ABSTRACT Title of Dissertation: PLANT?ARTHROPOD ASSOCIATIONS FROM THE WESTERN INTERIOR OF NORTH AMERICA DURING THE LATE CRETACEOUS S. Augusta Maccracken Doctor of Philosophy, 2020 Dissertation co-directed by: Professor Jeffrey W. Shultz, PhD Department of Entomology University of Maryland, College Park Curator Conrad C. Labandeira, PhD Department of Paleobiology Smithsonian Institution, National Museum of Natural History Insects are unparalleled in species diversity and breadth of ecological associations. The most prominent of these ecological associations is insect herbivory on vascular plants, which has shaped terrestrial ecosystems for hundreds of millions of years. Only recently have scientists begun to understand the diversity and intensity of plant?insect associations in the fossil record. The majority of these studies have documented episodes of rapid change in Earth?s history, such as intervals of global warming. However, there are few studies documenting plant?insect associations around longer time intervals, including the radiation of flowering plants (angiosperms) during the Cretaceous Period from 145 to 66 Ma (Mega-annum), which set the stage for many modern plant?insect associations. Herein, I present the results of specimen-based surveys of Campanian Age (83.6?72.1 Ma) macrofossil floras and their associated insect damage from the Kaiparowits Formation of Utah, USA, a fossiliferous deposit within the Western Interior. First, I describe a new genus of fossil laurel (Lauraceae), and analyze the plant?insect associations found on this taxon. After, I describe the diversity and intensity of plant?insect associations from the a single, well-sampled locality. I then describe a new fossil lyonetiid moth leaf mine, which represents the oldest fossil evidence of a cemiostomine leaf-mining moth, as well as the second oldest record of the Yponomeutoidea?Gracillarioidea clade. Then, I describe acarodomatia (mite houses) on fossil leaves, which constitute the oldest evidence for plant?mite mutualisms in the fossil record. Finally, to understand broad-scale and long-term patterns of insect damage in the fossil record, I analyze all available fossil plant?insect associational datasets spanning the Age of Angiosperms (ca. 76?2 Ma). These results indicate that insect preference for plant hosts may have changed through time as local plant diversity increased, but this may stem from differences in sampling regimes and difficulties in identification of fossil angiosperms. My findings collectively indicate that Late Cretaceous plant?insect associations are often novel, diverse, and may be evolutionarily tied to modern plant? insect associations, as well as the acquired insight into the limitations and future directions for this field of research. PLANT?ARTHROPOD ASSOCIATIONS FROM THE WESTERN INTERIOR OF NORTH AMERICA DURING THE LATE CRETACEOUS by S. Augusta Maccracken Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2020 Advisory Committee: Professor Jeffrey Shultz, Co-chair Curator Conrad C. Labandeira, Co-chair Professor Daniel S. Gruner Professor Charles F. Delwiche Curator Ian M. Miller ? Copyright by S. Augusta Maccracken 2020 Dedication For my mother, Karen. Thank you for thirty-one years of unwavering love, support, and for fostering my connection with nature. You are unrivaled in all the 3.48 billion years of life on Earth. ii Foreword With the approval of the dissertation co-directors, Dr. Jeffrey Shultz and Dr. Conrad Labandeira, the dissertation committee members, and the Department of Entomology Graduate Director, Chapter 2 of this dissertation is included as previously published research. The citation for the publication is as follows: Maccracken, S. A., I. M. Miller, and C. C. Labandeira. 2019. Late Cretaceous domatia reveal the antiquity of plant?mite mutualisms in flowering plants. Biology Letters 15(11):20190657. Under the guidelines of the graduate catalogue for the inclusion of one?s own previously published materials in a dissertation, I affirm that I was responsible for the inception of this manuscript and the majority of the manuscript preparations. This manuscript was reformatted to meet all dissertation requirements set forth by the Graduate School. All other aspects of the previously published manuscript were preserved in the dissertation. A letter from the dissertation co-directors, committee members, and the Department Chair was sent to the Dean of the Graduate School certifying that the examining committee has approved the inclusion of the manuscript. A copy of this letter can be found in Appendix A. iii Acknowledgements First, I thank my co-advisers, Conrad Labandeira and Jeffrey Shultz. Conrad, you have changed the way I see the world. I am forever indebted to you for the many years of kindness, patience, and tutelage. I will always treasure our months of fieldwork in Saltillo, Mexico. Jeff, your guidance and advice gave me the confidence to navigate life as a professional scientist. I took your critiques to heart and was fortified by your hard-won complements and dark sense of humor. My co-advisors are very different people and very different scientists. I am beyond lucky have benefited from both pools of knowledge. Thank you to the rest of my dissertation committee, Dan Gruner, Chuck Delwiche, and Ian Miller. The completion of this dissertation would not have been possible without their thoughtful guidance and encouragement. Not all graduate students are as fortunate as I am to have a committee that is as dedicated to their success as are Dan, Chuck, and Ian. Above all, I thank Ian Miller for his decade-long mentorship and friendship. As a na?ve college student asking for an internship, I couldn?t have imagined the expeditions and research projects we would undertake over the next decade. I look forward to a lifetime of scientific collaboration. Also, thanks to Robyn Rissman and Wilson Rissman-Miller for their hospitality during my many and often lengthy visits to Denver. I also thank Charles Mitter, who served as my first advisor and who helped me grow as a scientist and writer. I tremendously enjoyed our bi-weekly meetings, which could range from the newest scientific discoveries, to the latest departmental news, and back again. Your edits of my early writings were panic inducing?as if iv someone haphazardly splashed red paint on the paper. Thank you. You pushed me to find my voice. I would also like to thank my collaborators, who are also lifetime friends: Sandra Schachat, Claudia Serrano-Bra?as, Belinda Espinosa-Ch?vez, Joe Sertich, Kirk Johnson, Jay Cheon-Sohn, Vincent ?Skip? Lyles, Anshuman Swain, Lisa Boucher, and Tyler Lyson. A huge thanks goes out to the faculty and staff of the Entomology Department, especially Leslie Pick, Josh Kiner, Amy Yaich, Pam Biery, Jamie Carrigan, Eileen Jewison, Greg Hess, Bill Katsereles, and Kelly Hamby. I also owe a great deal of gratitude to my undergraduate volunteers, Reuven Bank, Gabrielle Bates, Elijah Boswell, James Kavanaugh, Garrett Kelly, and Tarlan Vatan. I thank the DMNS Leaf Whackers as well as the DMNS and NMNH collections staff members over the years. Thank you to my family members for a lifetime of encouragement, as well as my colleagues, peers, and friends for their ceaseless support. In alphabetical order, I thank Alex, Heidi, & Andrew Adatto, Rich Barclay, Kay Behrensmeyer, Peter Coffey, Caitlin Colleary, Crystal Cooke, Mike Donovan, Boyce Drummond, Becca Eckert, Andrew Garavito, Hannah Franklin Grisham, Ryan Gott, Gene Hunt, Sarah Jacobs, Advait Jukar, Jeff Kirn?, Karen Kirn, Kathryn Kirn, Mike Kirn, Weez Kirn, Hans Lemke, Emma Locatelli, Chris Maccracken, Joan Maccracken, Winnie Maccracken-Keshawerz, Emma Parenteau, Andrew Simpson, Karla Sosa, Chris Taylor, Elske Tielens, Nichole Tiernan, Becca Wilson, and Scott Wing. Most importantly, and with all my love, I thank my fianc? Yama Keshawerz. I am most grateful to you, my best friend, my quarantine buddy. These past six and a v half years have been some of the best years of my life and I look forward to spending a lifetime with you. Funding for my graduate studies and research included: The University of Maryland Department of Entomology & Gahan Fellowship The University of Maryland Graduate School The BIG TEN Academic Alliance Smithsonian Predoctoral Fellowship The Wiley Dissertation Completion Fellowship The Smithsonian Institution Scholarly Studies Award Explorer?s Club Washington Chapter Student Awards The Paleontological Society?s Bearded Lady Student Research Grant The Society for Sedimentary Geology Student Assistance Grant Western Interior Paleontological Society John Jenkins Memorial Scholarship vi Table of Contents Dedication ..................................................................................................................... ii Foreword ...................................................................................................................... iii Acknowledgements ...................................................................................................... iv Table of Contents ........................................................................................................ vii List of Tables ................................................................................................................ x List of Figures .............................................................................................................. xi Chapter 1: Introduction and Summary of Dissertation Findings .................................. 1 Evolutionary Background ......................................................................................... 4 The Rise of Angiosperms ...................................................................................... 4 Insect Diversity and the Fossil Record ................................................................. 9 The Fossil Record of Plant?Insect Associations ................................................. 13 Geologic Background ............................................................................................. 19 Research Objectives ................................................................................................ 23 Brief Methodology .................................................................................................. 23 Summary of Dissertation Findings ......................................................................... 27 Chapter 2: Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA) .............................................. 31 Abstract ................................................................................................................... 31 Introduction ............................................................................................................. 32 Geologic and Biologic Setting ................................................................................ 35 Materials and Methods ............................................................................................ 39 Results ..................................................................................................................... 44 Leaf Morphology and Systematics ..................................................................... 44 Insect Herbivory on Catula gettyi ....................................................................... 53 Insect Herbivory on Late Cretaceous Laurels ..................................................... 70 Discussion ............................................................................................................... 74 Kaiparowits Formation Insect Richness ............................................................. 74 Antiherbivore Resistance and Herbivore Specialization .................................... 76 Late Cretaceous Insect Herbivory ....................................................................... 79 Conclusions ............................................................................................................. 83 Acknowledgments ................................................................................................... 84 Chapter 3: Plant?insect associations of a Kaiparowits Formation locality, Upper Cretaceous of Utah, USA ............................................................................................ 85 Abstract ................................................................................................................... 85 Introduction ............................................................................................................. 85 Geological Setting ................................................................................................... 89 Materials and Methods ............................................................................................ 91 Results ..................................................................................................................... 94 Plant Diversity .................................................................................................... 94 Damage Intensity ................................................................................................ 96 Diversity of Insect Damage ................................................................................ 97 vii Discussion ............................................................................................................. 117 JARS Damage-Type Richness and Comparisons to Catula gettyi ................... 117 Host Specialization and Potential Insect Culprits ............................................. 120 Biogeography of Odonate Oviposition ............................................................. 123 Conclusions ........................................................................................................... 125 Acknowledgements ............................................................................................... 126 Chapter 4: A new Late Cretaceous leaf mine Leucopteropsis spiralis gen. et sp. nov. (Lepidoptera: Lyonetiidae) and the deep time origin of a common agricultural pest ................................................................................................................................... 127 Abstract ................................................................................................................. 127 Introduction ........................................................................................................... 128 Geological Setting ................................................................................................. 130 Materials and Methods .......................................................................................... 133 Systematic Paleontology ....................................................................................... 135 Results and Discussion ......................................................................................... 141 Identity of the leaf miner ................................................................................... 142 Phylogeny of the Yponomeutoidea?Gracillarioidea Group ............................. 144 Conclusions ........................................................................................................... 150 Acknowledgments ................................................................................................. 150 Chapter 5: Late Cretaceous domatia reveal the antiquity of plant?mite mutualisms 152 Abstract ................................................................................................................. 152 Background ........................................................................................................... 152 Materials and Methods .......................................................................................... 156 Results ................................................................................................................... 156 Discussion ............................................................................................................. 158 Distribution of fossil and modern acarodomatia ............................................... 158 Antiquity of plant?arthropod associations and the evolution of acarodomatia 162 Acknowledgments ................................................................................................. 165 Chapter 6: Widespread biases in deep time plant?insect associational studies obscure potential patterns of insect preferences throughout the Age of Angiosperms .......... 166 Abstract ................................................................................................................. 166 Introduction ........................................................................................................... 167 Methods................................................................................................................. 170 Data Inclusion ................................................................................................... 170 Data Analyses ................................................................................................... 181 Results ................................................................................................................... 184 Discussion ............................................................................................................. 190 Fossil Record Quality and Sampling Biases as a Function of Age ................... 190 Plant Community Diversity and Insect Herbivory ............................................ 193 Patterns of Insect Herbivory at Finer Temporal and Spatial Scales ................. 194 Guidelines for the Study of Ancient Deep Time Plant?Insect Associations .... 196 Conclusions ........................................................................................................... 197 Acknowledgments ................................................................................................. 198 Chapter 7: Conclusions ............................................................................................. 199 Future Directions .............................................................................................. 200 Appendices ................................................................................................................ 204 viii A. Letter to the Dean of the Graduate School ....................................................... 204 B. Chapter 2 Supplementary Information ............................................................. 205 Modern Insect Herbivory on Lauraceae ........................................................... 205 Antiherbivore Resistance in Modern Lauraceae ............................................... 211 C. Chapter 3 Supplementary Information ............................................................. 216 D. Chapter 4 Supplementary Information ............................................................. 217 Locality Description of Fossil Leaf Morphotype KP90 that bears Leucopteropsis spiralis .............................................................................................................. 217 E. Chapter 5 Supplementary Information ............................................................. 220 Locality Description .......................................................................................... 220 Leaf Description ................................................................................................ 221 G. Chapter 6 Supplementary Information ............................................................. 227 The Fruitland and Kirtland Formations ............................................................ 227 Bibliography ............................................................................................................. 251 ix List of Tables Table 1.1????????????????????????????. 21 Table 2.1????????????????????????????. 53 Table 2.2????????????????????????????. 71 Table 2.3????????????????????????????. 81 Table 3.1????????????????????????????. 96 Table 3.2????????????????????????????. 98 Table 3.3????????????????????????????. 99 Table 4.1????????????????????????????.134 Table 5.1????????????????????????????.161 Table 6.1????????????????????????????.171 Table 6.2????????????????????????????.173 Supplementary Table 2.1??????????..???????????..213 Supplementary Table 6.1??????????..???????????..229 Supplementary Table 6.2??????????..???????????..232 x List of Figures Figure 1.1????????????????????????????. 3 Figure 1.2????????????????????????????. 5 Figure 1.3????????????????????????????. 6 Figure 1.4????????????????????????????. 10 Figure 1.5????????????????????????????. 14 Figure 1.6????????????????????????????. 20 Figure 1.7????????????????????????????. 25 Figure 2.1????????????????????????????. 36 Figure 2.2????????????????????????????. 37 Figure 2.3????????????????????????????. 47 Figure 2.4????????????????????????????. 49 Figure 2.5????????????????????????????. 54 Figure 2.6????????????????????????????. 55 Figure 2.7????????????????????????????. 56 Figure 2.8???????????...???..????????????? 58 Figure 2.9????????????????????????????. 60 Figure 2.10???????????...???????????????? 61 Figure 2.11???????????...???????????????? 63 Figure 2.12???????????...???????????????? 65 Figure 2.13???????????...???????????????? 66 Figure 2.14???????????...???????????????? 68 Figure 2.15???????????...???????????????? 70 Figure 2.16???????????...???????????????? 71 Figure 2.17???????????...???????????????? 72 Figure 2.18???????????...???????????????? 73 Figure 3.1????..???????...???????????????? 89 Figure 3.2???????????...???..????????????? 90 Figure 3.3???????????...???..????????????? 95 Figure 3.4???????????...???..?????????????102 Figure 3.5???????????...???..?????????????103 Figure 3.6???????????...???..?????????????105 Figure 3.7???????????...???..?????????????106 Figure 3.8???????????...???..?????????????108 Figure 3.9???????????...???..?????????????110 Figure 3.10?..?????????...???..?????????????111 Figure 3.11?..?????????...???..?????????????112 Figure 3.12?..?????????...???..?????????????114 Figure 3.13?..?????????...???..?????????????115 Figure 3.14?..?????????...???..?????????????116 Figure 3.15?..?????????...???..?????????????119 Figure 4.1???????????...???..?????????????131 Figure 4.2???????????...???..?????????????136 xi Figure 4.3???????????...???..?????????????144 Figure 4.4???????????...???..?????????????146 Figure 4.5???????????...???..?????????????149 Figure 5.1???????????...???..?????????????154 Figure 5.2???????????...???..?????????????160 Figure 6.1???????????...???..?????????????178 Figure 6.2???????????...???..?????????????185 Figure 6.3???????????...???..?????????????187 Figure 6.4???????????...???..?????????????188 Figure 6.5???????????...???..?????????????189 Supplementary Figure 2.1??????????..???????????..214 Supplementary Figure 2.2??????????..???????????..215 Supplementary Figure 3.1??????????..???????????..216 Supplementary Figure 4.1??????????..???????????..219 Supplementary Figure 5.1??????????..???????????..224 Supplementary Figure 5.2??????????..???????????..225 Supplementary Figure 5.3??????????..???????????..226 xii Chapter 1: Introduction and Summary of Dissertation Findings The evolutionary history of plants and their insect adversaries is a story told by the scars on fossil leaves. Insect damage on a single leaf captures one moment in time when an insect fed upon a plant, but it also reflects the millions of years of evolution leading up to that moment. The effects of insect herbivory on terrestrial ecosystems through time has been immeasurable over the past 400 million years (Labandeira 2007, Labandeira et al. 2014), and only recently have scientists begun to understand major themes of the diversity and intensity of plant and insect associations in the fossil record. Studies on deep time plant?insect associations have captured dramatic periods of Earth?s history, starting with the alien floras of the Carboniferous Period (385? 298.9 Ma (Ma; mega-annum)) and Permian Period (298.9?251.9 Ma) (e.g. Maccracken and Labandeira 2020, Schachat et al. 2015, Scott and Taylor 1983, Xu et al. 2018). Recent studies also have revealed the profound changes of ecosystems immediately before and after the Cretaceous?Paleogene (K/Pg) extinction event 66 million years ago (Ma) (ex. Donovan et al. 2018, Donovan et al. 2014, Labandeira et al. 2002b, Wilf et al. 2006) and during a brief period of intense global climate change, the Paleocene-Eocene Thermal Maximum at 55 Ma (Currano et al. 2010, Currano et al. 2008). However, there remains a wide gap in our knowledge about how insect herbivores responded to the rise and initial early radiation of flowering plants (angiosperms) throughout the Cretaceous Period. 1 Plants and insects of the Cretaceous Period (145?66 Ma) formed associations that are important precursors to those of today. During this period angiosperms overtook most ecosystems in a geologically brief period of time (Coiffard et al. 2012, Doyle et al. 1999, Heimhofer et al. 2005) and angiosperms now make up the majority of vascular plant life on earth today (Willis 2017). Despite being the inception of extant ecosystems we know today, the Cretaceous Period is one of the most poorly understood intervals of time for plant?insect associational studies (Figure 1.1). Plant? insect associations from the dawn of flowering plants to the terminal Cretaceous (~130?66 Ma) are a roadmap for the diversity of interactions we see in extant ecosystems and yet our understanding of Cretaceous plant?insect associations currently is insufficient. The research presented in this dissertation is among the first to step into the world of Cretaceous plant?insect associations and includes the first systematic study of plant?insect associations from the Campanian Age (83.6?72.1 Ma). To highlight the importance of this new research and because studies of deep time plant?insect associations broadly explore the two most diverse groups of terrestrial organisms, angiosperms and insects, this chapter includes a history of plants, insects, and their ecological associations. I also outline the geologic context, methodology, and summarize the findings for the research presented in this dissertation. 