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1 Population Dynamics of the Entomophilic Nematode 1 POPULATION DYNAMICS OF THE ENTOMOPHILIC NEMATODE ROMANOMERMISCULICIVORAX by G. A. TINGLEY, B. Sc. Thesis submitted for the degree of Doctor of Philosophy and Diploma of Imperial College in the Faculty of Science'of the University of London. September 1983 Department of Pure and Applied Biology, Imperial College of Science and Technology, Prince Consort Road, London, SW7. TO MY PARENTS 2 POPULATION DYNAMICS OF THE ENTOMOPHILIC NEMATODE ROMANOMERMISCULICIVORAX by G. A. TINGLEY The major population parameters involved in the life-cycle of the entomophilic nematode Romanomermis culicivorax were estimated quantitatively by controlled laboratory experimentation using the mosquito Culex ippiens fatigans as the host. Parameters estimated included the rates of survival, immigration and emigration for, and between, each of the five stages in the nematode life-cycle. Emphasis was placed upon estimation of the rate of parasite transmission (in- fection) and the influences of the density and age of both infective stage and host were investigated, together with duration of exposure and the size of the infection arena. The sex of individual nematodes was shown to be environmentally determined: dependent upon the parasite burden per host. A close study of the statistical distribution of the numbers of parasites within the host population, linked with the density-dependent sex determination of the nematode, showed that the parasite population would be regulated in a density-dependent manner. A mathematical model, incorporating the parameters estimated in the laboratory, was used to predict the equilibrium level of infection in the host population. Predictions obtained from the model were compared with the results from long-term, free-running, experiments. The parasite was found to depress the equilibrium host population significantly. Results from both experimental and theoretical investigations are discussed in relation to such host-parasite interactions in the field. The major factors which regulate the parasite population are also considered. Finally, given the density-dependent nature of the environmental sex determination, the statistical distribution of the numbers of parasites within the host population and the model predictions, the potential of the parasite as a biological control agent of mosquitoes is critically assessed. 3 CONTENTS Page ABSTRACT 2 CONTENTS 3 LIST OF TABLES 7 LIST OF FIGURES 15 CHAPTER 1 INTRODUCTION 22 CHAPTER 2 POPULATION DYNAMICS OF R. CULICIVORAX 26 2.1 BIOLOGY OF THE HOST 27 2.2 BIOLOGY OF THE PARASITE 31 2.3 MATER IALS AND METHODS 39 39 (i) Host and Parasite Species 39 (ii) Maintenance of the Host (iii) Maintenance of the Parasite 39 (iv) Volumetric Estimation of Preparasite Density 41 2.4 INFECTION OF THE HOST MOSQUITO LARVA 43 (i) Preparasite Survival 45 (ii) Preparasite Density 57 (iii) Exposure Duration 69 (iv) Preparasite Age 79 (v) Host Density 93 (vi) Host Age 103 (vii) Volume of the Infection Arena 108 (viii)Discussion 113 4 Page 2.5 DYNAMICS OF THE PARASITIC STAGE 117 (i) Parasite Survival 117 (ii) Length of the Parasitic Stage 128 (iii) Discussion 140 2.6 SEX DETERMINATION 142 (i) Environmental Sex Determination 142 (ii) The Effects of Parasite Burden and the Statistical Distribu- tion of the Parasites 145 (iii) The Effect of Temperature 163 (iv) Discussion 179 2.7 DYNAMICS OF THE POSTPARASITIC NEMATODES 182 (i) Postparasitic Juvenile Survival 182 (ii) Moulting to the Adult Stage 184 (iii) Adult Survival 187 (iv) Mating Characteristics 195 (v) Egg Development 202 (vi) Discussion 205 2.8 DYNAMICS OF THE POPULATION OF EGGS 208 (i) Birth Rate 208 (ii) Rate of Hatching 214 (iii) Egg Survival 220 (iv) Discussion 224 2.9 GENERATION TIME AND REPRODUCTIVE RATE 226 CHAPTER 3 HOST POPULATION DYNAMICS 230 3.1 IN THE ABSENCE OF PARASITES 233 3.2 PRESENCE OF PARASITES 240 3.3 DISCUSSION 263 5 Page CHAPTER 4 THEORETICAL STUDIES OF THE POPULATION DYNAMICS OF R. CULICIVORAX 267 4.1 THE BASIC MODEL 268 4.2 DENSITY-DEPENDENT REGULATION OF THE PARASITE POPULATION 303 4.3 THE EFFECT OF THE PARASITE DISTRIBUTION 311 4.4 NON-LINEAR PARASITE-INDUCED HOST MORTALITY 316 CHAPTER 5 THE USE OF NEMATODES AS AGENTS OF BIOLOGICAL CONTROL, WITH EMPHASIS UPON MOSQUITO CONTROL 323 GENERAL DISCUSSION 332 SUMMARY 337 ACKNOWLEDGEMENTS 342 BIBLIOGRAPHY 343 APPENDICES I TABLE A. 1 364 II TABLES A. 2.4.1 - A. 2.8.4 367 III TABLES A. 3.1.1. - A. 3.2.1 390 IV PREDATION OF INFECTED AND UNINFECTED MOSQUITO LARVAE 393 V ESTIMATION OF RATE PARAMETERS 401 6 ENCLOSURE Hominick, W. M. and Tingley, G. A. (1982). Use of mermithid nematodes to control insect vectors of human disease. In: Invertebrate pathology and microbial control p. 369-373. Proceedings of the third international colloquium on invertebrate pathology. University of Sussex, Brighton, United Kingdom, 1982. 