)
a Source: Dubey, J.P., Lindsay, D.S, Speer, C.A., 1998, Clinic. Microbiol. Rev., 11, 267–299.381 For references see this paper.
b No. of infected animals/no. of animals fed T. gondii. Pepsin digests of tissues (50 g) were bioassayed in mice.
Table 2.3 Prevalence (%) of Viable T. gondii in Brain and Muscles of Naturally Infected Animalsa
Host No. Bioassayed Brain Muscle (Organ) Reference
Sheep 31 29.0 58.0 (diaphragm) Jacobs et al. (1963)
Chickens 136 49.2 89.5 (heart) Dubey (2010)
Goats 10 30.0 100.0 (skeletal muscle) Dubey (1983)
Dogs 43 46.5 81.3 (heart) Dubey et al. (2007a–2007c)
Cats 60 20.0 56.6 (skeletal muscle) Dubey (1981); Dubey et al. (1986);
Dubey et al. (2006); Dubey et al. (2007)
Source: Dubey, J.P., 2010, Toxoplasmosis of Animals and Humans, 2nd ed., CRC Press, Boca Raton. For references see
this book.403
a 50–100 g of tissue was digested in pepsin and homogenates bioassayed in mice.
Table 2.4 Prevalence (%) of Viable T. gondii in Brain, Heart, and Leg Muscles of Naturally Infected Chickens and Cats
a Chickens (n = 26)431 bCats (n = 15)387
No. of chickens No. of Mice Positive/130 No. Bioassay No. of Mice Positive/75
Tissue Bioassay Positive (%) Mice Inoculated (%) Positive (%) Mice Inoculated
Brain 3 (11.5) 5 (3.8) 4 (26.6) 18 (24.0)
Heart 26 (100.0) 115 (88.4) 13 (86.6) 50 (66.6)
Leg muscle 11 (42.3) 28 (21.5) 9 (60.0) 38 (50.6)
a Whole brain, whole heart and 100 g of leg muscle bioassayed; total mice per tissue: 130 (5 per tissue of each chicken).
b 50 g of each tissue bioassayed; total per tissue 75 (5 mice per tissue of each cat).
Table 2.5 Presence of Viable T. gondii in Skeletal Muscle Samples of Naturally Infected Lambs and Goats Determined by
Bioassay in Mice
No. of Positive Samples/Total Samples No. of Positive Mice/
Host Sample Size (g) Tested (%) Total Mice Inoculated (%)
Lambs 5 8/24 (33.3) 13/48 (27.0)
10 12/24 (50.0) 18/48 (37.5)
50 17/20 (85.0) 63/100 (63.0)
Goats 5 15/24 (66.6) 28/48 (50.0)

10 20/24 (83.3) 31/48 (64.5)
50 20/20 (100.0) 99/100 (99.0)
Source: Rani, S., Cerqueira-Cézar, C.K., Murata, F.H.A., Kwok, O.C.H., Dubey, J.P., Pradhan, A.K., 2020, J. Food.
Protect., 83, 1396–1401.1040
Table 2.6 Distribution of Viable T. gondii in Tissues of Naturally Infected Pigs, Goats, and Lamb
Grams of Tissue
Host No. Bioassayed Infected Tissues Reference
Pig 4 50 Arm picnic of 3, Boston butt of 2, ham of 1, spare ribs of 2, 351
bacon of 1, tongue of 3, diaphragm of 2, heart of 2, and
brain of 1, but not from kidney and liver
Goat 5 50 Liver of 1, kidneys of 1, hearts of 4, diaphragms of 4, rear leg 340
muscles of 5, and brain of 1
Lamb 8 100 Legs of 8, lamb chops of 7, tongue of 7, and heart of 3 357
2.3 LIFE CYCLE IN THE 3 infectious stages of T. gondii, i.e., tachyzoites, brady-
DEFINITIVE HOST, THE CAT zoites, and oocysts. Prepatent periods (time to the excre-
tion of oocysts after initial infection) and frequency of
Cats, not only domestic (Felis catus) but nearly oocyst excretion vary according to the stage of T. gon-
all species of felids (Table 2.7), can excrete T. gondii dii ingested (Table 2.8). Prepatent periods are 3–10 days
oocysts. Cats excrete oocysts after ingesting any of the after ingesting tissue cysts, and more than 18 days after
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the Lake Tchad. He observed them in flocks, and in considerable
numbers. Hitherto they have been sparingly seen by travellers, and
few specimens have reached our collections.
Genus. Ciconia. Briss.
Species 18.—Ciconia Marabou.
Ciconia Argala. Temm. Pl. Col. 301.