2 Figure 1.1: Localities analyzed for insect herbivory through time. Background color corresponds to Period, from the Devonian Period (here starting at 400 Ma) to the Quaternary Period (present). Localities included in this dissertation are denoted by the box-patterned bar (ca. 75 Ma). The green dashed line marks the first appearance of angiosperm fossils during the Early Cretaceous and the red dashed line marks the Cretaceous/Paleogene (K/Pg) extinction event. Only entire floras analyzed for herbivory were included in this analysis, although there are many more instances of herbivory described from specific plant hosts and assessments of specific damage types. Data for plot compiled by S. A. Maccracken using literature search. 3 Evolutionary Background The Rise of Angiosperms We live on an earth dominated by angiosperms. Today, flowering plants make up 96% of the terrestrial vegetation and there are an estimated 369,000 species (Pennisi 2009, Willis 2017). However, in the context of vascular plants, the world is only recently dominated by angiosperms. Knowledge of the history of vascular plants gives us a baseline to better understand the importance for the evolution of angiosperms. The earliest land plants were relatively simple spore-producing, non- vascular plants similar to extant bryophytes (mosses, liverworts, hornworts) (Delwiche and Cooper 2015); among the earliest spores known in the fossil record, tetrad spores from the late Ordovician (ca. 450 Ma) (Gray et al. 1982) and early Silurian (ca. 430 Ma) (Gray and Shear 1992, Taylor and Taylor 1993) provide strong evidence for the spore-producing phase of land plants (Willis and McElwain 2014). Non-vascular charophytes (freshwater green algae), bryophytes, and some extinct Devonian lineages were then preceded by vascular plants, such as lycophytes (fern allies), sphenopsids (horsetails), and ferns by ca. 430 Ma (Figure 1.2) (Willis and McElwain 2014). Seed plants evolved from the hornwort lineage around 380 Ma and greatly expanded during the Permian Period (299?252 Ma) (Willis and McElwain 2014), a time of great environmental change. It was not until the Mesozoic Era that the first angiosperms evolved (Crane et al. 1995, Herendeen et al. 2017, Hughes and McDougall 1994, Lupia et al. 1999), and even longer still until they became predominant on the landscape (Coiffard et al. 2012, Heimhofer et al. 2005, Wing et al. 1993). The rapid rise and ascendency of angiosperms is unrivaled in magnitude in 4 the evolutionary history of plants (Berendse and Scheffer 2009, Dilcher 2001) (Figure 1.3). Age (Ma) Figure 1.2: Phylogeny of land plants using a composite hypothesis of clade relationships. Figure created from hypothesized relationships between plant clades in Palmer et al. 2004, Sessa et al. 2014, and Stevens and Davis 2001. 5 Figure 1.3: Seed plant and fern species through time. Note the rise and radiation of angiosperms in the Cretaceous Period. Figure redrawn from Crane 1987, Lidgard and Crane 1988, de Boer et al. 2012, Fagua et al. 2017, reproduced with permission from journal (license for content #4926051157679). 6 Darwin referred to the sudden appearance of angiosperms in fossil deposits as an ?abominable mystery? (Darwin and Seward 1903). Despite 150 years of paleontological, ecological, and genetic discoveries, the rapid rise of angiosperms has many unanswered questions, including when they originated. The timing of angiosperm evolution is hotly, and on occasion, tactlessly debated (ex. Wang 2017). The oldest undisputed angiosperm fossils are pollen grains that date to the Early Cretaceous Period (ca. 136 Ma) (Crane et al. 1995, Herendeen et al. 2017, Hughes and McDougall 1994, Lupia et al. 1999). The earliest angiosperms likely predate their fossil record, common in many lineages, making fossil-calibrated molecular phylogenies important tools for dating this clade. Molecular phylogenies have placed the origin of angiosperms in the Cretaceous Period (139.35?136 Ma) (Magall?n et al. 2015), the Jurassic Period (179?158 Ma) (Wikstr?m et al. 2001), and even the Triassic Period (228?217 Ma) (Smith et al. 2010). Regardless of the uncertainty around the origination of flowering plants, of which Magall?n et al. (2015) appear to have the most realistic calibration dates when compared to the fossil record, herbaceous angiosperm mesofossils and macrofossils are diverse and abundant by the Barremian?Aptian transition (late Early Cretaceous, ca. 125 Ma (Feild et al. 2011, Friis et al. 2011, Oakley and Falcon-Lang 2009, Philippe et al. 2008, Wheeler and Lehman 2009, Wheeler and Baas 1991). Throughout this time interval there are major ecological transitions as angiosperms diversify and outcompete older lineages of plants (Coiffard et al. 2012). From the early to mid Mesozoic Era, gymnosperms and ferns dominated terrestrial ecosystems and filled most available plant niches until the rise of 7 angiosperms (Lidgard and Crane 1990). Coiffard et al. (2012) divided the rise and radiation of angiosperms into three phases. The first phase (136?125 Ma) consisted of relatively exclusive environments of gymnosperms and ferns, with rare aquatic angiosperms. Gymnosperms and ferns occupied all non-aquatic habitats and angiosperms became established in riparian corridors. During the second phase (112? 100 Ma) angiosperms increased in species number and occupied a greater ecological breadth. In addition to aquatic and riparian niches, flowering plants began to colonize floodplains. During the third phase (100?94 Ma) angiosperms were widespread, speciose, and filled most ecological niches. Arborescent life-habits of angiosperms were also evolving, which further increased competition between angiosperms and gymnosperms attributable to overlapping niche space (Coiffard et al. 2012). By the Campanian Age (83.6?72.1 Ma), many of the major eudicotyledon clades had differentiated (Crane et al. 1995). It is in this relatively short time interval during the Cretaceous Period that we see the ascendancy of angiosperms; however, ecological interactions between angiosperms and insects during this time interval are poorly known and the fossil record of insects is likewise depauperate (Grimaldi and Engel 2005, Ross et al. 2000). The limited number of insect body fossil deposits and plant? insect research projects in this interval is problematic because the associations between insects and vascular plants, including herbivory and pollination, are hypothesized to play a major role in the diversification of both groups of organisms (ex. Bagchi et al. 2014, Bascompte and Jordano 2007, Cruaud et al. 2012, Ehrlich and Raven 1964, Janz 2011, McKenna et al. 2009, Wiens et al. 2015). 8 Insect Diversity and the Fossil Record Insects (Phylum Arthropoda, Class Hexapoda) are the most speciose and abundant animals on Earth today, with recent predictions for total species diversity ranging between 5 and 20 million (Foottit and Adler 2009, Gaston 1991, Mora et al. 2011, Nielsen and Mound 2000, Stork 1988). Insects are found in every major terrestrial environment and the combined effect of insects on ecosystems through time is immense. The insect fossil record spans ca. 410 million years (Shear et al. 1984, Whalley and Jarzembowski, 1981) and it is hypothesized that insects first evolved at ca. 480 Ma (Misof et al. 2014) based on molecular data with fossil calibrations (Figure 1.4), with herbivorous insects evolving by ca. 410 Ma (Labandeira et al. 2014). The insect fossil record can be considered both moderately complete at the family taxonomic level, but distressingly incomplete at the genus and species level when the fossil record is compared to hypothesized insect species diversity through time (Labandeira and Eble 2005, Labandeira and Sepkoski 1993). Although the body fossil record of insects capture all known orders of insects (32 modern orders, ca. 14 extinct orders) and over 1300 families, including approximately 70% of modern families (Labandeira 1994), the vast majority of ancient species have either not been discovered yet or are wholly unpreserved as fossils (Schachat and Labandeira in press). Furthermore, the record of insect fossil diversity is not evenly distributed through time and space, which can distort signals of diversity, such as the Signor? Lipps effect (Signor et al. 1982) and the Pull of the Recent effect (Raup 1979). At first glance, the Cretaceous insect fossil record may be considered well sampled due 9 to a small number of extensive amber deposits (Ding et al. 2003, Grimaldi and Engel 2005), yet in general, Cretaceous, especially the Late Cretaceous, insect fossils are remarkably sparse. Age (Ma) Figure 1.4: Generalized molecular phylogeny of extant insect orders through time. Nine of the 31 insect orders include herbivorous species (denoted by green text), including all four of the largest orders (Coleoptera, Diptera, Hymenoptera, and Lepidoptera). Figure adapted from hypothesized relationships presented in Misof et al. 2014), reproduced with permission from journal (license for content #4926050801134). Pal. Palaeoptera; Con. Condylognatha. The best record of Cretaceous insects comes from the Burmese (Myanmar) amber, which dates to ca. 99 Ma and comprises 34 orders, 300 families, and 867 10 described species (Ross 2015, 2018). However, phytophagous insect fossils from the Western Interior of North America are relatively rare and mostly known from a small number of Late Cretaceous amber deposits (Hillaire-Marcel et al. 2008, McKellar and Wolfe 2010, Pike 1994, 1995). Despite the past 30 years of highly productive Cretaceous insect research (Grimaldi and Engel 2005), insect diversity curves for this time period remain contentious, especially in response to extinction and radiation events, such as how the radiation of angiosperms influenced insect diversity (and vice versa) throughout the Cretaceous Period (Jarzembowski and Ross 1996, Labandeira and Sepkoski 1993, Ross et al. 2000, Schachat et al. 2019). Labandeira and Sepkoski (1993) found that the taxonomic family-level diversity of insects was nearly static throughout the Early and Late Cretaceous, notably during the rise of angiosperms. This was an unexpected and highly contentious result within the paleoentomology community, as it was assumed that insect diversity would increase in-step with flowering plants. These findings were interpreted as being at odds with longstanding ?coevolutionary arms race? theories, in which herbivorous insects and angiosperms fueled successive species radiations in one another (Ehrlich and Raven 1964, Farrell 1998, Janz 2011, McKenna et al. 2009, Mitter et al. 1988, Moreau et al. 2006). Subsequently, there have been several independent re-analyses of family level diversity during this interval (Jarzembowski and Ross 1996), most notably Schachat et al. (2019), which used mark-recapture methodology and found a steady increase in family-level diversity in the Early Cretaceous and a steep increase in diversity during the Albian. This increase, however, started before and during the early evolution of angiosperms, when they 11 were not especially diverse or abundant (Schachat et al. 2019). Why didn?t the number of insect families change during the Cretaceous in relation to the diversification of angiosperms? First, the relative stasis of family-level diversity for herbivorous insects may reflect the evolutionary timing of insect lineages; many families of insects originated throughout the late Paleozoic and early Mesozoic Eras (see Misof et al. 2014) and in association with spore-bearing and seed- producing plant hosts (Labandeira 2002b, 2005, Rasnitsyn 1988). Parasitoid insects, a large component of modern insect diversity, also diversified throughout the Jurassic Period and underwent a radiation during the Aptian?Albian interval prior to the ecological dominance of angiosperms (Labandeira 2002b, 2005, Rasnitsyn 1988, Schachat et al. 2019). Labandeira and Sepkoski (1993) postulated that diversification of insects during the rise of angiosperms might have occurred at subfamilial taxonomic ranks. Origination and extinction rates may have also impacted the diversity curve for Cretaceous insect families; if extinction and origination rates are equal, including if both spike dramatically, there would be stasis in the number of insect families (Labandeira 2005, Labandeira 2014, Schachat and Labandeira in press). As conifers, cycads, other now-extinct gymnosperm lineages, and to a lesser extent ferns (Schneider et al. 2004) were replaced by new species of angiosperms (Coiffard et al. 2012, Lidgard and Crane 1990, Lupia et al. 1999), it is likely that some herbivorous insects lost their host plants and went extinct, while other herbivorous and pollinating insects became more speciose (Fagua et al. 2017, McKenna et al. 2009, McKenna et al. 2015, Ross and Jarzembowski 1993, Ross et al. 2000, Zhang and Wang 2017). Finally, changes in insect plant host preference may 12 have also spurred the coevolution between angiosperms and herbivorous insects without an increase in family-level diversity (Labandeira 2014). The host plant preferences of phytophagous insect families from the Jurassic Period to the Paleogene Period generally shift from gymnosperms to angiosperms, coupled with the extinctions and originations of other insect clades (Labandeira 2014) (Figure 1.5). Continuing research into insect diversity before and throughout the rise of angiosperms will undoubtedly shed light on this event. Complementary lines of evidence into how herbivory changed during this time period, such as the record of insect damage on fossil leaves, can provide independent evidence of insects when the body fossil record is sparse and, moreover, provide novel information on the ecologies of ancient insects and their associations with plants (Labandeira 1998b). The Fossil Record of Plant?Insect Associations Fossil plant material, including insect damaged leaves, is the basis for reconstructing the diversity of ancient terrestrial landscapes and their ecological interactions. The fossil record of plant?arthropod associations is comprised of mimicry (Wang et al. 2012), mutualisms (Maccracken et al. 2019, O'Dowd et al. 1991), notably insect pollination (Labandeira 2010, Labandeira et al. 2007b, Peris et al. 2017, Wappler et al. 2015b), and insect herbivory, which is among the most dynamic and copious of these associations (see Pinheiro et al. 2016). Evidence for the damage that herbivorous insects inflict?the punctures, skeletonization, galls and leaf mines in fossil leaves?constitute one of the richest ecological sources of evidence available on species interactions of any kind from the distant past. Many studies on deep time insect herbivory have focused on epochal floras or single plant?insect 13 180 160 140 angiosperm radiation 120 100 80 60 40 20 0 JURASSIC CRETACEOUS PALEOGENE 200 180 160 140 120 100 80 60 40 Age (Ma) Figure 1.5: Insect family diversity and host plant preference changes throughout the late Jurassic Period to the Paleocene Period. Dark green is gymnosperm-feeding and light green is angiosperm-feeding families. Modified from Labandeira (2014). Reproduced with permission from journal (license for content #4926060730978). 14 No. Herbivorous Insect Families associations. Collectively, the temporal and spatial patterns of deep time plant?insect associations provide fundamental information on ancient food-web structure (Dunne et al. 2014, Feng et al. 2017, Prevec et al. 2009, Wilf 2008), changes in climate (Currano 2009, Currano et al. 2010, Currano et al. 2008, Winkler et al. 2009a), the evolution of insect feeding guilds and specific insect clades (Labandeira 2006b, Sarzetti et al. 2008, Sohn et al. 2019a), host plant specialization (Jud and Sohn 2016, Wilf et al. 2000, Winkler et al. 2009a), and extinction events (Donovan et al. 2016, Donovan et al. 2018, Donovan et al. 2014, Labandeira et al. 2002b, Wappler et al. 2009, Wilf 2008, Wilf et al. 2006). Among the first instances of fossil insect herbivory reported in the scientific literature were descriptions of galls on fossil leaves from the Oligocene Period (Scudder 1886), Cretaceous galls (Lesquereux 1892), and now dubious leaf mines on Permian ferns (Potoni? 1893). Other early descriptions of insect damage includes galls from the Oligocene Period (Brues 1910) and Pleistocene Period (Berry 1909); Eocene galls on figs (Cockerell 1910); and various fossil plant?insect associations described during the mid-twentieth century (ex. Brooks 1955, Chaney 1920, Hoffman 1932) and in wood (Brues 1936). Systematic descriptions of insect damage on fossil leaves began in the mid-1970s through the 1990s (ex. Crane and Jarzembowski 1980, Hickey and Hodges 1975, Liebhold et al. 1982, Opler 1973, 1982, Rozefelds and Sobbe 1987, Scott et al. 1985, Scott and Paterson 1984, Scott and Taylor 1983) and since the 1990s, the insect damage research has become more widespread, systematic, and formalized, most notably with the advent of the Guide to Insect (and Other) Damage Types on Compressed Fossil Plants (Labandeira et al. 2007c). 15 The renaissance of fossil insect herbivory studies occurred during the 1990s, when paleobiologists began systematically analyzing and quantifying insect damage across periods of time and for entire floras (Beck and Labandeira 1998, Labandeira 1998a, b, Labandeira et al. 1994, Labandeira et al. 1995, Wilf and Labandeira 1999). The seminal paper for implementing the functional feeding group?damage type system of plant?insect analysis was Wilf and Labandeira (1999). During the 2000s and 2010s insect herbivory studies expanded into previously unstudied geographic regions and time periods (ex. Adroit et al. 2018a, Adroit et al. 2018b, Adroit et al. 2016, Currano 2009, Currano et al. 2010, Currano et al. 2008, Khan et al. 2014, Knor et al. 2012, Labandeira et al. 2016, M?ller et al. 2017, M?ller et al. 2015, Pinheiro et al. 2012, Prokop et al. 2010, Su et al. 2015, Wappler et al. 2009, Wappler and Gr?msson 2016, Wappler et al. 2012). Recent neontological studies have ground- truthed observations from the fossil record (Adams et al. 2010, Carvalho et al. 2014, Sohn et al. 2019b) and paleontological studies have also undertaken new statistical analyses and sampling regimes, which are more closely aligned with techniques of neontologists (Currano 2009, Currano et al. 2010, Currano et al. 2019, Gunkel and Wappler 2015, Maccracken and Labandeira 2020, Schachat et al. 2015, Schachat et al. 2014, Schachat et al. 2018, Schachat et al. 2020). In general, the study of deep time plant?insect associations has become more sophisticated, detailed, and rigorous through time, as well as more finely partitioning the types of insect damage seen on fossil plant specimens. Finally, a formative study by Pinheiro et al. (2016) recently analyzed a large dataset (>70,000 specimens) of plant?insect associational studies for the past 385 million years and found that damage type diversity generally increased 16 with geologic age and temperature (Pinheiro et al. 2016). The earliest unequivocal arthropod herbivory, geologically speaking, consists of sporangial and stem consumption from the earliest Devonian Period (ca. 410 Ma) of Europe (Kevan, Chaloner, and Savile, 1975, Labandeira 2007, Labandeira et al. 2014). Very limited herbivory has been documented for the Mississippian Epoch between 359?323 Ma (Iannuzzi and Labandeira, 2008). By the Carboniferous Period, between 327?309 Ma, arthropods herbivorized roots, leaves, seeds, and wood, and all major herbivorous arthropod feeding guilds had evolved (Labandeira 1998a, 2001, Scott and Taylor 1983), except for leaf mining, which first appears in the earliest Triassic of Russia (Krassilov and Karasev, 2008) and the Late Triassic Period of South African deposits (Labandeira and Anderson 2005). By the Early Cretaceous Period, the damage types created by insect herbivores appear essentially modern (Labandeira 1998c); hole feeding, margin feeding, skeletonization, surface feeding, piercing-and-sucking phloem and xylem sap feeding, leaf mining, galling, wood boring, and seed predation are extensive and well known before the advent of angiosperms (see Labandeira et al. 2007c and recent addenda for a record of Paleozoic and Mesozoic damage types). However, the Mesozoic Era in general and Cretaceous Period in particular is the poorest-sampled period of time for plant?insect associational studies (Pinheiro et al. 2016), and we expect to see both novel types of insect damage that would extend the record of many Cenozoic damage types into the early rise of angiosperms. The majority of described Mesozoic plant?insect associations are isolated Triassic, Jurassic, and Cretaceous damage types, often single occurrences, on 17 particular plant hosts (Cenci and Adami-Rodrigues 2017, Est?vez-Gallardo et al. 2019, Jud and Sohn 2016, Khan et al. 2014, Krassilov 2007, Krassilov and Shuklina 2008, Krassilov 2008a, Krassilov 2008b, Labandeira 1998c, Labandeira et al. 1994, Moisan et al. 2012, Vasilenko 2008, Wilf et al. 2000). There are a total of five descriptions of insect herbivory for entire floras in the early to mid-Mesozoic Era from ca. 250?90 Ma (Arens and Gleason 2016, Krassilov and Shuklina 2008, Labandeira et al. 2016, Scott et al. 2004, Wappler et al. 2015a), of which only two are mid-Cretaceous in age and include floras with angiosperms present (Arens and Gleason 2016, Krassilov and Shuklina 2008). Six studies analyze plant?insect associations at the terminal Cretaceous, with the goal of tracing insect herbivory across the K/Pg boundary and into the early Paleogene (Donovan et al. 2016, Donovan et al. 2018, Donovan et al. 2014, Labandeira et al. 2002a, Labandeira et al. 2002b), and several additional studies examine the recovery of plant?insect associations during the early Cenozoic (Donovan et al. 2014, Wappler et al. 2009, Wilf et al. 2006). For comparison to the Campanian Age floras described in this dissertation, the studies of terminal Cretaceous plant?insect associations provide an important baseline, since they are 1) within 10 million years of one another, 2) use the same insect damage classification system, and 3) include large sample sizes across numerous localities. For example, a total of 9,292 fossil plant specimens were examined from the terminal Cretaceous Hell Creek Formation in the Williston Basin and the diversity of damage types was found to be moderate (North Dakota USA) (Labandeira et al. 2002a, Labandeira et al. 2002b). The diversity of plant?insect 18 associations from the latest Cretaceous (Maastrichtian) Lefip?n Formation in Argentina was significantly greater than that of the Hell Creek, when data were standardized (Donovan et al. 2016, Donovan et al. 2018). Based on these Maastrichtian studies, the Campanian Age localities analyzed in this dissertation are expected to have a moderate- to high-diversity of damage types, made by insect herbivores that range from monophagous (fed upon a single plant host species) to polyphagous (fed upon many, unrelated plant host species). Geologic Background The research in this dissertation is focused on the Late Cretaceous of North America. By the Campanian Age (83.6?72.1 Ma), the Cretaceous Western Interior Seaway divided North America into several landmasses, with Laramidia to the west and Appalachia to the east (Hancock and Kauffman 1979) (Figure 1.6). Laramidia was an elongate, north-to-south oriented landmass that stretched from present day north-central M?xico to northern Alaska and covered approximately 4 million km2 (Sampson et al. 2010a). A north-south-trending mountain chain, the Sevier Orogeny, formed the backbone of this ancient landmass in the mid-latitudes of present-day California and Oregon. Rapid uplift and erosion, combined with foreland subsidence, preserved alluvial and fluvial plains (Roberts et al. 2013). These depositional settings entail flat, gently sloping depositional landforms created by rivers that carried sediment from the mountainous region eastward to the Laramidian coastline (Roberts et al. 2013). The broad alluvial/fluvial plain blanketing the shoreline is preserved as a number of fossil-bearing geologic formations, including the principal formation 19 examined for this dissertation. The Kaiparowits Formation The Kaiparowits Formation is located on the Kaiparowits Plateau in the Grand Staircase-Escalate National Monument in southern Utah, USA (paleolatitude 46.2oN (Miller et al. 2013)) (Figure 1.6). Almon H. Thompson, a member of the Powell Figure 1.6: Map of North America during the late Campanian (ca. 75 Ma). Kaiparowits Formation is noted by the yellow dot. Map used with permission from Colorado Plateau Geosystems (Blakey 2011). 20 Survey in the 1870s, popularized the name ?Kaiparowits? (Blake 2017), although the area was inhabited by indigenous peoples for over 10,000 years (Spurr et al. 2004) and this was not among the earliest names for this region. Kaiparowits is a Paiute Indian word that translates to ?Home of our People? (Blake 2017). It is a 1005-meter- thick package of sandstones, siltstones, mudstones, and conglomerates (Table 1.1) (Beveridge et al. 2020, Roberts et al. 2013). 