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DIPTERA: CERATOPOGONIDAE) ) Stet '1+ Nf ? 1`R3 I1 A MORPHOF ETRIC ANALYSIS OF THE CULICOIDES PULICARIS SPECIES COMPLEX (n.1'1 (DIPTERA: CERATOPOGONIDAE) ) stet '1+ nf ? 1`r3 I1 BY Richard Paul Lane, B.Sc. (London), A.R.C.S. A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College Department of Zoology and Applied Entomology, Imperial College, London, S.W.7. August 1979 ABSTRACT This study assesses the value of currently available multivariate morphometric techniques in the analysis of the Culicoides pulicaris complex. This midge complex is typical of species groups which are difficult to separate into discrete clusters (species). Initially, emphasis is given to the study of eight nominal taxa in Britain: C. delta Edwards, fagineus Edwards, grisescens Edwards, impunctatus Goetghebuer,.lupicaris Downes & Kettle, newsteadi Austen, pulicaris Linnaeus and punctatus Meigen. Subsequently, material from other parts of the Palaearctic Region is included. Morphological characters of adults are tested to evaluate the nature and extent of variation. Size is rejected as unreliable, since both intraspecific and seasonal variation is excessive. Allometry of size in legs, antennae and palps is studied in large homogeneous samples of three species and the implications for taxonomy discussed. A new system for coding wing pattern,utilising pattern elements, is developed and compared to a mechanical scanning method. The former, based on only 13 characters, is preferable, on practical and theoretical grounds, to the scanning method involving 420 characters. In constructing a classification, two points are considered. Firstly, whether a large number of characters is required for a reliable classification and secondly, whether the recognised species are homogeneous. Using subsets from a total of 72 characters, selected by inspecting inter—character correlations, loadings on principal components, or traditional use, approximately three quarters are found to be superfluous. Using individual specimens as operational taxonomic units to test the homogeneity of species, lupicaris is rejected and another, sp. A, is recognised as new. Percentiles about the means of each species are incorporated into canonical variate diagrams, for the accurate identification of additional specimens. A system of classification is developed, in which species are considered as sets with indistinct boundaries. Under these conditions, transition from membership to non—membership of each set is gradual rather than abrupt. The relationship of these findings with current species concepts is discussed. 2 TABLE OF CONTENTS PAGE ABSTRACT 1 TABLE OF CONTENTS 2 ACKNOWLEDGEMENTS 5' 1. INTRODUCTION 1.1. The genus Culicoides Latreille.(Diptera: Ceratopogonidae) 7 1.2. The phylogenetic relationships of Culicoides to other Diptera 8 1.3. Importance of Ceratopogonidae as pests and vectors of parasitic organisms 9 1.4. Species concepts as applied to Diptera 18 1.5. The taxonomic problem of species complexes in biting flies 25 1.6. Species complexes in the Ceratopogonidae 32 2. OBJECTIVES OF THIS STUDY 2.1. Objectives 34 2.2. Rationale and limitation of the approach 34 3. MORPHOLOGY 3.1. Aspects of the term 'character' 37 3.1. The anatomy of Culicoides 39 4. TAXONOMIC REVIEW OF THE CULICOIDES PULICARIS COMPLEX 4.1. Definition of higher taxa 56 4.2. Formal description and nomenclature 61 4.3. Geographical distribution 74 4.4. Immature stages 75 4.5. Biosystematic data on the C. pulicaris complex 76 4.6. Applied importance of the pulicaris group 78 5. ENTOMOLOGICAL METHODS 5.1. General methods and techniques 81 5.2. Restriction of study to females 84 3 PAGE 6. STATISTICAL METHODS 6.1. Introduction 85 6.2. Character types 85 6.3. Primary data matrices 86 6.4. Standardisation 86 6.5. Association matrix 87 6.6. Cluster analysis 90 6.7. Ordination methods 91 6.8. Discrimination 96 7. BIOMETRIC STUDY OF TAXONOMIC CHARACTERS AND THEIR VARIABILITY 7.1. Review of previous work 99 7.2. Seasonal variation in size 101 7.3. Geographical variation 108 7.4. Variation in segments of the antennae 110 7.5. Allometry of size 119 8. ESTABLISHMENT OF NEW CHARACTERS 8.1. Cibarium 142 Chaetotaxy 145 8.3. Wing pattern 148 9. NUMERICAL CLASSIFICATION OF THE C. PULICARIS COMPLEX 9.1. Introduction 183 9.2. Selecting characters from a single body region 186 9.3. Removal of the influence of size from the analysis 196 9.4. Reduction of characters by objective means 213 9.5. Selection of variables by subjective means 251 9.6. Summary 267 10. DISCRIMINATION AND IDENTIFICATION 10.1. Introduction 279 10.2. Discrimination of species 283 10.3. Identification using the results of canonical variate analysis 294 11. GENERAL DISCUSSION PAGE 11.1. Evaluation of numerical methods 300 11.2. Taxonomy of the C. pulicaris complex 311 11.3. Species groups in Culicoides 312 11.4. An alternative approach — species as non— disjoint sets 313 SUMMARY 327 REFERENCES 331 ADDENDA 357 APPENDIX 359 5 ACKNOWLEDGEMENTS This study was carried out in the Department of Entomology, British