A TAXONOMIC AND PHYLOGENETIC STUDY OF THE IMMATURE STAGES OF BRITISH MIRIDAE (HEMIPTERA-HETEROPTERA) by George Cumming McGavin BSc (Hons), Edinburgh A thesis submitted for the degree of Doctor of Philosophy of the University of London and ,for the Diploma of Imperial College Department of Entomology British Museum (Natural History) London SW7 5BD June, 1979 - i - ABSTRACT A taxonomic and phylogenetic study of the immature stages of British Miridae (Hemiptera-Heteroptera) George Cumming McGavin This thesis describes the Vth instar nymphs of the British Miridae, an heteropteran family of 206 species. Keys to subfamilies, tribes and selected species are given, together with measurements for 24 body characters based on 10 individuals per species where possible. The dorsal abdominal gland openings are figured and the histology of the gland is examined. The morphology of the trichobothria occurring on the mesothoracic and metathoracic femora is investigated using scanning electron microscopy, and maps of their distribution in 116 species are drawn. The nymphal and adult patterns are found to be the same. The possible functions of trichobothria and their use in phylogenetic consideration of the group are examined. The structure of the pretarsus is found to be constant throughout the life cycle. One tribe, the Stenodemini, is investigated using numerical taxonomic techniques and the results are compared to those of conventional taxonomy. Average linkage cluster- ing shows exact agreement with the latter. The interrelations of the genera of this tribe are examined using canonical variate analysis. CONTENTS page ABSTRACT INTRODUCTION 3 MATERIALS AND METHODS 14 Collection 14 Scanning electron microscopy 14 Slide mounts 15 Histology 16 Photography 16 Breeding 17 Numerical taxonomy 17 GENERAL MORPHOLOGY OF MIRID NYMPHS 19 Head 19 Rostrum 19 Antennae 20 Pronotum 20 Mesonotum and metanotum 21 Abdomen 21 Prothoracic leg 22 Mesothoracic leg 22 Metathoracic leg 23 Antennal growth 42 Campaniform sensillae 49 TRICHOBOTHRIA 55 Bryocorinae 60 Deraeocorinae 61 Phylinae 61 Dicyphinae 63 Orthotylinae 64 Mirinae 66 Discussion 68 DORSAL ABDOMINAL GLANDS 157 NUMERICAL TAXONOMY 195 Clustering analysis 196 Canonical variate analysis 202 page KEY TO THE SUBFAMILIES OF Vth INSTAR BRITISH MIRIDAE 214 Bryocorinae 217 Deraeocorinae 217 Phylinae 218 Dicyphinae 225 Orthotylinae 227 Mirinae 234 DESCRIPTIONS OF BRITISH MIRID NYMPHS 261 Bryocorinae 264 Deraeocorinae 266 Phylinae - 274 Dicyphinae 326 Orthotylinae 341 Mirinae 380 DISCUSSION 441 APPENDICES A Collectors 449 B Collecting sites 450 C Statistical data for the Stenodemini 452 D Altered county designations 459 ACKNOWLEDGEMENTS 460 BIBLIOGRAPHY 461 - iv - List of figures page 1-4 SEMs - general features 25-32 5-8 SEMs - pretarsal structures 34-41 9-12 Antennal growth 43-46 13 Campaniform sensillae 50 14-18 SEMs - trichobothria 72-81 19 Femoral trichobothrial legends and maps 83-155 20-40 DAGO drawings 166-186 41-43 Micrographs and sections - DAGOs 188-193 44 Dendrogram 200 45-47 Canonical variate analysis 205-207 48 Ratios of antennal and body length in the Stenodemini 211 49-63 Key drawings 244-258 64 States of trichomae around a recessed bothrium 259 65 Body measurements 263 66 Deraeocorinae - head and pronotum 267 67 Oncotylus viridiflavus (Vth instar nymph) 276 68 Plagiognathus arbustorum (Vth instar nymph) 309 69 Chlamydatus pullis, C. saltitans and Strongylocoris leucocephalus(Vth instar nymphs) 313 70,71 Dicyphinae - head and pronotum 327 & 334 72 Cyllecoris histrionicus (Vth instar nymph) 354 73 Dryophilocoris flavoquadrimaculatus 357 (Vth instar nymph) 74 Lygus rugulipennis (Vth instar nymph) 384 75 Liocoris tripustulatus (Vth instar nymph) 387 76 Camptozygum pinastri (Vth instar nymph) 393 77 Calocoris quadripunctatus (Vth instar nymph) 405 78 Megacoelum infusum (Vth instar nymph) 416 79 Collecting sites 451 - v - List of colour plates page 1 Heterotoma planicornis (adult) 2 2 Heterotoma planicornis (Vth instar nymph) 13 3 Orthonotus rufifrons (adult) 18 4 Orthonotus rufifrons (IIIrd instar nymph) 24 5 Psallus salicellus (Vth instar nymph) 33 6 Dryophilocoris flavoquadrimaculatus (Vth instar nymph) 48 7 Alloeotomus gothicus (Vth instar nymph) 54 8 Megacoelum infusum (IVth instar nymph) 71 9 Megacoelum infusum (IVth instar nymph) 82 10 Pilophorus perplexus (Vth instar nymph) 156 11 Pilophorus cinnamopterus (Vth instar nymph) 165 12 Deraeocoris ruber (IVth instar nymph) 187 13 Deraeocoris ruber (Vth instar nymph) 194 14 Phytocoris tiliae (IVth and Vth instar nymphs) 213 15 Phytocoris varipes (Vth instar nymph) 216 16 Adelphocoris lineolatus (Vth instar nymph) 243 17 Dicyphus pallicornis (Vth instar nymph) 260 18 Dicyphus errans (Vth instar nymph) 330 19 Dicyphus errans (Vth instar nymph) 