Table Of ContentTHE BIOLOGY AND IDENTIFICATION
OF THE COCCIDIA (APICOMPLEXA)
OF RABBITS OF THE WORLD
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THE BIOLOGY AND
IDENTIFICATION
OF THE COCCIDIA
(APICOMPLEXA)
OF RABBITS OF
THE WORLD
DONALD W. DUSZYNSKI
UniversityofNewMexico,Albuquerque,NM
LEE COUCH
UniversityofNewMexico,Albuquerque,NM
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Dedication
This book is dedicated to Dr. Steve J. Upton prodigious and included: 225 original research
(June 14, 1953dJuly 29, 2010), who finished his papers in refereed journals; 11 book chapters;
M.S. degree in our laboratory in 1981. Steve three books (including the 2009 seminal work,
went on to complete his Ph.D. (1983) in The Coccidia of Snakes of the World, with D.W.
Zoology-Entomology, under the direction of Duszynski). Unfortunately, he was taken from
Dr. W.L. Current, Auburn University, Auburn, us much too soon, after a courageous, decade-
Alabama.From1983to1984,hewasapostdoc- long battle against cancer, in Manhattan, Kan-
toral fellow in parasitology in Bill Current’s sas, where he had lived the past 24 years.
laboratory. He spent 1984e1986, as a Visiting Steve was an extraordinary collector of hard-
Assistant Professor at the University of Texas- copy reprints throughout his life. One of his
El Paso, Texas, where he taught many classes great friends and colleagues at KSU was Bob
(GeneralBiology,MedicalParasitology,Human LaHew,alsoinBiologicalSciences,whohelped
Parasitology, Marine Invertebrate Zoology, Steve in the last decade of his life, and who
Protozoology, Human Anatomy and Physi- preserved Steve’s reprint collection so that one
ology)andworkedcloselywithDrs.JackBristol ofus(DWD)could transportittoNewMexico;
andLillianMayberry,withwhomhedeveloped a collection without which this book could not
a close and life-long friendship. In the fall of have been completedin its currentdetail.
1986,hebeganasanAssistantProfessorinBio- Steve’s work ethic and accomplishments
logical Sciences at Kansas State University were the stuff of which legends are made.
(KSU), where he progressed rapidly through Nonetheless,Steveremainedlow-key,humble,
theprofessorialranksanddevelopedapowerful and very human. We never met a person who
international reputation as the expert on the did not like or love Steve Upton. Steve would
basic biology, taxonomy, systematics, life have been proud to be a part of this under-
history, in vitro cultivation, and immunology of taking. His passing has created a noticeable
numerous coccidia (e.g., Caryospora, Eimeria, void and a large tear in the fabric of coccidian
Isospora, etc.) and Cryptosporidium species. His parasitology. He is, and always will be,
contributions toward our knowledge and deeply missed by both of us and by so many
understanding of the parasites he loved were others.
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Contents
EimeriaprincepsisDuszynski&Brunson,1973 42
Preface and Acknowledgments xi
EimeriaqinghaiensisYi-Fan,Run-Roung,Jian-Hua,
Jiang-Hui&Duszynski,2009 43
1. Introduction EimeriaworleyiLepp,Todd&Samuel,1972 44
IsosporamarquardtiDuszynski&Brunson,1972 45
RabbitsareFood,Pets,LabAnimals,andPests 2 IsosporayukonensisHobbs&Samuel,1974 47
RabbitsandtheHistoryofDiscoveryoftheCoccidia 2 SpeciesInquirendae(5þ) 48
HighPrevalenceandMultipleSpecies 4 DiscussionandSummary 50
AnEmergingDiseaseProblem 5
Coccidiosis:Disease,Symptoms,Perpetrators 5
EpidemiologyofDiseaseinRabbitsanditsLimitations 7 4. Coccidia (Eimeriidae) from the Family
TheSpeciesConcept 8 Leporidae: Genus Brachylagus
TaxonomyandSystematicsCrisesAffectBiodiversity 9
ModernDNATaxonomy 12 EimeriabrachylagiaDuszynski,Harrestien,
Taxonomyvs.Barcoding 13 Couch&Garner,2005 56
Parasites,ShrinkingEcosystems,andDisease 14
5. Coccidia (Eimeriidae) from the Family
2. Lagomorpha Origins and Diversification Leporidae: Genus Lepus
LagomorphBiodiversityandFamilialRelationships 18 Introduction 62
PhylogeneticRelationshipsandHistorical EimeriaamericanaCarvalho,1943 64
Biogeography 19 EimeriaathabascensisSamoil&Samuel,1977a 64
EimeriaauduboniiDuszynski&Marquardt,1969 65
EimeriabainaeAoutil,Bertani,Bordes,Snounou,
3. Coccidia (Eimeriidae) of the Family Chabaud&Landau,2005 66
Ochotonidae: Genus Ochotona EimeriacabaretiAoutil,Bertani,Bordes,Snounou,
Chabaud&Landau,2005 67
Introduction 26 Eimeriacampania(Carvalho,1943)Levine&Ivens,
EimeriabalchanicaGlebezdin,1978 26 1972 68
EimeriabanffensisLepp,Todd&Samuel,1973 27 EimeriacoquelinaeAoutil,Bertani,Bordes,Snounou,
EimeriabarrettiLepp,Todd&Samuel,1972 29 Chabaud&Landau,2005 69
EimeriacalentineiDuszynski&Brunson,1973 30 EimeriaeuropaeaPelle´rdy,1956 71
EimeriacircumborealisHobbs&Samuel,1974 32 EimeriaexiguaYakimoff,1934 73
EimeriacryptobarrettiDuszynski&Brunson,1973 33 EimeriagantieriAoutil,Bertani,Bordes,Snounou,
EimeriadauricaMatschoulsky,1947a 35 Chabaud&Landau,2005 73
EimeriaerschoviMatschoulsky,1949 36 EimeriagobiensisGardner,Saggerman,Batsaikan,
EimeriahaibeiensisYi-Fan,Run-Roung,Jian-Hua, Ganzorig,Tinnin&Duszynski,2009 74
Jiang-Hui&Duszynski,2009 37 EimeriagroenlandicaMadsen,1938Emend.