Museum (Natural History), London. I would like to thank the Keeper, Dr. P. Freeman, not only for suggesting the topic, but also for his continual support throughout the duration of the study. Sincere thanks are due to my Director of Studies, Mr. R. G. Davies, Department of Zoology and Applied Entomology, Imperial College. His encouragement and informative discussions throughout the course of my work have been invaluable. Thanks also go to my Supervisor, Dr. G. B. White, formerly of the British Museum (Natural History), who gave much helpful advice and sufficient rope — but never quite enough to hang myself:: Within the Museum, colleagues in the Medical Insects Section offered much assistance, by way of constructive criticism and technical assistance. I am indebted to Dr. M Hills and Miss K. Shaw, of the Biometrics Section, for guiding me through statistical theory and for help with computer programming. I wish to thank the following specialists for the loan or donation_of specimens: Mr. J. Boorman, Animal Virus Research Institute, Pirbright; Dr. A. Campbell, University of Edinburgh; Dr. J. Clastrier, Museum Nationale d'Histoire Naturelle, Paris; Dr. R. M. Gornostaeva, Martsinovsky Institute of Parasitology and Tropical Medicine, Moscow; Prof. A. V. Gutsevich, Zoological Institute, Leningrad; Dr. S. Kitaoka, National Institute of Animal Health, Tokyo; Mr. E. C. Pelham—Clinton, Royal Scottish Museum, Edinburgh; Prof. Y. Wada, Nagasaki School of Medicine, Nagasaki; Dr. W. Wirth, U.S. National Museum, Washington. Finally, I must thank my wife, Maureen, who despite her advanced pregnancy, still managed to sit close enough to the typewriter to produce this thesis: 6 FRONTISPIECE Culicoides pulicaris (Linnaeus). (Drawing by Terzi from Edwards, Oldroyd & Smart, British Bloodsucking Flies). Section 1. •INTRODUCTION 1.1. THE GENUS CULICOIDES LATREILLE (DIPTERA• CERATOPOGONIDAE). The genus Culicoides is composed of approximately 1000 species of small biting midges belonging to the family Ceratopogonidae. Culicoides have a world wide distribution, except for New Zealand and Southern Chile. Most species are small, with a wing length averaging 1.5mm. and reaching a maximum of approximately 2mm. The wings are often characteristically patterned. The females have well developed biting mouthparts in most species. The males do not bite. Some species having females with atrophied mouthparts, associated with an autogenous life cycle, have been found in the, Canadian Arctic (Downes, 1970). In most species, the females need a blood meal for the development of the eggs, although some, as noted above, are completely autogenous. Others will lay a first batch of eggs autogenously and require a blood meal for maturation of subsequent batches (e.g., C. impunctatus, one of the species studied here (Service, 1968)). The majority of species are crepuscular and biting activity continues into the night. Others however, bite during the day. Their attack is usually inhibited by wind speeds of greater than 3 metres per second. Those species living in exposed environments, such as salt marshes, will fly during higher wind speeds. Host specificity is not well understood for most species, although it appears that the majority of species have preference for one primary host and a range of secondary hosts (Kettle, 1962). The tendency of adults to collect in large numbers and bite unceasingly makes them extremely troublesome to man and domestic animals. Their unpleasant attention to man has led to the coinage of a number of vernacular names. In Britain they are called midges; in the West Indies, southern U.S.A. and Australia they are somewhat ambiguously called sandflies ( a term usually reserved elsewhere for Phlebotominae);in French Canada as brClots; as arabis (midi) and muchits (Blavais) in France; jejenes in Cuba; punkies or no—see—ums in U.S.A.; maruins in Amazon basin; nonos in Tahiti; makanagi or nukaga in Japan; mout—mout in French Guinea. Mating may take place on the ground (e.g., C. melleus,(Linley & Adams, 1972) or in swarms (Downes, 1955). The eggs are elongate 8 ovoids in shape, and are laid on moist substrates. Immersion in water does not impede their development. The eggs are usually hatched after 5 — 9 days, halophilic species often after much less (2 — 3 days) and in one species, C. grisescens, a period of 205 — 223 days elapse before hatching (Parker, 1950). The latter case probably represents a period of hibernation. In temperate regions, over- wintering takes place aS a fourth instar larva. The larvae are apneustic, swimming in a characteristic eel—like manner. Edwards (1939) quotes a description of a larva and pupa of what is apparently Culicoides, given by a Rev. W. Derham, as long ago as 1712. In more recent times, the larvae and other immature stages have been described; West African Culicoides by Carter, Ingram and Macfie (1920, 1921); British Culicoides by Hill (1947), Kettle & Lawson (1952); European species by Lenz (1934), Mayer (1934a, 1934b) and Thienemann (1954).
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