POPULATION ECOLOGY OF CARE&MINE PRATENSIS L. AND ANTHOCHARIS CARDAMINES L. ANNETTE ELAINE DUGGAN B.A. (HONS) , M.A., OXFORD A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College Department of Pure and Applied Biology Imperial College Silwood Park Ascot Berkshire September 1988 To my parents 2. ABSTRACT This study addresses the question of how the interaction between a perennial Cardamine pratensis (L.) and one of its seed predators Antho- charis cardamines (L.) influences the dynamics of each population. The phenology and dynamics of C. pratensis (Cruciferae) are described. Failure to realise potential seed production due to physiological factors and seed mortality due to herbivores are quantified. The importance of a given factor is highly variable. The worst damage is inflicted on high density stalks by slugs and weevils. Seed mortality is as high as 98%, however field germination experiments demonstrate that the impact of this seed loss is small. High densities of seedlings are unable to establish in the closed sward of marshy vegetation. The effect of flowerhead feeding on rhizcme weight, over-winter plant survivorship, flowering and host plant selection the next year is explored and is also small. The dynamics of A. cardamines (Pieridae) are described, and the in­ fluence of C. pratensis is assessed in the context of other factors such as sunshine hours, predation and the usage of alternative host plants. The quantity of food available to the fifth instar and temperature both in­ fluence female pupal weight, egg load, wing span and daily oviposition rate. Realised fecundity is affected by flcwerstalk density, 5-10% of stalks at a site are utilised. It is suggested that discovery of new food plants by larvae occurs most frequently in high density clumps of stalks and that interference competition between females for such plants results in the overall low proportion of stalks utilised. Greenhouse experiments lend support to this hypothesis. Larval survivorship is also correlated with flowerstalk size, but evidence of density dependent egg predation is also presented and parasitism by a species of Hyposoter is recorded for the first time. It is concluded that this plant-herbivore relationship is asymmetric, the plant has a much greater effect on the herbivore than the herbivore has on the plant. 3 TABLE OF CONTENTS Page ABSTRACT ..................... 2 TABLE OF CONTENTS ........ 3 LIST OF TABLES ............... 7 LIST OF FIGURES AND MAPS 9 CHAPTER 1. GENERAL INTRODUCTION 17 1.1 Introduction ........ 17 1.2 Reasons for Using the A. cardamines - C pratensis system 20 1.3 Approach to the Problem 20 1.4 The System in Brief 20 CHAPTER 2. ANTHOCHARIS CARDAMINES 23 2.1 General Introduction 23 2.2 Adults ............... 23 2.2.1 Potential Fecundity 25 2.2.1.1 Introduction 25 2.2.1.2 Methods and Results 26 2.2.1.3 Discussion ....... 32 2.2.2 Factors Influencing the Efficiency of the Mati ng Process ... ... ... .. 37 2.2.2.1 Introduction 37 2.2.2.2 Methods and Results 38 2.2.3 Realized Fecundity ....... 40 2.2.3.1 Introduction 40 2.2.3.2 Methods and Results ' 52 2.2.3.3 Discussion ....... 114 2.2.4 Competition for Resources Required by Adults 124 2.2.4.1 Host Plants ....... 124 2.2.4.2 Mates .............. 124 2.2.4.3 Nectar and Pollen 124 2.2.5 Predation and Disease ....... 125 2.2.6 Migration and Vagility ....... 125 2.3 The Egg and Larval Stages ....... 127 2.3.1 Introduction to Factors Affecting Growth and Mortality Rates .............. 127 2.3.1.1 Environmental Factors .. 127 2.3.1.2 Plant Related Factors .. 129 4. Page 2.3.1.3 Competition Factors ........ 134 2.3.1.4 Non Plant Related Factors ... 135 2.3.2 Methods and Results ............... 138 2.3.2.1 Development and Feeding Rates 138 2.3.2.2 Survivorship and Larval Mobility 160 2.3.3 Discussion ........................... 199 2.3.3.1 Effect of Environmental Factors 201 2.3.3.2 Effect of Plant Related Factors 202 2.3.3.3 Effects of Competition ... 209 2.3.3.4 Non-Plant Induced Mortality 211 2.4 The Pupal Stage ........ 213 2.4.1 Introduction ........ 213 2.4.1.1 Diapause ... 213 2.4.1.2 Pupal Mortality 213 2.4.2 Methods and Results 217 2.4.3 Discussion ........ 226 2.4.3.1 Factors Affecting Pupal Diapause 226 2.4.3.2 Assessment and Causes of Pupal Mortality 226 CHAPTER 3. CARDAMINE PRATENSIS 229 3.1 General Introduction 229 3.1.1 Geographical and Altitudinal Distribution 230 3.1.2 Habitat ............... 232 3.1.3 Communities ............... 232 3.1.4 Response to Biotic Factors 233 3.1.5 Habit and Adaptive Traits 234 3.1.6 Form, Genetics and Physiology 235 3.1.7 Phenology 239 3.1.8 Sexual Reproduction 239 3.1.9 Natural Enemies 240 3.1.10 History 241 3.1.11 Aims ....... 241 3.2 Seed and Seed Production 243 3.2.1 Introduct ion ... 