Causes and consequences of body armour in the group-living lizard, Ouroborus cataphractus

167 Pages·2015·7.51 MB·English

Causes and consequences of body armour in the
group-living lizard, Ouroborus cataphractus
(Cordylidae)

by

Chris Broeckhoven

Dissertation presented for the degree of

Doctor of Philosophy in the

Faculty of Science at

Stellenbosch University

Supervisor: Prof. P. le Fras N. Mouton

March 2015
Stellenbosch University https://scholar.sun.ac.za
DECLARATION

By submitting this thesis electronically, I declare that the entirety of the work contained therein is
my own, original work, that I am the sole author thereof (save to the extent explicitly otherwise
stated), that reproduction and publication thereof by Stellenbosch University will not infringe any
third party rights and that I have not previously in its entirety or in part submitted it for obtaining
any qualification.

March 2015

Copyright © 2015 Stellenbosch University

All rights reserved
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ABSTRACT

Cordylidae is a family of predominantly rock-dwelling sit-and-wait foraging lizards endemic to
southern Africa. The significant variation in spine length and extent of osteoderms among taxa
makes the family an excellent model system for studying the evolution of body armour.
Specifically, the Armadillo lizard (Ouroborus cataphractus) offers an ideal opportunity to
investigate the causes and consequences of body armour. Previous studies have hypothesised that
high terrestrial predation pressure, resulting from excursions to termite foraging ports away from
the safety of the shelter, has led to the elaboration of body armour and a unique tail-biting
behaviour. The reduction in running speed associated with heavy body armour, in turn, appears to
have led to the evolution of group-living behaviour to lower the increased aerial predation risk.
In this thesis, a comparative and integrative approach is used to provide more insight into
the conditions under which body armour could have evolved in O. cataphractus and the
consequences of body armour for life-history traits. Chapter 2 attempts to investigate how
competitive and predatory pressures affect the activity patterns of O. cataphractus. Analysis of
activity patterns, obtained via remote camera trapping techniques, show low levels of activity
during summer in O. cataphractus, resulting from increased competition for food and high
predation pressure. In contrast, a shift in activity to spring, when food availability is relatively
high, appears to override the negative effects of body armour and group-living behaviour in O.
cataphractus. Chapter 3 tests the hypothesis that body armour serves as protection against attacks
from predators during foraging excursions away from the safety of the shelter. The relatively high
skin toughness, due to the presence of thick osteoderms in the dermis, protects O. cataphractus
against most terrestrial predators, while the skin toughness values for other cordylid lizards are
well-below the bite forces of potential mammalian predators.
The remaining chapters focus strongly on the feeding behaviour of O. cataphractus and
how it is linked to body armour. Chapter 4 investigates the consequences of a reduction in running
speed for the diet and tests for the presence of compensatory alternative performance capacities
(i.e. increased bite force or jaw closing velocity). A comparative phylogenetic analysis shows that
the possession of body armour affects the proportion of evasive prey items that can be included
into the diet, thereby restricting the prey spectrum of heavily armoured taxa, such as O.
cataphractus, to slow-moving prey (e.g. Coleoptera). Although the results indicate a relatively
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high bite force in O. cataphractus, the primary selection pressure seems to be tail-biting behaviour,
rather than the consumption of hard-bodied Coleoptera (Chapter 5). Bite force, however, trades-
off with jaw closing velocity in lizards. A novel lingual prehension mode, exclusive to O.
cataphractus (Chapter 6) appears to have evolved in response to the force-velocity trade-off. Given
the slow nature of lingual prehension, increased prey capture efficiency appears to be the main
selection pressure (Chapter 7), rather than miminsing exposure to predators by reducing the time
spent in the open.

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ACKNOWLEDGEMENTS

Firstly, I would like to thank my supervisor le Fras Mouton for introducing me to the remarkable
Armadillo lizard and guiding me throughout my thesis. Our numerous philosophical conversations
helped me to come up with interesting questions, which contributed immensely to the overall topic
of this thesis. I hope we can continue doing research together in the future, as many aspects of
cordylid lizard biology still remain a mystery.

Special thanks to my girlfriend Genevieve Diedericks for her love, support and encouragement
throughout my entire thesis and our many insightful conversations. Although the frustration of
catching cordylid lizards often turned into a personal fight, this thesis would not have been possible
without you as the best field assistant one can imagine! Genevieve also helped me with the
construction of the phylogenetic trees used in Chapter 3 and 4.

