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STUDIES on MALARIA PARASITES of RODENTS by R. KILLICK

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STUDIES on MALARIA PARASITES of RODENTS by R. KILLICK STUDIES ON MALARIA PARASITES OF RODENTS by R. KILLICK-KENDRICK A thesis submitted for the degree of Doctor of Philosophy of the University of London Department of Zoology and Applied Entomology Imperial College of Science and Technology January 1972 ABSTRACT This work is in five parts: in the first there is a general introduction and an historical account of the discovery of malaria parasites of rodents and the elucidation of their life-cycles. In Part II the complete life-cycle of Plasmodium berghei from Nigeria is described, and its distribution examined. Important faunal barriers exist between Nigeria and the localities of named subspecies of P. berghei and because of this, and morph- ological differences, it is concluded that the Nigerian parasite is a new subspecies. Part III deals with malaria of African scaly-tailed flying squirrels in the Ivory Coast. Two new species of Plasmodium are described from Anomalurus peli 5/15 of which had malaria parasites. Two out of six A. derbianus also had malaria, but parasitaemias were too low to identify the parasites. All anomalurines had pigmented spleens. No malaria parasites were found in 16 Idiurus macrotis. In Part IV the concept of the protozoan species and subspecies, and the taxonomy and origins of murine malaria parasites are dis- cussed. It is concluded that, with modifications, genetic defin- itions of species and subspecies apply well to malaria parasites, though not to protozoa in which. exchange of genetic material does occur. The assumption that trypanosomatids do not conjugate is considered not to be conclusive. The taxonomic position of sub- species of P. berghei is examined and from the morphology and Carter's work on electrophoretic mobilities of enzymes it is concluded that P. berghei could be divided into two species, one from the highlands of Katanga, and the other from the lowland forests. P. vinckei, on the other hand, may be a cline, or four populations deserving subspecific rank. From the phylogenetic relationships and evolution of rodent hosts, it is postulated that, as murine rodents acquired arboreal habits, murine malaria parasites evolved from those of anomalurids. Part V is a comprehensive checklist and host index of malaria parasites, haemoproteids, piroplasms and haemogregarines of rodents of the World. In Appendix 1 parasites of flying squirrels, other than Plasmodium are considered. Descriptions are given of (i) Trypanosoma denysi in A. peli, (ii) a new trypansome (subgenus He.tpetosoma) in A. derbianus, and (iii) two new haemogregarines of I. macrotis. Appendix 2 is work published in 1970 and 1971, offered as subsidiary matter. ACKNOWLEDGEMENTS I thank Prof. P.C.C. Garnham F.R.S. for advice and encourage- ment throughout this work; it is a privilege to have studied malaria under his supervision. I am grateful to Prof. T.R.E. Southwood and Dr Elizabeth Canning for the facilities they have provided. I have recieved support from a grant to Dr Canning from the Medical Research Council. For much of the experimental work mosquitoes were provided