This bird was met with rather plentifully in the neighbourhood of
large towns, in company with the Vultures, to the manners of which
we have already referred, page 195. Like them, they were protected
by the natives, in consideration of the services they performed in
clearing away all the offensive substances which were thrown out to
them from the towns. In India, we find that the corresponding
species, Ardea Argala, Lath., is held in equal estimation for similar
services. Major Denham mentions his having frequently been a
witness of their voracious and omnivorous habits.
M. Temminck first figured and characterized this African species
as distinct from that of India. He has given it the name of Argala,
while for the Indian bird, which had already received that name from
Dr. Latham, he proposes the name of Marabou. We have ventured to
reverse the order of these names; and while we retain for the Indian
species the original name conferred on it by Dr. Latham, which, it is
to be recollected, is an Indian word, we have assigned the African
species the title of Marabou, which, it is equally to be observed, is a
word peculiar to Africa.
The specimen brought home by the present expedition appears to
be a young bird, and answers to the description given of the young
of this species by M. Temminck. The colours are nearly black in the
bird before us, which are grey in the adult bird figured by that
gentleman. Major Denham mentions his having noticed some birds
nearly allied to this species, which were larger, and different in
colour, and which he conceived to be distinct. They probably were
the adult birds of this species.
Ordo. Natatores. Ill.
Fam. Anatidæ. Leach.
Subfam. Anserina. V. in Zool. Journ.
Genus. Plectropterus. Leach.
Species 19.—Plectropterus Gambensis.
Plectropterus Gambensis. Steph. in Shaw’s Zool. XII. Part 2. p.

7. pl. 36.
Anas Gambensis. Linn. I. 195.
Spur-winged Goose. Lath. Gen. Hist. X. 241.
This bird was found in flocks of great numbers on all the lakes.
The flesh was very coarse, and of a fishy taste, and afforded very
bad eating.
Species 20.—Plectropterus melanonotus.
Plectropterus melanotos. Steph. in Shaw’s Zool. XII. Part 2. p. 8.

Anser melanonotus. Forst. Zool. Ind. p. 21. t. 11.
Anas melanonotus. Lath. Ind. Orn. 839.
Oye de la côté de Coromandel. Pl. Enl. 937.
Black-backed Goose. Penn. Ind. Zool. p. 12. t. 11.
This species, of which fine specimens of the male and female are
preserved in the collection, was met with on the lake Tchad. It was
not seen in any abundance, and was found in company with other
species of the family. The protuberance on the bill of the male is
much more enlarged and prominent than is represented in the
“Planches Enluminées.”
Subfam. Anatina. V. in Zool. Journ.

Genus. Anas. Auct.
Species 21.—Anas viduata.

Anas viduata. Linn. I. 205.
Canard du Maragnan. Pl. Enl. 808.
Spanish Duck. Penn. Gen. of Birds, p. 65. t. 13.
This species was very common, both on Lake Tchad and on all
the smaller lakes. It was excellent eating. Mr. Pennant has described
the species as an inhabitant of America and Africa. Linnæus says
only, that it is found in the lakes of Carthagena; those, it is supposed,
of New Spain. Our bird accords very accurately with his description
of the species, and also with the figure quoted above from the
“Planches Enluminées.” We have every reason to conclude with Mr.
Pennant, that the species inhabits both the Old and New Continent.
The bend of the wing exhibits the rudiments of a spur.
Fam. Pelecanidæ. Leach

Genus. Onocrotalus. Briss.
Species 22.—Onocrotalus Brissonii.
Pelicanus Onocrotalus. Linn. I. 215.

Le Pelican. Pl. Enl. 87.
White Pelican. Edw. t. 92.
This well known species has been described to us by Major
Denham as very abundant on the borders of Lake Tchad. The genus
Onocrotalus was first instituted by M. Brisson; but, according to his
custom, he left the present species without any specific name. M.
Cuvier, in his “Regne Animal,” acknowledges the genus; but neither
has he specifically distinguished the bird. We feel much pleasure in
now assigning it a name, in memory of the first characterizer of the
group; an ornithologist, whose works cannot be studied without the
highest advantage, but whose labours have never as yet been
sufficiently appreciated.
Genus. Phalacrocorax. Briss.

Species 23.—Phalacrocorax pygmæus.
Pelecanus pygmæus. Pall. Reise. II. 712. t. G.

Dwarf Shag. Lath. Gen. Hist. X. 431.
Cormoran pygmée, jun. Temm. Man. d’Orn. p. 901.
This bird, which agrees very accurately with M. Temminck’s
description of the young of his Cormoran pygmée, was met with by
Major Denham on one of the smaller lakes in central Africa. He
describes the species as very rarely occurring.
Genus. Plotus. Linn.
Species 24.—Plotus melanogaster.
Plotus melanogaster. Gmel. I. 580.