I am grateful to my own and surrogate family for their support at various levels. I am especially
grateful to my sister and mother, for being there when I needed them even though they were on
the other side of the world.

Thanks to the following people whose contributions made this study possible: Alex Flemming for
helping me with the histology techniques and introducing me to the previously not-so-interesting
field of histology. The various land-owners that allowed me to conduct research and collect lizards
on their property: the Engelbrecht family (Fonteintjie farm, Lambert’s Bay), Johan van der
Westhuizen (Keurbosfontein, Cederberg), Elzette & Llewellyn Angus (Wisp-Will Game Farm,
Arlington), Victor Burke (Agama Tented Camp, Garies), Rika du Plessis (Matjiesrivier,
Cederberg) and Hein de Waal (Kagga Kamma Nature Reserve, Cederberg). The Functional
Morphology lab at the University of Antwerp (Belgium), especially Raoul van Damme and Jan
Scholliers for helping me with the analysis of skin toughness. Jan Scholliers also constructed the
bite plates used to measure bite force in several chapters of this thesis. Bart Spotbeen from Squama
Reptiles (Herent, Belgium) for allowing me to film the cordylid lizards in his care. Philipp Shultz
(blueduiker.com) for supplying the mongoose skulls used for the skin toughness experiments. The
support staff of the Department of Botany & Zoology (Stellenbosch University), especially Mari
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Sauerman and Janine Basson for helping me with various problems and requests. The various
provincial conservation authorities for issuing the permits to collect specimens and the Research
Ethics Committee of the Faculty of Science (Stellenbosch University) for approving the
experimental procedures.

In addition, I am grateful to John Measey and several anonymous reviewers for their helpful
comments on the submitted manuscripts.

Finally, I would like to thank the Department of Botany & Zoology (Stellenbosch University) and
the National Research Foundation (NRF) for provided financial support during my study, as well
as the National Geographic Society for awarding me the Young Explorers Grant.

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TABLE OF CONTENTS

DECLARATION.......................................................................................................................................... I
ABSTRACT ................................................................................................................................................ II
ACKNOWLEDGMENTS ........................................................................................................................ IV
LIST OF FIGURES ................................................................................................................................... X
LIST OF TABLES .................................................................................................................................. XII

CHAPTER 1 ............................................................................................................................................ 1-4
GENERAL INTRODUCTION

CHAPTER 2 ........................................................................................................................................... 5-34
EFFECTS OF PREDATION RISK, COMPETITION AND WEATHER CONDITIONS ON THE
ACTIVITY PATTERNS OF OUROBORUS CATAPHRACTUS AND KARUSASAURUS
POLYZONUS

ABSTRACT ................................................................................................................................................. 5
INTRODUCTION ....................................................................................................................................... 6
MATERIALS AND METHODS ............................................................................................................... 8
STUDY SITE ........................................................................................................................................ 8
ACTIVITY DATA ............................................................................................................................... 8
METEOROLOGICAL DATA.............................................................................................................. 9
PREDATION PRESSURE ESTIMATE .............................................................................................. 9
STATISTICAL ANALYSES ............................................................................................................. 10
RESULTS .................................................................................................................................................. 11
ACTIVITY PATTERNS .................................................................................................................... 11
EFFECT OF WEATHER CONDITIONS ON ACTIVITY PATTERNS .......................................... 12
PREDATION PRESSURE ................................................................................................................. 12
DISCUSSION ............................................................................................................................................ 13
TABLES ..................................................................................................................................................... 17
FIGURES ................................................................................................................................................... 22

CHAPTER 3 ......................................................................................................................................... 35-56
FUNCTIONAL BASIS FOR VARIATION IN BODY ARMOUR IN CORDYLID LIZARDS

ABSTRACT ............................................................................................................................................... 35
INTRODUCTION ..................................................................................................................................... 36
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MATERIALS AND METHODS ............................................................................................................. 38
SKIN TOUGNESS ............................................................................................................................. 38
SKIN MORPHOLOGY ...................................................................................................................... 39
PHYLOGENETIC TREE ................................................................................................................... 40
RESULTS .................................................................................................................................................. 41
SKIN TOUGNESS ............................................................................................................................. 41
SKIN MORPHOLOGY ...................................................................................................................... 41
PHYLOGENETIC TREE ................................................................................................................... 42
DISCUSSION ............................................................................................................................................ 42
FUNCTIONAL SIGNIFICANCE OF BODY ARMOUR IN O. CATAPHRACTUS ......................... 42
ALTERNATIVE CAUSES OF BODY ARMOUR IN CORDYLID LIZARDS ............................... 44
TABLES ..................................................................................................................................................... 46
FIGURES ................................................................................................................................................... 48

