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Terri Jade Cleary ECTOTHERM DIVERSITY THROUGH TIME: THE INTERPLAY OF SAMPLING BIASES, ENVIRONMENTAL DRIVERS AND MACROEVOLUTION by Terri Jade Cleary A thesis submitted for the degree of Doctor of Philosophy University College London September 2018 1 [This page intentionally left blank] 2 I, Terri J. Cleary, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. ____________________________ 3 [This page intentionally left blank] 4 Abstract The fossil record is inherently biased, but few studies have examined the effects of these biases on our understanding of non-marine vertebrate ectotherms through time. Here, I investigate the taxon richness of non-marine lepidosaurs and turtles from the Triassic–Paleogene (252–23 Ma) using subsampling methods and completeness metrics to correct for/highlight sampling and preservation biases. Additionally, I used generalized least-squares regressions to study the relationships between taxon richness and other potential explanatory variables (e.g. temperature, sampling proxies). The lepidosaur record is more poorly sampled than the turtle record, but for both clades the Southern Hemisphere is clearly undersampled compared to the Northern Hemisphere. Consequently, the majority of sequential richness signal is observable in Northern Hemisphere continents only. Lepidosaur and turtle richness patterns differed prior to the Eocene, but were very similar afterwards. Across the K-Pg boundary, North American lepidosaurs decreased in richness while turtles increased. Both clades exhibited high richness in the Late Cretaceous and in the early and late Eocene, often corresponding to times of very warm global climates. During these times richness was greater at higher latitudes than at lower latitudes, which is the opposite of the modern latitudinal biodiversity gradient. Richness decreased at the Eocene–Oligocene boundary in the Northern Hemisphere, coincident with a steep drop in global temperatures, but remained relatively high compared to the Mesozoic. It is unclear whether taxa with lower cold tolerance migrated south at these times or went extinct, due to poor sampling in the tropics. 5 Ectotherm taxon richness through time is strongly influenced by sampling biases, including the number of collections available and the prevalence of Lagerstätten (localities of exceptional preservation). Temperature might have influenced lepidosaur richness, but other factors not tested for might have also been important for ectotherm richness, such as precipitation (particularly for freshwater turtles). 6 Impact Statement The work done in this thesis adds to the wealth of literature on the effects of biases on the fossil record, and how we can account for and ameliorate these biases. Prior to this thesis there had been few studies on the fossil records of turtles, and almost none on lepidosaurs, that accounted for these biases when discussing richness through time. My results provide a useful comparison to uncorrected face-value observations of richness in the literature, and a cautionary tale against interpreting richness changes based on poorly sampled areas or time periods. I have also added non- marine lepidosaur and turtle richness studies to the pool of comparative results for future researchers who wish to try the same methods on other clades; I edited R code included in the appendices that could be very useful to others who want to do this. One chapter of this thesis is already published (Chapter 2), and I aim to publish the rest in the future to disseminate my results more widely. I will also speak (and have spoken previously) at conferences about this work, creating opportunities for future collaborations based on the work I have done here. Outside of my field, my results may provide a useful deep-time comparison for those examining the predicted responses of ectotherms to present anthropogenic climate change. Ectotherms are expected to respond strongly to changes in temperature, and researchers often examine past occurrences of rapid climate change in order to learn about potential future responses of organisms. Having a record of long-term richness that has been corrected for the majority of sampling biases may provide a very useful resource for these researchers. Alongside journal articles and conference talks, I have participated in public engagement and outreach activities where I have discussed my work in this light, so this aspect of my research is very easy to disseminate outside of academia. In addition, the knowledge gained with regards to how past ectotherms 7 responded to climatic changes, and how this relates to the current situation, could be applied to reports which are used to influence government policy. 8 Acknowledgements There are many people, both inside academia and outside without whom I would have been unable to reach the end of this journey. First and foremost, I have been fortunate to have three incredible supervisors: Paul Barrett, Susan Evans and Roger Benson, who supported me both in my research and in my development as an independent researcher. You three are the kind of people I aspire to be in science, and I hope I can support students of my own even half as well someday. Elsewhere in academia, I would like to thank Phil Mannion and Pat Holroyd for their very helpful discussions of aspects of this thesis. David Nicholson’s work on turtles prior to mine inspired some of this thesis, and he was happy to help me understand how all the methods worked when I was first starting out. Paul Valdes provided Cenozoic land area data that was invaluable to one chapter of this thesis. Richard Butler was always on hand in the early days of my entering data into the Paleobiology Database, and I am very thankful for every answer he readily gave to my (many) questions. Everyone I interacted with while editing the PBDB was incredibly gracious, and I am thankful to all of them. Outside of academia, there are too many people to name. Most of them know how much I appreciate them, so I will keep this short. Special thanks go to my ever- supportive family, my flatmate (who put up with my nerdy pursuits and took pity on my lowly student status by treating me to dinner more than a few times), and my office-mates who shared in my frustrations and my triumphs. I made it. 9 [This page intentionally left blank] 10 Table of Contents Title Page ............................................................................................................................. 1 Declaration ........................................................................................................................ 3 Abstract .............................................................................................................................. 5 Impact Statement .............................................................................................................. 7 Acknowledgements ........................................................................................................... 9 Table of Contents .............................................................................................................. 11 List of Tables .......................................................................................................... 17 List of Figures ........................................................................................................ 19 Table of Contents for Electronic Appendices ..................................................... 23 Chapter 1: Introduction ................................................................................................... 27 1.1 Accounting for geological and anthropogenic biases in the fossil record ...................................................................................................... 27 1.1.1 Background ................................................................................... 27 1.1.2 Measuring preservation biases ..................................................... 30 1.1.3 Modelling approaches to biases .................................................... 31 1.1.4 Subsampling approaches to biases .............................................. 34 1.2 Fossil record biases and ectotherms ............................................................ 39 Chapter 2: Non-marine Lepidosaur Richness from the Triassic–Paleogene ................ 43 2.1 Introduction .................................................................................................. 43 11 2.2 Methods .......................................................................................................... 47 2.2.1 Data ................................................................................................ 47 2.2.2 Subsampling .................................................................................. 48 2.2.3 Comparing richness to proxies for sampling and environmental factors .................................................................... 51 2.3 Results ............................................................................................................ 53 2.3.1 Global face-value and subsampled curves ................................... 53 2.3.2 Continental-level subsampling .................................................... 56 2.3.3 Generalized least-squares analyses .............................................. 64 2.4 Discussion .....................................................................................................
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