40Ar/39Ar dating from throughout the formation indicate that it was deposited between 76.49 ? 0.14 and 74.69 ? 0.18 Ma, and is divided into one formal member and three informal members: the newly described and uppermost Upper Valley Member, and the informal upper, middle, and lower members, of which the middle member is richest in fossils (Beveridge et al. 2020, Roberts et al. 2013). The Kaiparowits Formation was formed from coastal plain deposits, occurring in a subtropical and relatively wet climate (mean annual temperature ca. 20oC and mean annual precipitation ca. 1.8 m) (Miller et al. 2013). Table 1.1: Six facies associations and paleoenvironmental interpretations of the Kaiparowits Formation, as described by Roberts et al. (2013). Facies Associations. Paleoenvironment. Description. Intraformational High energy flow environments in May be thalweg deposits, sometimes conglomerates river channels sandy mudstones Major tabular and Meandering or anastomosing river Bankfull widths 20-80m; bankfull lenticular sandstones channels depth 3-10m; often with adjacent crevasse splays Minor tabular and Crevasse splay and crevasse channel Plant material abundant lenticular sandstones deposits Finely laminated Large shallow lakes Plant material abundant, especially calcareous siltstone aquatic fern taxa Inclined heterolithic Point bar lateral accretion in a tidally Rare in the Kaiparowits Fm.; DMNS sandstone and influenced channel Loc. 3642 mudstone Sandy mudstone and Range of overbank deposits: Suggestive of ever wet, low lying carbonaceous perennial ponds & lakes, oxbow alluvial system with large, slow mudstone lakes, marshes, swamps, and large, moving channels and well vegetated slow moving channels overbank sequences. Plant material abundant 21 These sediments are estimated to have been deposited between 10 to 100 km from the paleocoastline (Roberts et al. 2013). Abundant large and small river channels, ponds, lakes, and swamps dominated the landscape and preserved a wealth of organisms and trace fossils in this formation (Roberts et al. 2013). The Kaiparowits is well-known for its exceptional diversity of organisms, including non-avian dinosaurs (Carr et al. 2011, Decourten and Russell 1985, Gates and Sampson 2007, Lund et al. 2016, Sampson et al. 2010b, Sampson et al. 2013, Zanno et al. 2013), birds (Farke and Patel 2012), pterosaurs (Farke and Wilridge 2013), squamates (Lively 2016, Lyson et al. 2017, Nydam 2013), amphibians (Gardner and DeMar 2013, Ro?ek et al. 2013), crocodyliforms (Farke et al. 2014, Irmis et al. 2013), mammals (Cifelli 1990a, b, Eaton and Cifelli 1988, Eaton et al. 1999), fish (Brinkman et al. 2013, Kirkland et al. 2013), aquatic invertebrates (Roberts et al. 2008, Tapanila and Roberts 2013), and plants (Maccracken et al. in review-a, Miller et al. 2013). Insect body fossils from this formation are virtually absent, despite the high probability that insects were abundant and diverse (Labandeira 2006a, Labandeira and Eble 2005). Kaiparowits Formation specimens are housed at the Denver Museum of Nature and Science in Denver, Colorado. The Kaiparowits Flora was collected by Dr. Ian Miller and colleagues from 2008?2020. 22 Research Objectives Plant?insect associations from the Late Cretaceous of western North American ecosystems are poorly known and the research in this dissertation aims to identify and quantify Campanian plant?insect associations from the Kaiparowits Formation. Across the next five chapters, the overarching objectives are as follows: 1. Document the diversity of insect damage on fossil leaves from the Campanian Age flora from the Kaiparowits Formation (Chapters 2, 3) 2. Taxonomically describe new plant host species, novel arthropod damage types, and important plant?arthropod associations. (Chapters 2?5) 3. Analyze all available and suitable datasets of plant?insect associations during the age of angiosperms (ca. 140 Ma ? present) for large-scale patterns of insect preference of plant hosts. (Chapter 6) Brief Methodology The first step in the analysis of plant?insect associations is to identify all plant hosts in the flora. Due to the high numbers of fossil leaf species at many localities, identification and description of Linnaean leaf taxonomy for each possible species was not feasible. Instead, leaves were categorized (i.e., binned) into macrofossil 23 morphotypes following the system devised by Johnson (1989) and elaborated by the Leaf Architecture Working Group (1999) (Figure 1.7). Binning allows the use of morphological characters to demarcate discrete taxonomic units before a morphotype is formally applied and described. Leaf venation, leaf margin features, leaf base and overall leaf shape are among the key features for morphotyping foliage within a flora. The Kaiparowits Flora was morphotyped by SA Maccracken and IM Miller. In some instances, taxonomic descriptions of plant hosts are necessary. All taxonomic descriptions follow the guidelines of the International Code of Nomenclature for Algae, Fungi, and Plants (Shenzhen Code) (Turland et al. 2018). Morphological descriptions of dicotyledonous angiosperms follow the terminology of the Manual of Leaf Architecture (Ellis et al. 2009). The following criteria were used to distinguish herbivore-induced insect damage from physical damage, such as tearing, detritivory, or taphonomic processes. The first criterion is the presence of reaction tissue, in which cells are enlarged or multiplied along the site of damage (Brues 1924, Johnson and Lyon 1991, MacKerron 1976, Vincent et al. 1990). A second criterion is the targeting of a specific host-plant taxon or a particular plant organ that can be attributed to insect- specific patterns of damage, such as linear rows of punctures on or along primary veins, or small cusps occurring on the cut edge of a plant tissue (Gangwere 2017, Kazakova 1985, Keen 1952). A third criterion is the repetition of a damage pattern based on shape, size, and position of the damage on the plant (Bodnaryk 1992, Heron 2003). After herbivore damage was identified, it was classified by feeding guild, or functional feeding group, and damage type (Labandeira et al. 2007c). 24 Plants Other plant parts Lycopod 5 Leaves 1 Winged 2 Isolated, non- Equisetum 6 seeds, winged seeds, Fern 7 winged fruits flowers, fruits Cycad 8 3 Repro. 4 Indet., but Ginkgo 9 axes, attached distinct flowers or fruits fragments, Conifer 10 or cones spines, roots, Dicot Monocot 11 or strobili nonreproductive axes Petiole attached 12 Petiole attached inside margin outside margin Unlobed Lobed 13 Pinnately Palmatelylobed lobed 14 Pinnate Palmate Toothed Smooth Toothed Smooth Agrophics No Agrophics Agrophics No No Agrophics Agrophics Agrophics Agrophics No Agrophics Semi- 15 Semi- 16 27 Crasp 28 Semi- 31 Semi-crasp crasp Crasp crasp crasp 32 Brochid 35 Brochid 36 Crasp 17 Crasp Eucampt 29 Eucampt 30 Crasp 33 Crasp 34 Crasp 37 Crasp 38 Brochid 22 Brochid Eucampt 39 Eucampt 40 Ovate Elliptic Oblong Obovate Ovate Elliptic Oblong Obovate 41 Unsortable, 18 19 20 21 23 24 25 26 but may be possible to recognize Figure 1.7: Flow chart showing a morphological binning of leaf macrofossils to assist in the morphotyping process devised by Johnson (1989) and elaborated by the Leaf Architecture Working Group (1999). The ?bin? system in this flow chart is not formally published. It is in use by the working group at the Denver Museum of Nature & Science and redrawn here with permission (pers. comm. I.M. Miller). Please inquire with the Denver Museum of Nature & Science Department of Earth Sciences for reproduction permission. Brochid = brochidodromous, Crasp = craspidodromous, Eucampt = eucaptodromous. 25 The classification of each instance of herbivore damage followed the system of Labandeira et al. (2007c), including recent addenda to the Guide to Insect (and other) Damage Types on Compressed Plant Fossils. The damage was initially categorized into one of several functional feeding groups: 1) hole feeding; 2) margin feeding; 3) surface feeding; 4) skeletonization; 5) piercing and sucking; 6) oviposition; 7) galling; and 8) leaf mining. Discrete, diagnosable damage types were documented within each functional feeding group and assigned a damage type number. Damage types are defined by the distinctive shape, size, extent, and location of herbivore damage on the affected leaf, as well as being rated for host specificity: 1 or generalized (polyphagous), 2 or intermediate (oligophagous), and 3 or specialized (monophagous) (Labandeira et al. 2007c). The convergence of herbivore mouthparts and feeding behaviors make genus or species level identifications of the insect culprit rare, although some margin feeding, leaf mines, galls, and scale-insect feeding marks can be traced to extant lineages (ex. Jud and Sohn 2016, Sarzetti et al. 2008, Wappler and Ben-Dov 2008, Wilf et al. 2000, Winkler et al. 2010). Pathogen damage was not documented because of the difficulty of recognition, although the next version of the Guide to Insect (and other) Damage Types on Compressed Fossils will provide keys and other diagnostic criteria for recognition. Plant?insect associational data includes both qualitative and quantitative data. The qualitative data, outlined above, consist of functional feeding groups, damage types, and host plant specificities. The qualitative data determine if the insect feeding guilds on a particular host-plant taxon, the diversity of damage types, host specificities, and occasionally identities of the phytophagous insect responsible for 26 the damage. Quantitative data collection consists of the proportion of damaged leaves, the richness of damage types, and the percent of surface area herbivorized by insects (herbivory index). Summary of Dissertation Findings Documentation and analyses of plant?insect associations from the Late Cretaceous Kaiparowits Formation provides the first evidence of the diversity and ecology of herbivorous insects from this formation. These findings are not only important for future reconstructions of the Kaiparowits ecosystems, but also document the earliest occurrence of a lineage of lepidopteran leaf miners and of plant?mite mutualisms in the fossil record. Please note that each chapter is prepared for publication in a specific peer-reviewed journal and some repetition occurs among chapters, as well as differences in style, spelling (American versus British English), and supplementary materials, based on the prospective journal?s requirements. In Chapter 2, ?Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA)?, I present the first formal description of a plant taxon from the Kaiparowits Formation and survey the insect herbivory found on the leaves of this new species. With over 1,500 specimens from a single locality, Catula gettyi is one of the best-sampled fossil plant taxa from the Late Cretaceous, and there is a total of 40 patterns of insect damage found on these specimens. This relatively high diversity of damage types also provides 27 evidence for a number of different types of insect herbivores, including those with chewing mouthparts (i.e. beetles, grasshoppers, caterpillars, etc.), insects that puncture the leaf surface with stylet-like mouthparts (i.e. hemipterans, thrips, etc.), insects adapted for leaf mining, and galling insects. Chapter 3, ?Plant?insect associations from the Campanian (Late Cretaceous) of Utah, USA?, also includes quantitative analyses of plant?insect associations from the Kaiparowits, which encompasses all plant host specimens from the JARS locality (DMNH loc. 3725). The diversity of plant hosts at JARS include angiosperms, as well as a small number of lycopsids, pteridophytes, sphenophytes, gymnosperms, and unassociated reproductive plant organs. The results of this study include a moderate diversity of insect damage when compared to that of Catula gettyi, the targeting of several plant hosts by particular clades of insect herbivores, as well as a possible intercontinental distributional range of oviposition on the floating aquatic angiosperm Quereuxia spp. Chapter 4, ?A new Late Cretaceous leaf mine Leucopteropsis spiralis gen. et sp. nov. (Lepidoptera: Lyonetiidae) and the deep time origin of a common agricultural pest?, describes a new fossil leaf mine from the Kaiparowits Formation, which is the earliest record of a lyonetiid leaf-mining moth, as well as the second oldest record of the Yponomeutoidea?Gracillarioidea clade. This discovery provides an important Late Cretaceous (~76 Ma) calibration point within the lepidopteran phylogeny and is an indicator for the antiquity of the most diverse lepidopteran group, Ditrysia. It also underscores the importance of ichnofossils in the lepidopteran fossil record, since body fossils of butterflies and moths are rare (Sohn et al. 2014). 28 The discovery of acarodomatia (mite houses) in fossil leaves from the Kaiparowits Formation in Chapter 5, ?Late Cretaceous Domatia Reveals the Antiquity of Plant?Mite Mutualisms in Flowering Plants?, documents the oldest known acarodomatia in the fossil record (ca. 75.5 Ma). This fossil acarodomatia extends the record of fossil domatia by over 25 million years and I describe the evolutionary timing of suitable host plants and the first acarodomatia. Acarodomatia are found almost exclusively on woody angiosperm species, and woody angiosperms are not common until ~100 Ma. Consequently, acarodomatia likely first evolved in conjunction with early woody dicot angiosperms, which first appeared approximately 25 million years preceding the newly discovered Campanian acarodomatia. Finally, in Chapter 6 ?Widespread biases in deep time plant?insect associational studies obscure potential patterns of insect preferences throughout the Age of Angiosperms?, I analyzed all available datasets of plant?insect associations from the Cretaceous Period to the Quaternary Period to understand how insect herbivory has changed though time. Although insect preference for plant hosts significantly changed through time and as plant diversity increased within an ecological community, these results illuminate how sampling regimes and the difficulties of taxonomic identification for older fossil plants prevents us from understanding the causal mechanisms that drive insect herbivory over long periods of geologic time. In total, the discoveries and analyses presented in this dissertation allow us to better reconstruct the ancient ecosystems of the Kaiparowits Formation, recognize 29 some of the first plant?insect associations from a Campanian Age deposit, and trace the evolutionary trajectories of modern insect lineages and ecological associations back in time to the Late Cretaceous. 30 Chapter 2: Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA) Abstract The Upper Cretaceous (Campanian Stage) Kaiparowits Formation of southern Utah, USA, preserves abundant plant, invertebrate, and vertebrate fossil taxa. Taken together, these fossils indicate that the ecosystems preserved in the Kaiparowits Formation were characterized by high biodiversity. Hundreds of vertebrate and invertebrate species and over 80 plant morphotypes are recognized from the formation, but insects and their associations with plants are largely undocumented. Here, we describe a new fossil leaf taxon, Catula gettyi gen et. sp. nov. in the family Lauraceae from the Kaiparowits Formation. Catula gettyi occurs at numerous localities in this deposit that represent ponded and distal floodplain environments. The type locality for C. gettyi has yielded 1,564 fossil leaf specimens of this species, which provides the opportunity to circumscribe the leaf shape, attachment, and venation patterns of this new plant morphospecies. In addition to describing the ecology of this taxon, including an extensive catalog of feeding damage on C. gettyi caused by herbivorous insects. We recorded more than 800 occurrences of insect damage belonging to five functional feeding groups indicating that insect-mediated damage on this taxon is both rich and abundant. C. gettyi is one of the best-sampled 31 host plant taxa from the Mesozoic Era, and its insect damage is comparable to other Lauraceae taxa from the Late Cretaceous. Introduction Lauraceae Juss. (Order Laurales) is a speciose and anatomically diverse family of aromatic magnoliid angiosperms. Today, the family is generally thought to consist of 45 genera and 2,850 species (Christenhusz and Byng 2016) to perhaps as many as 52 genera and 3,500 species (Rohwer 1993b). The Lauraceae are almost exclusively trees and shrubs, although species in the genus Cassytha L. may exhibit herbaceous or parasitic growth forms (Rohwer 1993b, Weber 1981). The family is mostly evergreen and occupies ecologically important roles in tropical and warm- temperate forests across a significant altitudinal range (Reis-Avila and Oliveira 2017, van der Werff and Richter 1996). Economically important genera in the Lauraceae include Persea Mill. (avocados), Cinnamomum Schaeff. (cinnamon), Laurus L. (bay laurel), and Umbellularia Nuttall (California bay). Leaves of Lauraceae are often dark green and glossy on their adaxial surfaces and villous and grey-green on their abaxial surfaces (Rohwer 1993b). Notably, the leaves are often leathery, which improves their preservation potential in the fossil record. The Lauraceae has a particularly good fossil record compared to other major dicot lineages. The oldest unequivocal occurrence of reproductive organs attributed to the Lauraceae are charcoalified flowers of Potomacanthus lobatus von Balthazar et al. (2007) from the Potomac Group, a Lower Cretaceous deposit (ca. 108 Ma), from eastern North America. The oldest fossil leaves assigned to Lauraceae are of similar 32 age. They include examples such as those from the from the Dakota Formation (ca. 102 Ma), described as Rogersia dakotensis Wang and Dilcher (2018), Wolfiophyllum heigii Wang and Dilcher (2018), Pandemophyllum Upchurch and Dilcher (1990), and Pabiana Upchurch and Dilcher (1990). In Upper Cretaceous strata, fossil occurrences of Lauraceae are abundant and worldwide. Notable examples include 1) charcoalified flowers, peduncles, fruits, and stems of Mauldinia sp. from the Vocontian Basin in southeastern France (ca. 97 Ma) (Moreau et al. 2016); 2) carbonized flowers and inflorescences of Mauldinia bohemica Eklund and Kva?ek (1998) from the Peruc- Korycany Formation (ca. 95 Ma) in the Czech Republic; 3) carbonized flowers of Perseanthus crossmanensis Herendeen et al. (1994) of the Raritan Formation (ca. 91 Ma), New Jersey, U.S.A.; and 4) wood of Paraphyllanthoxylon vancouverense Jud et al. (2018) from the Comox Formation (ca. 89 Ma) in British Columbia, Canada . By the latest Cretaceous, taxa attributable to Lauraceae are found in many deposits bearing abundant fossil leaves. For example, Marmarthia trivialis Johnson (1996) and Marmarthia pearsonii Johnson (1996) from the Hell Creek Formation (ca. 67.5-66 Ma) of the Williston Basin, North Dakota, USA, are widespread within the upper third of the rock unit. Alongside inferences from molecular diversification proxies, fossil occurrences of Lauraceae indicate that the family evolved and began to diversify in the Early Cretaceous. Furthermore, fossil attributions indicate that the family was substantially diverse by the end of the Cretaceous (Chanderbali et al. 2001, Michalak et al. 2010, Tank et al. 2015). However, evidence for Cretaceous diversification of the family is limited compared to the Cenozoic diversity of Lauraceae (von Balthazar et 33 al. 2007). Additional research on the taxonomy and ecological associations of Cretaceous Lauraceae will assist paleobotanists as they map the evolution of this important angiosperm family in time and space. Due to several field campaigns since the 1990s, the biota of the Kaiparowits Formation (Upper Cretaceous, 76.6?74.5 Ma (Roberts et al. 2013)) is increasingly well known (see Titus et al. 2016, Titus and Loewen 2013). Fossils from this formation number in the thousands and are present in several major museum collections in the United States. Dinosaurian and associated vertebrate fauna, as well as aquatic and infaunal invertebrates, have been extensively described in At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah, edited by Titus and Loewen (2013). Large collections of megafossil plants, including leaves and wood, and palynoflora have been collected and are presently being described (Miller et al. 2013). The stratigraphy, sedimentology, and geochronology of the formation are increasingly well understood (Crystal et al. 2019, Roberts 2007, Roberts et al. 2005, Titus and Loewen 2013). Despite this growing body of work, insects, the most diverse group of animals and a cornerstone of terrestrial ecosystems, have not received much attention. Insect body fossils are poorly known worldwide from the Campanian (83.6?72.1 Ma) (Labandeira 2006b), particularly when compared with insect amber and compression-impression deposits from ca. 120 to 90 Ma (Grimaldi and Engel 2005, Ross 2015). Except for social insect nests (Roberts and Tapanila 2006), and dermestid beetle bone borings (Roberts et al. 2007), the diversity and ecological roles of Kaiparowits Formation insects, such as detritivores, predators and their prey, parasitoids, and herbivores are largely unknown. This provides an 34 opportunity to use insect-damaged leaves as a proxy for the guilds of herbivorous insects that existed in this ecosystem. The first paleobotanical exploration of the Kaiparowits Formation began in the late 1990s (Titus and Loewen 2013). The approach taken by the Denver Museum of Nature & Science (DMNS) team was to discover and extensively quarry sites with well-preserved fossil leaves to build a comprehensive collection of plant taxa as a baseline for future work. One highly productive locality (Lost Valley, DMNH loc. 4150), yielded more than 4,000 identifiable leaf fossils, all of which were collected and housed at DMNS. This collection included more than 1,500 specimens of the leaf morphospecies described in this paper, providing a rare opportunity to analyze insect damage on a very large sample of leaves from a single species. Using these fossils, we describe a new species within the family Lauraceae and document the evidence of plant?insect interactions on this new species as an indicator for the richness and intensity of insect herbivory within the middle Kaiparowits ecosystem. The aims for this study are threefold: 1) Describe and name the new taxon based on fossil leaves; 2) measure the richness and intensity of insect damage on the new taxon; are 3) compare the richness and intensity of insect damage to that of other Late Cretaceous taxa attributed to Lauraceae. Geologic and Biologic Setting The Kaiparowits Formation is located in south-central Utah, USA, largely within the newly diminished boundaries of the Grand Staircase-Escalante National Monument (Figure 2.1). The formation comprises ~1005 m of alternating sandstone 35 Figure 2.1. Map of the Grand Staircase-Escalante National Monument and the Kaiparowits Formation outcrop (green). Solid yellow denotes new monument boundaries (December 2017) and former monument areas are stippled in lighter yellow. DMNH loc. 4150, the Lost Valley locality, is denoted by a star. Adapted from Crystal et al. (2019). and mudstone beds from an array of depositional environments, including channels, lakes, and a variety of floodplain deposits that include crevasse splays, perennial ponds, and oxbow lakes (Roberts et al. 2005, Roberts et al. 2013) (Figure 2.2). The depositional environment of the Kaiparowits Formation is interpreted as an alluvial to coastal plain, with source material originating from the west along the Sevier orogenic belt and directed to the Western Interior Seaway in the east. 40Ar/39Ar dating from the Kaiparowits Formation provides an age of ~76.6?74.5 Ma (Roberts et al. 2013), placing it within the Campanian Age (83.6 to 72.1 Ma) of the Upper Cretaceous. Penecontemporaneous formations include the Dinosaur Park Formation 36 in Alberta, Canada, and the Two Medicine and Judith River formations of Montana, USA, among other paracontemporaneous formations from Mexico to Alaska. The paleoenvironment likely was extensively ponded and annually flooded, based on the paludal deposits, floral and faunal composition, leaf physiognomy (Miller et al. 2013), and isotopic composition of dinosaur teeth (Crystal et al. 2019). This interpretation, along with temperature estimates from fossil leaves, suggests the climate was humid and subtropical, similar to the present-day Gulf Coast or certain areas of Southeast Asia (Miller et al. 2013, Roberts 2007). The Kaiparowits Formation is informally divided into upper, middle, and lower units, as well as the newly described Upper Valley Member (Beveridge et al. 2020), with the middle unit producing the bulk of floral and faunal specimens. During the past ten Figure 2.2: Representative stratigraphic column for the Kaiparowits Formation redrawn from Roberts (2007) showing major sedimentary modes. The stratigraphic position of DMNH loc. 4150, where the type and referred material for C. gettyi was collected, was located by directly measuring section from the contact with the Wahweap Formation with the assistance of J. Hagadorn and M. Marshall in 2015. 