EimeriaklondikensisHobbs&Samuel,1974 38 Levine&Ivens,1972 75
EimeriametelkiniMatschoulsky,1949 40 EimeriaholmesiSamoil&Samuel,1977a 76
EimeriaochotonaMatschoulsky,1949 41 EimeriahungaricaPelle´rdy,1956 77
vii
viii CONTENTS
EimeriaintestinalisCheissin,1948 79 EimeriaintestinalisCheissin,1948 131
EimeriairresiduaKessel&Jankiewicz,1931 79 EimeriairresiduaKessel&Jankiewicz,1931 137
EimeriakeithiSamoil&Samuel,1977a 79 EimerialeporisNieschulz,1923 141
EimerialapierreiAoutil,Bertani,Bordes,Snounou, EimeriamagnaPe´rard,1925b 141
Chabaud&Landau,2005 80 EimeriamatsubayashiiTsunoda,1952 150
EimerialeporisNieschulz,1923 81 EimeriamediaKessel&Jankiewicz,1931 151
EimeriamacrosculptaSuga´r,1979 85 EimerianagpurensisGill&Ray,1960 156
EimeriamagnaPe´rard,1925b 86 EimerianeoleporisCarvalho,1942 157
EimeriamatsubayashiiTsunoda,1952 87 EimeriaoryctolagiRay&Banik,1965b 157
EimeriamediaKessel,1929 87 Eimeriaperforans(Leuckart,1879)Sluiter&
EimeriaminimaCarvalho,1943 88 Swellengrebel,1912 159
EimerianeoleporisCarvalho,1942 88 EimeriapiriformisKotla´n&Pospesch,1934 165
EimerianicolegeraeAoutil,Bertani,Bordes,Snounou, EimeriaroobrouckiGre´s,Marchandeau&
Chabaud&Landau,2005 88 Landau,2002 168
Eimeriaperforans(Leuckart,1879)Sluiter& Eimeriastiedai(Lindemann,1865)Kisskalt&
Schwellengrebed,1912 89 Hartmann,1907 169
EimeriapierrecoudertiAoutil,Bertani,Bordes, Eimeriavejdovskyi(Pakandl,1988)Pakandl&
Snounou,Chabaud&Landau,2005 90 Coudert,1999 181
EimeriapiriformisKotla´n&Pospesch,1934 91 SpeciesInquirendae(1) 183
EimeriapunjabensisGill&Ray,1960 92 DiscussionandSummary 183
EimeriareniaiAoutil,Bertani,Bordes,Snounou,
Chabaud&Landau,2005 92
Eimeriarobertsoni(Madsen,1938)Carvalho,1943 94
7. Coccidia (Eimeriidae) of the Family
EimeriarochesterensisSamoil&Samuel,1977a 97
Leporidae: Genus Sylvilagus
EimeriarowaniSamoil&Samuel,1977a 98
EimeriaruficaudatiGill&Ray,1960 98
Introduction 190
EimeriasculptaMadsen,1938 100
EimeriaauduboniiDuszynskiandMarquardt,
Eimeriasemisculpta(Madsen,1938)Pelle´rdy,1956 101
1969 191
EimeriaseptentrionalisYakimoff,Matschoulsky&
EimeriaazulWigginsandRothenbacher,1979 192
Spartansky,1936 103
EimeriaenvironHoness,1939 193
EimeriastefanskiiPastuszko,1961a 104
EimeriaexiguaYakimoff,1934 195
Eimeriastiedai(Lindemann,1865)Kisskaltand
Eimeriahonessi(Carvalho,1943)Emend.Levineand
Hartmann,1907 105
Ivens,1972andPelle´rdy,1974 195
EimeriasylvilagiCarini,1940 106
EimeriairresiduaKesselandJankiewicz,1931 196
EimeriataillieziAoutil,Bertani,Bordes,Snounou,
EimerialeporisNieschulz,1923 197
Chabaud&Landau,2005 106
EimeriamagnaPe´rard,1925b 197
Eimeriatownsendi(Carvalho,1943)Pelle´rdy,1956 107
EimeriamaiorHoness,1939 197
SpeciesInquirendae(7) 110
EimeriamediaKessel&Jankiewicz,1931 199
DiscussionandSummary 113
EimeriaminimaCarvalho,1943 199
EimerianeoirresiduaDuszynskiandMarquardt,
1969 200
