SCUTTLE : THE SCUTTLE FLIES: THE PHORIDAE

R. H. L. Disney Field Studies Council Research Fellow, Cambridge University, UK

Phorids are the least studied of all the large families ofDiptera (Naumov,1985)

il t1lJ SPRINGER-SCIENCE+BUSINESS MEDIA. B.V. Flrst edltlOn 1994 © 1994 R H L Disney Originally published by Chapman & Hall in 1994

Typeset In 10/11 Bembo by Type Study, Scarborough

ISBN 978-94-010-4562-9 ISBN 978-94-011-1288-8 (eBook) DOI 10.1007/978-94-011-1288-8

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Colour plate appears between pages 20 and 21

Foreword IX Preface X

1. Introduction 1 1.1 Introduction 1 1.2 Historical perspective 2 1.3 What are scuttle flies? 4 1.4 Why study phoridae? 9 1.5 A brief history of phoridology 9

2. Eggs 13 2.1 Introduction 13 2.2 Fecundity, batch size and clutch size 14 2.3 Development 18 2.4 Egg maturation 18 2.5 Oviposition 20

3. Larvae 25 3.1 Introduction 25 3.2 Feeders on dead or decaying organic matter (saprophage species) 32 3.3 Fungus-feeding/fungus-breeding larvae 45 3.4 Plant-feeding/plant-breeding larvae 57 3.5 Predator, parasitoid and parasitic larvae 61 3.6 Miscellaneous rearing records 91 3.7 Enemies 92

4. Pupae 94 4.1 Introduction 94 4.2 Pupation 99 4.3 Overwintering 99 4.4 Enemies 99

5. Development 103 5.1 Introduction 103 5.2 Number oflarval instars 103 CONTENTS

5.3 Development times 104 5.4 Pupariation and pupation 108 5.5 Adult development 108 5.6 Alleged protandrous hermaphroditism and parthenogenesis 109 5.7 Sex determination 110 5.8 Sex ratios 112 5.9 Diapause 112 5.10 Effects of crowding 112 5.11 Polymorphism 112

6. Adults 116 6.1 Introduction 116 6.2 Flower visiting 121 6.3 Feeding 132 6.4 Special associations 140 6.5 Courtship and mating 154 6.6 Longevity 160 6.7 Phoresy by mites on scuttle flies 162 6.8 Enemies 165

7. Ecology 170 7.1 Introduction 170 7.2 The phorid faunas of different habitats 170 7.3 The dearth oflarvae in soil extractions 182 7.4 Habitat preferences 182 7.5 Special microhabitats and resources 183 7.6 Diurnal patterns 188 7.7 Phenology 189 7.8 Cold-adapted adults 196 7.9 Niche separation and competition 196 7.10 Dispersal 197 7.11 Agricultural and medical significance 199 7.12 Conservation evaluation using Phoridae 202

8. Identification 203 8.1 Introduction 203 8.2 Keys to genera 211 8.3 Guide to literature for species identification 265 8.4 Fossil Phoridae 294 8.5 The current debate on phorid classification 296

9. Methods 380 9.1 Introduction 380 9.2 Collecting and sampling 380 9.3 Rearing 384 9.4 Culturing in the laboratory 385 9.5 Marking flies for population studies 385

VI CONTENTS

9.6 Control of pest species 385 9.7 Slide mounting Phoridae 386

References 389 Author index 439 Phoridae index 447 Index ojother organisms 458 Subject index 464

Vll Advance in the knowledge of the natural history of a group of is dependent upon taxonomic knowledge. The following have served phori• dology well with their taxonomic expertise, both by publication and by identifying specimens for others. The importance of the latter service is too often taken for granted. Theodor Becker 1840-1928 John Henry Wood 1841-1914 William Lundbeck 1863-1941 Filippo Silvestri 1873-1949 John Russell Malloch 1875-1963 Hermann Schmitz 1878-1960 Charles Thomas Brues 1879-1955 Thomas Borgmeier 1892-1975 Charles Norman Colyer 1908-1970