37 years of field exploration, the authors have found and collected more than 100 megafloral localities within the formation. Most of these localities occur in the middle unit, which ranges stratigraphically from about 90?110 m at its base to about 550 m at its uppermost level within the formation (Roberts 2007). For the middle unit, the majority of megafloral localities are restricted to the stratigraphic interval between about 300 m and 450 m (Miller et al. 2013). Based on correlation to the local stratigraphic section for the Fossil Ridge area (Roberts et al. 2013), the Lost Valley Locality (DMNH Loc. 4150), is located in the middle unit of the Kaiparowits Formation, approximately 415 ? 10 m above its base. Using a depositional rate of 41 cm/1,000 years (Roberts et al. 2013), which was calculated using 40Ar/39Ar ages on sanidine crystals from volcanic ash beds, we estimate the age of DMNH Loc. 4150 at 75.6 ? 0.18 Ma. The error of this estimate was propagated from the error associated with the age on the nearest ash bed (Death Ridge Ash, (Roberts et al. 2013)) and the stratigraphic positions of the ash bed and the fossil locality. At DMNH Loc. 4150, leaves are preserved as compression-impression fossils in stacked 5?10 cm thick, fine-grained sandstone beds with minor mud partings. The depositional environment is interpreted as a medial to distal crevasse splay resulting from an event or events that infilled a perennial pond or small lake. Using the facies associations of Roberts (2007), the fossils occur in the FA5 stratum, which consists of minor tabular and lenticular sandstone, immediately above the FA9 stratum, which is carbonaceous mudstone. FA5 is interpreted as forming from crevasse splays and crevasse channels, whereas FA9 is interpreted as forming in swamp and oxbow lake environments (Roberts 2007). 38 Materials and Methods The plant megafossils from the Lost Valley locality (DMNH loc. 4150) were collected using standard bench-quarrying techniques. We collected all identifiable specimens and did not make a field census because the flora had not been previously sorted into morphotype categories. In the lab, the megafossils were sorted into morphotypes following the concept and procedure described by Johnson (1989). This method uses the morphological characters of disassociated plant organs, such as leaves, fruits, and stems, to circumscribe discrete operational taxonomic units prior to erection of a formal taxonomy. These morphotypes, based on multiple, well- preserved specimens, closely approximate biological species. We use the morphotype prefix, KP, to designate the Kaiparowits Formation, followed by a sequential listing of the number of morphotypes in the formation (see Miller et al. 2013). The Lost Valley locality (DMNH loc. 4150) contains 4,004 specimens identified to 101 morphotypes. The non-reproductive morphotypes include 8 ferns, 1 lycopod, 1 sphenopsid, 1 gymnosperm, and 59 angiosperms. The reproductive morphotypes include 31 seeds, fruits, and flowers. Of all specimens from this locality, 1,564 (~39%) were assigned to KP89 and formally described and named below. Specimens of KP89 that were more than a third complete were examined for insect- mediated damage. The majority of specimens were over fifty percent complete. A formal description of this taxon was erected to 1) advance our understanding of the Kaiparowits Flora; 2) provide a foundation for ecological analyses, described below; 39 and 3) allow for comparisons of specialized plant?insect associations between other, described Lauraceae taxa from the Late Cretaceous of North America. Insect herbivory was documented following a system of identification and classification frequently employed in plant?insect associational studies (Currano et al. 2010, Currano et al. 2008, Donovan et al. 2016, Donovan et al. 2014, Labandeira et al. 2002a, Labandeira et al. 2002b, Labandeira et al. 2007c, Wilf and Labandeira 1999). There are several criteria used to distinguish herbivore induced insect damage from other types of damage, such as physical damage resulting from tears occurring along leaf veins, detritivory involved in the consumption of dead tissue, or taphonomic processes that alter leaf tissue. The first criterion is the presence of reaction tissue. Reaction tissue often occurs as anomalous parenchymatous enlargement, such as callus, that results from hypertrophic (enlarged) or hyperplasic (multiplied) cells produced by the plant along insect damaged areas (Brues 1924, Johnson and Lyon 1991, MacKerron 1976, Vincent et al. 1990). A second criterion for insect damage is the targeting of a specific host-plant taxon or a particular plant organ that would be attributable to insect-specific patterns of damage. Examples of this type of damage are linear rows of punctures on or along primary veins, or small cusps occurring on the cut edge of a plant tissue (Gangwere 2017, Iannuzzi and Labandeira 2008, Kazakova 1985, Keen 1952). A third criterion is a repeated damage pattern based on shape, size, and position of the damage on the plant (Bodnaryk 1992, Heron 2003). After herbivore mediated damage was identified on the plant host, it was classified by feeding guild, or functional feeding group, and into specific, 40 diagnosable patterns of insect plant-tissue modification, the damage type (Labandeira et al. 2007c). Insect damage was scored following the Guide to Insect (and other) Damage Types on Compressed Plant Fossils (Labandeira et al. 2007c) and subsequent published and unpublished addenda. The damage was initially categorized into one of eight functional feeding groups: 1) hole feeding; 2) margin feeding; 3) surface feeding; 4) skeletonization; 5) piercing and sucking; 6) oviposition; 7) galling; and 8) leaf mining. Oviposition is not herbivory per se, but does represent damage to the foliar tissue of plants that elicits defense responses and has a persistent fossil record (ex. Gnaedinger et al. 2014, Laa? and Hoff 2015, Lin et al. 2019, Meng et al. 2019, Moisan et al. 2012, Vasilenko 2008). Similarly, galls may be created by insects, mites, nematodes, fungi, bacteria, or viruses (Mani 1964). Galls may be formed in conjunction with oviposition or maturation and may or may not be associated with herbivory (Meyer 1987), but are herein categorized as insect damage. Discrete, diagnosable damage types were documented within each functional feeding group and assigned a damage type (DT) number. Damage types are specifically defined, diagnosable effects of insect feeding on plants that are classified by the shape, size, extent, and location of herbivore damage on the affected leaf (Labandeira et al. 2007c). Damage types are rated for host specificity: 1 or generalized (polyphagous), 2 or intermediate (oligophagous), and 3 or specialized (monophagous) (Labandeira et al. 2007c). The convergence of herbivore mouthparts and feeding behaviors make genus or species level identifications of the insect culprit rare. Except for some margin feeding, most leaf mines, most galls, and many scale-insect feeding marks 41 that are traceable to lineages with living representatives (ex. Jud and Sohn 2016, Sarzetti et al. 2008, Wappler and Ben-Dov 2008, Wilf et al. 2000, Winkler et al. 2010). Herbivory data collected from insect damaged leaves includes both qualitative and quantitative data. The qualitative data, outlined above, determine the overall insect feeding guilds on a particular host-plant taxon, the richness of damage types, host specificities, and occasionally identities of the phytophagous insect responsible for the damage (see Chapter 4). Quantitative data collection consisted of three basic metrics: 1) the proportion of damaged leaves, 2) the richness of damage types, and 3) the percent of surface area herbivorized by insects (herbivory index). For calculating the surface area of leaf tissue herbivorized by insects, a subset of 156 specimens of the new taxon (10% of total specimens) was randomly selected using the random number generator package ?Rando? for R statistical software (R Development Core Team 2013). Four additional taxa attributed to the family Lauraceae from the Hell Creek Formation by Johnson (2002) were included in the final analysis: Marmarthia pearsonii (DMNH loc. 900), Marmarthia trivialis (DMNH loc. 428), ?Artocarpus? lessigiana (DMNH loc. 428), and ?Ficus? planicostata (DMNH loc. 428) (Hartman et al. 2002, Johnson 2002). Each Hell Creek Formation taxon with a sample size of at least 20 specimens from a single locality was analyzed for insect damage as outlined above. Comparisons were made to these taxa to provide context for the level of 42 herbivory on the Kaiparowits laurel described herein, as well as to determine if there are any specialized damage types that persist throughout the Late Cretaceous. Detailed photographs were taken using a Canon EOS 50D camera with a Canon EF-D 60mm f/2.8 macro lens and microphotographic images were taken using an Olympus DP25 camera attached to an Olympus SZX12 microscope. Digital images were processed using Adobe Photoshop CC? (2017.01) and Zerene Stacker? software. Surface area for all five taxa in this study was measured using Adobe Illustrator Draw? for iPad Pro and ImageJ (Rasband 2012). Plates were created using Adobe InDesign CC? (2017.1). Sample-based rarefaction was calculated for the damage type richness and sampled surface areas of the plant hosts, as it allows for comparisons of insect damage richness between taxa. Rarefaction by total sampled surface area was used instead of number of specimens because this standardizes differences in leaf size and leaf completeness between species. A rarefaction analysis and curve were created using code developed by S. Schachat (Schachat et al. 2018, Schachat et al. 2020) for R statistical software (R Development Core Team 2013). Rarefaction curves were bootstrapped 5,000 times to generate 95% confidence intervals. Herbivory index was calculated for the Hell Creek and Kaiparowits taxa and 95% confidence intervals were bootstrapped 10,000 times. Nonmetric multidimensional scaling (NMDS) ordinations, which used a Bray- Curtis dissimilarity matrix, were produced via the metaMDS function of the vegan package, in R version 3.1.2 (R Development Core Team 2013), also used in previous studies (Maccracken and Labandeira 2020, Schachat et al. 2015). NMDS plots 43 represent the positions of data in multidimensional space and allow for visual comparisons between plant hosts. The NMDS plot was produced with the R package ggplot2 (R Development Core Team 2013). To standardize for sampling effort and to quantify uncertainty, each of the Kaiparowits and Hell Creek taxa were subsampled 500 times to a given amount of surface area. This process was repeated nine times, setting the seed in R from 1 to 9. For the first series of NMDS plots, all five taxa were subsampled to 850 cm2 of surface area; ?A.? lessigiana is represented by 884.85cm2 of surface area. For the second series of NMDS plots, ?A.? lessigiana was removed from the dataset and the remaining four taxa, which are represented by between 1420.36 and 1707.48 cm2 of surface area, were subsampled to 1400 cm2 of surface area. Ellipses contain 84% of points closest to the centroid of each taxon and represent 84% confidence intervals. Results Leaf Morphology and Systematics Leaves of the new fossil taxon are herein described based on specimens exhibiting a range of vein preservation, leaf arrangement and attachment, and leaf shape. A formal description is forthcoming in a peer-reviewed journal and all future work citing this new genus and species should reference that publication (Maccracken et al. in review-a). 44 SYSTEMATICS Order: Laurales (Juss. ex Bercht. & Presl, 1820) Family: Lauraceae (Jussieu, 1789 nom. cons.) Catula Maccracken, Miller, Johnson, Sertich, Labandeira, gen. nov. Generic diagnosis. Leaves simple; when attached, distichous, exhibiting opposite or slightly subopposite arrangement and axillary buds. Lamina primarily ovate, occasionally elliptic, or rarely obovate; nearly always slightly asymmetrical in the apex, middle, and base of the leaf. Overall, leaves are highly variable in length, width, and size leading to considerable variation in shape. Leaf margin entire and unlobed. A fimbrial vein observable in well-preserved specimens. Leaf apex typically acute and often exhibiting a mucronate termination. Leaf base typically acute and markedly decurrent, with laminar tissue extending down the petiole. Primary venation pinnate. Secondary venation simple brochidodromous; associated with simple agrophic veins. Secondary veins basally crowded to form 1 or 2 pairs of acute basal secondary veins. Tertiary venation opposite percurrent with a variety of courses and an inconsistent angle relative to the primary vein. Exterior tertiary veins and ultimate observable venation looped. Higher order venation more or less disorganized and the leaf rank is 2r. Quaternary vein fabric regular to irregular reticulate and quinternary vein fabric irregular reticulate. No cuticular or fertile material has been recovered or associated with these leaf fossils. 45 Derivation of the generic name. From the masculine noun catulus, a Classical Latin noun meaning a young animal (Pliny), especially a young dog, puppy or whelp (Cicero, Lucretius, Vergil). The genus epithet is, in part, named for Mike Getty?s dog, Javelina, who also answers to the name, Puppy. The diminutive suffix ?ulus/-a also describes the small size of many of the leaves in this genus. Catula gettyi Maccracken, Miller, Johnson, Sertich, Labandeira, sp. nov. Figures 2.3 A?E, 2.4 A?C, Supplementary Figure 2.1 A?G. Specific diagnosis. Same as the generic diagnosis by monotypy. Holotype. Designated here: DMNH 54376 (Figure 2.3 A?E). Paratypes. Designated here: DMNH 54378 (Figure 2.4 A, B ? stem with many attached leaves), DMNH 54377 (Figure 2.4 C ? stem with 3 attached leaves), DMNH 41570 (Supplementary Figure 2.1 A ? single leaf), DMNH 54371 (Supplementary Figure 2.1 B ? single leaf) DMNH 54379 (Supplementary Figure 2.1 C ? single leaf) DMNH 54370 (Supplementary Figure 2.1 D ? single leaf) DMNH 41584 (Supplementary Figure 2.1 E ? single leaf) DMNH 41567 (Supplementary Figure 2.1 F ? single leaf) DMNH 54380 (Supplementary Figure 2.1 G ? single leaf). Other figured specimens. Figures 2.7 ? 2.14 Derivation of the specific epithet. In recognition of Michael A. Getty for his nearly two decades of incredible support and leadership in uncovering the paleontological treasures of Grand Staircase-Escalante National Monument. 46 Figure 2.3 (A?E): Overall and detail images of the holotype specimen (DMNH 54376, DMNH loc. 4150) of Catula gettyi Maccracken et al. gen. et sp. nov. (A) Complete leaf. (B) Detail showing upper left section of the leaf with looping and simple brochidodromous secondary venation. The dark area on the leaf is a blotch mine. The primary vein of the leaf parallels the right side of the figure. (C) Detail showing a medial section on the right side of the leaf, with the primary vein on the left side of the figure. Note the epimedial tertiary veins with variable course, and the irregular to regular reticular quaternary venation. (D) Detail showing lower left section of the leaf with simple agrophic veins, looping ultimate marginal venation, and a fimbrial vein. (E) Detail showing the base of the leaf with 2 pairs of acute basal secondary veins and laminar tissue extending down the petiole. Note the decrease in the primary vein width with the departure of the secondary veins. All scale bars = 0.5 cm. Source, age, and stratum. Catula gettyi is found throughout middle unit of the Kaiparowits Formation spanning perhaps as much as 1 myr. All C. gettyi specimens are housed at the Denver Museum of Nature & Science. Precise GPS locality information is available upon request. 47 Description. Catula gettyi occurs mostly as isolated leaves, while a few specimens show leaves attached to stems. Leaf attachment petiolate; leaf arrangement opposite to subopposite, appearing distichous; even and odd pinnate terminus on the stem; leaf organization simple. Auxiliary buds present in leaf axils. Petiole twisted, sometimes flanked with a thin wing of laminar tissue from the blade; petiole base slightly swollen. Blade attachment marginal. Laminar size notophyll, rarely nanophyll to mesophyll; laminar length variable but generally 4 to 8 cm; laminar width variable but generally 2.5 to 4.5 cm; laminar length to width ratio generally 1:1.0 to 3:1; laminar shape ovate or occasionally elliptic, or rarely obovate; medial symmetry slightly asymmetrical, rarely symmetrical. Laminar base slightly asymmetrical, rarely symmetrical, occasionally with a slight asymmetrical basal insertion; base angle acute; base shape decurrent. Laminar apex angle acute, rarely obtuse; apex shape straight to acuminate; laminar apex with a mucronate termination in some specimens, otherwise appearing slightly retuse. Leaf margin entire, unlobed; laminar edge appearing thickened or with an observable fimbrial vein of tertiary or higher order; laminar surface texture appearing smooth. Primary venation pinnate; thickness of primary vein up to ~1.3mm; course of primary vein approximately straight; primary vein markedly decreases in width after giving rise to major secondary veins, particularly near the base of the leaf. Secondary vein organization simple brochidodromous; agrophic veins present, simple; 1?5 or rarely 7 basal veins including both primary and secondary veins; naked basal veins present, of secondary or tertiary vein order; spacing of secondary veins on primary vein decreases proximal to the leaf base, forming 1 or 2 pairs of acute basal secondary veins; typically 4 pairs 48 Figure 2.4 (A?C): Paratype specimens of Catula gettyi. (A) Attached leaves of C. gettyi on a stem showing opposite leaf attachment, probable distichous arrangement, and an odd-pinnate leaf terminus (DMNH 54378). Scale bar = 1 cm. (B) Enlarge section of dashed inset box in Figure 2.4 a showing leaf attachment (DMNH 54378). Arrows highlight axillary buds. Scale bar = 0.5 cm. (C) Attached leaves of C. gettyi on a stem showing opposite leaf attachment and an odd-pinnate leaf terminus (DMNH 54377). Scale bar = 1 cm. of secondary veins; angle of secondary vein departure from primary vein acute; secondary vein course generally arching towards leaf apex, decurrent on the primary vein, course deflected at the origin of minor secondary veins; minor secondary vein course simple brochidodromous; interior secondary veins absent; intersecondary veins absent. Intercostal tertiary vein organization opposite percurrent and sinuous to convex; tertiary vein course angle with respect to the primary vein acute; tertiary vein angle variability with respect to the primary vein inconsistent. Epimedial tertiary veins alternate percurrent; proximal course acute to the midvein, distal course basiflexed. Exterior tertiary course looped. Quaternary vein fabric regular to irregular 49 reticulate. Quinternary vein fabric irregular reticulate. Higher order venation obscured. Marginal ultimate venation appearing looped. No cuticular or fertile material recovered or associated with these leaf fossils. Remarks. We compared the Catula gettyi specimens to Cretaceous through Eocene leaves (e.g. Berry 1925, Brown 1962, Hickey et al. 2006, Johnson 1996, 2002, Knowlton 1900, Lesquereux 1878, Manchester 2014). Despite the abundance of fossil ?lauroid? leaves in the literature, we found few favorable matches. Of the fossils most similar to C. gettyi were fossils assigned to the extant genus Cinnamomum in the Lauraceae. In particular, ?Cinnamomum? newberryi Berry (1925) and ?Cinnamomum? newberryi ellipticum Berry (1925) from the Maastrichtian Ripley Formation in Texas are similar in many aspects to C. gettyi but differ by having a more narrow leaf shape, prominent agrophic veins and better organized opposite percurrent epimedial tertiaries with more or less straight courses. ?Cinnamomum? affine Lesquereux in Knowlton (Knowlton 1900) from the Campanian Mesaverde Formation, and ?C.? affine Lesquereux (Lesquereux 1878) from the Maastrichtian Laramie Formation share characters with C. gettyi based on leaf shape and two pairs of acute, basal, secondary veins, but differ by exhibiting better organized opposite percurrent epimedial tertiaries with straight courses. The lauraceous taxon Marmarthia pearsonii Johnson (Johnson 1996) from the Maastrichtian Hell Creek Formation resembles C. gettyi, particularly from the perspective of higher order venation and overall low leaf rank. However, M. pearsonii differs from C. gettyi by having primary venation that is basal acrodromous as opposed to pinnate, only one pair of prominent basal veins (primary or secondary), more prominent epimedial 50 tertiary veins, and a naked base. Finally, ?Cinnamomum? linifolium Knowlton (Knowlton 1917) from the Paleocene Raton Formation bears resemblance in overall shape and primary and secondary venation to C. gettyi, but the specimens are too poorly preserved for taxonomic comparison outside the formation. We have assigned C. gettyi to Lauraceae based on the combination of the following characteristics. Catula gettyi has simple leaves, distichous and opposite or slightly subopposite leaf arrangement with axillary buds, entire margins, pinnate primary venation, simple brochidodromous secondary venation, and a markedly decurrent base with 1 or 2 pairs of acute basal secondary veins. While this set of characters is perhaps not unique to Lauraceae, we are confident, based on the current material, that the familial placement is warranted. In Lauraceae, C. gettyi exhibits a leaf shape and primary, secondary, and tertiary venation consistent with species in extant Cinnamomum (see Klucking 1987). Several workers have argued that Cinnamomum exhibits two characteristic primary venation patterns (Hernandez 1997, Lorea-Hernandez 1997, Ravindran et al. 2003): acrodromous venation typified by Cinnamomum verum (cinnamon), and pinnate venation typified by Cinnamomum camphora (camphor). We examined herbarium sheets of 133 species of Cinnamomum (~38-53% percent of the 250 (Ravindran et al. 2003) to 350 (Rohwer 1993a) species) in the Smithsonian?s National Museum of Natural History virtual botany collections and the New Botanical Gardens Steere Herbarium C.V. Starr Virtual Herbarium and found additional support for these venation patterns, plus a third pattern. These patterns are: 1) an acrodromous primary venation pattern that with weakly expressed brochidodromous to eucamptodromous 51 secondary veins and prominent, usually well-organized opposite percurrent tertiary veins. 2) A pinnate primary venation pattern with prominent basal secondary veins that have an acrodromous or brochidodromous course. In the distal portions of these leaves, additional well-defined brochidodromous secondary veins occur. Tertiary veins in this category are typically alternate percurrent to mixed opposite and alternate percurrent. And 3) a pinnate venation pattern that does not have prominent basal secondary veins. Secondary veins in this category are typically of the same gauge or are reduced in gauge uniformly from the base of the leaf to the apex. Tertiary veins in this category range considerably in course and organization. Considering these venation patterns, Catula gettyi appears more closely allied with the ?intermediate? category exhibiting pinnate venation with prominent basal secondary veins. The 15 most comparable taxa that we observed are listed in Supplementary Table 2.1 (Appendix B). While C. gettyi compares favorably to these taxa, there are notable differences in vein organization. Collectively, these differences show that the veins of C. gettyi are less organized, leading to an overall lower leaf rank (Hickey and Doyle 1977), than any taxa we observed in Cinnamomum. Given the poorly organized leaf venation of C. gettyi, and without floral, epidermal, and petiolar/laminar (e.g. domatia) characters (e.g. Ravindran et al. 2003) to place the new taxon in Cinnamomum, we have elected to erect the new genus and species Catula gettyi. Catula gettyi represents the single most abundant leaf megafossil found in the Kaiparowits Formation based on the current collection at the Denver Museum of Nature & Science. In many proximal crevasse-splay floras from the formation, C. 52 gettyi is the dominant taxon. While a comprehensive analysis of splay, channel, and pond floras in the formation has yet to be completed, it nonetheless appears that C. gettyi tracks stream margins, and thus disturbed, environments in the formation. Insect Herbivory on Catula gettyi We identified 40 distinct patterns of herbivore damage (DTs) on Catula gettyi leaves at Lost Valley (DMNH loc. 4150) (Table 2.1; Figure 2.5). A total of 863 damage-type occurrences were present and the percentage of C. gettyi leaves with at least one type of insect damage at this locality was 38.75% (606 damaged specimens, including some specimens with multiple damage types). For 156 randomly selected C. gettyi leaves, the herbivory index, or the percentage of herbivorized surface area is 2.102% (Figure 2.6). The 95% confidence interval ranges from 1.36% to 3.03%. Rarefaction was calculated for damage types and total sampled surface area (156 specimens subsampled, 2,985.841 mm2). Table 2.1: Richness of damage types by functional feeding group and host plant specialization on Catula gettyi. Abbreviations are: HF, hole feeding; MF, margin feeding; SK, skeletonization; SF, surface feeding; PS, piercing and sucking; OV, oviposition; LM, leaf mining; and GL, galling. Host plant specificity Damage Types HF MF SK SF PS OV LM GL Total Generalist 6 3 1 3 0 0 0 0 13 Intermediate 5 3 3 1 0 1 0 2 15 Specialist 0 0 1 0 4 0 5 2 12 Total 11 6 5 4 4 1 5 4 40 53 Figure 2.5: Histogram of all damage types encountered on Catula gettyi by functional feeding group. Red bars = generalist host specificity, gold bars = intermediate host specificity, and green bars = specialized host specificity. 