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Embryonic Development and Functional Morphology Of THE POST- EMBRYONIC DEVELOPMENT AND FUNCTIONAL MORPHOLOGY OF THE FEMALE REPRODUCTIVE SYSTEM IN GRAPHOCEPHALA FENNAHL (HOMOPTERA : CICADELLIDAE) by Gareth Cape IWilliams Being a thesis submitted for the Degree of Doctor of Philosophy Imperial College of Science and Technology South Kensington London S.W.7 September 1978 2. ABSTRACT A number of fields of study are brought together to provide a deeper under- standing of the reproductive system in Cicadellids. The external genitalia of Graphocephala fennahi (Young) are discussed, together with their postembryonic development. Associated with this, the histology and development of the internal organs of reproduction and the abdominal musculature are described in detail. The gonapophyses and basal genital structures are for the first time in Cicadellidae examined with the scanning electron microscope and this, combined with behavioural observations, permits a better functional understanding of the ovipositor.' By comparing the genital structure in three species of British Cicadellids in relation to their oviposition habits it is possible to demonstrate the adaptive nature of ostensible taxonomic characters and to illustrate clearly that variation in ovipositor structure principally of the gonapophyses can be associated with characteristics of the oviposition site. The development and histology of the reproductive system is followed from the earliest nymph and the origin of the efferent ducts described. A detailed account of the adult reproductive system and oogenesis is provided, including some electron- microscopic observations. Oogenesis in the telotrophic ovariole and the probable origin of certain nutritive substances is determined, using histological and cyto- chemical techniques. The ovarioles of Graphocephala were found to be contained within an ovariole sheath and an electron microscopic study of its structure was made. The sheath contains "lumen cells" and their possible phagocytic function is discussed. To provide a clearer understanding of the terminal abdominal segments the genital musculature was examined and compared with the typical pregenital abdominal musculature. Myology was followed from the basic nymphal arrangement and the 3. associated myogenesis examined and found to occur along four major routes involving two different methods of free myoblast incorporation. A table is drawn up which allows the direct comparison of nymphal and adult muscles and the status of the nymphal muscles in the adult. Some functional aspects of the reproductive and genital systems are combined in a discussion of the sexual behaviour of G. fennahi, concerned with pre- and post-mating behaviour and also with oviposition. Data relating to the epigamic communication between receptive pairs is presented and the importance of substrate- borne vibrations in G. fennahi indicated. The results are discussed in relation to other work on the postembryonic develop- ment of the reproductive system and on sexual behaviour. 4. TABLE or CONTENTS INTRODUCTION 9 1. EXTERNAL GENITAL REGION OF THE ADULT FEMALE 1. Introduction 17 2. Morphology of the adult female external genitalia (a) First gonocoxa 21 (b) First gonapophyses 26 (c) Second gonocoxa 33 (d) Second gonapophyses 35 (e) Linkage of the gonapophyses 45 (f) Gonangulum 47 (g) Gonoplac 49 3.' Production of movement in the basal structures and its transmission to the ovipositor shaft 51 4. Discussion 54 2. DEVELOPMENT OF THE FEMALE EXTERNAL GENITALIA 1. Previous work on the developmental morphology of the female genitalia in the Hemiptera 55 2. Method 56 3. Development of the ovipositor in Graphocephala fennahi (a) Development of the gonapophyses 57 (b) ,Development of the basal components of the ovipositor (i) Development of the gonocoxae 72 (ii) Development of the gonangulum 76 4. Discussion 77 5. 3. DEVELOPMENTAL ANATOMY OF THE FEMALE REPRODUCTIVE SYSTEM 1. Introduction 79 2. Methods 81 3. Gross anatomy of the adult female reproductive system 83 4. Post embryonic development of the reproductive system (a) Ovary 85 (b) Lateral oviduct 97 (c) Median oviduct 98 (d) Spermatheca 102 (e) Accessory gland 106 5. Histology of the adult reproductive system (a) Ovary 107 (i) Terminal filament 108 (ii) Germarium 108 (iii) Follicular epithelium 114 (iv) Ovariole sheath 125 (v) Pedicel 131 (b) Lateral oviduct 132 (c) Median oviduct and vagina 132 (d) Spermatheca 136 (e) Accessory gland 138 6. Discussion 140 4. ABDOMINAL MUSCULATURE Introduction 0 145 6.. 