243 3.2.1.1 Physiological and Ecological Determinants of Flower and Seed Production 243 3.2.1.2 Pollination ........ 246 3.2.1.3 Defloration ........ 246 5. Page 3.2.1.4 Seed Predation .................... 247 3.2.2 Methods and Results ..................... 249 3.2.3 Discussion .................................. 287 3.2.3.1 Physiological and Ecological Determinants 287 3.2.3.2 Mortality Factors ............... 289 3.3 Seedlings and Recruitment ..................... 292 3.3.1 Introduction .................................. 292 3.3.1.1 Seed B a n k ........................... 293 3.3.1.2 Seed Immigration ..................... 293 3.3.1.3 Germination Microsites ............... 294 3.3.1.4 Seedling Establishment and Competition 295 3.3.1.5 Herbivore Effects ............... 296 3.3.2 Methods and Results ..................... 297 3.3.3 Discussion .................................. 314 3.3.3.1 Seed Immigration and Seed Bank ... 314 3.3.3.2 Germination Microsites, Intra and Inter­ specific Competition 316 3.3.3.3 Herbivore Effects ... 318 3.4 Flowering and Mature Plants ........ 319 3.4.1 Introduction ..................... 319 3.4.2 Methods and Results ........ 321 3.4.3 Discussion ..................... 339 3.4.3.1 Annual Variations in Flowerstalk Numbers 341 3.4.3.2 Phenology ............... 341 CHAPTER 4. GENERAL DISCUSSION ............... 343 CHAPTER 5. SUMMARY ........................... 357 5.1 Interactions .......................... 357 5.2 Potential Fecundity and Pupal Weight of A. cardamines 357 5.3 Mating .......................... 357 5.4 Realized Fecundity of A. cardamines ... 358 5.4.1 Greenhouse Experiments ........ 358 5.4.2 Field Experiments and Observations 358 5.5 Egg and Larval Stage ............... 359 5.5.1 Feeding and Development ........ 359 5.5.2 Survivorship and Dispersal 360 5.6 Pupal Stage .......................... 362 5.7 362 6 . Page 5.8 Seed Production ................................. 362 5.9 Seedlings and Recruitment ..................... 363 5.10 Survivorship Curve of C. pratensis and Mature Plants 364 5.11 General Conclusions ........................... 364 ACKNOWLEDGEMENTS ... ... ... ... ... ... ... 366 REFERENCES ... ... ... ... ... ... ... ... 367 APPENDICES ... ... ... ... ... ... ... ... 403 7. LIST OF TABLES Page Seme examples of the literature concerning the chemical/nutritional/physical arms race between in­ teracting species. ..................... ... 18 Seme examples of the literature concerning the in­ fluence of the plant on herbivore canmunity structure. 18 Sane examples of the literature on pollination and the beneficial effects of herbivores...................... 18 Sane examples of the literature on palatability and preference tests. ................................. 19 Sane examples of the literature on physiological responses to feeding on different host plants. 19 Host plant attributes affecting oviposition choice. ... 45 Hypotheses to explain the disproportionate usage of isolated peripheral plants............................. 50 Effect of aphid infestation on choice of host plant. 99 Effect of surrounding vegetation on choice of host plant. ... ... ... ... ... ... ... ... 104 Comparison of attributes of chosen flowerstalks and a randan selection of stalks - site survey. ........ 107 Comparison of host plant attributes of stalks chosen by females and a randan selection of those not chosen. ... 112 Effect of stalk density on the proportion of pods surviving attack by 4/5th instar larvae on stalks: a) with young pods, b) with old pods. ............... 140 Estimated food consumption for the 5th instar at differing temperatures. ........................... 157 Key to causes of egg mortality......................... 166 To show significant correlations between instar reached (all stadia) and plant attributes. ............... 177 To show significant correlations between instar reached (3rd - pupa) and plant attributes. ............... 178 To show relationship between plant transfers and plant de ns x ty . ... ... ... ... ... ... ... ... 184 Between site variation in host plant depletion and 8. Page failure to find a new host plant ...................... 192 Table 2.14 Summary of the results from a number of studies on the effect of temperature and photo-period on diapause in Pierids. ... 214 Table 2.15 Proportion of pupae successfully eclosing. ....... 219 Table 2.16 To show the proportion of pupae (under various treat­ ments) which survived in the field: a) from 24/7/81 to 8/4/82, b) over winter 1982/83........................ 221 Table 3.1 Variables measured in Holyport Field Experiment, 1982. 264 Table 3.2 Variables measured at Warfield, 1982.................. 274 Table 3.3 Life table to show mortality factors acting on seed production