Anhinga melanogaster. Forst. Zool. Ind. p. 22. t. 12.
Anhinga de Cayenne. Pl. Enl. 959.
Black-bellied Anhinga. Penn. Ind. Zool. p. 13. t. 12.
Black-bellied Darter. Lath. Gen. Hist. X. 451.
This bird was seen but once or twice during the course of the
expedition. It was met with on one of the smaller lakes. It seems to
have a very extensive geographical distribution, being found in the
New World, in the islands of Java and Ceylon, and now in the interior
of Africa.
There are remnants of several other species of birds in the

collection, consisting chiefly of bills, legs, and wings. Among them
we can trace the apparent remains of the Ciconia alba, Briss.; Ardea
garzetta, Linn.; different species of the genus Lamprotornis, Temm.;
with various others, of which we regret that we cannot venture to
give any description. The foregoing twenty-four species are all that
we can undertake to determine upon with accuracy.
Classis. Reptilia. Auct.
Ordo. Sauriens. Cuv.
Tribus. Lacertiens. Cuv.
Genus. Monitor. Cuv.
Species 1.—Monitor Niloticus.
Lacerta Nilotica. Linn. I. 360.

Varanus Dracæna. Merr. Syst. Amph. p. 59.
Tupinambis Niloticus. Daud. Rept. III. 51.
Monitor du Nile, ou Ouaran. Cuv. Reg. Anim. II. 25.
Tribus. Cameleoniens. Cuv.

Genus. Chamæleo. Lacép.
Species 2.—Chamæleo vulgaris.
Chamæleo vulgaris. Daud. Rept. IV. 181.

Chamæleo carinatus. Merr. Syst. Amph. p. 162.
Lacerta chamæleon. Linn. I. 364.
FOOTNOTES:
[82]Voyage, ii. 20.

[83]Desmarest states, (Ency. Meth. note), that he cannot find
any work of Lacépède in which the genus Fennecus is proposed.
[84]Perhaps M. Cuvier was led into this mistake by an error of
the pen or press, in M. Desmarest’s translation of Bruce’s
description of the animal. Bruce says, “from the snout to the anus,
he was about ten inches long;” the translation, “Ce Fennec avoit
six pouces de longueur, depuis le bout du nez jusqu’ à l’origine de
la queue.” The same mistake occurs in M. Geoffroy Saint Hilaire’s
quotation of Bruce; but this cannot be a misprint, for the length is
not expressed by the word six, but by the Arabic cypher 6.
[85]Taken as the stuffed specimen stands.
[86]Oubara seems to be a general name for the Bustards in
Africa. A smaller species than the present, of that country, has
received this name as a specific title from M. Gmelin.
No. XXII.
BOTANICAL APPENDIX.
BY ROBERT BROWN, ESQ. F.R.SS. L. & E., F.L.S.
The Herbarium formed during the expedition, chiefly by the late