1. Abdominal musculature of the adult female 146 (a) Musculature associated with the genital region of the adult female 146 (b) Musculature of the pregenital segments in the adult female (i) Segment 7 153 (ii) A typical pregenital segment 156 2. Postembryonic development of the abdominal musculature (a) Methods 159 (b) Abdominal musculature of the second instar nymph 161 (c) Abdominal musculature of the third instar nymph 163 (d) Abdominal musculature of the fourth instar nymph 166 (e) Abdominal musculature of the fifth instar nymph (i) A generalized pregenital segment 169 (ii) Genital region 171 3. Myogenesis of the abdominal muscles (a) Myogenesis during the second and third instars 175 (b) Myogenesis during the fourth and fifth instars 181 4. Discussion 186 5. STRUCTURE OF THE OVIPOSITOR RELATED TO OVIPOSITION SITE 1. Introduction 192 2. Methods 193 3. The external genitalia and associated musculature of three species (a) Graphocephala fennahi 193 (b) Ulopa reticulata 195 7. (i) First gonapophyses 195 (ii) Second gonocoxa 202 (iii) Second gonapophyses 207 (iv) Gonangulum 212 (v) Linkage mechanisms 213 (c) Macropsis scutellata (i) First gonapophyses 215 (ii) Second gonocoxa 219 (iii) Second gonapophyses 222 Gonangulum 228 (v) Linkage mechanisms 230 4. Discussion 231 6. SEXUAL BEHAVIOUR OF GRAPHOCEPHALA FENNAHI (a) Behaviour prior to mating 1. The courtship dance 236 2. Sexual communication 239 (a) Vision 240 (b) Acoustic stimuli 243 (c) Substrate-borne vibrations 244 3. Physical factors affecting pre-mating behaviour (i) The effect of time of day 253 I .. (ii) The effect of temperature 256 (iii)) The effect of day length 259 (iv) The effect of wind 259 (b) Mating behaviour (i) The effect of duration and frequency of mating 260 (ii) The mating frequency of males 263 (iii) The effect of temperature on fertilization 265 (iv) The effect of age on mating 265 (v) Mating response in the older leaf-hopper 269 (c) Description of the act of mating 271 Discussion 272 Oviposition and site selection (a) Characters used in site selection 273 (b) Oviposition and the method of incision by Graphocephala fennahi 280 7. GENERAL DISCUSSION 287 SUMMARY 300 ACKNOWLEDGEMENTS 306 REFERENCES 307 9. , INTRODUCTION Graphocephala fennahi (Young) was first introduced into Britain from the United States in 1931-2, at which time it was confused with Graphocephala coccinea, and it was not named as a separate species until 1977. In America 'G. fennahi has a more restricted range than G. coccinea and is more selective in its host plants. In Britain it is only occasionally collected from plants other than Rhododendron, and the eggs are found only in the overwintering buds of this genus. The role of leaf-hoppers as vectors of certain plant virus diseases has led to extensive research to define the vector-disease relationships. A major problem associated with such investigations concerns.the biology of the vector and this forms the object of the present study. While G. fennahi is not associated, in any part of its range, with economically important plant diseases, it is linked with the spread of bud-blast in Rhododendron caused by the wound-parasite fungus Pycnostysanus azaleae. Despite its relatively minor economic importance a suitable population of G. fennahi was available and it was considered that much valuable information on Cicadellid biology and morphology could be gained from an intensive study of a single species. Extensive studies are reported in the literature which adequately describe Hemipteran morphology, particularly that of the head, and many of these dealt with the Auchenorryncha (e.g., Ali 1958; Butt 1943; Duporte 1946, 1957; Evans 1946, 1957; Ferris 1943; Kramer 1950; Muir & Kershaw 1911, 1912; Parsons 1964; Ribaut 1952; Ross 1957; Snodgrass 1927, 1938; Spooner 1938). Much of this work has led to controversies regarding the homologies and terminology of the various sclerites, but it is not intended that this aspect of Cicadellid morphology be pursued further in this study. 10. The present account is restricted to the genital region and associated reproductive system of the female, and attempts to describe these regions on a functional and developmental basis. While the morphology of this region has an extensive literature, it is mostly superficial and incomplete; the deyelopment of the systems and their function in sexual behaviour are fields in which the literature is extremely limited. The first writer to describe the ovipositor of Auchenorrynchan Homoptera was Aristotle. Illustrations and descriptions are provided by Malpighi (1687) and illustrations by Reaumur (1740). All the early work was concerned with unidentified Cicadidae, the small size most Cicadel lids preventing their study until the nine- teenth century. The first workwork( of importance on the Auchenorryncha was that of Dufour (1825), in which he studied the digestive and reproductive systems of a cicada. Two papers by Doyere (1837) discussed the structure and function of the Cicadid ovipositor, and showed that the movement of the gonapophyses is brought
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