V111 Foreword

Today the topic of 'biodiversity' is a matter of general interest; national leaders refer to it in international meetings, such as the one at Rio de Janeiro. However, the assessment of biodiversity depends on detailed work of a careful and often unglamourous type. We are very uncertain as to the actual biodiversity of the Earth. All biologists will accept that many species are undescribed, a majority will agree that we know considerably less than half the living species. Ifwe are really to understand our 'house', our 'oikos' that gives us the name of the now popular science of ecology, we must be able to do more than put names on the organisms that share our Earth, we must know about their biology, their life style - their bionomics. Insects constitute more than half the known species of living organisms and probably a greater proportion of the unknown ones. Entomologists therefore face a formidable task. Fortunately there are those rare persons who devote themselves to a particular group and over their lifetime gain a real understanding of its species and their biology. Henry Disney is one such person and we are extraordinarily fortunate that after 20 years of study he has provided us with this overview of his chosen group, it is an assemblage of the 'world knowledge' on the Phoridae. We will all hope that it will not be another couple of decades before he provides a second oeuvre. The magnitude of the task he has achieved, as well as that ahead, can be appreciated when it is recognized that there may be five times as many species ofscuttle as birds in the world. The family evolved a long time ago, at least 80 million years; scuttle flies coexisted with the dinosaurs and were undoubtedly a diverse group when the first hominoids appeared around 10 million years ago. This long evolutionary history expresses itself in the wide diversity of habit and form described in this volume. Although in the 230 years since a phorid was first described many entomologists have made contributions to our knowledge of the members of the family, it has been relatively neglected until Dr Disney turned his attention to it. This comprehensive account of existing knowledge, so much of which is due to the author, should encourage others to join in the study of this widespread and abundant, yet hitherto obscure, group.

Professor Sir Richard Southwood FRS Oxford February, 1994 Preface

I am well aware that I have probably overlooked important observations published in unexpected places. I should welcome references to any such omissions which readers may encounter. Some omissions have been deliberate, where I have doubts about their correctness or the identity of the species involved. In some of the latter cases, however, I have cited the observations but indicated the doubts. In many cases those who refer to a work cited will find the species referred to by a subsequently discarded synonym or an identification of the species which has been subsequently revised. These changes are covered by the catalogues cited in section 1.5 or the literature recommended for the (8.3). I have only rarely burdened the text by the citation of synonyms. I remain particularly aware that I have probably not done justice to the ecological literature. I would especially welcome notification of interesting quantified data I have overlooked. A glance at the bibliography will quickly reveal that observations on Phoridae have been published in some decidedly obscure journals. Indeed some references cited in the literature defeated the library services of the United Kingdom. Some articles could not be traced, and in some cases the journal cited was not listed in any of the standard reference works. A late aunt, Sheila Disney, encouraged my interest in natural history when I was a boy, and her legacy enabled me to buy my dream compound microscope. Without this good microscope I would never have been in a position to tackle the of such small insects as the scuttle flies. With it I have been able to produce many detailed descriptions and the hundreds of drawings used to illustrate both these and the identification keys I have published. While a less sophisticated microscope is adequate for the identification of phorids, one needs a superior instrument to produce detailed drawings and descriptions. I thank Professor G. Horn FRS and Dr K. A. Joysey for facilities in the Cambridge University Department of Zoology and the Zoology Museum. The writing of this book was made possible by funding from the Isaac Newton Trust (Trinity College, Cambridge) and the Harold Hyam Wingate Foundation (London). I am most grateful for this support. I am also very grateful to Dr Jeff Barnes (Biological Survey, Cultural Education Center, Albany, New York) for his constructive comments on early drafts of most chapters, and to Dr Sally Corbet (Department of Zoology, University of Cambridge) for casting her critical eye over a PREFACE

complete draft. Dr Zakaria Erzin~lioglu (Department of Zoology, Univer• sity of Cambridge) also commented on some sections, and has been a source of encouragement over many years. Ken G. V. Smith (formerly of the Natural History Museum, London) has also been a considerable en• couragement, especially in the early years of my attempts to get to grips with phorid taxonomy. As ajournal editor and referee he has shown himself not to be allergic to unorthodoxy, for which I am grateful. I am grateful to numerous librarians, in particular to those of the Balfour Library, Department of Zoology, the Scientific Periodicals Library and the University Library at Cambridge University, the Royal Entomological Society ofLondon and the libraries of the Natural History Museum, London. I am grateful to Margaretha Harriott for the translation of some papers in Dutch. Dr John Linley (University of Florida, Institute of Food and Agricultural Sciences) kindly allowed me to use his superb SEM photographs of the egg of (Fig. 2.1). Dr Michael E. N. Majerus (Cambridge University, Department of Genetics) kindly allowed me to use his photo• graph of the living phorid in Plate 1. John W. Rodford (Cambridge University, Department of Zoology) drew Figs 9.2 and 9.3. Mr Peter V. York (Photographic Unit, The Natural History Museum, London) kindly took the photograph in Fig. 1.1(a). Mr Neal C. Maskell (Photographic Section, Cambridge University Department of Zoology) kindly took the photograph in Fig. 1.1 (b). I am grateful to Donald Azuma (Academy of Natural Sciences, Philadel• phia) for the loan of a male Neodohrniphora and to Dr Brian Brown (Natural History Museum, Los Angeles) for information regarding a character of Parasyneura, and for allowing citation of some of his unpublished obser• vations. The following have kindly permitted me to reproduce the figures given in brackets:

American Naturalist (3.6) E. Schweizerbart'sche Verlagsbuchhandlung - Archiv for Hydrobiologie (3.3, 4.4) Archivos do Instituto de Biologia Vegetal, Jardin Botanico Rio de Janeiro (3.8, 4.6) Royal Entomological Society of London - Ecological Entomology (6.13) Dr K. Kaneko - JapaneseJournal of Sanitary Zoology (2.2a) Makunagi (6.11,6.15) Mushroom Growers Association - MGA Bulletin (7.1) E. J. Brill, Leiden - Nematologica (6.16) Treubia Deel (4.3a-d) The Orion Publishing Group Ltd (incorporating Weidenfeld and Nicol• son) (8.95) Professor 1. Eibl-Eibesfeldt - Zeitschrijt for Tierpsychologie (3.9) Gustav Fischer Verlag - Zoologische Jahrbucher (Anatomie) (5.1)

The rest of the figures are by myself. Most of these have appeared in previous

Xl PREFACE publications. I acknowledge, with thanks, the following journals and organizations for allowing me to reproduce the figures given in brackets: Annales Entomologici Fennici (2.3b,c, 8.5a) Aquatic Insects (Swets Publishing Service) (2.2b, 4.3e,f, 8.9a) Museum Alexander Koenig, Bonn - Bonner zoologische Beitriige (1.4, 6.4, 8.23b,c, 8.24, 8.63a, 8.84b, 8.85) BENH Society - British Journal oj Entomolgy and Natural History (2.6a, 8.21b,c, 8.40c, 8.54a, 8.70a, 8.75b, 8.78c-e, 8.91b) International Institute of Entomology - Bulletin oj Entomological Research (3.7, 8.2b,c) Entomologica Fennica (8.13a, 8.81) Entomologica Scandinavica (3.1-3.4, 3.5a, 4.1, 4.5, 6.1d, 6.7, 8.2a, 8.4a, b, 8.6a,b, 8.25b, 8.31a, 8.40a, 8.46, 8.56b, 8.57a, 8.60d, 8.61, 8.80b) Royal Entomological Society of London - The Entomologist (1.2) The Gem Publishing Company - Entomologist's Monthly Magazine (1.1 b, 6.5a, 8.6c, 8.33a, 8.56a, 8.62, 8.64, 8.76,8.77, 8.96) The Entomologist's Record (4.2) Giornale Italiano di Entomologia (8.10, 8.19, 8.20, 8.26, 8.29, 8.43b,c, 8.44, 8.49a, 8.60a-c) Glasgow Naturalist (8. 12a-b) Journal oj African Zoology (8.2d, 8.30, 8.56c-e, 8.57b, 8.58, 8.71, 8.72, 8.93c) Taylor and Francis Ltd - Journal oj Natural History (1.3a, 2.7, 3.5b, 5.2, 6.5c, 6.8--6.10, 8.47a,b, 8.49, 8.50, 8.59, 8.66-8.68, 8.92, 8.93a,b) The Zoological Society of London - Journal oj Zoology, London (8.7, 8.8, 8.15a) Naturalist (8.9b, 8.14a, b) Associated Publishers, Gainesville - Oriental Insects (3.10, 6.14, 8. 78a, b) Sociobiology (2.6b, 6.3, 6.5b, 6.6, 8.11a,b, 8.16, 8.17a, 8.34, 8.35, 8.38, 8.42a,c,d, 8.45b, 8.51b,c, 8.52-8.54, 8.74a, 8.79d, 8.80a) Royal Entomological Society of London - Systematic Entomology (8.4e, 8.11c, 8.12c, 8.13b, 8.39f, 8.41b,c, 8. 63b-d, 8.69a,b,d, 8.70c,d, 8.73b, 8.82a-d, 8.83, 8.84c,d, 8.86-8.90) University of Newcastle upon Tyne, Agriculture Environment Research Group (9.2, 9.3) Dunger and Humblot GHBH - ZeitschriJt for angewandt Zoologie (1.1 a, 2. Sa, b, 8.18b, 8.27, 8.28a) Academic Press Ltd - Zoological Journal oJthe Linnean Society (6.1a-c, 6.12, 8.37, 8.65) Gustav Fischer Verlag - Zoologischer Anzeiger (8.31 b,c, 8.32) Note: Throughout, all scale bars on the figures are 0.1 mm. R.H.L.D. Cambridge, November, 1993

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