Dr. Oudney, contains specimens, more or less perfect, of about three
hundred species. Of these one hundred belong to the vicinity of
Tripoli; fifty were collected in the route from Tripoli to Mourzuk, thirty-
two in Fezzan, thirty-three on the journey from Mourzuk to Kouka,
seventy-seven in Bornou, and sixteen in Haussa or Soudan.
These materials are too inconsiderable to enable us to judge
correctly of the vegetable productions of any of the countries visited
by the mission, and especially of the more interesting regions,
Bornou and Soudan.
For the limited extent of the herbarium, the imperfect state of
many of the specimens, and the very scanty information to be found
respecting them, either in the herbarium itself, or in the Journal of the
collector, it is unfortunately not difficult to account.
Dr. Oudney was sufficiently versed in Botany, to have formed
collections much more extensive and instructive, had the
advancement of natural history been the principal purpose of his
mission. His time and attention, however, were chiefly occupied by
the more important objects of the expedition: as a botanist he had no
assistant; and the state of his health during his residence in Bornou
must, in a great degree, have rendered him unable to collect or
observe the natural productions of that country.
For the few specimens belonging to Soudan, we are indebted to
Captain Clapperton, who, after the death of Dr. Oudney,
endeavoured to preserve the more striking and useful plants which
he met with. His collection was originally more considerable; but
before it reached England, many of the specimens were entirely
destroyed. It still includes several of the medicinal plants of the
natives; but these being without either flowers or fruit, cannot be
determined.
In the whole herbarium, the number of undescribed species hardly
equals twenty; and among these not one new genus is found.
The plants belonging to the vicinity of Tripoli were sent to me by
Dr. Oudney, before his departure for Fezzan. This part of the
collection, amounting to one hundred species, was merely divided
into those of the immediate neighbourhood of Tripoli, and those from
the mountains of Tarhona and Imsalata.
It exceeds in extent the herbarium formed by Mr. Ritchie near
Tripoli, and on the Gharian hills, which, however, though containing
only fifty-nine species, includes twenty-seven not in Dr. Oudney’s
herbarium.
The specimens in Mr. Ritchie’s collection are carefully preserved,
the particular places of growth in most cases given, and
observations added on the structure of a few; sufficient at least to
prove, that much information on the vegetation of the countries he
visited might have been expected from that ill-fated traveller.
In these two collections united, hardly more than five species are
contained not already published in the works that have appeared on
the botany of North Africa; particularly in the Flora Atlantica of M.
Desfontaines, in the Flore d’Egypte of M. Delile, and in the Floræ
Libycæ Specimen of Professor Viviani, formed from the herbarium of
the traveller Della Cella.
The plants collected in the Great Desert and its oases, between
Tripoli and the northern confines of Bornou, and which somewhat
exceed a hundred, are, with about eight or ten exceptions, also to be
found in the works now mentioned. And among those of Bornou and
Soudan, which fall short of one hundred, very few species occur not
already known as natives of other parts of Equinoctial Africa.
A complete catalogue of the herbarium, such as I have now
described it, even if the number and condition of the specimens
admitted of its being satisfactorily given, would be of but little
importance, with reference to the geography of plants. Catalogues of
such collections, if drawn up hastily, and from imperfect materials, as
must here have been the case, are indeed calculated rather to injure
than advance this department of the science, which is still in its
infancy, and whose progress entirely depends on the scrupulous
accuracy of its statements. To produce confidence in these
statements, and in the deductions founded on them, it should in
every case distinctly appear, that in establishing the identity of the
species enumerated, due attention has been paid to the original
authorities on which they depend, and, wherever it is possible, a
comparison actually made with authentic specimens.
In the account which I am now to give of the present collection, I
shall confine myself to a slight notice of the remarkable known plants
it contains, to characters or short descriptions of the more interesting
new species, and to some observations on such of the plants as,
though already published, have either been referred to genera to
which they appear to me not to belong, or whose characters require
essential alteration.
In proceeding on this plan, I shall adopt the order followed in the
botanical appendix to Captain Tuckey’s Expedition to the River
Congo. And as there will seldom be room for remarks on the
geographical distribution of the species I have to notice, I shall
chiefly endeavour to make my observations respecting them of some
interest to systematic botanists.
Cruciferæ. Fifteen species belonging to this family exist in the
collection, one of which only appears to be undescribed, and of this
the specimens are so imperfect, that its genus cannot with certainty
be determined. Of those already published, however, the generic
characters of several require material alterations, some of which
suggest observations relative to the structure and arrangement of
the natural order.
Savignya Ægyptiaca, (De Cand. Syst. 2. p. 283,) is the first of
these. It was observed near Bonjem, by Dr. Oudney, whose
specimens slightly differ from those which I have received from M.
Delile, by whom this plant was discovered near the pyramid of
Saqqârah, and who has well figured and described it in his Flore
d’Egypte, under the name of Lunaria parviflora. By this name it is
also published by M. Desvaux. Professor Viviani, in giving an
account of his Lunaria libyca, a plant which I shall presently have
occasion to notice more particularly, has remarked[87], that Savignya
of De Candolle possesses no characters sufficient to distinguish it as
a genus from Lunaria; and still more recently, Professor Sprengel
has referred our plant to Farsetia[88]. The genus Savignya, however,
will no doubt be ultimately established, though not on the grounds on
which it was originally constituted; for the umbilical cords certainly
adhere to the partition, the silicule, which is never absolutely sessile,
is distinctly pedicellated in Dr. Oudney’s specimens, the valves are
not flat, and the cotyledons are decidedly conduplicate. In describing
the cotyledons of his plant as accumbent, M. De Candolle has
probably relied on the external characters of the seed, chiefly on its
great compression, its broad margin or wing, and on the whole of the
radicle being visible through the integuments. It would appear,
therefore, that the true character of the cotyledons of Savignya has
been overlooked, chiefly from its existing in the greatest possible
degree. To include this degree of folding, in which the margins are
closely approximated, and the radicle consequently entirely exposed,
a definition of conduplicate cotyledons somewhat different from that
proposed in the “Systema Naturale” becomes necessary. I may here
also observe, that the terms Pleurorhizæ and Notorhizæ, employed
by M. De Candolle, to express the two principal modifications of
cotyledons in Cruciferæ, appear to me so far objectionable, as they
may seem to imply that in the embryo of this family, the position of