54 Figure 2.6: Herbivory index for the subsampled Catula gettyi dataset with 95% confidence intervals. The ectophytic functional feeding groups of hole feeding, margin feeding, skeletonization, and surface feeding, were the most diverse and abundant modes of feeding on C. gettyi, with a total of 26 distinct damage types and 498 occurrences. There were 14 damage types and 365 damage-type occurrences of endophytic functional feeding groups (i.e. piercing and sucking, oviposition, mining, and galling) on C. gettyi. In addition, the presence of fungal necroses is commonly associated with insect herbivory; however, no clear insect-mediated fungal damage was encountered on C. gettyi, as it was difficult to distinguish fungus from discoloration associated with decay and burial. Fungus was most commonly found on poorly preserved and physically damaged specimens, which indicates that fungal attack occurred post- senescence. Hole Feeding. ? Hole feeding is the consumption of a leaf, which includes the entire thickness of the lamina and does not reach the leaf margin. Hole feeding on Catula gettyi is common and diverse, with eleven damage types and 207 occurrences of DT1, DT2, DT3, DT4, DT5, DT7, DT8, DT9, DT51 and DT64 (Figure 2.7). Circular hole 55 Figure 2.7 (A?J): Eleven hole-feeding damage types found on Catula gettyi produced by mandibulate insects: (A) DT1; Circular holes under 1mm in diameter (DMNH 41564); (B) DT2; Circular holes between 1 mm and 5 mm in diameter (DMNH 41580); (C) DT4; Circular holes greater than 5 mm in diameter (DMNH 41596); (E) DT3; Polylobate holes between 1 mm and 5 mm in diameter (DMNH 41576); and (H) DT5; Large polylobate holes over 5 mm in diameter (DMNH 41583). Less common hole-feeding types consist of (G) DT7 & DT8 (DMNH 41590); Rectilinear holes and slot feeding, respectively (DMNH 41590); (F) DT9; Scattered, comma-shaped holes (DMNH 39733); (D) DT64; Holes located along the margin of the leaf (DMNH 41584); (I) DT51; Overlapping slot feeding holes (DMNH 41571); and (J) DT50; A series of holes associated with a primary vein (DMNH 41574). Black scale bars= 5 mm; white scale bars= 1 mm. 56 feeding damage types include holes below 1 mm in diameter (DT1) (Figure 2.7 A), holes between 1 mm and 5 mm in diameter (DT2) (Figure 2.7 B), holes above 5 mm in diameter (DT4) (Figure 2.7 C), and a series of three or more circular holes along the leaf margin (DT64) (Figure 2.7 D). Polylobate hole feeding includes holes between 1 mm and 5 mm (DT3) (Figure 2.7 E), and holes over 5 mm in diameter (DT5) (Figure 2.7 H). DT7 are rectilinear feeding (Figure 2.7 G); DT51 consists of overlapping slot feeding (Figure 2.7 I); and DT9 are elliptical to comma-shaped holes scattered across the leaf surface (Figure 2.7 F). Finally, DT50 is a linear series of holes alongside a primary or secondary vein that occur on one side or on alternating sides (Figure 2.7 J). Margin Feeding. ? Margin feeding is the consumption of the entire thickness of the lamina along the leaf edge by a chewing phytophagous insect. The six distinct margin-feeding damage types on C. gettyi specimens are DT12, DT13, DT14, DT15, DT198 and DT214 (Figure 2.8). DT12 is the cuspate and moderately incised, and isolated removal of tissue at the leaf margin; it represents the most common damage type on C. gettyi (Figure 2.8 C). DT13 is the removal of tissue at the leaf apex (Figure 2.8 B), whereas DT14 is the removal of leaf tissue along the margin and to the primary vein (Figure 2.8 A). DT15 is a deeper, trenched incision that is deeply incised and is parallel sided or expands towards the primary vein (Figure 2.8 D), whereas DT198 also is a deep incision but narrows medially (Figure 2.8 E). DT214 is a series of cuspate feeding traces with three or more, distinctively shaped, scalloped incisions (Figure 2.8 F). 57 Figure 2.8 (A?F): Margin feeding damage types found on Catula gettyi at the Lost Valley Locality: (A) DT14; Excision of the leaf to the primary vein (DMNH 41575); (B) DT13; The removal of the apex of leaf by the insect (DMNH 41578); (C) DT12; A common semi-circular excision of the leaf margin (DMNH 41579); (D) DT15; An excision that expands medially (DMNH 41585); (E) DT198; A deep, narrow excision with broad reaction tissue surrounding the herbivorized section (DMNH 41595); and (F) DT214; Multiple, connected excisions along the leaf margin (DMNH 41586). Black scale bars= 5 mm; white scale bars= 1 mm. 58 Skeletonization. ? Skeletonization is similar to hole feeding via consumption of the entire thickness of the leaf, but the veins remain intact, often creating a lace-like appearance. The five skeletonization damage types on C. gettyi are DT16, DT19, DT22, DT24, DT61 and DT333 (Figure 2.9). DT16 is the most frequently encountered skeletonization damage type and is the nondescript removal of laminar tissue with veins remaining undamaged but lacking a reaction rim of tissue produced by the plant host (Figure 2.9 E). DT19 damage consists of elongate, rectilinear patches of skeletonized tissue with a length-to- width ratio of 2.5 or greater (Figure 2.9 B). DT22 are linear or curvilinear, elongate skeletonized areas parallel to and along the leaf margin (Figure 2.9 A). DT61 is composed of an elongate swath of skeletonization that occurs on one side of a primary or secondary vein (Figure 2.9 D); by contrast, DT24 are three or more circular, skeletonized areas adjacent to a primary or secondary vein (Figure 2.9 C). Surface Feeding. ? Surface feeding is the consumption of one or more layers of surface tissues but not the entire blade thickness and occurs on either the abaxial or adaxial surface of the leaf lamina. The three examples of surface feeding damage types on Catula gettyi are DT29, DT30 and DT31, and one previously undescribed damage type of DT333 (Figure 2.10). DT29 is a commonly occurring, circular to polylobate area of surface-feeding damage that is recognizable by the absence of or minimal development of reaction tissue around the perimeter of the feeding zone (Figure 2.10 E). In contrast, DT30 has a well-developed reaction rim with a polylobate margin bordering the surface abrasion patch (Figure 2.10 D), whereas DT31 has a circular bordering margin and also a well-developed reaction rim (Figure 59 2.10 C). The new surface feeding DT333 consists of polylobate surface abrasions nestled between primary and secondary veins, which leave primary, secondary, and third order venation intact (Figure 2.10 A,B). This damage type is similar to some skeletonization damage types if the fossil leaf counterpart is not preserved; however, inspection of the undamaged side of the laminar tissue clearly reveals that surface feeding is confined to one surface of the leaf. Figure 2.9 (A?E): Skeletonization, the removal of tissue between veins, is represented by five damage types in the Catula gettyi: (A) DT22; Skeletonization which follows a primary vein (DMNH 41565); (B) DT19; Broad swaths of skeletonized tissue in a rectilinear shape (DMNH 41568); (C) DT24; Circular areas of skeletonization adjacent to the primary vein (DMNH 41578); (D) DT61; Elongate areas of skeletonization adjoining primary and secondary venation (DMNH 41591); and (E) DT16; Unadorned and common areas of tissue removal between veins (DMNH 41594). Black scale bars= 5 mm; white scale bars= 1 mm. 60 Figure 2.10 (A?E): Surface feeding on Catula gettyi at the Lost Valley Locality consists of three previously known damage types and one new damage type: (A,B) DT333 (DMNH 39725); This new damage type (DT) entails large areas of herbivory in which one surface of the leaf is removed and third-fourth order venation is left intact. Part A exhibits the rank of undamaged venation and does not have surface tissue removed. Counterpart B illustrates the tissue removal and the presence of intact third and fourth order veins. The other three surface feeding damage types are: (C) DT31; Removal of surface tissue with a distinct circular to ellipsoidal reactions rim (DMNH 41589); (D) DT30; Surface feeding with a polylobate reaction rim (DMNH 41566); and (E) DT29; Surface feeding with a weak reaction rim (DMNH 41593). Black scale bars= 5 mm; white scale bars= 1 mm. 61 Piercing and Sucking. ? Piercing-and-sucking insects puncture and suck foliar tissues, such as epidermis, mesophyll, phloem, and xylem. This fluid feeding is accomplished by use of mouthpart elements modified into elongate stylets, often encompassed by an external sheath. There are four piercing and sucking damage types on C. gettyi, including the two previously described damage types of DT46 and DT47, and the two recently described damage types of DT219 and DT330 (Figure 2.11). The most common piercing and sucking damage was DT46 (Figure 2.11 B). This damage type consists of one to several concave punctures with an approximate random distribution. DT47 includes many convex punctures that are irregularly distributed along and between secondary veins (Figure 2.11 C). A newly described DT330 consists of a large number (> 50) of punctures covering a substantial portion of the lamina, frequently blanketing smaller areas in a dense sheet (Figure 2.11 D). These punctures occur along, veins of all ranks from primary to tertiary as well as vein inter-areas. These punctures differ from oil glands in that they are more irregular in size and shape and have a highly patchy distribution on the leaf surface. The enigmatic DT219 is a distinct piercing-and-sucking pattern that consists of two parallel, mirrored lines of punctures indicating a directionality to movement as the putative insect moved across the lamina surface (Figure 2.11 A). Although the identity of this insect herbivore remains unknown, it is possible that this feeding damage represents a sap feeder with mandibulate mouthparts. Because the punctures are paired and evenly spaced, they could be the result of paired mandibles puncturing the leaf surface, followed by ingestion of leaf exudate. Descriptions of this damage 62 Figure 2.11 (A?D): Insect damage caused by piercing-and-sucking insects. (A) DT219; This damage type (DT) consists of two mirrored lines of puncture marks, which are potentially made by mandibles (DMNH 39724). Additional evidence of piercing-and-sucking insects comes from circular, concave puncture marks DT46 (B) (DMNH 41590); and circular, convex puncture marks DT47 (C) (DMNH 41588). A second new piercing and sucking damage type (D) involves many puncture marks across large portions or the entirety of the leaf lamina (DT330) (DMNH 41569). Scale bars= 1 mm; arrows indicate a single puncture for clarity. 63 type were figured in two previous studies and redescribed herein. The first description of this unique damage type was from the Late Cretaceous of Israel (Krassilov 2007), which was incorrectly diagnosed as a possible agromyzid leaf-mine damage. We find no evidence of leaf mining for DT219. This type of damage was subsequently identified as surface feeding and described as paired mandibulate ?chew marks? of Araciphyllites tertiaries, a monocot from the middle Eocene Messel Formation (Wappler et al. 2012). We agree with this latter description, but have reassigned this DT219 to the piercing-and-sucking functional feeding group. Oviposition. ? Oviposition is the deposition of eggs into plant tissue, accomplished by a slicing or piercing insect ovipositor. Oviposition lesions are uncommon on C. gettyi leaves. There is one oviposition damage mode, DT101, with only three occurrences of all examined C. gettyi specimens (Figure 2.12 D). All three occurrences are represented by one to four oval lesions, replete with robust reaction rims. Mining. ? The most notable and distinctive insect damage type exhibited on C. gettyi are leaf mines, which are produced by several lepidopteran (moth) miners (Figure 2.13). There are three types of blotch mines, DT35, DT36 and DT37 (Figure 2.13 F?H), and the two serpentine mines of DT45 and DT332 on C. gettyi (Figure 2.13 A?E). The new leaf-mine DT332 is exceptionally abundant on this taxon, occurring on 112 leaf specimens, despite being previously unknown in the fossil record (Figure 2.14). The oviposition site for DT332 mines generally occurs along the leaf margin, and up to seven individual mines may occur on the same leaf specimen. The mines range from 1.4 to 7.1 mm at the broadest width of their mine trajectory. 64 Figure 2.12 (A?D): Galling and oviposition damage on Catula gettyi. (A) DT33 & DT34; Galls located on primary veins and secondary veins, respectively (DMNH 41577). (B) DT32; Galls located on the laminar surface, but avoiding primary and secondary venation (DMNH 41573). (C) DT85; Galls located on the petioles of leaves or petiolules of leaves (DMNH 41592). (D) DT101; Oviposition consists of multiple, scattered ovate-shaped scars produced by an insect bearing a robust ovipositor (DMNH 41570). Black scale bars= 5 mm; white scale bars= 1 mm. 65 b c a d e f g h Figure 2.13 (A?H): Leaf mining insect damage at the Lost Valley Locality, Kaiparowits Formation, Utah. (A?E) DT45; Leaf mines attributed to the lepidopteran family Gracillariidae. These five mines illustrate the variation in overall shape, projection, and length, potentially due to the number of instars completed during the mining life history stage (A: DMNH 39732; B: DMNH 41582; C: DMNH 39735; D: DMNH 47124; E: DMNH 39733). The three types of blotch mines include: (F) DT36; A blotch mine lacking internal frass and a central chamber (DMNH 41572); (G) DT35; A blotch mine with frass present in circular central chamber (DMNH 41581); and (H) DT37; A blotch mine with an internal serpentine phase (DMNH 39734). Black scale bars= 5 mm; white scale bars= 1 mm. The earlier instars produce a minuscule, broadly serpentine shaped mine (Figure 2.14 H?J), while later instars produce a tightly sinuous, intestiniform pattern that often becomes blotch-shaped (Figure 2.14 A?G). Although the insect culprit is unknown, an analogous mine morphology currently appears on several plant hosts today, such as the leaf miners in the genera Bucculatrix Zeller 1839 (Lyonettidae) (Opler 1982), 66 which are similar in size, trajectory, and position compared to DT332 on C. gettyi. Based on overall similarities to modern leaf mining moths, including mine size, non- overlapping mine trajectories and presence of solid frass, we posit that DT332 was created by a microlepidopteran leaf miner such as Bucculatrix or a related form (Hering 2013, Winkler et al. 2010). The second, most common leaf-mine is DT45, with 122 specimens on C. gettyi, exhibiting one to four mines per leaf (Figure 2.13 A?E). This mine is attributed to the lepidopteran leaf mining family Gracillariidae and was first described by Labandeira and colleagues (Labandeira et al. 2002a, Labandeira et al. 2007c) on specimens of the lauraceous Marmarthia pearsonii from the late Maastrichtian Hell Creek Formation (66 Ma) of the Williston Basin in North Dakota, USA. The DT45 mine on C. gettyi has a characteristic oviposition site and is initially thread-like and highly coiled, then is succeeded by repeated curvilinear phases, and ends in a sub- rectilinear to ovoidal terminal chamber. Frass is packed and is deployed continuously throughout the serpentine phases of the mine trajectory, with thick, modified bordering tissue constituting roughly 25% of the mine width on both sides of the frass trail. This mine generally is confined between primary and secondary veins, although this feature is variable on smaller leaves. DT45 varies substantially in size and length, which may be attributed to conspecific aborted mines and behavioral differences in larval instar activities. 67 b c a d e g h f i j Figure 2.14. (A?J): New leaf mine damage type on Catula gettyi. DT332 includes a range of leaf mine shapes, including (A) roughly circular mines with serpentine trajectories visible within the mine (DMNH 39726), close up of mines outlined (B, D); (E) leaf mines with a circular chamber and no evident serpentine trails (DMNH 41587); (C) a linear phase followed by a solid, circular chamber (DMNH 47126), (F) (DMNH 39737), close up of mine outlined (G,I) (DMNH 41597); and (H) (DMNH 41597), (J) (DMNH 41597) mines with linear trajectories. Differences in mine form are likely attributable to the number of instars completed by each individual. These mines are typically found along the margin of C. gettyi leaves. Black scale bars= 5 mm; white scale bars= 1 mm. 68 Three blotch-mine damage types are found on C. gettyi leaves in the Lost Valley Locality. DT36 is the most frequently encountered of the blotch mine damage types (Figure 2.13 F). The DT36 mine consists of variously shaped compartments that lack a central chamber and sometimes contain spheroidal fecal pellets among the frass (Labandeira et al. 2007c). A similar mine is DT35, a blotch mine with a central chamber present, also commonly associated with spheroidal frass (Figure 2.13 G). The third blotch mine, DT37, consists of a polylobate shaped blotch with an internal serpentine stage (Figure 2.13 H). Galling. ? Galls are envelopes of plant tissue that are induced and inhabited by insects, mites, nematodes, fungi, or bacteria. Insect galls generally consist of a hardened outer wall for protection and an inner layer of softer nutritive tissue connected to the host-plant organ by vascular tissue, all of which encapsulate an innermost chamber or chambers (Meyer 1987). The four gall damage types on C. gettyi are located on the leaf lamina, consisting of nondescript DT32, DT33 and DT34, and the petiole gall DT85 (Figure 2.12). DT32 consists of circular to ellipsoidal galls occurring on the leaf lamina and avoidance of major veins (Figure 2.12 B). DT33 and DT34 represent galls similar in form to DT32, but instead occur on secondary veins and primary veins, respectively (Figure 2.12 A). The distinctive DT85 is small, lenticular to ellipsoidal gall situated lengthwise along a midrib or petiole, with indistinct inner nutritive tissue and a thick, dark outer wall located on the petiole of C. gettyi (Figure 2.12 C). 69 Insect Herbivory on Late Cretaceous Laurels The four Maastrichtian-aged laurel taxa (Marmarthia pearsonii, M. trivialis, ?Artocarpus? lessigiana, and ?Ficus? planicostata) and the Campanian-aged Catula gettyi had comparatively similar damage-type richnesses (Figure 2.15). The 95% confidence intervals of all five taxa overlapped in the rarefaction analysis for damage- type richness by total surface area. Intensities of insect herbivory, i.e. herbivory index, were also relatively similar among four of the five taxa (Table 2.2; Figure 2.16). Herbivory indices ranged between 2.86% and 0.37%, with 95% confidence intervals overlapping for all taxa except ?A.? lessigiana, which has a lower herbivory index than C. gettyi and M. trivialis (Figure 2.16). Figure 2.15: Rarefaction of damage types and total sampled surface area for Catula gettyi and the four Hell Creek taxa (Marmarthia pearsonii, M. trivialis, ?Artocarpus? lessigiana, and ?Ficus? planicostata). 70 2) Figure 2.16: Herbivory indices of four Hell Creek taxa (?Ficus? planicostata, Marmarthia trivialis, M. pearsonii, and ?Artocarpus? lessigiana) and Catula gettyi. Confidence intervals are set at 95%. Table 2.2: Comparisons of herbivory between Late Cretaceous taxa in the family Lauraceae: Catula gettyi (Kaiparowits Formation, 75.6 Ma), and the Hell Creek taxa (66.5 Ma) Marmarthia pearsonii (Loc. 428), M. trivialis (Loc. 900), ?Artocarpus? lessigiana (Loc. 428), and ?Ficus? planicostata (Loc. 428) (Labandeira et al. 2002a). Catula Marmarthia Marmarthia ?Artocarpus? ?Ficus? gettyi* trivialis pearsonii lessigiana planicostata Number of 156 67 167 32 23 specimens analyzed for surface area Proportion of 40.76% 47.76% 20.40% 21.88% 60.87% specimens with herbivory Total surface area 142036.327 170748.468 147371.987 88484.531 148379.603 (mm2) Herbivorized 2985.841 4886.361 1598.448 325.244 3921.650 surface area (mm2) Herbivory index 2.102% 2.862% 1.085% 0.368% 2.643% Number of 19 17 17 6 11 damage types 71 Finally, the spectrum of insect herbivory differed among the five laurel taxa (Figures 2.17, 2.18). The nonmetric multidimensional scaling (NMDS) ordination plot that was subsampled to 85,000 mm2, which included all five taxa, illustrated a great deal of overlap between C. gettyi and M. pearsonii (Figure 2.17). Moreover, both C. gettyi and M. pearsonii were strongly associated with endophytic feeding groups of leaf mining and oviposition, as well as piercing and sucking. 0.8 0.8 1.0OV GL OV 0.4 0.50.4 LM F. planicostata M. pearsonii M. pearsonii PS M. trivialis LM 0.0 EFF C. gettyi0.0 M. trivialisEFF C. gettyi EFFPS 0.0 M. trivialis C. gettyi F. planicostata M. pearsonii F. planicostataLM PS ?0.5 ?0.4 ?0.4 GL GL OV ?1.0 ?0.8 ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 0.8 OV GL OV 0.5 0.4 0.5 M. pearsonLiiM LM F. planicostata M. pearsonii PS EFF M. trivialis0.0 C. gettyi PS 0.0 EFF EFF C. gettyi 0.0 C. gettyi M. trivialis PS M. trivialis F. planicostata M. pearsonii F. planicostata LM ?0.4 ?0.5 GL ?0.5 GL OV ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 0.8 1.0 0.5 GL GL 0.4 OV0.5 F. planicostata M. trivialis F. planicostata LM 0.0 M. pearsoniiPS C. gettyi M. trivialis PS EFF 0.0 EFF C. gettyi EFF M. pearsonii 0.0 M. trivialis M. pearsonii C. gettyi LM F. planicostata LM OV ?0.5 ?0.4 PS ?0.5 GL OV ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 Figure 2.17: Non-metric multidimensional scaling (NMDS) ordination subsampled at 85,000 mm2 with elipses, which include 84% of the datapoints closest to the centroid, for . Catula gettyi and the four Hell Creek taxa (Marmarthia pearsonii, M. trivialis, ?Artocarpus? lessigiana, and ?Ficus? planicostata). 72 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 Marmarthia trivialis, ?F.? planicostata, and ?A.? lessigiana were tightly clustered in morphospace and associated with external functional feeding groups and gall makers. These patterns were more pronounced in the NMDS ordination plot that subsampled 140,000mm2, which clearly shows the overlap in morphospace between C. gettyi and M. pearsonii, and their shared association of leaf mining (Figure 2.18). 1.0 1.0 1.0 GL GL 0.5 0.5 OV 0.5 PS F. planicostata LM F. planicostata M. trivialis C. gettyi M. trivialis 0.0 M. pearsoniiA. lessEiFgiFana 0.0 A. lessEiFgiFana 0.0 A. lEeFssFigiana C. geMttyiC. gettyi . pearsonii M. trivialis M. pearsonii F. planicostataLM LM ?0.5 PS ?0.5 PS ?0.5 OV GL OV ?1.0 ?1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 ?1.5 ?1.0 ?0.5 0.0 0.5 NMDS1 NMDS1 NMDS1 1.0 1.0 1.0 GL GL 0.5 0.5 0.5 OV PS F. planicostata M. trivialis F. planicostata LM 0.0 C. gettyiA. lEeFssFigiana M. trivialis A. lEeFssFigianaM. pearsoniiM. pearsonii C. gettyi 0.0 EFF 0.0 A. lessigiana M. pearsonii M. trivialis LM C. gettyi F. planicostata ?0.5 OV PS LM ?0.5 ?0.5 PS OV GL ?1.0 ?1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 ?0.5 0.0 0.5 1.0 1.5 NMDS1 NMDS1 NMDS1 1.0 1.0 1.0 GL 0.5 GL 0.5 0.5 OV PS F. planicostata LM M. trivialis F. planicostata 0.0 EFF M. trivialis C. gettyiA. lessigiana M. pearsonii C. geMtty. ipearsonii 0.0 A. lEeFssFigiana A. lEeFssFigianaM. pearsoCn. ii 0.0 LM gettyi M. trivialis PS LM F. planicostata?0.5 OV ?0.5 PS OV ?0.5 GL ?1.0 ?1.0 ?1.0 ?1.5 ?1.0 ?0.5 0.0 0.5 ?0.5 0.0 0.5 1.0 1.5 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 Figure 2.18: Non-metric multidimensional scaling (NMDS) ordination subsampled at 140,000 mm2 with elipses, which include 84% of the datapoints closest to the centroid, for Catula gettyi and three Hell Creek taxa (Marmarthia pearsonii, M. trivialis, and ?Ficus? planicostata). 