by Mr P.G. Shute O.B.E., Miss M. Maryon and Mr G.S. Gill all of whom I wish to thank. Field work in West and Central Africa was carried out while I was acting as a Consultant for the World Health Organization. wish to acknowledge the help received during the trip from Mr J.P. Adam in Brazzaville; Mr A.O. Lambo, Mrs. R.I. Otitoju and Dr David Happold in Nigeria; Mr and Mrs. Louis Bellier in the Ivory Coast; and Dr B.O.L. Duke in West Cameroons. I wish to thank Miss Rosemary Church for the diligence and speed with which she typed this thesis, and Mrs. Angela Bishton for obtaining many works of reference for me. Finally, it is a pleasure to record my gratitude to my wife, without whose support this work would never have been done. 4 CONTENTS Abstract • • •• •• • • .. .. .. .. 1 Acknowledgements .. •• •• •• .. .. .. .. 3 Contents • • • • •• • • .. .. .. .. 4 List of Illustrations and Tables .. .. • . .. 8 PART I General Introduction • . • • •• •• • • 13 History of the Discovery of Malaria Parasites of Rodents, and the Elucidation of their Life-cycles • • 15 References in Part I .. 4.• ••• • • • • W.! •• 23 PART II PLASMODIUM BERGHEI (NIGERIA) Introduction • • •• •• •• • • • • •• 29 Materials and Methods .. •• •• •• • • • • • • 29 Life-cycle of P. berghei (Nigeria) •• •• •• •• 31 Sporogony .. 0 • • • S. 00 1.• 31 Effect of temperature on sporogony 00 • • •• 35 Infectivity of sporozoites •• • • •• 41 Exoerythrocytic schizogony •• •• •• 42 Erythrocytic schizogony •• 00 • • 48 Distribution of P. berghei (Nigeria) .. O. 0. •• 52 Hosts • • • • • • 52 Limits of geographical range 06 • • 00 e• 54 Discussion • • •• • • •• 00 • e 00 .0 • • 58 Diagnosis of P. berghei (Nigeria) •• 0, .. •• 69 References in Part II •• •• • • •• •• • 0 74 PART III MALARIA PARASITES OF FLYING SQUIRRELS IN THE IVORY COAST. Introduction .. .. .. .. .. .. .. .. 79 Materials and Methods . .. .. .. .. .. .. 79 Locality . • .. .. .. .. .. .. .. 79 Flying Squirrels . .. .. .. .. .. 80 Techniques.• .. .. .. .. .. .. .. 86 Results of a Survey .. .. .. .. .. .. .. 86 Malaria Parasites in A. peli No 70/35 .. ... .. 91 Malaria Parasites in A. peli No 70/37 .. .. .. 94 Discussion .. .. .. .. .. .. .. .. •• 97 References in Part III .. .. .. .. .. .- 103 PART IV TAXONOMY OF MURINE MALARIA PARASITES Introduction .. .. .. .. .. .. .. .. 106 The concept of protozoan species .. .. .. 106 The subspecies .. .. .. .. .. .. .. 113 Demes and clines .. 00 .. .. 00 .. 116 Syngens .. .. .. .. .. .. .. .. 117 Taxonomy of P. berghei and subspecies .. .. .. 119 Taxonomy of P. vinckei and subspecies .. .. .. 128 Origins of Malaria Parasites of African Rodents .. 130 References in Part I V .. .. .. .. .. .. 137 PART V PROTOZOA IN THE BLOOD CELLS OF RODENTS Introduction •• 00 .. 00 00 • • 144 An Annotated Checklist • • • • • • • • • • • • 146 Hepatozoidae • • • • • • • • • • • • • • 146 Plasmodiidae •• • • • • • • • • • • • • 159 Haemoproteidae • • • • • • 0 • • • • • • • 163 Babesiidae •• • • • • •• • • • • • • 166 Dactylosomidae • • • . • • • • • • • 0 • • 178 Host-Index .. • • • • • • • • • • • • • • 180 SCIUROMORPHA •• • • • • • • .• • • • • 180 Sciuridae • • • • • • • • • • • • • • 180 Sciurinae • • • • • • • • • • • 0 • 180 Petauristinae .. .. .. .• 00 186 SCIUROMORPHA incertae sedis .. .. •• •• 187 Ctenodactylidae .. .. 