the radicle is variable, and that of the cotyledons fixed. It is at least
deserving of notice, that the reverse of this is the fact; though it is
certainly not necessary to change these terms, which are now
generally received.
On the subject of Savignya, two questions naturally present
themselves. In the first place: Is this genus, solely on account of its
conduplicate cotyledons, to be removed from Alyssineæ, where it
has hitherto been placed, to Velleæ, its affinity with which has never
been suspected, and to whose genera it bears very little external
resemblance? Secondly: In dividing Cruciferæ into natural sections,
are we, with M. De Candolle, to expect in each of these subdivisions
an absolute uniformity in the state of the cotyledons? As far as
relates to the accumbent and flatly incumbent states, at least, I have
no hesitation in answering the latter question in the negative; and I
believe that in one case, namely Hutchinsia, these modifications are
not even of generic importance; for it will hardly be proposed to
separate H. alpina from petræa, solely on that ground. I carried this
opinion farther than I am at present disposed to do, in the second
edition of Mr. Aiton’s Hortus Kewensis, where I united in the genus
Cakile plants which I then knew to differ from each other, in having
accumbent and conduplicate cotyledons; and I included Capsella
bursa pastoris in the genus Thlaspi, although I was aware, both from
my own observations, and from Schkuhr’s excellent figure[89], that its
cotyledons were incumbent. I am at present, however, inclined to
adopt the subdivision of both these genera, as proposed by several
authors, and received by M. De Candolle; but to this subdivision the
author of the Systema Naturale must have been determined on other
grounds than those referred to; for in these four genera, in which the
three principal modifications of cotyledons occur, he has taken their
uniformity for granted.
As to the place of Savignya in the natural family, I believe, on
considering the whole of its structure and habit, that it ought to be
removed from Alyssineæ to a subdivision of the order that may be
called Brassiceæ, but which is much more extensive than the tribe
so named by M. De Candolle; including all the genera at present
known with conduplicate cotyledons, as well as some others, in
which these parts are differently modified.
There are two points in the structure of Savignya, that deserve
particular notice. I have described the æstivation of the calyx as
valvular; a mode not before remarked in this family, though existing
also in Ricotia. In the latter genus, however, the apices of the sepals
are perhaps slightly imbricate, which I cannot perceive them to be in
Savignya.
The radicle is described by M. De Candolle as superior, with
relation to the cotyledons. I am not sure that this is the best manner
of expressing the fact of its being horizontal, or exactly centrifugal,
the cotyledons having the same direction. This position of the seed is
acquired only after fecundation; for at an earlier period the foramen
of the testa, the point infallibly indicating the place of the future
radicle, is ascendant. From the horizontal position of the radicle in
this and some other genera, especially Farsetia, we may readily
pass to its direction in Biscutella, where I have termed it descendant;
a character which I introduced to distinguish that genus from
Cremolobus. But in Biscutella the embryo, with reference to its usual
direction in the family, is not really inverted, the radicle being still
placed above the umbilicus. On the contrary, in Cremolobeæ, a
natural tribe belonging to South America, and consisting of
Cremolobus and Menonvillea, though the embryo at first sight seems
to agree in direction with the order generally, both radicle and
cotyledons being ascendant, it is, in the same sense, not only
inverted, but the seed must also be considered as resupinate: for the
radicle is seated below the umbilicus, and also occupies the inner
side of the seed, or that next the placenta,—peculiarities which,
taken together, constitute the character of the tribe here proposed. It
appears to me singular that M. De Candolle, while he describes the
embryo of these two genera as having the usual structure of the
order, should consider that of Iberis, in which I can find no peculiarity,
as deviating from that structure[90].
Lunaria libyca of Viviani[91] is the second plant of Cruciferæ, on
which I have some observations to offer. This species was described
and figured, by the author here quoted, in 1824, from specimens
collected in 1817 by Della Cella. The specimens in the herbarium
were found near Tripoli, where the plant had also been observed in
1819 by Mr. Ritchie, who referred it to Lunaria, and remarked that
the calyx was persistent. Professor Sprengel, in his Systema
Vegetabilium, considers it a species of Farsetia.
That this plant ought not to be associated either with the original
species of Lunaria, or with Savignya, as now constituted, is
sufficiently evident. And if it is to be included in Farsetia, it can only
be on the grounds of its having a sessile silicule, with compressed
valves, an indefinite number of seeds in each cell, and accumbent
cotyledons. But in these respects it accords equally with Meniocus, a
genus proposed by M. Desvaux, and with some hesitation received
by M. De Candolle, and with Schivereckia of Andrzejowski, which he
has also adopted. It does not, however, agree with either of those
genera in habit, and it is easily distinguished from both by its simple
filaments and other characters, which I shall notice hereafter. Is this
plant, then, sui generis? ought it to be united with Alyssum, the
character of that genus being modified to receive it? or does not
Alyssum require subdivision, and may not our plant be referred to
one of the genera so formed? A brief result of the examination of
these questions, so far as they are connected with the subject under
consideration, will be found annexed to the character which is given
of the genus formed by the union of Lunaria libyca with Alyssum
maritimum, a plant also in the collection, from the neighbourhood of
Tripoli.
Alyssum maritimum, which is described both as an Alyssum and
as a Clypeola by Linnæus, is the Konig of Adanson, who founded his
generic distinction on the monospermous cells and supposed want
of glands of the receptacle; and M. Desvaux, admitting Adanson’s
genus, has named it Lobularia. In the second edition of Hortus
Kewensis I included this plant in Alyssum, which M. De Candolle has
also done in his great work.
For the genus here proposed I shall adopt Adanson’s name,
altering only the termination, and wishing it to be considered as
commemorating the important services rendered to botany by my
friend Mr. Konig, of the British Museum[92]. In comparing these two
species of Koniga, their agreement is very striking in habit, in leaves,
in the closely pressed bipartite pubescence, in the calyx, petals,
stamina, and stigma. They correspond also in some other points,
less obvious but equally important, which I shall separately notice.
The first of these is in having eight glands on the receptacle; a
character peculiar, I believe, to these plants, and which first
suggested the generic name Octadenia. The glands in Alyssum
maritimum were entirely overlooked by Adanson, are not noticed by
M. Desvaux, and M. De Candolle has described only the four that
subtend the longer stamina. These certainly are much more
conspicuous than the remaining four, which, however, occupy the
place of the only glands existing in several of the most nearly related
genera.
