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Success and Failure of Cyzenis Albicans in Controlling SUCCESS AND FAILURE OF CYZENIS ALBICANS IN CONTROLLING ITS HOST THE WINTER MOTH by JENS ROLAND B.Sc. (Hons), University of Alberta, Edmonton, 1976 M.Sc, University of British Columbia, Vancouver, 1981 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Department of Zoology and Institute of Animal Resource Ecology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA July 1986 (c) Jens Roland, 1986 HJTV In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of Io^0^ The University of British Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3 Date Jul* 14' 1986- ii ABSTRACT Situations in which the parasitic fly Cyzenis albicans appears to control numbers of its host the winter moth, were compared with situations where it does not. Comparisons were made by field observation and experimentation during the first four years of winter moth decline following introduction of C. albicans and Agirypon f laveolatum in Victoria, British Columbia, Canada. Successful control of winter moth on oaks was compared with failure on apple trees. Phenology of winter moth development differs on the two tree species, giving rise to potential asynchrony between host and parasite on apple trees. Difference in the degree of asynchrony on the two tree species does not, however, result in a difference in level of parasitism of winter moth. Aggregative attack by Cyzenis, in response to host density, occurs when winter moth are on oaks, but is absent when winter moth are on apple. Difference in pattern of attack did not result in difference in mortality from parasitism at high density but did so at low density. The manipulation of predatory beetle abundance by as much as 100-fold did not affect the magnitude of mortality of winter moth, and affected mortality of the parasitoid only slightly. Large, density-dependent mortality of Cyzenis in the soil did not preclude their increase to high density, and hence would not affect the impact of Cyzenis on winter moth densities. The magnitude and degree of density-dependence of winter moth pupal mortality in the soil (regardless of beetle abundance) suggests that mortality of this stage, rather than parasitism of larvae iii by introduced parasites, has caused population decline in both British Columbia and Nova Scotia. The factor causing most mortality in the soil in British Columbia appears to be pathogens. Suggested mechanism for the increase in soil mortality during the four years of study are: (1) introduction of and/or increased pathogen transmission via Cyzeni s or (2) activation of latent infection by density-induced stress of the host. This study implicates factors other than parasitism by introduced parasitoids in the suppression of winter moth numbers. Correlation between degree of aggregation in response to host density and degree of successful control, however, supports the claim that parasitoids can stabilize host populations at low density. iv TABLE OF CONTENTS ABSTRACT . i i LIST OF TABLES/. '....viii LIST OF FIGURES .. .......... x ACKNOWLEDGEMENTS .• -xi ii CHAPTER ONE: GENERAL INTRODUCTION . ...1 CHAPTER TWO: PLANT PHENOLOGY AND HOST-PARASITOID SYNCHRONY 8 Introduction ........8 Methods .12 Study sites ...12 Time scale .' 15 Population phenology ...18 Parasitism •• 2 0 Control of phenology ....2 1 Effect of plant species on winter moth development ...21 Effect of plant species on winter moth survival 22 Results . 23 Population phenology . .. ... 2 3 Pa ra s i t i sm 23 Timing of attack ..23 Levels of parasitism .27 Control of spring emergence 34 Effect of plant species on winter moth development ...34 Effect of plant species on winter moth survival ......42 Close vs Spartan apple varieties 46 Discussion ... .46 CHAPTER THREE: EFFECT OF HOST PLANT SPECIES ON LEVEL AND PATTERN OF CYZENIS OVIPOSITION ...52. I nt roduct ion 52 Methods .54 Cage experiments 54 Field studies ...55 Host abundance 55 Parasitoid abundance ...56 Oviposition and parasitism 57 Oak-leaf extract on apple trees 59 Results 60 Cage experiments 60 Oviposition in the field 60 Egg numbers ..60 Oviposition in response to defoliation 62 Oviposition in response to host density 67 Statistical aggregation of Cyzenis eggs 72 Aggregation on foliage 72 Aggregation of attacks among hosts .75. Host mortality from parasitism 78 Percent parasitism vs defoliation. ....78- Percent parasitism vs host density 78 Oak-leaf extract on apple trees ...86 Di scussion . ".. 89 Parasitoid behaviour 89 Host mortality ...92 CHAPTER FOUR: MANIPULATION OF MORTALITY IN THE SOIL .....100 Introduction . ... 