73 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 Discussion The damage intensity and richness of insect damage on fossil leaves of Catula gettyi from the Kaiparowits Formation, combined with that of the latest Cretaceous Hell Creek Formation (Labandeira et al. 2002a, Labandeira et al. 2002b), provide a baseline to better understand Late Cretaceous herbivorous insect fauna and their associations with plants. Below, we discuss overall patterns of Kaiparowits insect herbivory, compare these results to other Late Cretaceous taxa, and consider the impact of sampling effort and damage-type richness for insect herbivores in the Late Cretaceous fossil record. Kaiparowits Formation Insect Richness The plant?insect associations of the Kaiparowits Formation are both diverse and abundant on Catula gettyi leaves. We found evidence for eight functional feeding groups, 40 damage types, 863 occurrences of insect damage, an herbivory index of 2.102%, and 38.1% of C. gettyi leaves exhibiting insect herbivory. Interestingly, there are an elevated number of scale insect species on particular host species of extant Lauraceae (Foldi and Watson 2001, Green 1917, Hutton 1997, Miller and Davidson 2005), although no scale insects were found on C. gettyi. By contrast, the frequency of leaf miners on modern Lauraceae are minimal (Spencer 2012), yet diverse and abundant on C. gettyi. In general, the spectrum of insect damage on Catula gettyi is similar to that found on modern laurels (for a discussion on modern Lauraceae herbivory, see the Supplementary Material in Appendix B). The external foliage feeding damage types of hole, margin and surface feeders as well as skeletonizers, are 74 at typical levels of richness expected for a moderately diverse host-plant family such as Lauraceae. The distribution of host specificity was nearly evenly divided among damage types, wherein specialized (12 total), intermediate (15 total), and generalist (13 total) damage types each accounted for approximately one third of the total number of damage types. Nevertheless, the distribution of host specificity for individual occurrences was bimodal, with greater generalist and specialist insect damage. Approximately half of all damage-type occurrences were assigned to the generalist category (51.9%), a small number were intermediate (8.8%), and specialist damage was also relatively high (39.3%). For qualitative categories, hole feeding (198 instances) and margin feeding (214 instances) had the most occurrences of generalist damage. Specialist damage was closely associated with endophytic feeding modes, most notable of which were the five leaf mining damage types constituting 311 occurrences, likely dominantly monophagous in host specificity. The combination of high damage-type richness ? including many distinct specialist damage types ? suggests that C. gettyi likely hosted a high richness of insect herbivores. In modern communities, endophytic insects most often make one, characteristic damage type on a single plant-host species (Bairstow et al. 2010, Carvalho et al. 2014, Currano et al. 2008, Wilf and Labandeira 1999). This is because feeding behavior often is highly constrained and can sometimes be attributed to a taxonomic level of the subfamily, especially for endophytic feeders such as scale insects, leaf miners, and gallers (Jud and Sohn 2016, Labandeira et al. 2007c, Wilf et al. 2000). Alternatively, ectophytic (chewing) insects are more likely to consume a 75 wider range of host-plant species and often produce more numerous and diverse damage on leaves than their endophytic counterparts, which makes estimating ectophytic insect richness difficult in the fossil record (Carvalho et al. 2014). Furthermore, a particular generalist damage type may be produced by multiple species of insects and, alternatively, one species of insect may be capable of producing several damage types. While we do not hypothesize an exact number of insect herbivores on Catula gettyi, we estimate that the specialized insect damage provides evidence for at least 12 specialist insect herbivores from the 40 total damage types. For comparison, the number of arthropod herbivores on a single host-plant species in modern ecosystems varies greatly, with up to 205 phytophage species on leaves of certain taxa (e.g. Basset and Novotny 1999, Kennedy and Southwood 1984, Novotny et al. 2002b, Novotny et al. 2006). Our survey of C. gettyi captures many fewer herbivores. However, we are not able to measure fossil plant?insect associations with the same accuracy as modern plant?insect associations. As a result, the observation of 40 damage types on a single fossil taxon is among the highest of any known fossil taxon (e.g. Adroit et al. 2018b, M?ller et al. 2017, Wappler et al. 2012). Antiherbivore Resistance and Herbivore Specialization Modern Lauraceae produce significant levels of secondary compounds and structural defenses. Many species of Lauraceae are noted for their elevated concentrations of essential oils that typically are employed in defenses against a wide range of insect herbivores today (Gonz?lez-Coloma et al. 1994a, Gonz?lez-Coloma et al. 1994b). For example, lauraceous foliage is known to be rich in monoterpenes 76 (Goralka and Langenheim 1996, Niogret et al. 2013); sesquiterpenes (Niogret et al. 2013); phenols of vanillic, chlorogenic, p-coumaric and ferulic acids (Ingersoll et al. 2010); as well as cyanoid diterpenes, extracts of cyandol, cyanoids and cinnceylanol (Gonz?lez-Coloma et al. 1994b). These are known to have negative effects when fed to insects; the physiological outcomes of these extracts range from subtle antifeedent effects to toxins causing death (Gonz?lez-Coloma et al. 1994a). Growth inhibition also is known for several lepidopteran (moth), coleopteran (beetle), and blattodean (termite) herbivores (Gonz?lez-Coloma et al. 1994b, Kishimoto-Yamada et al. 2013). In addition to chemical defenses, Lauraceae possess considerable structural defenses. Features frequently found in Lauraceae indicating mechanical impediments to insect herbivory principally involve leaf toughness, such as thickened epidermis layers, cell- wall rigidity, thick cuticle, and robust fiber strands (Grubb 1986). As with the majority of modern Lauraceae, a combination of structural and chemical defenses was likely present in C. gettyi (also see Supplementary Materials in Appendix B). Although antiherbivore defenses in Catula gettyi can only be inferred, the morphology of the leaves suggest tough, long-lived leaves, similar to many extant Lauraceae species (Bentley 1979). The leaves of C. gettyi have relatively thick petioles compared to their leaf area suggesting a high leaf mass per area quotient, though this analysis is pending. Furthermore, they show generally less physical damage, such as blade tearing and necrotic tissue, compared to other leaf morphotypes at the Lost Valley locality. The antiherbivore defenses of long-lived leaves generally are constitutive (ever-present) whereas the metabolites are typically qualitative defenses, such as digestibility-reducers that are present at high levels 77 (Coley 1988, Karban and Baldwin 2007), and are known to decrease the probability of insect herbivory from a wide range of both generalist and specialist insect herbivores (Feeny 1976, Rhoades and Cates 1976). Furthermore, long-lived leaves typically have lower photosynthetic rates and lower nitrogen content and greater structural tissues, which makes them less nutritious and palatable to insects (Coley et al. 1985). The morphology of the leaves and the bimodal distribution of generalist and specialist damage types on C. gettyi are indicative of a plant species with constitutive defenses, such as the structural defenses that slow or prevent processing of leaf material by insect herbivores. At present, secondary metabolites are poorly known in fossil leaves though efforts to detect and identify them are increasing (Labandeira et al. 2014, McCoy et al. in press). Nevertheless, specialized insect damage types can be used, such as those made by leaf miners, to provide predictions about the role of secondary metabolites in Catula gettyi. A longstanding hypothesis is that elevated secondary compound defenses in plants often lead to taxon-specific coevolutionary relationships between the plant host and insect herbivore (Ali and Agrawal 2012). Specialist insects frequently have physical adaptions to their host plant?s secondary compounds, particularly involving tolerance, expulsion, or sequestration, although it is acknowledged that specialist herbivores also are negatively impacted by these toxins at high levels (Cornell and Hawkins 2003). Moreover, insects instead use one or more particular toxic compounds as a cue to recognize potential plant hosts as edible or suitable as an oviposition site (Rosenthal and Berenbaum 2012, Tallamy 1986). 78 Catula gettyi hosts both abundant and diverse, specialized damage types, such as piercing and sucking, galling, and most notably leaf mining. The elevated number of leaf-mine occurrences is exceptional in the fossil record compared to other plant host species (ex. Arens and Gleason 2016, Donovan et al. 2018, Donovan et al. 2014, Krassilov 2007, Krassilov and Shuklina 2008, Krassilov 2008a, Labandeira et al. 1994, Labandeira et al. 2002a, Labandeira et al. 2002b); 7.8% of C. gettyi specimens have the leaf mine DT45 and 7.2% have DT332, which are both attributed to lepidopteran miners. Lepidopteran leaf miners are well known for their abilities to disarm, digest, and/or tolerate plant secondary metabolites as an ever-present threat while living inside the leaf mesophyll (Nishida 2002). The exceptionally high number of these two damage-type occurrences, the specialist nature of these leaf mines, and the lack of these mines on other plant taxa from the same locality indicates that two leaf mining lepidopteran taxa were actively seeking out C. gettyi as an oviposition site for their larvae. Late Cretaceous Insect Herbivory Insect herbivory studies in the Mesozoic are lacking relative to those of the late Paleozoic and Cenozoic (Pinheiro et al. 2016), with only a small number of Late Cretaceous floras having been analyzed for insect herbivory (Labandeira 2006b). Among these studies, there are only a handful of descriptions for isolated Mesozoic damage types (ex. Cenci and Adami-Rodrigues 2017, Jud and Sohn 2016, Krassilov 2007, Krassilov 2008a, Labandeira 1998c, Labandeira et al. 1994, Stephenson 1992, Vasilenko 2008, Wilf et al. 2000) and two, fully described, insect damaged floras from the Late Cretaceous that predate the Kaiparowits Formation (Table 2.3). Of the 79 two floras for which the damage has been fully described, the Soap Wash Formation of Utah (98.1 Ma) has an admittedly small sample size (152 specimens) (Arens and Gleason 2016), and the Ora Formation Flora of Israel (91 Ma) (Krassilov and Shuklina 2008) does not use the damage type scheme (Labandeira et al. 2007c). The lack of damage type designations, small sample sizes, and the approximation of specimen numbers and herbivory occurrences precludes a direct comparison of the Ora and Soap Wash formations to the Kaiparowits Formation regarding insect herbivory. Aside from these Late Cretaceous deposits, only the Late Maastrichtian Hell Creek Formation in North America and the Lefip?n Formation in South America, both of which are ca. 8?10 million years younger than the Kaiparowits Formation, provide a comparable Late Cretaceous dataset of insect herbivory. The Hell Creek and Lefip?n formation studies (Table 2.3) have yielded relatively high damage-type richness, between 32 and 60 damage types (Donovan et al. 2016, Donovan et al. 2014, Krassilov 2007, Labandeira et al. 2002a, Labandeira et al. 2002b, Wappler et al. 2009, Wilf et al. 2006). However, differences in habitat type, sampling intensity, sampling protocol, floral diversity, time averaging, deposit size, taphonomic variability, number of localities, and latitudinal position make comparisons among floras inequitable. Although comparisons between the Kaiparowits Formation insect herbivory and the insect herbivory in these floras are inadvisable for these reasons, individual taxa from the Maastrichtian of North America collected from a single locality are analogous to the sampling of C. gettyi and therefore permit a more appropriate comparison. Given this context, we selected all taxa belonging to the family Lauraceae that had at least 20 specimens from a 80 Table 2.3. Late Cretaceous floras analyzed for herbivory. Number of Number of Herbivorized Number of Formation State, Country Age (Ma) Plant Taxa Specimens Specimens DTs References Soap Wash Utah, USA 98.4 18 152 64 19 Arens and Gleason (2016) Krassilov and Shuklina Ora Negev, Israel ~91 ~50 ~1500 N/A ~60* (2008) Kaiparowits Utah, USA ~75.6 1 1564 606 40 This study North Dakota, Hell Creek USA 67-66 191 4149 657 32 Labandeira et al. (2002a,b) Patagonia, Lefip?n Argentina 67-66 53 856 533 50 Donovan et al. (2016, 2018) *Does not use damage type classification from Labandeira et al. (2007) 81 single locality in the Hell Creek Formation (Johnson 2002), which between the two terminal Cretaceous studies is geographically closest to the Kaiparowits Formation. Four lauraceous taxa from the Hell Creek Formation met these requirements: Marmarthia pearsonii (HC162, Locality 900), Marmarthia trivialis (HC105, Locality 428), ?Artocarpus? lessigiana (HC179, Locality 428), and ?Ficus? planicostata (HC4, Locality 428) (Table 2.3) (Supplementary Figure 2.2). Catula gettyi has similar richness of damage types when compared to Marmarthia pearsonii, M. trivialis, ?Artocarpus? lessigiana, and ?Ficus? planicostata (Figure 2.15). Although C. gettyi has a high number of damage types across all 1,564 specimens, rarefaction analysis of damage-type richness by surface areas illustrates that the levels of insect damage are comparable to the Hell Creek laurels. Regarding the types of insect damage found on each taxon, C. gettyi and M. pearsonii are most tightly associated with leaf miners. Notably, the specialist leaf mine DT45 only occurs on C. gettyi and M. pearsonii among the five lauraceous taxa, perhaps due to similar antiherbivore defenses. It is possible that this leaf miner is well accommodated to the secondary metabolites of some Lauraceae species. DT45 is also present on morphotypes ?LEF5? and ?LEF9? from the Lefip?n Formation, although their taxonomy is currently unresolved (Donovan et al. 2018). Future analyses comparing C. gettyi to other Late Cretaceous plants in Lauraceae and other angiosperm lineages should clarify the insect damage associations between these Late Cretaceous plant hosts. Indeed, we advocate for more taxonomic work in Late Cretaceous floras, coupled with ecological data for each plant host. This would particularly be useful for elucidating the forces driving patterns of Late Campanian 82 regionalism and disparities in taxonomic richness observed in vertebrates (Gates et al. 2012, Loewen et al. 2013, Nydam 2013, Woolley et al. 2020) and invertebrates (Tapanila and Roberts 2013). Latitudinally dispersed floras and associated indicators of insect richness from penecontemporaneous or paracontemporaneous geologic units in the Western Interior are key to understanding how abiotic factors, such as sea level, climate, and tectonics influenced Late Cretaceous ecosystems. Conclusions Herein we describe the new genus and species, Catula gettyi (Laurales: Lauraceae), from the Campanian Age Kaiparowits Formation of southern Utah, USA and catalog the insect damage on the taxon. With 1,564 studied museum voucher specimens, C. gettyi is among the best-sampled Mesozoic taxa in the fossil record for insect damage. Insect herbivory on C. gettyi is both rich and abundant, including eight functional feeding groups, 40 damage types, an herbivory index of 2.1, and 38.1% of the specimens exhibiting at least one type of insect damage. There was a large damage component of generalist, ectophytic feeding as well as six specialist leaf miners. These results, in combination with the analysis of four Late Cretaceous lauraceous taxa from the Hell Creek Formation, show similar damage-type richnesses for these Late Cretaceous lauraceous plant hosts and possible specialization on lauraceous plant hosts. Taken together, this first analysis showing the richness, abundance, and intensity of insect damage on a single taxon in the Kaiparowits Formation, which 83 complements the high richness seen in vertebrates, invertebrates, and plants known from this geologic formation. Future work will assemble the insect?plant ecosystem and investigate how the base of the food web reflects diversity seen at higher trophic levels, including that of the diverse Kaiparowits Formation dinosaurs. Acknowledgments We dedicate this paper to the memory of our dear friend and colleague, Mike Getty. We are grateful to the Denver Museum of Nature & Science?s Leaf Whackers for preparation of the Kaiparowits fossil specimens and to K. MacKenzie, G. Rossetto, T. Foreman, N. Toth, N. Neu-Yagle, and R. Rissman for their support. Thanks to R. Wicker for his photographs of the Hell Creek Formation specimens. BLM Cooperative Agreement L14AC00302 and donors to the Denver Museum of Nature & Science Laramidia Project provided financial support for fieldwork. The Denver Museum of Nature & Science provided additional financial support for collections work during the summer and fall of 2017. Thanks to J. Shultz for his mentorship and S. Schachat for her guidance and skills in R, which she generously shares with colleagues. We thank the three reviewers and editorial team at PLoS ONE. Finally, we thank President Bill Clinton, Secretary of the Interior Bruce Babbitt, and countless public servants for the creation of the Grand Staircase- Escalante National Monument, and all those who fight to protect our national public lands today. This is contribution 372 from the Evolution of Terrestrial Ecosystems consortium at the National Museum of Natural History in Washington, D.C. 84 Chapter 3: Plant?insect associations of a Kaiparowits Formation locality, Upper Cretaceous of Utah, USA Abstract The Upper Cretaceous Kaiparowits Formation (76.49 ? 0.14 to 74.69 ? 0.18 Ma), located primarily within the Grand Staircase-Escalante National Monument of south-central Utah, has a well-documented paleontological record that continues to enhance our understanding of Campanian Age (83.6?72.1 Ma) ecosystems. To date, there are no insect body fossils described from the Kaiparowits Formation and the diversity of herbivorous insects is as yet unknown. However, the abundant evidence of insect herbivory?the chew marks, holes, punctures, galls, and leaf mines in fossil leaves?provides evidence for the intensity and richness of Kaiparowits insect feeding behaviors and mouthpart morphologies. A total of 719 plant specimens comprising angiosperms, lycopsids, pteridophytes, sphenophytes, gymnosperms, and unassociated reproductive organs from the JARS locality were analyzed for signs of insect herbivory. This is the first examination to describe and quantify plant?insect associations for an entire Campanian locality. Introduction Paleontologists have studied the fossil fauna and flora of the Campanian Age Kaiparowits Formation (Upper Cretaceous, 76.49 ? 0.14 to 74.69 ? 0.18 Ma) for over 85 four decades in order to reconstruct these exceptionally diverse ancient ecosystems (Titus and Loewen 2013). This diversity includes non-avian dinosaurs (Carr et al. 2011, Decourten and Russell 1985, Gates and Sampson 2007, Lund et al. 2016, Sampson et al. 2010b, Sampson et al. 2013, Zanno et al. 2013), birds (Farke and Patel 2012), pterosaurs (Farke and Wilridge 2013), squamates (Lively 2015, 2016, Lyson et al. 2017, Nydam 2013), amphibians (Gardner and DeMar 2013, Ro?ek et al. 2013), crocodyliforms (Farke et al. 2014, Irmis et al. 2013), mammals (Cifelli 1990a, b, Eaton and Cifelli 1988, Eaton et al. 1999), fish (Brinkman et al. 2013, Kirkland et al. 2013), aquatic invertebrates (Roberts et al. 2008, Tapanila and Roberts 2013), plants (Maccracken et al. in review-a, Maccracken et al. 2019, Miller et al. 2013), and fossil traces of insect behavior (Maccracken et al. in review-a, Roberts et al. 2007, Roberts and Tapanila 2006). However, insect body fossils from this formation are virtually absent, despite the high probability that insects were the most abundant and diverse group of animals in the Kaiparowits Formation (Labandeira 2006a, Labandeira and Eble 2005). This absence means that, to date, reconstructions of the Kaiparowits ecosystems and food webs are very much incomplete (Titus and Loewen 2013). Insect body preservation during the Late Cretaceous (100?66 Ma) in the Western Interior of North America is poor (Ross et al. 2000), and is not only restricted to within the Kaiparowits Formation. Insect body fossils from Upper Cretaceous deposits of North America are primarily known from Campanian Age Canadian Amber found in the Foremost Formation (Carpenter et al. 1937, McAlpine and Martin 1969, Pike 1994), and Turonian Age (93.9?89.8 Ma) Raritan Amber of New Jersey, USA (Grimaldi and Agosti 2000, Grimaldi et al. 2010). The general lack 86 of insect body fossils, especially compression-impression fossils, from the Late Cretaceous may be due to high global sea levels, which flooded large swaths of the North American landmass and greatly reduced the extent of depositional environments conducive to insect fossilization (Gale 2000, Ross et al. 2000, Szwedo and Nel 2015). However, it remains puzzling as to why insect fossils nonetheless are rare in Upper Cretaceous deposits, particularly extensive freshwater habitats that ostensibly could preserve insects. Insect preservation commonly requires rapid burial in anoxic conditions, most often in lakes and ponds (Smith 2012). Water depth, alkalinity, temperature, sediment type, grain size, insect size, and insect morphology all contribute to preservation potential for insects (Grimaldi and Engel 2005, Smith 2012, Smith et al. 2006). Although preservation of insects in the Kaiparowits Formation seems promising, the lack of insect body-fossil discoveries may be due to unsuitable aquatic chemistry, although further exploration is required. Nonetheless, trace fossils of insect herbivory are exceedingly abundant in the Kaiparowits Formation. Insect trace fossils in the Kaiparowits Formation have been previously described in sedimentary rocks (Roberts and Tapanila 2006) and dinosaur bone (Roberts et al. 2007), but insect herbivory on fossil leaves is only now being documented (Maccracken et al. in review-a). Traces of insect herbivory on fossil leaves not only provide vital clues to what insect feeding guilds were present when insect body fossils are unknown (Labandeira et al. 2007c), but also are among of the richest sources for evidence of organisms interacting in the fossil record and often predate their respective body fossil record (Labandeira 2006a, Maccracken et al. in 87 review-b, Wilf et al. 2001). Fossil plant?insect traces are used to infer food web evolution and response to internal and external perturbations (Dunne et al. 2014, Wilf 2008); the presence and richness of insect feeding guilds (i.e. leaf miners, galling insects, piercing-and-sucking insects bearing stylet-like mouthparts) (Schachat et al. 2015, Schachat et al. 2014); diversity of damage types (Carvalho et al. 2014, Donovan et al. 2018, Donovan et al. 2014, Maccracken et al. in review-a); rarely to taxonomically identify damage patterns to a particular species or lineage of insect culprits (Maccracken et al. in review-b, Wilf et al. 2000); and host plant specialization (Donovan et al. 2016). However, few studies have measured plant?insect associations during the Late Cretaceous (ex. Arens and Gleason 2016), the majority of which document terminal Cretaceous fossil deposits (Donovan et al. 2016, Donovan et al. 2018, Donovan et al. 2014, Labandeira et al. 2007a, Labandeira et al. 2002a, Labandeira et al. 2002b, Wappler et al. 2009) or individual insect damage patterns (ex. Jud and Sohn 2016, Krassilov 2007, Krassilov 2008a, Labandeira 1998c, Vasilenko 2008, Wilf et al. 2000). Here, we describe and quantify plant?insect from the JARS locality (DMNH I. 3725) in the Kaiparowits Formation, Utah, USA. The objectives of this study are to: 1) analyze the richness and intensity of insect damage on fossil leaves from the JARS locality of the Kaiparowits Formation; 2) identify any potential insect culprits responsible for the damage types; and 3) compare the richness and intensity of JARS insect damage to a previously documented Late Cretaceous taxon. 88 Geological Setting The Campanian-aged Kaiparowits Formation (76.49 ? 0.14 to 74.69 ? 0.18 Ma) (Roberts et al. 2013) is located in southern Utah, USA (Figure 3.1). The formation now occurs within and outside the boundaries of the recently diminished Grand Staircase?Escalante National Monument (Eilperin 2017, Kolbert 2018, Light and Hale 2018, Miller 2018, Penn-Roco 2018, Underwood 2017). The Kaiparowits Formation comprises ~1005 m of alternating sandstones and mudstones, which preserve several depositional environments, such as channels, lakes, and a variety of Figure 3.1: Map of the Kaiparowits Formation outcrop (green). Solid yellow denotes new boundaries for the Grand Staircase-Escalante National Monument (December 2017) and former monument areas are stippled in lighter yellow. DMNH loc.3725, the JARS locality, is denoted by a blue star. Map modified from Crystal et al. (2019). 89 floodplain deposits that include crevasse splays, perennial ponds, and oxbow lakes (Beveridge et al. 2020, Roberts 2007, Roberts et al. 2013). The majority of paleobotanical localities occur in the middle member of the formation (ca. 90-110 to ca. 550 m) (Roberts 2007). The JARS locality, (DMNH I. 3725) occurs at 365 ? 20 m above the base of the formation (Figure 3.2). With an estimated depositional rate of 41 cm/1,000 years in calculating 40Ar/39Ar ages on sanidine crystals from volcanic ash beds (Roberts et al. 2013), we estimate the age of the JARS locality at 75.7 ? 0.05 Ma, which corresponds to the late Campanian Age (Walker et al. 2018). Specimens were collected in 2008 and are reposited at the Denver Museum of Nature & Science (DMNS) in Denver, Colorado, USA. The leaves occur as compression-impression fossils on mudstone, siltstone, and fine grained sandstone matrices (Locatelli et al. 2017, McMahon et al. 2016), and the JARS locality facies association is interpreted as forming in lacustrine settings (Roberts 2007). Figure 3.2: Stratigraphic column for the Kaiparowits Formation, Utah, USA, redrawn from Roberts (2007). The stratigraphic position of DMNH loc. 3725, where the JARS locality specimens were collected is noted. 