The number and position of the glands in this genus give some
support, perhaps, to the hypothesis which I have formerly advanced,
of the divisions of an hypogynous disk being in most cases formed of
abortive filaments; an opinion more strikingly confirmed, however, in
this family of plants, by their form and texture in Alyssum calycinum,
and minimum.
The second point in which the two species of Koniga agree is in
the structure of the septum. On this, which I consider as a new
source of character in Cruciferæ, I shall offer some remarks in
speaking of Farsetia.
The third point of agreement is the adhesion of the funiculi
umbilicales to the septum. This adhesion, though really existing, is
not very obvious in the monospermous cells of Koniga maritima; but
in the supposed variety of this species from Teneriffe, in which the
cells are occasionally dispermous, it is manifest, and is very
remarkable in all states of Koniga libyca.
I first introduced this adhesion of the funiculi to the septum, as a
generic character, in distinguishing Petrocallis from Draba. It has
since been advantageously employed in the character of Lunaria by
M. de Candolle, who, however, supposes this structure of much rarer
occurrence in Cruciferæ than it really is. According to my
observations, it is neither unfrequent, nor always of generic
importance. Thus, I find it to exist in some species only of Arabis,
namely A. Turrita, pendula, and canadensis, and hence I did not
introduce it into my generic character of Parrya, though I have
noticed it in my description of the species.
The principal difference existing between these two species of
Koniga is that the cells of the ovarium and silicula of K. maritima are
monospermous, while those of libyca are polyspermous, the number
being variable, apparently indefinite, but not exceeding six. There
are, however, other instances in this family, in which the mere
difference between definite and indefinite number of seeds is of
specific importance only, as in Draba and Meniocus, in each of which
a species exists with dispermous cells; and the objection arising from
the apparently still greater difference between unity and indefinite
number in the two species of Koniga is removed by a supposed third
species or variety of K. maritima, in which two seeds are
occasionally produced in each cell. It may even be observed, that
from unity to the indefinite number in this case, where the ovula in
the different cells are alternate, the transition is perhaps more easy
than from the binary to the indefinite, in cases where, as in Alyssum
properly so called, the ovula are placed opposite in the different
cells, and are in the same cell equidistant from its apex; this
symmetry, probably, admitting of addition only by fours.
The next genus of Cruciferæ to be noticed is Farsetia, a
fragment of the original species of which is in the collection. There
are also several specimens of a plant, found in the desert, supposed
to be new, and which, though without flowers, and considerably
different in the form of its stigma, I am inclined, from the
resemblance in habit, in pubescence, in silicula, in seeds, and
especially from the exact similarity in the structure of the septum, to
refer to the same genus[93].
As the introduction of the structure of the dissepiment into the
generic characters of Cruciferæ is now proposed for the first time,
and as I believe that its texture and appearance should always be
attended to in constituting genera in this family of plants, I shall here
offer a few remarks respecting it.
According to the particular view which I briefly but distinctly
published in 1818, and which M. de Candolle first adopted in 1821,
of the composition of the pistillum in Cruciferæ[94], the dissepiment in
this family is necessarily formed of two lamellæ, derived from the
parietes of the fruit. These lamellæ are in many cases easily
separable, and where their union is more intimate, their existence is
still evident from the want of correspondence, and consequent
decussation, of their areolæ. The lamellæ, which are usually very
thin and transparent, have their surface divided into areolæ, in
different genera of very different forms, some of which may, with
sufficient clearness, be described. In many cases no other
appearance exists; in some, however, the axis of the septum
resembles either a single nerve, or two distinct parallel nerves; and
from this axis, whether formed of one or two nerves, tubes having
the appearance and ramification of the veins of a leaf, and which
generally terminate within the margin, not unfrequently proceed. This
is remarkably the case in Farsetia, as I here propose to limit that
genus; the central vessels in both its species being closely
approximated, so as to form a single cord, extending from the apex
to the base of the septum, and the veins being numerous and
uncommonly distinct. Approaches more or less manifest to this
structure of Farsetia exist in several other genera, as in Parrya,
Savignya, and Koniga. But in this last mentioned genus the nerve,
which originates, as in all cases, at the apex, hardly extends, even in
the polyspermous species, beyond the middle of the septum, and the
veins, which are much less distinct, are descendent.
As far as my observations on this subject at present extend, I
expect, with great confidence, uniformity in the structure of the
septum of strictly natural genera, and in many cases, though
certainly not in all, I have found a resemblance in this respect in
more extensive groups. Thus Draba, Arabis, and Aubrietia, agree in
having amorphous areolæ, bounded by flexuose tubes or lines; while
Alyssum, Berteroa, and Fibigia, have narrow linear areolæ, bounded
by parallel or slightly arched lines. Capsella bursa differs from
Thlaspi and Æthionema, as Draba from Alyssum, and agrees with
Lepidium procumbens, Linn. improperly referred to Hutchinsia, and
which equally has incumbent cotyledons. Cochlearia differs in like
manner from Kernera. And numerous other examples of the same
agreement in nearly related plants, and of differences where the
usual sources of distinction are less available, might be noticed.
Hesperis nitens of Viviani is sparingly in the herbarium, both in
flower and fruit. The seeds, though not ripe, are sufficiently
advanced to show that the direction of the cotyledons is in this stage
accumbent; and, as I have found in Cruciferæ generally that the
ultimate agrees with the early state of cotyledons, I conclude they
are likewise accumbent in the ripe seed. The plant is also abundantly
different from Hesperis in other respects, and does not appear to be
referrible to any genus yet published. This new genus[95] I have
dedicated to the memory of Dr. Oudney, who found the present
species in many of the wadeys between Tripoli and Mourzuk, and
remarks that camels and mules eat it.
Hesperis ramosissima, which is also in the herbarium, was
found in Fezzan. This plant differs in aspect from most of the other
species of Hesperis, approaching in some points to Malcomia, in
others to Mathiola; and as its cotyledons are very obliquely
incumbent, it may form a section or subgenus, with a name,
Hesperis (Plagiloba) ramosissima, indicating that character.
Capparideæ, of which eight species occur in the collection, is the
family next to be noticed. I consider this order as belonging to the
same natural class with Cruciferæ; and that this class includes also
Resedaceæ, Papaveraceæ, and Fumariaceæ.
M. de Candolle, in defining Capparideæ, appears to regard the
ovarium as having in all cases only two placentæ, and therefore
formed of two pistilla or carpella. But to this, which is certainly the
