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A STUDY of SPOROZOAN PARASITES of STORED PRODUCTS COLEOPTERA By 1. A STUDY OF SPOROZOAN PARASITES OF STORED PRODUCTS COLEOPTERA By R.W. ASHFORD, B.Sc.(Lond.), A. thesis submitted for the Degree of Doctor of Philesopy in the Faculty of Science of the University of London. Dept. of Zoology and Applied Entomology, Imperial College Field Station, Ashurst Lodge, Sunninghill, Ascot, Berkshire. FEBRUARY, 1967 2. ABSTR2,CT A new species of neogregarine protozoan, Lymphotropha tribolii Ashford(1965) is described from the haemocoele of the red flour beetle, Tribolium castaneum (Herbst). The trophozoites, which live extracellularly in the haemolymfa are larse, and have longitudinal striae. There is only one type of schizogony, in which about eight merozoites are produced, and this is rarely seen. Gametogony produces 32 gametes, but instead of the expected 16, an average of 9 or 10 lemon shaped spores (oocysts) are formed. Young larvae only of T. castaneum were susceptible, and a dose of 105 spores per sL. of culture medium caused 50 mortality. Larvae of four other species of Tribolium were also cuseerti111,?, but T.confusum proved refractive to infection. The parasites produced a pronounced host reaction in the form of encapsulation. However, as only encysted gametocytes were affected, little benefit could be had by the insect. The parasites had remarkably little effect on the physiology of the host; no gross changes could be discerned in larval oxygen uptake, susceptibility to D.D.T., or activity. The disease caused severe reduction of the food reserves in the ft body, and slowed the rate of larval gain in weight. Death was thought to be caused by the physical obstruction of the host/ssystem, and by a form of tissue starvation. Adults, which were not susceptible, sometimes survived larval infection. About 25% of the survivors had a decreased longevity and feale oviposition rate, but the remainder were apparently unaffected. The taxonomy of Farinocystis tribolii Weiser, and Triboliocystis garnhami Dissanaike has been investigated, and it is concluded that clete onlykspecies is involved, which must be called Farinocystis tribolii but that the original description requires considerable amplification. 3. ACKN0:lLODGEMENT6 I should like to express my gratitude to Dr. E.U. Canning for her supervision and guidance throughout this course of utudy, without which the work could not have been carried out. I am grateful to Professor O.W. Richards for allowing tie to work in his department, and to the many other members of staff who have constantly advised and encourago'd me. Professors A.S. Dissanaike of the University of Ceylon, Colombo, and P.C.C. Garnhau of the London School of Hygiene and Tropical Nedicine are to be thanked for the loan of original slider:, of Triboliocystis garnhami. Grateful appreciation is hereby ex.;ressed to the people mentioned in the text who kindly supplied infective material of FarinocystAs tribolii. Dr. R.W. Howe of the Pest Infestation Laboratories, Slough, must be thanked for supplying healthy flour beetles, as must Mr. O.U. Steele of this department whose Tribolium castanenu cultures fortunately produced Lymphotropha tribolii. Finally, my thanks are due to the Ministry of Overseas Development who s.:.onsored the research assistantship with which this work was financed. TABTF, OF CONTENTS rage INTRODUCTION 7 INTRODUCTORY REVIEU ..... 9 MATERIALS AND METHODS.... 23 1. Origins of the Parasites and Beetles. 2. Culture of the Beetles 2 (a)Medium ... 24 (b)Containers. 2)i. (c)Procedure 25 (d)Precautions...... 25 (e)Sexing o , 26 (f)Timing 26 3. Culture of Parasites. 26 (a)General 26 (b)Procedure 27 (c)Standardisation of infective doses 27 (d)Precaution. 28 (e)Mass production of infective material 28 4. Preparation of Sections 29 (a)Fixation... 29 (b)Embedding and sectioning 29 (c)Staining 29 5. Examination of Material. 30 RESULTS 31 PART 1 LYMPHOTROPHA TRIBOLII 31 A. THE PARASITE • 31 1. Description of the Stages and Life-cycle of Lymphotropha tribolii 31 (a)Spore hatching 31 (b)Description of the sporozoite. 33 5. Page (c)Development of the trophozoito 35 (d)Schizo gonj,...-\ .. (o) Gametogony' U (f)Sporogony 43 (g)Mode of infection. 48 (h)Duration of the stagesi 48 2. The Viability and Maintenance of Virulence of spores of L.tribolii - 50 3. The Host Range of L.tribolii in Species of Tribolium 56 B. PATHOLOGY OF L.TRIBOLII IN T.CASTANEUM 57 1. Macroscopic Effects of Infection ... 57 2. Histopathology of Infection 63 (a)Encapsulation of parasites by the host 63 (b)Effects on host organs, 65 3. Tho Susceptibility of Larva° at Different Ages to Infection 69 h.. The Effect of Standard Serial Doses of L.tribolii on the Mortality of T.castanoum Larvae 71 5. The Effect of Disease on Larval Gain in Weight 74 6. The Size at Death of Larvae. Exposed to Different Doses of L.tribolii 78 7. The Effect of L.tribolii Infection on the Activity of T.castanoum Larvae 80 8. The Effect of Disease on the Rate of Larval Oxygen Uptake... 