00 00 187 THERIDOMYOMORPHA .. 00 .. .. es 0. 188 Anomaluridae .• •• •• • 0 • • • • 188 Anomalurinae 00 00 00 O• 00 188 Zenkerellinae .. .. .. •• .. 188 MYOMORPHA .. 00 • • 0 • • • • • • • 0 • 188 Cricetidae ... • . .. .• .. •• •• 188 Cricetinae .. .. .. 00 00 .• 188 G erbillinae .. O. .. O. 00 192 Cricetomyinae •• •• • 6 • • • • 194 Muridae 00 0. O. O. 0. e. •• 194 Murinae 00 *0 00 00 00 00 194 Dendromurinae 00 .. 00 00 00 200, Otomyinae .. 00 .. .. 00 00 200 Dipodae 00 00 0. 00 00 00 201 Dipodinae .. •• •. .. .. 201 MYOMORPHA incertae sedis .. .. .. O. .• 202 Gliridae 00 0 • 00 00 • 0 • • .. 202 Glirinae .. .. .. O• 00 00 202 CAVIOMORPHA • • • • • • • • .. .. 203 Ctenomyidae • • • • • • • . .. .. 203 Caviidae • • • • • • • • .. .. 203 Cavinae • • • • • • • 0 .. .. 203 HYSTERICOMORPHA • • • • • • • • .. .. 203 Hystricidae 0 • • 0 . • 0 .. .. 203 Atherurinae • • • • • • .. .. 203 Thryonomyidae • • • • • • • .. .. 204 Discussion • 0 • 0 • 0 • • WO .. .. 205 References in Part V ... .. .. 210 APPENDIX I TRYPANOSOMES AND HAEMOGREGARINES OF AFRICAN FLYING SQUIRRELS Introduction • . .. .. .. .. .. .. •• 230 Trypanosomes of African Flying Squirrels .. .. .. 230 T. denysi in A. peli .. .. • • 0 • • • 231 Trypanosoma sp. in A. derbianus .. .. .. .. 234 Haemogregarines of African Flying Squirrels .. •• 237 Short haemogregarine of I. macrotis .. .. .. 238 Long haemogregarine of I. macrotis .. •• 241 References in Appendix I .. • • . • . • .. .. 246 APPENDIX II SUBSIDIARY MATTER Candidate's published work in 1970 and 1971 247 8 LIST OF ILLUSTRATIONS AND TABLES Plate 1. Nigerian Plasmodium berghei; 36 hr. old tissue schizont ... ... ... ... ... ... ... 43 Plate 2. Nigerian P. berghei; 49 hr. old tissue schizonts ... 00. .410 00. 000 .00 000 45 Plate 3. Nigerian P. berghei; nuclei of infected parenchymal cells ... ... ... ... ... 47 Plate 4. Nigerian P. berghei; erythrocytic stages ... 49 Plate 5. Anomalurus peli ... ... ... ... ... 81 Plate 6. Anomalurus derbianus ... ... ... oPeo 4." 83 Plate 7 Trees inhabited by A. derbianus ... ... 84 Plate 8. (i) Idiurus macrotis ... ... ... ... (ii) Tree inhabited by I. macrotis ea* ... 85 Plate 9 Malaria parasites of A. peli No 70/35 ... 93 Plate 10 Malaria parasites of A. peli No 70/37 ... 95 Plate 11 Schizont of haemogregarine of I. macrotis ... 245 FIGURES Fig 1. Nigerian P. berghei; ookinetes ... 32 Fig 2. Nigerian P. berghei; pigment patterns of young oocysts ... ... ... ... ... ... 34 Fig 3. Nigerian.P. berghei; drawings of the midlines of sporozoites • • • • • • • • • • • • • • • ▪ 36 Fig 4. Nigerian P. berghei; drawings of the midlines of microgametes • • • • • • • • • • • • • • • • 51 Fig 5. Map of Africa showing the distribution of murine malaria parasites • • • • • • • • • • 0 • • • • 56 Fig 6. Map of West Africa showing faunal barriers . 60 Fig 7. Dice-Leraas diagrams of lengths of sporozoites of P. berghei (Nigeria). 00O 000 4.06 • • • 64 Fig 8. Phylogeny of rodents showing positions of hosts of malaria parasites • •.• • .. • • • • • • 134 Fig 9. Trypanosoma denysi in the blood of A. peli... 233 Fig 10. Trypanosoma sp. in the blood of A. derbianus. 236 Fig.11. Hepatozoon sp. (short form) in the blood of I.
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