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Studies on the Ecology of Thistle Lace Bugs; In STUDIES ON THE ECOLOGY OF THISTLE LACE BUGS; IN PARTICULAR TINGIS AMPLIATA4k+.87.(HETEROPTERA: TINGIDAE). By William Enotiemwomwan Eguagie, B.Sc. A thesis submitted for the degree of Doctor of Philosophy in the Faculty of Science of the University of London. Imperial College of Science & Technology, Field Station, Silwood Park, Sunninghill, May, 1969. Ascot, Berkshire. 2 ABSTRACT The population dynamics of Tingis ampliata HrS. was studied in a relativel delimited area of thistles, Cirsium arvense (L.) at Silwood Park, Berkshire, in the three years 1965, 1966 and 1967. The relative roles of natality and different ecological factors influencing seasonal and annual variations in Tingis population density were assessed. Population budgets are presented for the period of study. Various biological characteristics of the insect, including reprod- uction, distribution, body weight, sex ratio, and overwintering were investigated in relation to its life cycle, population age and structure. The rate of dispersal of adults in a natural habitat was determined. An analysis of the distribution of dispersing individuals and of the climatic factors affecting dispersal rate and numbers were made to partly explain daily occurence and distribution of Tingis on a thistle patch. Histological studies were carried out on the seasonal relationship between flight musculature, reproductive physiological state and level of flight activity of thistle lace bugs. These are discussed in relation to habitat type, local and geographical distribution and abundance of the species. A short account is given on the bioecology of Tingis cardui L. on the spear thistle, Cirsium vulgare (Savi) Ten. 3 CONTENTS Ewa SECTION I : INTRODUCTION 7 1. Review of Literature 9 2. The Habitat and Host plant 13 (a) General description of the Habitat and Host plant 13 (b) The number of thistle plants in the study area. 19 (i) Estimation 19 (ii)Annual variation 21 (c) The average total number of primary leaf-buds in the study area 23 (i) Estimation 23 (ii)Seasonal variation 25 (iii)Annual variation • 26 3, Life history of Thistle Lace-bugs 29 (a)Tingis ampliata H.-S. 29 (b)Tingis cardui L. 32 SECTION II : STUDIES ON TINGIS AMPLIATA 34 1. Description of stages 34 (a)Adults 34 (b)Immature Stages 37 2. Aspects of the Biology of the adult 40 (a) Overwintering 40 Introduction 40 (i) Autumnal migration. 43 (ii)Survival ( mortality) during overwintering • • • • 46 (iii)Weight loss during overwintering. 56 (iv)Cold-hardiness. 60 (v) Seasonal variation in under000ling point ..... 65 (vi)Other factors affecting undercooling point. 70 4 Pane (a) Nature of the contact surface. 70 (b) Presence or absence of food in the gut. ... 71 (vii) Pre-emergence feeding 74 (b) Mating behaviour 76 (i) Season. 76 (ii) Time of day. 77 (iii) Body orientation of Tingis in copula 80 (iv) Frequency of copulation. 82 (v) Duration of copulation. 82 (c) Oviposition behaviour 84 (i) Parts of the plant where eggs are laid. 84 (a)In the field 84 (b)In the laboratory 84 Precise sites of oviposition in the field. 85 Types of oviposition in Tingis. 90 Periodicity of oviposition in the field. 93 Oviposition studies in the laboratory. 97 Changes in reproductive organs and body weight in the field. 101 Weight of females in Spring and number of egg rudiments. 119 State of ovaries at death of females. 122 An unusual ovarian condition in TinFis 124 (d) Dispersal 126 (i) Walking. 126 (a)Methods of study. 127 (b)Distances moved by adult Tingids. 128 (c)Effect of weather. 150 (ii) Flight. 158 (a)Methods. 158 (b)Reproductive state of females caught in suction trap. 162 (c)Seasonal changes in flight musculature. ...163 (d)Laboratory studies on flight activity. • ... 171 (iii) Discussion. 183 5 Page (e)Distribution on the host plant. 190 (f)Diurnal variation in the distribution of adults. 203 3. Aspects of the Biology of the Immature Stages 207 (a) Development of eggs and nymphs. 207 (i) Their size. 207 (ii)Weight of larvae. 207 (iii)Role of temperature in development. 209 (iv)Development in the field; (eggs & nymphs) 213 (v) Effect of humidity on developmental hatching of eggs. 216 (b) The distribution of eggs 219 (c) The distribution of nymphs 228 (d) The effects of feeding of nymphs on thistles. 233 4, Development of Life Budget 239 (a) Methods 239 (b) Analysis 253 (i) Survival and mortality of adults. 253 (ii)Sex ratio of adults. 2% (iii)Sex ratio of nymphs. 259 (iv)Estimation of recruitment and mortality in the immature stages. 261 (v) Fecundity. 264 (c) Mortality Factors 272 1. Causes of mortality in Adult Tingis 272 (i) Parasitism. 272 (ii) Winter losses. 275 (iii)Predation. 