7 LIST OF TABLES Table No. Page 2.1.1 Development times for C. p. fatigans. 28 2.4.1 Mean expected life-spans and mean instan- taneous rates of mortality of preparasitic nematodes over a range of temperatures. 56 2.4.2 The mean parasite burdens per host of two groups of hosts exposed consecutively to the same infective stages for four hours. 77 2.4.3 Parasite distribution with increasing host density. 98 2.4.4 Estimates of the transmission coefficient (ß) for the four host instars. 106 2.5.1 Mortality of hosts 16-24 hours post-infection for hosts exposed to a range of infective stage densities and two exposure times. 120 2.6.1 The proportion of female nematodes that emerged from field collected hosts, with mean parasite burdens and a guide to the level of overdispersion. 162 2.6.2 The relationship of the mean level of overdispersion measured as the average variance-to-mean ratio (Av. S2/R) and the proportion of female nematodes formed at different mean parasite burdens (m) 0 over a range of temperatures (T, C). 172 2.7.1 The mean time to mating of female R. culicivorax given fixed sex ratios. 201 hý- 8 Table No. Page 2.9.1 The mean developmental times of the various stages in the life-cycle of R. culicivorax at 25°C. 227 3.1.1 The proportion surviving, the develop- ment and mortality rates of larvae and pupae of C. p. fatigans. 238 3.2.1 The mean proportion of hosts, introduced into control and infected tanks, that developed to adults. 245 3.2.2 Infection levels in adult mosquitos. 247 3.2.3 The intercept (a) and slope (b) of the least-squares best-fit linear regression of the rate of emergence-induced host mortality (a/host/day) on the mean parasite burden per host (M), at four temperatures. 250 3.2.4 Estimates of the pathogenicity of the parasite to the host (6/host/parasite/ day) and the natural host mortality rate (u6/host/day). 252 3.2.5 Values of the equilibrium mean parasite burden per host (M*) obtained from equation (3.2.5) for a range of parasite distributions. 262 4.1.1 The standard rate parameter values 276 used in the model, estimated at 250 C. A. 1 Volumetric estimation technique. 365-366 k- 9 Table No. Page A. 2.4.1 The proportion of preparasitic nematodes remaining alive at time t, P(t), for six temperatures. 368 A. 2.4.2 Estimates of the age-dependent instan- taneous rate of preparasite mortality, u(t) per preparasite per hour, from equation (2.4.1) for six temperatures. 369 A. 2.4.3 The relationship between temperature and the mean life expectancy of the pre- parasitic nematodes. 369 A. 2.4.4 The relationship between initial infective stage density and the mean parasite burden (t), per host for two exposure times two and four hours. 370 A. 2.4.5 a. The relationship between the initial infective stage density and the percentage of exposed hosts which became infected during a four hour exposure period. 370 b. The relationship between the initial infective stage density and the variance- to-mean ratio of the number of parasites per host acquired during a four hour exposure period. 370-371 A. 2.4.6 The frequency distributions of parasites per host generated at different initial infective stage densities with a four 371 hour exposure period. A. 2.4.7 The relationship between the duration of exposure and the mean parasite burden per host with an initial infective stage density of 10/ml. 371-372 h- 10 Table No. Page A. 2.4.9 a. The relationship between the mean parasite burden per host and the age of the infective stages. 372 b. The relationship between the percentage of exposed hosts that became infected and the age of spontaneously active infective stages. 372 A. 2.4.10 The frequency distributions of parasites generated by preparasites of increasing age. 372-373 A. 2.4.11 The relationship between the variance-to- mean ratio of the number of parasites per host and the infective stage age. 373 A. 2.4.12 a. The relationship between the mean parasite burden per host and the age of spontaneously active infective stages. 373-374 b. The relationship between the percentage of exposed hosts that became infected and the age of spontaneously active infective stages. 373-374 A. 2.4.13 The relationship between the variance-to- mean ratio of the number of parasites per host and the age of spontaneously active infective stages. 374 A. 2.4.14 a. The relationship between the mean parasite burden per host and the host density. 374-375 kh. - 11 Table No. Page A. 2.4.14 b. The relationship between the trans- mission coefficient, ß (/host/infective stage/3 ml/hour), estimated using equation (2.4.19) and the host density.
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