more usual number, there are many exceptions. These exceptions
occur chiefly in the genus Capparis, which, as it is at present
constituted, includes species differing from each other in having an
ovarium with from two to eight placentæ, and, consequently,
composed of an equal number of pistilla. Capparis spinosa is the
most decided instance of the increased number of placentæ, and
this, as well as some other nearly related species, are also
remarkable in having septa subdividing the placentæ, and uniting in
the centre of the compound ovarium.
In the herbarium there are three species of the genus Cleome.
Two of these, C. pentaphylla and arabica, are in many respects well
known plants; the third I believe to be an undescribed species, but
nearly related to monophylla.
If the very natural group, formed by the Linnæan genus Cleome,
is not to be preserved entire, its subdivision must be carried much
farther, and established on other grounds, than has been done by M.
de Candolle, whose genera and sections appear to me to have been
equally founded on partial considerations. Thus, his Polanisia,
uniting all the Cleomes whose stamina exceed six, contains in its
first section, in addition to the species from which the genus was
formed, at least two sets of plants, having very little affinity either
with each other, or with the original species, whose only congener is
placed in a second section.
Gynandropsis also consists of two groups not very intimately
connected: the first is composed of species belonging to South
America, and having the usual æstivation of the family: the second,
of which C. pentaphylla may be taken as the type, is chiefly African,
and is readily distinguished by its very different æstivation,—the
great peculiarity of which consists in the petals not covering the
stamina at any period. To this mode of æstivation of petals, which
has never before been noticed, though it equally exists in Crateva
and in Resedaceæ, I shall apply the term aperta. It is constantly
conjoined, and, perhaps, necessarily connected with the early
opening of the calyx, whose segments are originally connivent and
slightly imbricate: for it may here be remarked, that in all the
modifications of what I have termed imbricate æstivation of petals,
they are, I believe, in the very early stage in like manner erect, and
the sexual organs equally exposed.
If the expediency of preserving the genus Cleome entire were
admitted, a question which I do not pretend at present to decide, it
would still be of the greatest importance to arrange its numerous
species according to their affinities, and carefully to distinguish the
subordinate groups that compose it. To such inferior groups, whether
termed subgenera or sections, names, in fact, have been of late
years very generally assigned, both by zoologists and botanists.
It has not yet been proposed, however, that these subgeneric
names should form an essential part of the name of the species;
although, by employing them in this manner, while the principal
groups would be kept in view, their subdivision would be carried to
the same extent, and the subordinate groups as well expressed as if
they had been actually separated into distinct genera.
The adoption of this method, which would not materially disturb
names already existing, would probably lead to a greater
consistency in the formation of genera, with reference to the natural
orders of which they are subdivisions. In this way also the co-
operation of two classes of naturalists, at present opposed to each
other on the question of the construction of genera, might to a
certain extent be expected, and greater uniformity in nomenclature
consequently secured.
These advantages appear to me so important, that some
expedient for obtaining them will, I am persuaded, at no distant
period, be generally adopted.
In favour of the present plan it may be remarked, that it is
analogous to the method followed by the Romans in the construction
of the names of persons, by which not only the original family, but
the particular branch of that family to which the individual belonged
was expressed. Thus the generic name corresponds with the nomen
(Cornelius), the name of the section with the cognomen (Scipio), and
that of the species with the prænomen (Publius).
Without attempting at present to obviate the objections to which
the proposed innovation is no doubt liable, I shall proceed to apply it
to Cleome pentaphylla. According to my view the genus Cleome
would include Gynandropsis, a name which, as that of a section,
may be continued to those species of M. de Candolle’s genus
belonging to equinoctial America, and having the common æstivation
of the family: while Gymnogonia, derived from its remarkable
æstivation, may be employed for the section that includes C.
pentaphylla, of which the name might be given in the following
manner:—
Cleome (Gymnogonia) pentaphylla. This plant, the earliest
known species of Cleome, and that on which the genus was chiefly
constituted, was found in Bornou. The species is regarded by M. de
Candolle as a native of the West India islands, and he doubts
whether it may not also belong to Egypt and India. On the other hand
I consider it a native of Africa and India, and am not satisfied with the
evidence of its being also indigenous to the American islands, where,
though now very common, it has probably been introduced by the
negroes, who use it both as a potherb and in medicine. It is not
unlikely that M. de Candolle, in forming his opinion of the original
country of this plant, has been in part determined by finding several
species of his Gynandropsis decidedly and exclusively natives of the
new continent. But if I am correct in separating these species from
the section to which Cleome (Gymnogonia) pentaphylla belongs, this
argument, which I have formerly applied to analogous cases[96],
would be clearly in favour of the opinion I have here advanced; those
species of the section with which I am acquainted being undoubtedly
natives of Africa or of India.
Cleome (Siliquaria) Arabica, (Linn. sp. pl. ed. 2. p. 939. De.
Cand. prodr. 1. p. 240), a supposed variety of which was found both
in the neighbourhood of Tripoli and in Soudan, belongs to another
subdivision of the genus, equally natural, and readily distinguishable.
The species of this subdivision are included in M. De Candolle’s
second section of Cleome, but are there associated with many other
plants, to which they have very little affinity.
All the species of Cleome Siliquaria are indigenous to North Africa
and Middle Asia, except violacea, which is a native of Portugal.
Cleome deflexa of M. De Candolle (prodr. 1. p. 240.), founded on
specimens in Mr. Lambert’s herbarium, which were sent by Don
Joseph Pavon as belonging to Peru, seems to present a remarkable
exception to this geographical distribution of the section. But on
examining these specimens I find them absolutely identical with
some states of violacea. I think it probable, therefore, either that they
are erroneously stated to have come from Peru, or that this species
may have been there introduced from European seeds.
Cadaba farinosa (Forsk. Arab. p. 68. De Cand. prodr. 1. p. 244)
is in the herbarium from Bornou. The specimen is pentandrous, and
in other respects agrees with all those which I have seen from
Senegal, and with Strœmia farinosa of my catalogue of Abyssinian
plants, collected by Mr. Salt, and published in his travels. M. De
Candolle, who had an opportunity of examining this Abyssinian plant,
refers it to his C. dubia, a species established on specimens found in
Senegal, and said to differ from farinosa, slightly in the form of the

