Ecology and Evolution of Dung Beetles

Leigh Simmons was born and educated in the UK, and is currantly Professor of Evolutionary Biology at the University of Western Australia. His research interests lie in all aspects of reproductive biology, from the evolution of sperm form and function, to mate searching and courtship behaviour. James Ridsdill-Smith was born and educated in the UK but carried out all his research in Australia working for CSIRO Entomology. He has been developing biological and ecological solutions to various pest problems and 15 years involved in the biological control of dung with scarabaeine dung beetles.

Preface xiii

Acknowledgements xv

Contributing authors xvii

1 Reproductive competition and its impact on the evolution and ecology of dung beetles 1
Leigh W. Simmons and T. James Ridsdill-Smith

1.1 Introduction 1

1.2 Competition for mates and the evolution of morphological diversity 2

1.3 Competition for resources and the evolution of breeding strategies 9

1.4 Ecological consequences of intraspecific and interspecific competition 14

1.4.1 Niche expansion 15

1.4.2 Regional distribution and seasonal activity 17

1.4.3 Community dynamics 18

1.5 Conservation 19

1.6 Concluding remarks 20

2 The evolutionary history and diversification of dung beetles 21
T. Keith Philips

2.1 Introduction 21

2.2 Scarabaeinae diversity and tribal classification issues 22

2.2.1 Dichotomiini and Coprini 24

2.2.2 Canthonini 25

2.2.3 Eucraniini 25

2.2.4 Phanaeini 25

2.2.5 Phanaeini + Eucraniini 26

2.2.6 Scarabaeini 26

2.2.7 Gymnopleurini 26

2.2.8 Eurysternini 26

2.2.9 Sisyphini 26

2.2.10 Onitini 27

2.2.11 Oniticellini 27

2.2.12 Onthophagini 27

2.3 Scarabaeine dung beetle phylogenies 27

2.4 The sister clade to the Scarabaeinae 31

2.5 The origin of the dung beetles 33

2.6 The oldest lineages and their geographical origin 34

2.7 Evolution of activity period 36

2.8 Evolution of feeding habits 36

2.9 Evolution of derived alternative lifestyles 37

2.10 Evolution of nidification: dung manipulation strategies 40

2.11 Evolution of nidification: nesting behaviour and subsocial care 42

2.12 Conclusions 44

2.13 Future work/gaps in knowledge 45

3 Male contest competition and the evolution of weapons 47
Robert Knell

3.1 Introduction 47

3.2 Dung beetle horns as weapons 49

3.3 Functional morphology of horns 50

3.4 Horns as predictors of victory 53

3.5 Are beetle horns simply tools? 55

3.6 The evolution of horns: rollers vs. tunnellers 56

3.7 The evolution of horns: population density 59

3.8 The evolution of horns: sex ratio 63

3.9 Future work 64

4 Sexual selection after mating: the evolutionary consequences of sperm competition and cryptic female choice in onthophagines 66
Leigh W. Simmons

4.1 Introduction 66

4.2 Sperm competition theory 68

4.3 Evolution of ejaculate expenditure in the genus Onthophagus 71

4.4 Evolutionary consequences of variation in ejaculate expenditure 72

4.5 Theoretical models of female choice 75

4.6 Quantitative genetics of ejaculate traits 76

4.7 Empirical evidence for adaptive cryptic female choice in Onthophagus taurus 78

Box 4.1 Indirect genetic benefits of cryptic female choice in Onthophagus taurus 81

4.8 Conclusions and future directions 83

4.9 Dedication and acknowledgement 86

5 Olfactory ecology 87
G.D. Tribe and B.V. Burger

5.1 Introduction 87

5.2 Orientation to dung and other resources 87

5.3 Olfactory cues used in mate attraction and mate recognition 91

5.3.1 Morphology of pheromone-producing and -dispersing structures 93

5.3.2 Pheromone-dispersing behaviour 94

5.4 Chemical composition of Kheper pheromones 95

5.4.1 Electroantennographic detection 98

5.4.2 Comparison of the responses of beetle species to attractant compounds 98

5.4.3 The pheromone-disseminating carrier material 102

5.5 Kairomones 103

5.6 Defensive secretions 104

5.7 Conclusions and future directions 105

6 Explaining phenotypic diversity: the conditional strategy and threshold trait expression 107
Joseph Tomkins and Wade Hazel

6.1 Introduction 107

6.2 The environmental threshold model 109

6.2.1 Does the development of a horn dimorphism in male dung beetles occur in a manner consistent with the assumptions of the ET model? 110

6.3 Applying the threshold model 118

6.3.1 Predicting the mean switchpoint of a population 118

6.3.2 Estimating the selection on thresholds using the ET model 119

6.3.3 Estimating selection under positive allometry 120

6.4 Future directions 123

7 Evolution and development: Onthophagus beetles and the evolutionary development genetics of innovation, allometry and plasticity 126
Armin Moczek

7.1 Introduction 126

7.2 Evo-devo and eco-devo – a brief introduction 127

7.3 Onthophagus beetles as an emerging model system in evo-devo and eco-devo 128

Box 7.1 Developmental genetic tools available in Onthophagus beetles: utility and limitations 129

