'Costs' of Caudal Autotomy in the Metallic Skink, Niveoscincus metallicus David Chapple B.Sc. (Qld) Submitted in fulfilment of the requirements for the degree ofBachelor of Science with Honours School of Zoology University of Tasmania 1999-2000 Acknowledgments ACKNOWLEDGMENTS I would like to thank a number of people in the School of Zoology who helped make this Honours Project possible, in particular: Roy Swain, my supervisor, for his continual encouragement and support throughout the project, and for always finding time to listen to my latest thoughts and ideas. Sue Jones, for allowing me to use her laboratory and equipment, and for advice and ideas concerning various aspects of my project. Colin McCoull for his invaluable assistance in the field, advice and information of all things herpetological (especially about N. meta/lints), and assistance in allowing certain sections of the project to become a reality. Leon Barmuta for his invaluable statistical advice. Thanks also to Steve Candy (Forestry Tasmania) for assistance with the Repeated Measures ANCOVA. Randy Rose for the use of his home, garden and surrounds as one of my urban field sites. Brett Gartrell, the lizard vet, for his lizard autopsies and treatment of sick lizards, but most of all for his assistance in removing lizard tails under anaesthesia. The technical staff of the School of Zoology: Kit Williams for his assistance with the digital camera and maintenance of my temperature probes; Wayne Kelly for his help with the use of ether and other technical matters; and Barry Rumbold for the supply of equipment used in certain parts of the project. A huge thanks goes to my fellow honours students past and present, for their assistance and comic relief during the honours year: Tammy Lockhart, Kirsty Dixon, Angela Maher, Victoria Cartledge, Sue Baker, Browyn Stott and Katie Flowers. Thanks also to Jane Girling for her help in various aspects of the project. And finally, thank-you to my family for their support from afar: Ken, Judy, Julie, Carolyn and Clydie. This work was carried out under the University of Tasmania, Animal Ethics Permit No. A0005657. Abstract ABSTRACT Caudal autotomy is a defensive mechanism utilised by squamate reptiles to survive predatory attacks. Although tail loss is an effective escape mechanism in lizards, autotomy may result in severe 'costs' being inflicted upon the animal. However, since the tail is capable of regeneration, these 'costs' may only be transient. An animal's ability to balance the costs and benefits of autotomy determines the adaptive advantage of tail loss. The locomotory, thermoregulatory, energetic, reproductive and behavioural 'costs' of caudal autotomy were investigated in the metallic skink, Niveoscincus metallicus. Niveoscincus metallicus is a small ground-dwelling skink that inhabits a wide range of microhabitats. It is a viviparous species that possesses a sinusoidal locomotory mode, and both caudal and abdominal fat reserves. High levels of tail loss are evident in most populations. Caudal autotomy was found to have two main impacts on N. metallicus: 1) restriction of mobility; and 2) depletion of energetic reserves. However, the species was found to possess several behavioural and anatomical modifications to limit the 'costs' incurred. Tail autotomy was found to severely restrict locomotory performance m N. metallicus. Terrestrial locomotion, sprinting and stamina, was found to be preferentially inhibited by caudal autotomy. Climbing ability was not affected by tail loss. In females, locomotory inhibition caused by caudal autotomy was relatively short-lived. However, in males there was no evidence of restoration of locomotory performance during this study. This was the first investigation of the temporal impact of caudal autotomy on performance in lizards. Behavioural modification was evident following caudal autotomy. Tailless N. metallicus were found to compensate for diminished locomotory abilities by selecting more cryptically located basking sites and remaining closer to refuge. This modification of basking preference was assumed to be the result of the animal adopting an alternative defensive strategy. ii Abstract Thermoregulatory behaviour was not modified following tail loss. However, females were found to lower their thermal preferences during gestation, presumably to enhance embryonic development. It was concluded that reproductive success represented higher priority than tail regeneration. Niveoscincus metallicus was demonstrated to store the majority ( -50-75%) of its energetic reserves in its tail. Most ( -90%) of these reserves were located within the proximal third of the tail. Depletion of abdominal fat stores was found to be related to periods of reproductive investment. There was some evidence that abdominal fat reserves were preferentially