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12.3 Prevalence of T. gondii DNA300

25.3 Clinical Infections447

J. P. Dubey, MVSc, PhD, 1,600 research papers in international journals, about

Introduction and History of Toxoplasma gondii

Table 1.1 (Continued) 

Table 1.1 (Continued) 

Biology of Toxoplasma gondii

Goats 5 15/24 (66.6) 28/48 (50.0)

Genus. Ciconia. Briss.

Species 18.—Ciconia Marabou.

Ciconia Argala. Temm. Pl. Col. 301.

Species 19.—Plectropterus Gambensis.

Plectropterus Gambensis. Steph. in Shaw’s Zool. XII. Part 2. p.

Species 20.—Plectropterus melanonotus.

Plectropterus melanotos. Steph. in Shaw’s Zool. XII. Part 2. p. 8.

Subfam. Anatina. V. in Zool. Journ.

Species 21.—Anas viduata.

Fam. Pelecanidæ. Leach

Species 22.—Onocrotalus Brissonii.

Pelicanus Onocrotalus. Linn. I. 215.

Genus. Phalacrocorax. Briss.

Pelecanus pygmæus. Pall. Reise. II. 712. t. G.

Genus. Plotus. Linn.

Species 24.—Plotus melanogaster.

Plotus melanogaster. Gmel. I. 580.

There are remnants of several other species of birds in the

Species 1.—Monitor Niloticus.

Lacerta Nilotica. Linn. I. 360.

Tribus. Cameleoniens. Cuv.

Species 2.—Chamæleo vulgaris.

Chamæleo vulgaris. Daud. Rept. IV. 181.

[82]Voyage, ii. 20.

BY ROBERT BROWN, ESQ. F.R.SS. L. & E., F.L.S.

The Herbarium formed during the expedition, chiefly by the late

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12.3 Prevalence of T. gondii DNA300

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Table 1.1 (Continued)

Table 1.1 (Continued)