7.4 The origin and diversification of novel traits 132

7.4.1 Dung beetle horns as novel traits 133

7.4.2 How horns develop 134

7.4.3 The developmental genetics of horn growth 135

7.4.4 The developmental genetics of pupal remodelling 137

7.4.5 The origin of adult thoracic horns through exaptation 138

7.5 The regulation and evolution of scaling 140

7.5.1 Onthophagine scaling relationships: the roles of nutrition and hormones 142

7.5.2 Onthophagine scaling relationships: the role of trade-offs during development and evolution 143

7.5.3 Onthophagine scaling relationships: developmental decoupling versus common developmental programme 144

7.5.4 Onthophagine scaling relationships: the developmental genetics of size and shape 147

7.6 The development, evolution, and consequences of phenotypic plasticity 148

7.6.1 Developmental mechanisms and the evolutionary consequences of plasticity 149

7.7 Conclusion 151

8 The evolution of parental care in the onthophagine dung beetles 152
John Hunt and Clarissa House

8.1 Introduction 152

8.2 Parental care theory 154

8.2.1 A conventional view of parental care theory 154

8.2.2 More recent developments in parental care theory 156

8.3 Testing parental care theory using onthophagine dung beetles 157

8.3.1 Parental care in onthophagine dung beetles 158

8.3.2 The costs and benefits of parental care in onthophagine dung beetles 160

8.3.3 Behavioural dynamics of the sexes during biparental care 163

8.3.4 Confidence of paternity and paternal care 166

8.3.5 Do parents optimize the care they provide? 169

8.3.6 Evolutionary quantitative genetics of parental care 173

8.4 Conclusions and future directions 174

9 The visual ecology of dung beetles 177
Marcus Byrne and Marie Dacke

9.1 Introduction 177

9.2 Insect eye structure 179

9.2.1 The apposition eye 179

9.2.2 The superposition eye 179

9.3 Eye limitations 181

9.4 Dung beetle vision 182

9.4.1 Dim light vision 182

9.4.2 The tapetum and enlarged rhabdoms 185

9.4.3 The canthus 186

9.5 Visual ecology of flight activity 187

9.5.1 Diel flight activity 187

9.5.2 Crepuscular flight activity 188

9.5.3 Endothermy and vision 188

9.5.4 Body size and flight activity 189

9.6 Sexual selection and eyes 190

9.7 Ball-rolling 192

9.7.1 Orientation by ball-rolling beetles 192

9.7.2 The polarization compass 194

9.7.3 Polarization vision 194

9.7.4 Polarization vision in dim light 196

9.8 Conclusions 198

10 The ecological implications of physiological diversity in dung beetles 200
Steven L. Chown and C. Jaco Klok

10.1 Introduction 200

10.2 Thermoregulation 201

10.3 Thermal tolerance 207

10.4 Water balance 208

10.5 Gas exchange and metabolic rate 215

10.6 Conclusion and prospectus 218

11 Dung beetle populations: structure and consequences 220
Tomas Roslin and Heidi Viljanen

11.1 Introduction 220

11.2 Study systems 221

11.2.1 The Finnish cow pat 222

11.2.2 The Malagasy lemur pellet 223

11.3 Range size 224

11.4 Habitat and resource selection 227

11.5 Dung beetle movement 230

11.6 The genetic structure of dung beetle populations 235

11.7 Consequences: spatial population structures and responses to habitat loss 238

11.8 Perspectives 243

12 Biological control: ecosystem functions provided by dung beetles 245
T. James Ridsdill-Smith and Penny B. Edwards

12.1 Introduction 245

12.2 Functions of dung beetles in ecosystems 246

12.2.1 Dung burial and nutrient cycling 246

12.2.2 Control of dung-breeding flies 247

12.2.3 Control of parasites 250

12.3 Dung beetles in pasture habitats 250

12.4 Seasonal occurrence and abundance of native dung beetles in Australia 251

12.5 Distribution and seasonal occurrence of introduced dung beetles in Australia 254

12.6 Long-term studies of establishment and abundance 257

12.6.1 Summer rainfall climate area of Queensland 258

12.6.2 Mediterranean climate area of south Western Australia 260

12.6.3 Long-term population trends 261

12.7 Competitive exclusion 262

12.8 Optimizing the benefits of biological control 264

13 Dung beetles as a candidate study taxon in applied biodiversity conservation research 267
Elizabeth S. Nichols and Toby A. Gardner

13.1 Introduction 267

13.2 Satisfying data needs to inform conservation practice 268

13.3 The role of dung beetles in applied biodiversity research in human-modified landscapes 270

13.3.1 Dung beetles as a viable candidate for biodiversity research 271

13.3.2 Dung beetles as reliable indicators of environmental change 272

13.3.3 Interpreting disturbance response patterns: application of a trait-based framework for ecological research 276

13.3.4 Dung beetles as ecological disturbance indicator taxa: applied examples 286

13.4 Dung beetle conservation 286

13.5 Some ways forward 290

References 293

Subject index 340

Taxonomic index 343