90 Materials and Methods All fossil plant specimens from the JARS locality that were at least 50% complete and identifiable were collected. Leaves were prepared to expose the entire leaf surface whenever possible, using Chicago pneumatic air scribes. Leaf specimens included in the analyses were morphotyped, a non-taxonomic categorization outlined in Johnson et al. (1989) and detailed in Chapter 2 of this dissertation. We did not distinguish between fossil leaves and leaflets, as they both represent distinct laminar structures. After being morphotyped, leaf specimens were analyzed for insect herbivory. We analyzed 719 fossil plant specimens, including seeds, reproductive structures and leaves from lycopsids, Equisetum, ferns, conifers, and monocotyledonous and dicotyledonous angiosperms. Several criteria were used to separate insect herbivory and oviposition from physical damage, detritivory, and taphonomic processes: (1) reaction tissue produced by the plant in response to herbivory, often in the form of hypertrophy (cell size increase) and hyperplasia (cell multiplication) (Brues 1924, Johnson and Lyon 1991, MacKerron 1976, Vincent et al. 1990); (2) targeting of specific host plant taxa or particular plant organs, which are indicative of host plant specialization (ex. Gangwere 2017, Iannuzzi and Labandeira 2008, Kazakova 1985, Keen 1952); (3) recurring stereotypy of a damage pattern based on shape, size, and position of the damage on the plant (Bodnaryk 1992, Heron 2003); and (4) atypical and distinctive, micromorphological features associated with consumption of plant tissues (Labandeira et al. 2007c), for example vein strings linked to the inability of some mandibulate phytophagous insects to process tough vein tissue. After damage was 91 identified as herbivory, the damage was classified by functional feeding guild and specific pattern (damage type). Qualitative insect herbivory was analyzed using the Guide to Insect (and other) Damage Types on Compressed Plant Fossils (Labandeira et al. 2007c). The guide is categorized into functional feeding groups, which are akin to insect feeding guilds. Within each functional feeding group are numbered damage types, each of which is a discrete, diagnosable damage pattern that is assigned a number. Damage types are designated by shape, size, extent, and location of herbivore damage and are scored for host specificity with respect to the plant host: 1 for specialized (monophagy) damage, 2 for intermediate (oligophagy) damage, and 3 for generalist (polyphagy) damage (Labandeira et al. 2007c). Convergent similarities in herbivore mouthparts and feeding behaviors rarely make genus or species level identification of the insect culprit possible, with the exception of some leaf mines, galls, margin feeding, and scale-insect feeding traces (ex. Maccracken et al. in review-b, Sarzetti et al. 2008, Wilf et al. 2000). The two major groups of insect damage are endophytic feeding and ectophytic feeding. Endophytic feeding is divided into four functional feeding groups: piercing and sucking, galling, leaf mining, and oviposition. Endophytic feeding is the consumption of plants by insect herbivores from within a plant tissue, or by insects using their piercing-and-sucking mouthparts to penetrate into, and feed from within the plant organ. Ectophytic feeding is also divided into four functional feeding groups: hole feeding, margin feeding, skeletonization, and surface feeding. Ectophytic feeding is caused by insects with mandibulate mouthparts that chew plant 92 tissues. Additional functional feeding groups include seed predation, borings, pathogen infection, Incertae sedis, and domatia. Furthermore, while all functional feeding groups fall under the umbrella of plant?insect associations, not all are herbivory per se. Oviposition, Incertae sedis, and pathogen associations with plant hosts represent damage to plant organs that reduce photosynthetic potential and are not feeding, but nonetheless destroy photosynthetic tissue. Alternatively, plant?insect mutualisms, such as mite domatia, are not included in measurements of herbivory because mutualisms are not antagonistic to the host plant. The quantitative measurements for insect herbivory in this study were richness of functional feeding groups and damage types, the percentage of insect damaged leaves, and the herbivory index, which is the proportion of surface area removed by an insect herbivore to the total surface area of the leaf. Leaf surface area was measured using Adobe Illustrator Draw? for iPad Pro and ImageJ (Rasband 2012). Piercing and sucking damage was particularly difficult to measure because puncture marks are often diminutive and can number from the tens to thousands. We measured the average puncture surface area for each leaf and multiplied that by the number of punctures on the leaf. Average puncture marks were below 0.025 mm2. All metrics were measured for the total flora and for each plant taxon. The proportion of insect damaged leaves in a flora is known to be highly variable (Schachat et al. 2018), and although we present this metric, we do not use it for the purpose of comparisons. All leaves were photographed using a Canon EOS 50D camera body with a Canon EF-D 60mm f/2.8 macro lens. Microphotographic images of insect damage were taken by an Olympus SZX12 microscope with an Olympus DP25 camera. Low 93 angle light produced by a Dolan-Jenner illuminator was used in some instances to enhance subtle insect damaged zones. Damage-type richness by total surface area measured was documented with a sample-sized-based rarefaction. We used code developed by S. Schachat (Schachat et al. 2018) for R statistical software (R Development Core Team 2013), in which data were bootstrapped 5000 times at a confidence interval of 95%. To visualize the differences in suites of functional feeding groups between specimens, we used a nonmetric multidimensional scaling (NMDS) ordination, which employed a Bray- Curtis dissimilarity matrix. The results of the NMDS were shown an ordination plots of the nine plant hosts and functional feeding groups present at the JARS locality for the three most abundant plant hosts and nine most abundant plant hosts. Ellipses were drawn containing 84% of the points closest to the centroid of each of the nine plant host ellipses to represent 84% confidence intervals. The NMDS ordinations were produced by the ?metaMDS? function of the vegan package, in R version 3.1.2 (R Development Core Team, 2013). Results Plant Diversity The JARS locality (DMNH I. 3725) in the Kaiparowits Formation yielded a total of 719 identified fossil plant specimens, 589 of which were angiosperm specimens (Table 3.1) (Figure 3.3). These plant specimens constituted 70 morphotypes, which were categorized into: 1) seeds and reproductive material; 2) 94 A B C D EDE F F G H I J K L Figure 3.3: Taxonomically identifiable plant hosts and plant hosts with more than 20 specimens from the JARS locality. A, Quereuxia sp., plant host (PH)12.1 (DMNH EPI.45447); B, Brasenites sp., PH12.2 (DMNH EPI.45532); C, Hydropteris sp., PH7.4 (DMNH EPI.45533); D, PH16.1 (DMNH EPI.45468); E, Cobbania cf. C. corrugata, PH11.1 (DMNH EPI.45531); F, PH13.1 (DMNH EPI.45432); G, PH36.1 (DMNH EPI.45431); H, PH16.2 (DMNH EPI.45429); I, PH30.1 (DMNH EPI.45430); J, PH15.1 (DMNH EPI.45440); K, PH39.1 (DMNH EPI.45428); L, PH41.1 (DMNH EPI.45455). Black scale bar = 1 cm; white scale bar = 1 mm. 95 lycopods; 3) horsetails; 4) ferns; 5) conifers; 6) monocotyledonous angiosperms (monocots); and 7) dicotyledonous angiosperms (dicots). There were 49 dicot morphotypes, which we will refer to as plant hosts that included herbaceous, aquatic, vining, and woody life forms. There were four plant hosts that were also taxonomically identifiable: Hydropteris sp., an aquatic fern (Plant Host (PH) 7.4) (Figure 3.3 C); Quereuxia sp., a floating aquatic dicot (PH12.1) (Figure 3.3 A); Cobbania cf. C. corrugata, a floating aquatic monocot (PH11.1) (Figure 3.3 E); and Brasenites sp., a floating aquatic dicot (PH12.2) (Figure 3.3 B). All other plant hosts are, as yet, of unidentified and/or undescribed species. Table 3.1: Summary of JARS locality morphotypes and specimens in each major taxonomic unit. Major taxonomic Number of Number of Percent of Percent of category morphotypes specimens Morphotypes Specimens Lycopoda 1 18 1.43 2.50 Equisetopsida 1 8 1.43 1.11 Pteridophytes 5 73 7.14 10.15 Coniferales 2 4 2.86 0.56 Angiospermophytina Reproductive 12 27 17.14 3.76 organs Monocot leaves 3 7 4.29 0.97 Dicot leaves 46 582 65.71 80.95 Total 70 719 - - Damage Intensity In total, there were 654 insect damage occurrences across 318 total damaged specimens (44.23% of specimens herbivorized) at the JARS locality (Table 3.2). Because multiple damage types may occur on a single leaf specimen, there were more damage type occurrences than damaged specimens. Insect herbivory at JARS was 96 almost entirely on angiosperms, with scant or no damage on conifers, lycopods, horsetails, and plant reproductive organs. The damage that did occur on non- angiosperm specimens was restricted to generalist, ectophytic feeding, with the exception of seed predation and two galls. Insect damage on foliar angiosperm specimens of angiosperm foliage totaled 615 occurrences across 301 specimens (51.1% of angiosperms were herbivorized). Although all identifiable angiosperm specimens were analyzed for herbivory, for the results and discussion we focused on plant hosts with at least 20 specimens, a precedent set forth by previous herbivory studies (Currano 2009). These targeted plant hosts are: PH16.1, PH39.1, PH36.1, Quereuxia sp. (PH12.1), PH30.1, PH16.2, PH41.1, PH15.1, and PH13.1 (Figure 3.3 A, D, F?L). The herbivory index, or the percent of surface area removed by the insect herbivore, was 3.97% for the JARS locality angiosperms (Table 3.3, Figure 3.4) and the 95% confidence interval was between 3.11% and 5.40%. Herbivory index calculations for individual plant hosts and the confidence interval ranges were highly variable for the 20 most abundant taxa; the plant host herbivory indices ranged between 0.68% and 10.54% (see Supplementary Figure 3.1 in Appendix C). Confidence intervals were very large for some taxa, especially those with limited total surface areas. Diversity of Insect Damage With a total of 12 functional feeding groups and the JARS locality, the only functional feeding group missing from JARS was wood borings, which is to be expected given that there are no wood specimens in the collection. The functional 97 Table 3.2: Richness of damage types, host specificities, and the number of damage occurrences per functional feeding group. Functional Generalist Intermediate Damage Specialist Number of Feeding Groups Damage Types Types Damage Occurrences Types Hole Feeding DT1; DT2; DT3; DT8; DT50; DT51; DT126 294 DT4; DT5; DT7; DT57; DT63 DT78 Margin Feeding DT12; DT13; DT15; DT26; DT198; 124 DT143 DT214; DT271 Skeletonization DT16; DT17 DT20; DT24 -- 8 Surface Feeding DT29; DT30; DT31 DT82 -- 29 Piercing and -- DT138 DT46; 53 Sucking DT330 Galling DT32; DT34; DT80; DT33; 95 DT194 DT85 Leaf Mining DT43; 6 DT176; DT295 Oviposition -- DT100; DT101 -- 29 Seed Predation -- DT74 -- 3 Pathogen/Enviro DT114 DT58; DT221; DT281 DT229 6 nment Incertae sedis DT106 -- -- 2 Domatia DT339 5 TOTAL: 12 17 Generalist 24 Intermediate 10 654 FFGs; Damage Types Damage Types Specialist Occurrences 51 Damage Types Damage Types 98 Table 3.3: Bulk floral data for the forty-nine angiosperm morphotypes from the Late Cretaceous (Campanian) JARS locality, Kaiparowits Formation. Specimens Surface Proportion Foliar area of total Number of Proportion of morphotypes Number of examined examined Total Herbivorize herbivor- Herbivory herbivor- herbivor- (abundance specimens of total of total surface d surface number area (cm2) area (cm2) ized index ized ranked) number specimens specimens ized (%) in flora specimens (%) (%) (%) 16.1 95 16.13 9.33 49937.758 1110.037 13.68 2.22 42 44.21 39.1 64 10.87 17.72 94803.400 693.643 9.12 0.73 28 43.75 36.1 48 8.15 5.55 29701.524 1455.934 9.77 4.90 30 62.50 12.1 41 6.96 1.04 5543.442 211.591 6.84 3.82 21 51.22 16.2 36 6.11 2.55 13624.559 92.764 3.26 0.68 10 27.78 30.1 36 6.11 7.04 37656.977 888.042 3.58 2.36 11 30.56 15.1 34 5.77 3.69 19751.933 632.351 4.56 3.20 14 41.18 41.1 34 5.77 20.18 107993.603 11378.745 10.10 10.54 31 91.18 13.1 30 5.09 6.58 35198.769 704.196 6.51 2.00 20 66.67 24.2 17 2.89 4.57 24444.698 424.267 3.91 1.74 12 70.59 25.1 16 2.72 2.09 11193.095 984.339 4.23 8.79 13 81.25 29.2 16 2.72 2.18 11651.556 73.114 2.28 0.63 7 43.75 41.4 12 2.04 2.12 11352.245 381.841 2.93 3.36 9 75.00 16.4 10 1.70 0.46 2475.621 8.498 1.63 0.34 5 50.00 24.1 10 1.70 1.89 10097.553 378.054 2.61 3.74 8 80.00 24.3 10 1.70 1.95 10414.686 23.922 1.63 0.23 5 50.00 32.2 7 1.19 0.67 3583.516 11.767 1.30 0.33 4 57.14 16.5 5 0.85 0.36 1917.809 9.564 1.30 0.50 4 80.00 29.1 5 0.85 0.49 2598.665 15.473 0.65 0.60 2 40.00 99 31.1 5 0.85 0.77 4126.236 161.647 0.98 3.92 3 60.00 31.2 5 0.85 0.19 1017.009 132.248 0.65 13.00 2 40.00 22.1 4 0.68 0.56 2997.324 123.303 0.98 4.11 3 75.00 24.4 4 0.68 0.73 3912.207 3.152 0.65 0.08 2 50.00 33.1 4 0.68 0.32 1706.432 167.958 1.30 9.84 4 100 11.1 3 0.51 0.23 1229.096 0.837 0.33 0.07 1 33.33 11.2 3 0.51 0.36 1943.496 20.121 0.33 1.04 1 33.33 22.2 3 0.51 0.39 2094.474 38.196 0.65 1.82 2 66.67 23.1 3 0.51 1.07 5742.184 215.431 0.33 3.75 1 33.33 30.2 3 0.51 0.25 1353.848 0.28 0.33 0.02 1 33.33 14.1 2 0.34 0.71 3773.891 158.433 0.33 4.20 1 50.00 23.2 2 0.34 0.62 3340.798 19.623 0.33 0.59 1 50.00 27.3 2 0.34 0.25 1328.499 190.145 0.33 14.31 1 50.00 28.3 2 0.34 0.03 181.625 0 0 0 0 0 35.1 2 0.34 0.22 1198.434 0 0 0 0 0 35.2 2 0.34 0.37 1954.827 0 0 0 0 0 11.3 1 0.17 0.14 740.14 0 0 0 0 0 12.2 1 0.17 0.06 344.107 9.544 0.33 2.77 1 100 17.1 1 0.17 0.63 3359.873 21.175 0.33 0.63 1 100 18.1 1 0.17 0.04 187.942 0.417 0.33 0.22 1 100 19.1 1 0.17 0.02 123.959 1.941 0.33 1.57 1 100 24.5 1 0.17 0.13 700.836 81.854 0.33 11.68 1 100 29.3 1 0.17 0.15 805.603 0 0 0 0 0 30.3 1 0.17 0.07 364.178 0 0 0 0 0 31.3 1 0.17 0.12 650.654 0 0 0 0 0 32.1 1 0.17 0.45 2388.515 173.784 0.33 7.28 1 100 34.1 1 0.17 0.25 1351.912 105.628 0.33 7.81 1 100 100 37.4 1 0.17 0.25 1356.058 99.854 0.33 7.36 1 100 41.2 1 0.17 0.12 664.354 0 0 0 0 0 41.3 1 0.17 0.05 247.203 0 0 0 0 0 Totals/perce nt sums & 100.05 averages 589 100.03 100.01 535127.123 21230.349 3.96 307 - 101 25 20 15 10 5 0 100000 200000 300000 400000 500000 Surface Area (mm 2 ) Figure 3.4: Herbivory index for the JARS locality. Center line represents the herbivory index and the upper/lower boundaries represent the 95% confidence interval range. feeding groups were: hole feeding, margin feeding, skeletonization, surface feeding, piercing and sucking, galling, oviposition, leaf mining, seed predation, pathogen, Incertae sedis, and domatia (Table 3.2). The number of damage types per functional feeding group ranged from one to 13, with a total of 51 damage types (Table 3.2). Among the angiosperm specimens there were a total of 49 damage types, the majority of which were ectophytic feeding damage types (455 occurrences, 69.6% of all occurrences) (Figure 3.5). The 29 ectophytic damage types at JARS are categorized into four functional feeding groups: hole feeding, margin feeding, skeletonization, and surface feeding. Hole feeding is the perforation through the leaf, including both adaxial and abaxial surfaces, that does not connect with the margin of the leaf. Hole feeding in the JARS locality was common and diverse, with thirteen damage types and 294 instances (Table 3.2; Figure 3.6). The most common hole-feeding damage types were circular 10 2 Herbivory Index (%) to ellipsoidal holes with diameters from <1 mm to >5 mm (DT1, DT2, DT4) (Figure 3.6 A) and polylobate holes from 1 mm to > 5 mm (DT3, DT5) (Figure 3.6 A, D, E). Slot feeding damage types included parallel-sided, curvilinear to rectilinear perforations (DT7) (Figure 3.6 A), rectilinear slots with parallel sides (DT8) (Figure 3.6 C), and overlapping slots forming a large, angulate hole (DT51) (Figure 3.6 J). Patterns of hole feeding included linear series of holes adjacent to a primary vein (DT50) (Figure 3.6 G), holes at the convergence of the primary veins (DT57) (Figure 3.6 H), and ellipsoidal holes connected by swaths of dark, necrotic tissue (DT126) 16.1 39.1 36.1 9 12.1 8 7 16.2 6 5 30.1 4 3 15.1 2 1 41.1 0 13.1 Hole Margin Skeleton Surf. P&S Gall Mine Ovip. Path. Incertae sedis Figure 3.5: Heat map plot for the richness of damage types found on each plant host (Y-axis) by functional feeding group (X-axis). The number of damage types range from zero (lightest purple) to nine damage types (darkest purple). 10 3 (Figure 3.6 B). Finally, hole feeding included a primary vein suspended by hole feeding on either side (DT63) (Figure 3.6 F) and large areas of foliar tissue removed between secondary veins (DT78) (Figure 3.6 I). Margin feeding is the consumption of the entire thickness of the lamina, which occurs along the margin of the leaf lamina. There were eight distinct margin feeding damage types at the JARS locality (Table 3.2; Figure 3.7). The most common margin feeding damage types were circular excisions (DT12) (Figure 3.7 H), excision of the leaf apex (DT13) (Figure 3.7 G), a deep excision of the margin that expanded as it approached the midline (DT15) (Figure 3.7 E), and a deep excision that narrowed towards the midline (DT198) (Figure 3.7 F). Other margin feeding damage types included the removal of large swaths of leaf margin that left veins intact (DT26) (Figure 3.7 C), a series of cuspate excisions with unherbivorized leaf margin separating each cuspule (DT143) (Figure 3.7 A), serial and adjoining cuspate excisions (DT214) (Figure 3.7 D), and the removal of over 50% of the laminar surface area with distinct cuspate feeding around the entire leaf (DT271) (Figure 3.7 B). Skeletonization, similar to hole feeding, entails the consumption of the entire thickness of the leaf, but veins of various orders are left intact by the herbivore (Figure 3.8 A?C, E). There were four skeletonization damage types, the most common of which was the removal of interveinal tissue without a reaction rim present (DT16) (Figure 3.8 B). Also found at the JARS locality was the removal of interveinal tissue surrounded by a pronounced reaction rim (DT17) (Figure 3.8 C), 10 4 Figure 3.6: Hole feeding damage types found at the JARS locality, Kaiparowits Formation (Utah, USA). A, Arrows denote hole feeding damage starting from top center and proceeding clockwise: elongate hole that lacks parallel sides (DT7, plant host (PH) 16.1, DMNH EPI.45452), a circular hole < 1 mm in diameter (DT1, PH33.1, DMNH EPI.45530), circular hole between 1 and 2 mm in diameter (DT2, PH33.1, DMNH EPI.45530), polylobate hole between 1 and 5 mm in diameter (DT3, PH33.1, DMNH EPI.45530). B, Circular to polylobate holes surrounded and connected by necrotic tissue (DT126, PH25.1, DMNH EPI.45537). C, A long, parallel-sided hole (DT8, PH33.1, DMNH EPI.45530). D, A circular hole > 5 mm in diameter (DT4, PH41.1, DMNH EPI.45455). E, Polylobate holes > 5 mm in diameter 10 5 (DT5, PH41.1, DMNH EPI.45456). F, Hole feeding on either side of a primary vein (DT63, PH16.1, DMNH EPI.45459). G, A series of three holes along a primary vein (DT50, PH13.1, DMNH EPI.45457). H, Holes at the convergence of major veins (DT57, PH15.1, DMNH EPI.45471). I, Hole feeding on entire intercostal areas (DT78, PH30.1, DMNH EPI.45466). J, Slot feeding holes joined together to form a large, angulate hole (DT51, PH30.1, DMNH EPI.45441). Black scale bar = 1 cm; white scale bar = 1 mm. Figure 3.7: Margin feeding damage types found at the JARS locality. A, Small cuspate incisions along the margin with a portion of the leaf margin preserved between the cusps (DT143, plant host (PH) 24.5, DMNH EPI.45443). B, Removal of the margin with cuspate edges where at least 50% of the leaf lamina is consumed (DT271, PH25.1, DMNH EPI.45449). C, Extreme removal of the leaf margin wherein large portions of the lamina are consumed, except for major veins (DT26, PH41.1, DMNH EPI.45437). D, Broad cuspate incisions connected to one another (DT214, PH25.1, DMNH EPI.45469). E, Removal of the leaf margin that expands towards the midvein (DT15, PH39.1, DMNH EPI.45426). F, Incision of the leaf margin that narrows towards the midvein (DT198, PH29.2, DMNH EPI.45536). G, Removal of leaf apex (DT13, PH36.1, DMNH EPI.45467). H, Removal of the leaf margin within a 180? arc (DT12, PH34.1, DMNH EPI.45451). Black scale bar = 1 cm; white scale bar = 1 mm. 10 6 elongate strings of skeletonized tissue (DT20) (Figure 3.8 A), and oval patches of skeletonized tissue (DT24) (Figure 3.8 E). Figure 3.8: Skeletonization and surface feeding damage types found at the JARS locality. A, Linear removal of leaf lamina with veins intact (DT20, plant host (PH) 16.2, DMNH EPI.45435). B, Herbivory of leaf lamina without consumption of the vein network (DT16, PH16.1, DMNH EPI.45442). C, Herbivory of the leaf lamina with maintenance of the vein network, and a pronounced reaction rim surrounding the herbivorized areas (DT17, PH16.1, DMNH EPI.45458). D, Removal of the leaf surface without a reaction rim produced by the plant (DT29, PH24.2, DMNH EPI.45463). E, Circular patches of skeletonization in a linear projection (DT24, PH12.1, DMNH EPI.45454). F, Surface feeding patches that are symmetrically arranged around the primary vein (DT82, PH24.1, DMNH EPI.45535). G, Removal of the leaf surface with a polylobate reaction rim (DT30, PH41.1, DMNH EPI.45427). H, Removal of the leaf surface accompanied by a circular reaction rim (DT31, PH41.1, DMNH EPI.45453). Black scale bar = 1 cm; white scale bar = 1 mm. 10 7 The final ectophytic feeding group was surface feeding, or the consumption of either the abaxial or adaxial surface of the leaf lamina (Figure 3.8 D, F?H). There were four described examples of surface feeding, the most common of which was the removal of surface tissue with no or minimal reaction rim present (DT29) (Figure 3.8 D). The three other surface feeding damage types were: the removal of surface tissue with a polylobate reaction rim (DT30) (Figure 3.8 G), the removal of surface tissue with a circular reaction rim (DT31) (Figure 3.8 H), and polylobate surface feeding that was symmetrical about the primary vein (DT82) (Figure 3.8 F). Endophytic feeding damage, made by insect herbivores that feed upon internal plant tissues, were present at modest levels in the JARS locality. There were a total of fourteen damage types and 183 instances belonging to the four function feeding groups of piercing and sucking, leaf mining, galling, and oviposition (Table 3.2). In general, the proportion of intermediate and specialist damage is greater in the endophytic functional feeding groups than the ectophytic feeding groups (Table 3.2). Piercing-and-sucking insects puncture and siphon cells and fluid using elongate, stylet mouthparts. There were three piercing-and-sucking damage types found at the JARS locality (Figure 3.9 G?H). Generic stylet punctures resulting in small (< 2 mm) circular craters (DT46) were most common (Figure 3.9 G), followed by a series of three or more punctures (DT138) (Figure 3.9 F), and high densities of small (usually < 1 mm), carbonized punctures on tertiary venation (DT330) (Figure 3.9 H). DT330 is distinct from pathogen damage and leaf oil glands because the punctures are targeted preferentially along tertiary veins, unlike fungal spots, and often are not evenly spaced or patterned as are oil glands. 