100 vi Methods 103 Manipulation and measurement of beetle abundance ....102 Experimental design 1983-84 ......102 Experimental design 1984-8.5 103 Beetle trapping in the oakwood ...106 Host and parasitoid abundance and survival ..........109 Effect of diazinon 111 Fate of pupae ........114 Forced pupation 114 Presence/absence of beetles 115 Predation cage experiments 116 Results .1 1 7 Beetle abundance 117 Total numbers 117 Functional response 121 Host and parasitoid mortality 126 Effect of diazinon 126 Effect of beetles 127 Effect of prey type 134 Effect of habitat type 134 Production of Cyzenis relative to its host 141 Fates of pupae 141 Fate in the presence/absence of beetles ...141 Effect of density 148 Interaction of predation and parasitism ...150 Predation over time ...150 Predation cage experiments 153 Discussion 1 53 vii CHAPTER FIVE: EFFECT OF FLY EXCLUSION ON SOIL MORTALITY AND GENERATION MORTALITY 1 70 Introduct ion . 1 70 Methods . ... 171 Fly exclusion ..171 Density and survival estimates ....172 Results . 173 Apple orchard, 1984 ..... ..........173 Apple orchard, 1985 .176 Oakwood, 1985 ........176 Discussion •„..... 1 78 CHAPTER SIX: EFFECT OF PARASITISM IN POPULATION MODELS ..181 I n t r oduc t i on 1 8 1 Methods .... 182 Model I 182 Model II . 190 Results ... 191 Model I ......191 Model II .....194 Discussion .1 94 CHAPTER SEVEN: GENERAL CONCLUSIONS .198" LITERATURE CITED 20 1 APPENDICES 209 v i i i LIST OF TABLES Table I. Difference in winter moth phenology on apple and oak 26 Table II. Effect of phenology on percent parasitism in Victoria 26 Table III. Effect of phenology on parasitism at five sites on Saanich Peninsula ...28 Table IV. Density of Cyzenis in the apple orchard and oak wood 28 Table V. Winter moth pupal weights and density of first-instar larvae on apple and oak .41 Table VI. Winter moth mortality from hatch to pupation on apple and oak .. 4 5 Table VII. Mortality from parasitism in years of good and poor host-parasitoid synchrony at Wytham Wood, England 49 Table VIII. Number of Cyzenis eggs oviposited on apple and oak foliage in cage experiments ...61 Table IX. Number of Cyzenis eggs oviposited on apple and oak in 1984 as a function of level of def ol iat ion . '... 65 Table X. Number of Cyzenis eggs oviposited on apple and oak in 1985 as a function of level of defoliation ..66 Table XI. Number of Cyzenis eggs oviposited on apple and oak in 1984 as a function of host density ..68 Table XII. Number of Cyzenis eggs oviposited on apple and oak in 1985 as a function of host density ..69 Table XIII. Distribution of Cyzenis attacks among winter moth larvae from oak and apple trees 76 Table XIV. Aggregation of Cyzenis eggs in apple and oak foliage, and levels of parasitism at five sites on Saanich Peninsula .....77 Table XV. Regression statistics for percent parasitism as a function of defoliation and host density 81 Table XVI. Percent parasitism of winter moth on apple and oak in Victoria ....85 ix Table XVII. Population estimates of predatory beetles ....120 Table XVIII. Anova table for the effect of beetle manipulation on winter moth mortality (k5) ..128 Table XIX. Anova table for the effect of beetle manipulation on Cyzenis mortality 129 Table XX. Anova table for the effect of prey type (host vs parasitoid) on mortality in the soil, in the orchard (k5a vs kcyz) 135 Table XXI. Anova table for the effect of prey type (host v_s parasitoid) on mortality in the soil, in the orchard (k5 vs kcyz) ....136 Table XXII. Anova table for the effect of prey type (host vs parasitoid) on mortality in the soil in the oakwood 137 Table XXIII. Anova table for the effect of habitat type (orchard vs oakwood) on winter moth mortality in the soil ....140 Table XXIV. Anova table for the effect of habitat type (orchard y_s oakwood) on Cyzenis mortality in the soi 1 142 Table XXV. Fate of pupae in the soil in response to manipulation of density 147 Table XXVI. Interaction between parasitism and predation on winter moth pupae in the field .149 Table XXVII. Fate of pupae in beetle removal and control plots 149 Table XXVIII. Predation on parasitized and unparasitized. pupae in cage experiments 154 Table XXIX. Predation on infected and uninfected pupae in cage experiments 155 Table XXX. Mortality of winter moth on: fly-exclusion trees, bird-exclusion trees, and control trees ...177 LIST OF FIGURES Figure 1. Winter moth population density, 1983-85 4 Figure 2. Schematic pattern of phenology of host pupation and parasitoid oviposition 10 Figure 3. Map of Saanich Peninsula with study sites 13 Figure 4. Winter moth development rate as a function of temperature ....16 Figure 5.
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