331 - 2 - Plate 1 Heterotoma planicornis (adult) lxLO 3 INTRODUCTION Although the majority of insect systematics has been based on characters of the adult stages, the importance of the immatures has been recognised by a number of authors (Hayes,1931; Jordan,1951; Van Emden,1955 & 1957; Stammer, 1957 and Klausnitzer,1969). Characters of the immatures have been used to support the primary division of the Coleoptera, Diptera and Hymenoptera and are as important • as the adult characters in the subdivision of the Odonata and the Neuroptera. Advances in the taxonomy and classifi- cation of the Aphididae and Coccidae have been made through studies of the nymphal* stages (Borner,1953; Borkhsenius, 1950). Van Emden (1955) gave examples of new families, tribes and genera and the transfer of species and species groups from one taxon to another, based upon the study of immature stages. Bibliographies of important works on the classification of the larvae and nymphs of various insect orders has been given by Van Emden (1955 & 1957), Stammer (1957) and Klausnitzer (1969). In theory, characters of the adult and immature stages are of equal importance in taxonomy since both are derived from the same gene pool. A study of the immatures, however, offers a number of advantages. Comparative studies of immature forms are valuable in attempts to correlate onto- geny with phylogeny, sometimes affording better characters for examination than the adults. Characters of immature insects will often define the same groups as will different characters in the adult insects. These are known as congruent groups. There are partial degrees of congruence and where characters of the immature stages define different groups; they are termed incongruent (Van Emden,1957). Some immature stages are of course secondarily adapted to their habitat, where this differs The term nymph is used to mean the immature stage of hemi- metabolous insects - those with direct metamorphosis - as opposed to the term larva which refers to the immature stage of holometabolous insects - those with indirect or complete metamorphosis. - 4 - from that of the adults. In some aquatic orders of hemi- metabolous insects secondary adaptations are a result of differences in biology between the aquatic nymphs and terrestrial adults. Where a resting pupal stage occurs, the characters may also be unrelated. In practice, either the adult or the immature stage of an insect species may exhibit more accessible, less variable and more useful characters for classification, but in general the adult shows a greater degree of differentiation than the immature and is thus more suited to species identification. How- ever, the characters of immature stages are likely to be of greater importance for classification in the broader sense, such as the definition of higher categories (Van Emden,1955). The majority of literature shows that, by and large, the characters of immature stages can be used in the same way as those of the adult stages. It has been stated that, in general, immature insects have a greater effect upon man and are more injurious than the adult stage, due to their presence in large numbers and for longer periods (Van Emden,1957), and their taxonomic study will therefore often be of great economic value. Nymphs and larvae of pest species are better targets for control measures, as in general their cuticle is softer and more vulnerable to various types of treatment. Immatures neither reproduce nor fly, which is beneficial in the field of biological control where parasites and predators have more chance of being effective. In general, control measures directed against immature stages are more likely to be quicker acting. Knowledge of the taxonomy of larval and nymphal stages is also of use to ecologists who 'require such information in quantitative ecological research. When studying complex habitats and examining the food ecology and energetics of ecological systems, it is necessary to be able to determine the species of larvae and nymphs which are present. It may be that one or more closely related species appear to coexist, but when the immature stages are examined, differ- ences in their biology, food preferences, etc., may be found. The study of the ontogeny of characters in hemimetabolous insects, and the more complex changes of characters and character complexes in the development of holometabolous insects, will provide interesting insights into the gene- tic mechanisms controlling their inheritance and occurrence in the adult stages. Each cell of an insect species contains the same DNA, and Wigglesworth (1975) has shown that each cell must contain the metabolic systems needed for the formation of both larval and adult cuticle. The role of hormones is to determine which of these