84 9. The Susceptibility to D.D.T. of Healthy and Infoctod T.castanoum Larvae 90 10. The Effoct of Disease on Surviving Adults 97 (a)Tho Size of survivors 97 (b)Sex ratio of survivors 98 (c)Longevity of survivors 99 (d)Oviposition rate of survivors. 102 6. Pap; PART P. FARINOCYSTIS TRIBOLII 107 1. Description of the Stages and Lifo-cyclo of Farincoystis tribolii WriA.sor 107 (a)Description of the trophezoite 107 (b)Schizogony 107 (c)Gamotogony , 112 (d)Sporogony. 115 2. Notes on Pathology 120 DISCUSSION 122 LIST OF REFERENCES. 139 7. INTRODUCTION Insect pests regularly cause heavy losses in stored produce throughout the world. Control of pest outbreaks usually depends on preventive measures such as the cleanliness of warehouses, and the rapid turnover of produce. Insecticidal methods of control depend mainly on fumigation, as solid or liquid insecticides tend to leave undesirable traces. Matever preventive `or control methods are used, they are expensive and require skilled operation. Stored products insects, particularly the beetles of the genus Tribolium are well suited to mass laboratory rearing, and arc commonly cultured for use in studies on such basic subjects as genetics and population dynamics, as well, as for insecticide assays. The importance of pathogens in these insects is thus two—fold. First, they may constitute a potential biological accessory method for the control of pest outbreaks, and secondly, laboratory cultures must he kept disease—free or misleading experimental results may be obtained. The widespread rearing of stored products pests for laboratory purposes had led to the discovery of many pathogens which might have passed unnoticed in nature. In 1953, a neogregarine pathogen of Tribolium castaneum (Herbst) was discovered in cultures in the Laboratory of Insect Pathology, Prague. This parasite, Farinocystis tribolii 'deiser, was subsequently found destroying cultures in many other insectaries, and also in wild populations of T.castaneum. A rather similar protozoan was described from the same 8. host species by Dissanaike (1955) as Triboliocystis garnhami. The original purpose for the work presented in this thesis was to sort out the taxonomic position of these two organisms, and to investigate the nature of their pathogenicity in Tribolium spp. However, early attempts to produce infections were diverted by the discovery of a third, and new, neogregarine in the Imperial College cultures of T.castaneum. This protozoan, which was described as Lymphotropha tribolii Ashford was easily cultured and after elucidat- ing its life cycle, it was decided to investigate various aspects of its pathogenicity. Infective material of F.tribolii later became available for study, and it was possible to clarify some points in its life cycle. The conclusions drawn from the life cycles of the two species studied have general relevance to the taxonomy of the neogregarines, which is discussed at the end of this thesis. 9• INTRODUCTORY REVIEW A fine review of the history of insect pathology is given by Steinhaus (1956a), in which the predominance of early observations on fungal and bacterial diseases is stressed. The first record of a protozoal insect disease probably came from Aristotle, who observed honey bees, Apis mellifera L., dying as a result of infection with what may have been Nosema apis Zander. Recognition of the importance of protozoa as insect disease agents came with Pasteur's work in the mid 1800's on pebrine„ the disease caused by Nosema bombycis Nggli in silkworms, Bombyx mori L. The first discovery of a pathogenic sporozoan infecting a stored products beetle came at the turn of the century when Leger, publishing a series of important works on the gregarine parasites of insects included the description of Ophryocystis mesnili from the larvae of the yellow meal worm, Tenebrio molitor L. Since that time, stored products insects have been the subjects of intensive research. Cotton (1956) gives a review of the species of importance in the United States, and Hinton (1945) extensively reviews the beetles of 12 families occurring in stored products. The completion of this monograph would represent a milestone in stored products entomology. Munro (1966) has given a popular review of the most important stored products pests, in which he mentions 47 beetles belonging to 15 families. The most important families are the Dermestidae and Tenebrionidae, though species of major importance belong also to the Anobiidae, Ptinidae, Cleridae, Nitidulidae, Cucujidae, Mycetophagidae, Bruchidae and Anthribidae. 10. Good (1933, 1936) has summarised the biology of the flour beetles, Tribolium spp. (Tenebrionidae), and has shoun how the preadaptation of T.confusum and T.castaneum has led to their becoming the most serious pests of stored grain products throughout the warmer parts of the world. Even in such a well known group of beetles, there has been very little work on their protozoan parasites.
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