CHAPTER 4 ......................................................................................................................................... 57-71
CONSEQUENCES OF BODY ARMOUR FOR FEEDING BEHAVIOUR IN CORDYLID
LIZARDS

ABSTRACT ............................................................................................................................................... 57
INTRODUCTION ..................................................................................................................................... 58
MATERIALS AND METHODS ............................................................................................................. 59
MORPHOLOGY ................................................................................................................................ 59
PERFORMANCE MEASURES ......................................................................................................... 60
DIET ................................................................................................................................................... 61
PHYLOGENETIC TREE ................................................................................................................... 62
PHYLOGENETIC ANALYSES ........................................................................................................ 62
RESULTS .................................................................................................................................................. 63
DISCUSSION ............................................................................................................................................ 64
ARMOUR AND PREY CAPTURE IN CORDYLID LIZARDS ...................................................... 64
PERFORMANCE CAPACITIES AND DIETARY NICHE .............................................................. 65
TABLES ..................................................................................................................................................... 67
FIGURES ................................................................................................................................................... 70

CHAPTER 5 ......................................................................................................................................... 73-93
MORPHOLOGICAL AND ECOLOGICAL CORRELATES OF BITE FORCE IN THE ROCK-
DWELLING LIZARD OUROBORUS CATAPHRACTUS AND KARUSASAURUS POLYZONUS

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ABSTRACT ............................................................................................................................................... 73
INTRODUCTION ..................................................................................................................................... 74
MATERIALS AND METHODS ............................................................................................................. 76
MORPHOLOGY AND BITE FORCE ............................................................................................... 76
DIET AND PREY HARDNESS ........................................................................................................ 77
FEEDING EXPERIMENTS ............................................................................................................... 78
DATA ANALYSIS ............................................................................................................................. 78
RESULTS .................................................................................................................................................. 80
MORPHOLOGY AND BITE FORCE ............................................................................................... 80
DIET ................................................................................................................................................... 81
FEEDING EXPERIMENTS ............................................................................................................... 81
DISCUSSION ............................................................................................................................................ 82
MORPHOLOGICAL CORRELATES OF BITE FORCE ................................................................. 82
INFLUENCE OF BITE FORCE ON DIETARY NICHE PARTITIONING ..................................... 83
TABLES ..................................................................................................................................................... 85
FIGURES ................................................................................................................................................... 90

CHAPTER 6 ....................................................................................................................................... 94-115
INFLUENCE OF DIET ON PREHENSION MODE IN CORDYLID LIZARDS

ABSTRACT ............................................................................................................................................... 94
INTRODUCTION ..................................................................................................................................... 95
MATERIALS AND METHODS ............................................................................................................. 96
STUDY ORGANISMS AND EXPERIMENTAL PROTOCOL ....................................................... 96
STATISTICAL ANALYSIS .............................................................................................................. 97
MORPHOLOGY OF THE TONGUE ................................................................................................ 99
RESULTS .................................................................................................................................................. 99
PREY PREHENSION EXPERIMENTS ............................................................................................ 99
QUANTITATIVE ANALYSIS OF KINEMATICS ........................................................................ 100
MORPHOLOGY OF THE TONGUE .............................................................................................. 101
DISCUSSION .......................................................................................................................................... 102
DIETARY SPECIALISATION AND PREHENSION MODE IN O. CATAPHRACTUS ............... 102
PREHENSION MODE AND FORAGING STRATEGY IN CORDYLIDAE ................................ 103
TABLES ................................................................................................................................................... 105
FIGURES ................................................................................................................................................. 111

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CHAPTER 7 ..................................................................................................................................... 116-122
FUNCTIONAL MECHANISMS UNDERLYING PREY CAPTURE EFFICIENCY IN
CORDYLID LIZARDS

ABSTRACT ............................................................................................................................................. 116
INTRODUCTION ................................................................................................................................... 117
MATERIALS AND METHODS ........................................................................................................... 118
HUSBANDRY .................................................................................................................................. 118
EXPERIMENTAL PROCEDURES ................................................................................................. 118
STATYSTICAL ANALYSES .......................................................................................................... 119
RESULTS ................................................................................................................................................ 119
DISCUSSION .......................................................................................................................................... 120
FIGURES ................................................................................................................................................. 122

CHAPTER 8 ..................................................................................................................................... 123-127
CONCLUSIONS

REFERENCES ................................................................................................................................. 128-150

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