6. Coccidia (Eimeriidae) of the Family EimerianeoleporisCarvalho,1942 201
Leporidae: Genus Oryctolagus EimeriapaulistanadaFonseca,1933 204
Eimeriaperforans(Leuckart,1879)Sluiterand
Introduction 122 Swellengrebel,1912 205
EimeriacoecicolaCheissin(Kheysin),1947 122 EimeriapintoensisdaFonseca,1932 205
EimeriaexiguaYakimoff,1934 126 EimeriapoudreiDuszynskiandMarquardt,
EimeriaflavescensMarotel&Guilhon,1941 129 1969 206
CONTENTS ix
Eimeriastiedai(Lindemann,1865)Kisskalt 9. Cryptosporidium and Cryptosporidiosis
andHartmann,1907 207
in Rabbits
EimeriasylvilagiCarini,1940 208
SpeciesInquirendae(3) 210 Introduction 241
DiscussionandSummary 210 CryptosporidiuminRabbits 242
FamilyLeporidaeG.Fischer,1817 243
HostGenusOryctolagusLilljeborg,1873 243
8. Sarcocystidae Poche, 1913, the Predator- SpeciesInquirendae(2) 249
ZoonoticPotentialofRabbitCoccidia 250
Prey Coccidia in Rabbits: Besnoitia,
Sarcocystis, Toxoplasma
Introduction 216 10. Strategies for Management, Control,
SarcocystinaePoche,1913 217 and Chemotherapy
SarcocystisLankester,1882,inRabbits 217
FamilyOchotonidaeThomas,1897 218 Introduction 253
HostGenusOchotonaLink,1795 218 Management 253
FamilyLeporidaeG.Fischer,1817 219 GenericMethodsofControl 254
HostGenusLepusLinnaeus,1758 219 ImmunologicalControl 255
HostGenusOryctolagusLilljeborg,1874 220 Chemotherapy/Chemoprophylaxis 256
HostGenusSylvilagusGray,1867 222
SarcocystisSpeciesInquirendae(13) 224
FamilyOchotonidaeThomas,1897 224 11. Summary and Conclusions
HostGenusOchotonaLink,1795 224
Introduction 263
FamilyLeporidaeG.Fischer,1817 225
OocystSize,StructuresandtheirStability 264
HostGenusLepusLinnaeus,1758 225
LocalizationintheRabbitHost:Tissue,Cells,
HostGenusSylvilagusGray,1867 227
andParasiteDevelopment 266
ToxoplasmatinaeBiocca,1957 228
PrepatentPeriod 267
BesnoitiaHenry,1913,inRabbits 228
Patency 268
FamilyOchotonidaeThomas,1897 229
Sporulation 268
HostGenusOchotonaLink,1795 229
DetectionandIdentification:Morphological,
FamilyLeporidaeG.Fischer,1817 229
Immunological,Molecular 269
HostGenusLepusLinnaeus,1758 229
OocystSurvival 272
HostGenusOryctolagusLilljeborg,1874 229
PreventionofContamination 275
NaturalInfectionsofBesnoitiainRabbits 233
Transmission:EntryofOocystsintotheHost 275
HostGenusSylvilagusGray,1867 233
ExcystationofOocystsintheDigestiveTract 276
BesnoitiaSpeciesInquirendae(2) 233
EndogenousDevelopmentandSomePeculiarities 276
ToxoplasmaNicolleandManceaux,1909,
HostSpecificityandCross-Transmission 277
inRabbits 234
Pathology 277
FamilyOchotonidaeThomas,1897 235
PhylogeneticRelationshipsofRabbitEimerians 278
HostGenusOchotonaLink,1795 235
FamilyLeporidaeG.Fischer,1817 235
Glossary and List of Abbreviations 297
HostGenusLepusLinnaeus,1758 235
Literature Cited (*) and Related
HostGenusOryctolagusLilljeborg,1874 235
HostGenusSylvilagusGray,1867 236 References 303
ClinicalToxoplasmosis 236 Index 335