allocated to reproductive effort. Caudal autotomy during vitellogenesis was associated with a reduction in the clutch size of tailless females. This reduced reproductive investment was related to the diversion of energy towards tail regeneration rather than the direct depletion of caudal fat stores. These tailless females were found to modify their reproductive strategy by producing a smaller number of larger and 'better' quality offspring. However, tail autotomy during gestation did not influence the weight or size of offspring. Maternal tail size and the presumed environment during gestation was not related to the phenotype of a female's offspring. The frequency and position of tail loss were found to vary between altitudes and populations. Predation pressure or basking behaviour failed to explain these differences. Predation efficiency, frequency of repeated tail breaks and the age structure of the population all appeared to be related to the frequency and position of tail loss. Niveoscincus metallicus was found to be capable of 'economy of autotomy', preferentially losing the more distal portions of its tail that do not contain significant fat stores. It is concluded that caudal autotomy inflicts several costs on N. metallicus. However, the existence of behavioural and anatomical modifications limits the impacts of these 'costs'. This study suggests that the costs and benefits of caudal autotomy have co­ evolved in N. metallicus, allowing it retain a successful defensive mechanism while limiting the associated 'costs'. iii Contents CONTENTS Acknowledgements 1 Abstract 11 Chapter 1: General Introduction 1.1 Introduction 1 1.2 Niveoscincus metallicus as a model species 4 1.3 The genus Niveoscincus 5 1.4 Niveoscincus metallicus 6 1.5 Research objectives 9 Chapter 2: General Materials and Methods 2.1 Description of study site 10 2.2 Lizard collecting techniques 13 2.3 General laboratory housing 13 2.4 Juvenile housing conditions 14 Chapter 3: Locomotory Performance 3.1 Introduction 16 3.2 Materials and Methods 18 3.2.1 Collection and preparation of animals 18 3.2.2 Test temperatures 19 3.2.3 Sprint performance 20 3.2.4 Climbing ability 20 3.2.5 Locomotory endurance 21 3.2.6 Neonatal tail loss and sprint speed 21 3.2.7 Data analysis 22 3.3 Results 24 3.3.1 Adult performance capabilities 24 3.3.2 Juvenile sprint speed 30 3.4 Discussion 31 iv Contents Chapter 4: Thermoregulatory Behaviour 4.1 Introduction 37 4.2 Materials and methods 40 4.2.1 Thermoregulatory characteristics 40 4.2.1.1 Collection and preparation of animals 40 4.2.1.2 Eccritic temperatures and basking setpoints 40 4.2.2 Basking behaviour 42 4.2.2.1 Collection and preparation of animals 42 4.2.2.2 Laboratory housing conditions 42 4.2.2.3 Observations 43 4.2.3 Data analysis 44 4.3 Results 44 4.4 Discussion 50 Chapter 5: Energetics of Tail Autotomy 5.1 Introduction 55 5.2 Materials and Methods 58 5.2.1 Energetic value and fat distribution within the tail 58 5.2.2 Tail regeneration rates of adults 59 5.2.3 Growth and tail regeneration rates of juveniles 60 5.2.4 Data analysis 60 5.3 Results 62 5.3.1 Energetic value and fat distribution within the tail 62 5.3.2 Tail regeneration rates of adults 66 5.3.3 Growth and tail regeneration rates of juveniles 67 5.4 Discussion 68 5.4.1 Energetic value and fat distribution within the tail 68 5.4.2 Costs and energetics of tail regeneration 72 5.4.3 The impact of tail loss on neonates 73 v Contents Chapter 6: Reproduction 6.1 Introduction 75 6.2 Materials and methods 77 6.2.1 Future reproductive costs 77 6.2.2 The effect of tail loss on facultative placentotrophy 78 6.2.3 Data analysis 79 6.3 Results 82 6.3.1 Future reproductive costs 82 6.3.2 Tail length and offspring phenotype 85 6.3.3 The effect of tail loss on facultative placentotrophy 86 6.4 Discussion 88 Chapter 7: Tail Loss Frequency and Basking Site Selection 7.1 Introduction 95 7 .1.1 Tail loss and survival 95 7 .1.2 Frequency of tail loss 96 7.2 Materials and methods 98 7 .2.1 Field site descriptions 98 7.2.1.1 Urban sites 98 7 .2.1.2 Central Plateau sites 98 7 .2.2 Collection and measurement of animals 101 7.2.3 Data analysis 102 7.3 Results 104 7.3.1 Sexual and morphological variation 104 7.3.2 The frequency and position of tail autotomy 105 7.3.3 Habitat structure and basking behaviour 107 7.4 Discussion 111 7 .4.1 Frequency and position of tail autotomy 111 7.4.2 The effect of tail loss on basking site selection 115 Chapter 8: General Discussion 119 References 125 vi Chapter 1: General Introduction CHAPTER 1 GENERAL INTRODUCTION 1.1 INTRODUCTION An animal's ability to evade and subsequently survive predatory attacks is central to its survival. Behaviours that enhance the likelihood of successful escape will be adaptively advantageous and may therefore be expected to be the result of strong selection pressures.