278 2. Causes of mortality in Immature stages 280 (a) Egg mortality 1 280 (i) Predation 280 (ii)Parasitism 282 (iii)Sterility 288 6 Page (b) Nymphal mortality 289 (i) Predation 289 (ii)Fungal diseases 296 (iii)Ectoparasites 298 (d) Population budgets, 1965-67 299 5. Discussion 309 SECTION III: SUPPLEMENTARY STUDIES ON T. CARDUI 311 SUMMARY 321 ACKNOWLEDGEMENTS 325 REFERENCES 4 327 SECTION I : INTRODUCTION This thesis is essentially an account of some ecological observations on Tingis ampliata 1L-S.and Tingis cardui L., the two species of lace bugs found on thistles in Britain. These lace bussoccur on different thistle species in nature; the former on the perennial creeping thistle Cirsium arvense (L.) Scop. and the latter on the biennial spear thistle Cirsium vulgare (Sale Ten. Of the two Tingis species; T. cardui was locally less abundant and in some years was virtually absent from thistles in Silwood Park. The information presented on this species (Section III), has therefore been limited to data on some aspects of its biology and the seasonal fluctuation in the population of a colony studied in 1966. Some attention has been given to details of the spatial and regional distribution of the insect on its host plant together with records of potential predators associated with the bug. The main part of the thesis (Sections I - II) deals primarily with the seasonal and annual variations in a population of T. ampliata on a delimited area of C. arvense in the period from April 1965 to Nov. 1967, and with the factors accounting for such variations. An attempt has been made at a quantitative assessment and interpretation of natality and mortality in relation to population changes, with a view to constructing a population budget for the bug. Mortality factors were identified and their significance assessed quantitatively whenever possible. Serological techniques were used to determine the predators of immature stages. 8 In some instances, population parameters were estimated by different methods which acted as mutual checks on one another. Seasonal and annual variations in host plant and vegetative bud density were estimated and related to insect population density in an attempt to demonstrate any influence of the carrying capacity of the food plant on the numbers of Tingis. The biological and behavioural characteristics of a species as well as its environment constitute some factors that may affect its abundance (Andrewartha & Birch 1954). Information on the biology of T. ampliata has hitherto been inadequate in scope and content. A considerable part of the present studies has therefore been devoted to various aspects of the biology of the bug. These include, detailed investigations on adult distribution, reproduction, overwintering and dispersal. In a species which overwinters as adults, the site of the post- hibernation population in spring depends partly on (a) the ability of the hibernating individuals to survive adverse, cold winter conditions and (b) the amount and rate of break down of their metabolic reserves, (Kiritani et al. 1966). In the present work much attention has been given to the determination of cold-hardiness and some factors affecting cold-hardiness in Tingis. The pattern of weight loss associated with breakdown of food reserves in winter is also examined. The distribution, development and feeding habits of immature stages were investigated in relation to population size and age. A brief account is given of the synchronisation of the life cycles of the Mymarid (Chalci- doidea) egg parasites of T. ampliata with that of their host. 9 1. Review of Literature Although some species of Tingidae are of considerable economic import- ance in different parts of the world (See Fink 1915; Tillyard 1926; Sweet- man 1936 and Roonwal 1952); yet comprehensive ecological studies of the group appear to have been neglected. Miller (1956) summarises the situation briefly; "On the whole, little is known about the ecology of the Tingidae". Indeed, with the exception of studies such as those of Connell & Beacher (1947) and Bailey (1951, 1962-63) on the phenology and seasonal occurence of some North American species, publications on the Tingidae to date, have in general dealt with outlines of life history, descriptions of immature stages and feeding habits. It has been suggested that the group has for long failed to attract extensive detailed investigations on account of the small size of its adults (Butler 1923) and eggs (Leston 1953). Prior to the present studies, there appears to be no published works on details of the bio -ecology of T. ampliata. Most of the limited literature on this species appeared mainly in the last fifty years, although the bug has been recorded as early as the late half of the nine- teenth century from Britain (Douglas and Scott 1865) and the continent of Europe (Lomnicki 1881; mainly Poland and Germany). The bulk of these publications concerned, (a) its association with thistles (Reclaire1940; Cobben 1948; Singer 1952; Southwood & Leston 1959) and different over- wintering habitats (Parshley 1923, Goddard 1934 and Massee 1963); (b) its geographical distribution in the U.K. (Butler 1923, Bedwell 1945, Massee 1963) and in Europe and Central Asia, i.e.
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