10 8 Oviposition, or egg laying into foliar tissue, was most common on the floating aquatic dicot Quereuxia sp. (PH12.2) (15 of the 29 oviposition occurrences at JARS). There were two oviposition damage types: oval oviposition scars arranged in parallel rows (DT100) (Figure 3.9 E), and oval oviposition scars that are not in a particular arrangement (DT101) (Figure 3.9C). Mines are produced by insect larvae that live and consume the plant organ from within, either in serpentine patterns, blotch patterns, or a combination of the two. There were three types of leaf mines found at the JARS locality and a total of six leaf-mining occurrences. The first mine was serpentine, packed with solid frass, a modest width expansion, and about 1 mm in length (DT43) (Figure 3.9 A). A second mine consisted of a short trajectory (< 1 cm in length) with no visible frass that began with a serpentine phase and ended in a relatively large blotch phase (DT176) (Figure 3.9 D). The third leaf mine was a blotch mine that had a polylobate margin and no visible frass (DT295) (Figure 3.9 B). Galls are envelopes of plant tissue elicited by a number of organisms, including insects and mites. Insect-mediated galls often provide nutrient supply and protection for the gall inhabitant. There were six gall damage types found at the JARS locality (Figure 3.10). The most frequently encountered galls were spheroidal to ellipsoidal in shape and occurred on the leaf lamina, which either avoided major veins (DT32) (Figure 3.10 E), occurred on primary veins (DT34) (Figure 3.10 D), or on secondary veins (DT33) (Figure 3.10 C). Other gall damage types included hemispheroidal galls (< 1 mm in diameter) that were tightly clustered (DT80) (Figure 10 9 Figure 3.9: Leaf mining, oviposition, and piercing and sucking damage types found at the JARS locality. A, Two serpentine mines with solid frass throughout and modest width expansion (DT43, plant host (PH) 31.2, DMNH EPI.45464). B, A blotch mine with polylobate margin and frass absent (DT295, PH12.1, DMNH EPI.45434). C, Oviposition scars occurring on the leaf lamina in no discernable pattern (DT101, PH12.1, DMNH EPI.45447). D, Two, short mines with an initial serpentine phase and a relatively large terminal chamber (DT176, PH41.1, DMNH EPI.45460). E, Oviposition scars arranged parallel to one another (DT100, PH12.1, DMNH EPI.45454). F, Three punctures along the margin of the leaf (DT138, PH16.1, DMNH EPI.45448). G, A puncture < 1 mm in diameter (DT46, PH36.1, DMNH EPI.45438). H, Numerous, small punctures oriented on tertiary venation (DT330, PH36.1, DMNH EPI.45470). Black scale bar = 1 cm; white scale bar = 1 mm. 11 0 3.10 A), ellipsoidal galls that occurred on the midvein (DT85) (Figure 3.10 F), and crater-like attachment points of deciduous galls (DT194) (Figure 3.10 B). Several functional feeding groups were outside the realm of endophytic and ectophytic feeding groups. These functional feeding groups included seed predation, pathogen infection, Incertae sedis, and domatia, which in total encompassed eight damage types (Figure 3.11). There was a single seed predation damage type, which consisted of small (< 0.5 mm in diameter) pits in the seed surface (DT74) (Figure Figure 3.10: Insect gall damage types found at the JARS locality. A, Small, hemispheroid galls of high density on the leaf surface (DT80, plant host (PH) 32.2, DMNH EPI.45433). B, A crater left behind by a deciduous gall (DT194, PH24.2, DMNH EPI.45461). C, A circular gall located on secondary veins (DT34, PH32.2, DMNH EPI.45450). D, A circular gall located on primary veins (DT33, PH16.1, DMNH EPI.45444). E, Circular galls on the leaf lamina that avoid primary and secondary veins (DT32, PH16.1, DMNH EPI.45445). F, An ellipsoidal gall located on a primary vein (DT85, PH29.2, DMNH EPI.45436). Black scale bar = 1 cm; white scale bar = 1 mm. 11 1 Figure 3.11 (following page): Pathogen damage, seed predation, Incertae sedis, and mite domatia found at the JARS locality in the Kaiparowits Formation (Utah, USA). A, Fungal damage along primary and secondary veins (DT221, plant host (PH) 36.1, DMNH EPI.45462).B, Fungal damage along the leaf margin (DT114, PH13.1, DMNH EPI.45472). C, Incertae sedis damage consisting of a pockmarked, roughened area (DT106, PH16.2, DMNH EPI.45447). D, Polylobate necrotic areas likely caused by a fungus (DT58, PH41.1, DMNH EPI.45427). E, Small, circular to ovoidal fungal spots in high density (DT281, PH13.1, DMNH EPI.45465). F, Seed predation with several small, circular pits (DT74, PH3.2, DMNH EPI.45534). G, Circular to polylobate fungal spots in medium density (DT229, PH36.1, DMNH EPI.45439). H, Mite domatia at the vein axils (DT339, PH41.1, DMNH.45456). Black scale bar = 1 cm; white scale bar = 1 mm. 11 2 3.11 F). Pathogen infection, usually associated with fungal infection, at JARS was relatively diverse yet uncommon, represented by five damage types and six occurrences. Fungal infection with polylobate margins (DT58) (Figure 3.11 D), necrotic tissue along the margin the leaf (DT114) (Figure 3.11 B), necrotic tissue along the primary and secondary veins (DT221) (Figure 3.11 A), small (< 1 mm), polylobate necrotic spots in clusters (DT229) (Figure 3.11 G), and very small spots of fungal necroses (< 0.5 mm) along major leaf veins and or margins (DT281) (Figure 3.11 E). Finally, one damage type of Incertae sedis (DT106) (Figure 3.11 C), which will likely be reassigned in the future and one type of mite domatia (DT339) (Figure 3.11 H) were discovered. Rarefaction for the richness of damage types by total surface area was calculated for the nine most common plant hosts at the JARS locality (Figure 3.12). Among individual plant hosts, the confidence intervals of most specimens overlapped and were not significantly different, with one notable exception. PH39.1 had a lower richness of damage types compared to PH41.1, PH12.1, and PH16.1. Additional sampling surface areas for many of the plant hosts will likely be needed to differentiate damage-type richnesses between the taxa. It is worth noting here that herbivory index, which is often not present in plant?insect associational studies due to the time-consuming nature of surface area measurements, standardizes leaf size, as shown here with the differences between the large-leaved PH41.1 and small-leaved PH12.1. Rarefaction by specimen count would yield tenuous curves considering the difference in average leaf size between several of the plant hosts. 11 3 0 20000 40000 60000 80000 100000 (mm 2 ) Figure 3.12: Rarefaction analysis of damage-type richness (Y axis) by surface area (X axis) for the nine individual plant hosts with > 20 specimens. 11 4 NMDS ordinations plots illustrated the predominant associations between the nine common plant hosts and the general categories of herbivorous insect damage (Figures 3.13?3.14). The plant host most associated with oviposition was Quereuxia sp. (PH12.1), whereas PH36.1 was most closely associated with piercing and sucking, Figure 3.13: Non-metric multidimensional scaling (NMDS) ordination with elipses, which include 84% of the datapoints closest to the centroid, for the nine dominant plant hosts (with at least a total of 5,000 mm2) and functional feeding groups present at the JARS locality. EFF is external foliage feeding, LM is leaf mining, GL is galling, IS is Incertae sedis, and OV is oviposition. 11 5 and PH16.2 trended towards pathogen and Incertae sedis damage (Figure 3.13). The elipses, which captured 84% of data points closest to the centroid, showed that PH36.1, PH12.1, and PH41.1 also occupied relatively distinct regions of the morphospace (Figure 3.14). The rest of the plant hosts (PH30.1, PH15.1, K16.1, PH39.1, and PH13.1) were clustered together with galling and external foliage 1.0 0.5 0.5 0.5 EFF sp39.1 EFF sp39.1 PS EFFPS 0.0 GL GLsp41.1 0.0 sp41.1 sp39.1 sp16.1 sp16.1 0.0 GL sp41.1 LM LM spP1S6.1 ?0.5 ?0.5 OVOV OV ?0.5 LM ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 1.0 0.5 OV LM 0.5 0.5 sp16.1 EFFEFF 0.0 sp41.1 sp39.1 sp39.1 GPLS 0.0 GL 0.0 GL PS sp41.1 sp39.1 PS sp41.1EFF sp16.1 sp16.1 ?0.5 ?0.5 OV LM ?0.5 OV LM ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 ?1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 0.8 0.8 0.5 0.4 0.4 EFF sp39.1 EFF sp39.1 EFFsp39.1 GL GL 0.0 GL 0.0 PS PS sp41.1 sp41.1 0.0 sp41.1 sp1PS6.1 sp16.1 sp16.1 LM OV ?0.4 ?0.4 OV ?0.5 OV LM LM ?1.0 ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 ?0.5 0.0 0.5 1.0 NMDS1 NMDS1 NMDS1 Figure 3.14 (following page): Non-metric multidimensional scaling (NMDS) ordination with elipses, which include 84% of the datapoints closest to the centroid, for the three most abundant plant hosts (with at least a total of 50,000 mm2) and functional feeding groups present at the JARS locality. EFF is external foliage feeding, LM is leaf mining, GL is galling, and OV is oviposition. 11 6 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 NMDS2 feeding, and PH41.1 was associated with this cluster and with leaf mining. When only plant hosts with high total surface areas were included in the ordination, we see that again PH41.1 occupies a distinct region of the morphospace (Figure 3.14). Discussion The JARS locality within the Kaiparowits Formation is the first flora to be systematically analyzed for plant?insect associations in the Campanian Age (83.6? 72.1 Ma). It captures a remarkable snapshot of a Late Cretaceous angiosperm- dominated landscape (Miller et al. 2013), as evidenced by the taxonomic diversity of plants, in which 70.0% of all plant hosts and 80.9% of all specimens at this locality are angiosperms. The Late Cretaceous was a time of large-scale shifts in insect diet from gymnosperms and ferns to angiosperms, coupled with extinction or diversification events for some herbivorous insect lineages (Labandeira 2014). In particular, the plant?insect associations at JARS illustrate specialization on host plants by Kaiparowits insects, biogeographic patterns in Campanian insect damage, and provides a strong baseline for comparisons to other Cretaceous floras and for future work in the Campanian. JARS Damage-Type Richness and Comparisons to Catula gettyi The richness of damage types for the nine most abundant plant hosts are relatively similar to one another, as seen by the overlap in confidence intervals (Figure 3.12). Only PH39.1 had a lower richness of damage types compared to PH41.1, Quereuxia sp. (PH12.1), and PH16.1. Based on this pattern, further sampling 11 7 may be needed to better understand the true diversities of all plant hosts, especially for small-leaved taxa. The NMDS also shows differences between several of the plant hosts, notably PH41.1, PH36.1, and Ph12.1, which also had different associated functional feeding groups. For the taxa that did have high damage type diversities and/or herbivory indices (PH41.1, Quereuxia sp. (PH12.1), and PH16.1) we also find interesting patterns when compared to one of the most well- sampled taxa for plant? insect associations in the fossil record, Catula gettyi (Figure 3.15) (Maccracken et al. in review-a). There are no other Campanian floras systematically analyzed for insect herbivory, but quantitative and qualitative comparisons of individual JARS locality plant hosts can be made to Catula gettyi. In Chapter 2, I analyzed insect damage on a single plant host species, C. gettyi, also from the Kaiparowits Formation. Insect damage on C. gettyi includes 40 damage types, with five leaf mines, three damage types previously unknown in the fossil record, and an herbivory index of 2.102% for a randomly selected subsample. The C. gettyi herbivory index is similar to that of PH13.1 (2.00%) and Quereuxia sp. (PH12.1) (3.82%), and lower than the herbivory index of PH41.1 (10.68%). This means that on average, the intensity of herbivory, or the amount of surface area removed by insect herbivores, is greatest for PH41.1. However, when we look at damage-type richness and composition across the four plant hosts the differences are more striking. When rarefaction analysis is calculated for damage type richness by total sampled surface area, we see that the JARS plant hosts are not significantly different than C. gettyi. Interestingly, there is only moderate overlap in the suites of damage types found on the JARS plant hosts and C. 11 8 gettyi. Notably, there is no overlap between leaf mining, as C. gettyi has five leaf mine damage types (DT35, DT36, DT37, DT45, DT332), whereas PH41.1 has two (DT43, DT176), and Quereuxia sp. has one (DT295). This is expected, as leaf miners tend to be highly specialized to one host plant (Sinclair and Hughes 2010). A (mm 2 ) B C (mm 2 ) (mm 2 ) D E (mm 2 ) (mm 2 ) Figure 3.15: Rarefaction analysis of the damage-type richness of Catula gettyi (indigo) and the JARS locality plant hosts (PH) 41.1 (lilac), PH13.1 (orange), and Quereuxia sp. PH12.1 (blue). A, Rarefaction by surface area (X axis) and number of damage types (Y axis). B, Herbivory index of C. gettyi with 95% confidence interval ranges. C, Herbivory index of PH41.1 with 95% confidence interval ranges. D, Herbivory index of Quereuxia sp. (PH12.1) with 95% confidence interval ranges. E, Herbivory index of PH13.1 with 95% confidence interval ranges. 11 9 Host Specialization and Potential Insect Culprits We documented a range of specialist insect damage on the plant hosts at the JARS locality, the majority of which were endophytic feeding types (Table 3.2). Functional feeding groups are established based upon both homologous and analogous mouthpart morphologies and on feeding modes (Labandeira 2019, Labandeira et al. 2007c). In general, endophytic functional feeding groups (piercing and sucking, leaf mining, galling, and oviposition) hold more clues to the identity of the insect culprit than that of ectophytic feeding groups (hole feeding, margin feeding, skeletonization, and surface feeding). This is due to greater plant host specificities (monophagous or oligophagous) among endophytic feeders (Sinclair and Hughes 2010) and their propensity towards distinctive feeding behaviors or morphologies resulting in unique signatures on leaves, such as leaf mines and scale insect impressions (ex. Hickey and Hodges 1975, Maccracken et al. in review-b, Sohn et al. 2019a, Wilf et al. 2000) compared to hole feeding insects, for example. These more distinctive damage types also often have analogues in modern plant?insect associations, which aid in the identification of the insect culprit (see Chapter 4). In contrast, ectophytic feeding groups are produced by the most common mouthpart type: insects with mandibulate mouthparts, which are represented by many different insect orders at various life stages (Labandeira 2019). In addition, the patterns of ectophytic feeding may be produced by a large number of insect species and in turn, an individual may make multiple damage types (Carvalho et al. 2014). There are exceptions to this generalization, for instance the leafcutter bee produces a distinct margin feeding damage type (DT81: a near perfect circular arc, not present at JARS) 12 0 (Sarzetti et al. 2008). However, based upon the ectophytic feeding damage types found at JARS, we cannot link any the ectophytic damage types to particular insect clades. We are able to, however, postulate about the potential identities of the endophagous insect culprits, which provides a baseline for the potential suite of herbivorous insects in the Kaiparowits Formation. Three of the four piercing and sucking damage types (DT46, DT47, DT330) at the JARS locality are made by herbivorous insects with a stylet-like mouthpart, such as Hemiptera (true bugs) and Thysanoptera (thrips). Moreover, the piercing and sucking damage types are not associated with impression marks, indicating that the JARS piercers and suckers are free-living herbivores as opposed to hemipteran scale insects. Although we cannot narrow the insect culprit identification beyond that of a free-living Hemiptera or Thysanoptera, we understand that Hemipteroidea (the clade of Hemiptera and Thysanoptera) evolved during the Mississippian (ca. 350 Ma) (Misof et al. 2014) and had a substantial diversity by the Cretaceous (Jarzembowski 1995, Ross et al. 2000). Furthermore, the diameter of the three piercing and sucking damage types are larger in size than thrips damage, as thrips are minute (usually ? 1 mm in length) and it is likely that the JARS piercing and sucking was produced by hemipterans, which are larger (between 1 mm and 15 cm in length). The three other endophytic feeding groups give clues to the identities of the damage-causing insects. First, leaf mining damage types are made by larval insects with mandibulate mouthparts and today are comprised of four orders: Lepidoptera (moths), Diptera (flies), Hymenoptera (sawflies), and Coleoptera (beetles), although moths and flies are the most common leaf miners (Cs?ka 2003, Hering 1951, Sinclair 12 1 and Hughes 2010). There are three leaf mining damage types at the JARS locality (DT43, DT176, DT295). The damage type DT43 is similar in morphology to nepticulid leaf mining moth mines (family Nepticulidae). Nepticulid moths are known from leaf mines of Early Cretaceous floras (Doorenweerd et al. 2015, Labandeira et al. 1994, Wahlberg et al. 2013) and are therefore likely candidates for the producers of DT43. The leaf mines DT176 and DT295 are not identifiable to clade, but are likely the work of leaf mining moths based on the size and trajectories of the mines (Donovan et al. 2014). Second, gall makers are known from the arthropod orders: Hymenoptera (gall wasps); Diptera (gall midges); Acari (mites); and a few Hymenoptera (sawflies); Lepidoptera (moths); and Coleoptera (beetles) (Meyer 1987), as well as fungal pathogens (Akai 1950). The gall damage types at JARS are ranked as intermediate (DT32, DT34, DT194) or specialist (DT33, DT85) in host plant specialization, but identification of gall to a particular arthropod clade is not possible. Third, oviposition of insect eggs into the tissue of a plant host is frequently encountered on Quereuxia sp. and PH36.1 (Figure 3.9 C). Oviposition on Quereuxia sp. is also reported from the Campanian of Russia and is attributed to dragonfly (Odonata) oviposition (Vasilenko 2008) (see below for an analysis of Quereuxia oviposition). The NMDS ordination plot for each of the nine common plant hosts and general categories of herbivorous insect damage also demonstrates insect specialization for particular plant hosts at JARS. As mentioned above, Quereuxia sp. (PH12.1) is often targeted by ovipositing insects, likely belonging to the order 12 2 Odonata. PH36.1, a putative moonseed (Menispermum), was targeted by piercing- and-sucking insects, likely an hemipteran. PH41.1 was also targeted by leaf miners, as well as external foliage feeders that caused generalized hole and margin feeding damage. Perhaps the most intriguing insect herbivory at JARS was targeted on PH41.1 (see Appendix E for a description of this taxa). This taxon has very large leaves on average 3176.28 mm2, which included a moderate to high diversity of damage types (23 damage types, Figure 3.12), a 91.2% specimen damage rate, and the greatest herbivory index of any JARS plant host (10.54%). The damage types that accounted for much of the insect damaged surface area were categorized as external foliage feeding, which, although moderately diverse may have been produced by the same insect pest. Interestingly, this plant host is also found at another Kaiparowits locality, DMNH loc. 4000, although the leaves are far less damaged by insects. This, coupled with the anomalously high herbivory index at the JARS locality, implies that PH41.1 was not universally herbivorized intensely and we cannot say that it is one of the most heavily herbivorized taxa in the paleobotanical record. Instead, the data point to an outbreak of insect herbivory, a rare event in the fossil record (Labandeira 2012). A quantitative analysis of insect damage on PH41.1 across the entire Kaiparowits Formation, which is outside the scope of this chapter, is needed to test this hypothesis. Biogeography of Odonate Oviposition Quereuxia is a morphogenus (genus identified solely by morphology and unassignable to a plant family) of an extinct aquatic angiosperm, sometimes 12 3 preserved as a rosette of small, circular leaves or as a detached leaf (Hickey 2001). Quereuxia are found in a range of Late Cretaceous to Paleocene deposits (Golovneva 2000). Specimens of this morphogenus are frequently collected in the Kaiparowits Formation (Miller et al. 2013) and are found in other Laramidian formations (Crabtree 1987, Crabtree 1989, Parrish and Spicer 1988, Spicer and Parrish 1987) as well as Asian and European floras of the same age (Golovneva et al. 2008, Herman and Kva?ek 2007, Kodrul et al. , Kva?ek and Herman 2004). Quereuxia of Campanian Age are especially common in the Amur region of Russia, and oviposition was extensively described on Q. angulata (Lesq.) Krysht. leaves from the Udurchukan locality of the Upper Kundar Formation (Vasilenko 2008). Vasilenko (2008) described multiple ichnospecies of Paleoovoidus, which was hypothesized to have been produced by damselfly and dragonfly oviposition. Many of the oviposition scars described by Vasilenko (2008) are lines of eggs or egg scars produced by the arcuate (fan-shaped) movement of an odonate ovipositor while the thorax was initially stationary on the leaf and the abdomen swung in broad arcs as the insect moved slightly forward (Hellmund and Hellmund 1996). Similar and abundant oviposition scars are also found on Quereuxia leaves from the Kaiparowits Fm., with 27.5% of the JARS Quereuxia specimens exhibiting oviposition damage (Figure 3.9 B,C,E). These damage types (DT100, DT101), although not in arcuate patterns, do include linear arrangements of eggs and are hypothesized to be odonate in origin. Interestingly, there were several species of aquatic and floating aquatic plants at the JARS locality, including Cobbania c.f. corrugata and Hydropteris sp., none of which 12 4 exhibited oviposition scars. This indicates that odonates targeted Quereuxia, even if there were other species of floating aquatic angiosperms available for oviposition. Although the species of Quereuxia and species of insect culprits of the Kaiparowits Formation and Upper Kundar Formation are likely different, this finding supports our hypothesis that ecological associations of Quereuxia extend over at least two continents and several million years. Intercontinental niche conservatism of deep time plant?insect associations can provide clues into biogeography of plants and their insect herbivores. During the Campanian, North American and Asia were connected across Cretaceous Beringia (LePage et al. 2005). With hospitable environments extending into the polar regions at this time, biotic interchange across the Beringian Corridor was likely established by the Albian at 100 Ma (LePage et al. 2005). Indeed, biotic interchange across this landmass is known from the Paleocene, but Late Cretaceous interchange is less well known (Fiorillo 2008, Vavrek et al. 2014, Wolfe 1975), and this finding may be the first evidence of widespread niche conservatism between North American and Asia during the Campanian. Further research is required to study the paleobiogeographic distributions of Quereuxia and its oviposition associations. Conclusions Our results indicate that the JARS locality within the Kaiparowits Formation included a moderate diversity of plant?insect associations. When compared to the extremely well-sampled Catula gettyi, damage type diversities for multiple JARS 12 5 taxa were likely greater, although additional sampling would be useful for more in- depth comparisons. The JARS locality also hosted a number of specialized herbivores, which included leaf-mining moths, chewing insects, piercing-and-sucking hemipterans, and galling insects. Several taxa were also preferentially targeted by different guilds of specialist insect herbivores, which included oviposition, leaf mining, and piercing and sucking. The diversity, intensity, and specialization of the JARS locality plant?insect associations appear to be on par with the overall diversity of the Kaiparowits Formation. Acknowledgements Thanks to the coauthors on this chapter: I. M. Miller, G. Bate, T. Vatan, and C. C. Labandeira. We are obliged to the Denver Museum of Nature and Science?s Leaf Whackers Group for preparation of the JARS fossil specimens, and to N. Neu-Yagle, K. MacKenzie, G. Rossetto, and R. Rissman for their support. The Denver Museum of Nature and Science provided financial support for collections work. Thanks to J. Shultz his ongoing mentorship; C. Mitter, D. Gruner, and C. Delwiche for their guidance; and to the undergraduate research assistants R. Bank, E. Boswell, G. Doyle, J. Kavanaugh, I. Rolfes, and S. Win. We are also grateful to K. Hamby and E. Tienens for their advice and edits. Finally, an enormous thanks to S. Schachat for her help with the analyses. 12 6 Chapter 4: A new Late Cretaceous leaf mine Leucopteropsis spiralis gen. et sp. nov. (Lepidoptera: Lyonetiidae) and the deep time origin of a common agricultural pest Abstract A new fossil leaf mine ichnogenus and species, Leucopteropsis spiralis gen. et sp. nov. (Lepidoptera: Lyonetiidae), from the Late Cretaceous Kaiparowits Formation (~76.6 to 74.5 Ma) in Utah, USA, is the earliest record (75.6 ? 0.18 Ma) and only reliably identified fossil of a lyonetiid leaf-mining moth, as well as one of the oldest known fossils within the Yponomeutoidea?Gracillarioidea clade. The morphology of the fossil mine is reliably associated with Cemiostominae in mine morphology and indistinguishable from mines produced by extant members of the genus Leucoptera, such as the mountain ash bent-wing moth, Leucoptera malifoliella O. Costa, 1836. This fossil provides an important Late Cretaceous (~76 Ma) calibration point for the lepidopteran phylogeny and underscores the importance of ichnofossils in the lepidopteran fossil record. 12 7 Introduction Ichnofossils, or the trace fossil evidence of biological activity, are important for the study of organisms in deep time. In particular, trace fossils provide direct evidence of behavior and ecological associations among species, of which the body fossil record alone often lacks (Labandeira et al. 2007c). These behaviors include feeding, oviposition, nesting, burrowing, boring, locomotion, and excretion (Buatois and M?ngano 2011). Ichnofossils are especially valuable for the study of organisms with relatively poor fossil records, such as insects (Labandeira 2006a, Labandeira et al. 2007c). While insects have the greatest described species diversity of any group of extant organisms (Adler and Foottit 2009, Gaston 1991, Nielsen and Mound 2000), their fossil record is sparse relative to their estimated diversity and abundance through time (Schachat et al. 2019). Deposits of exceptional preservation, or Lagerst?tten, on occasion provide vivid snapshots of insect faunas through time and space; however, most terrestrial fossil assemblages entirely lack insect body fossils. The fossil record of insects also is skewed by their taphonomic (fossilization) potential, which is categorized by insect inputs, such as insect size, morphology, fragility and taxonomic group, as well as external context, such as depositional environment, water depth, and energy levels (Smith 2012). In this context, many moths (Order: Lepidoptera), which have small and lightly sclerotized bodies, consequently are not well-represented in Lagerst?tten deposits (Labandeira and Sepkoski 1993). Indeed, the diversity of fossil moths and butterflies is about half that of the predicted fossil diversity based upon their extant 12 8 diversity (Labandeira and Sepkoski 1993). Nevertheless, the fossil record of lepidopterans is bolstered by phylogenomics (Kawahara et al. 2019, Misof et al. 2014, Sohn et al. 2013) and an extensive trace fossil record (Kozlov 1988, Labandeira 1994, Sohn et al. 2012). The most prolific insect trace fossils are the feeding traces on leaves by herbivorous insects (Labandeira et al. 2007c). Such fossilized plant?insect associations form the basis for estimates of the diversity and intensity of herbivory in ancient floras (ex. Adroit et al. 2018a, Currano et al. 2019, Donovan et al. 2018, Filho et al. 2019, Gunkel and Wappler 2015, Labandeira et al. 2002b, Maccracken and Labandeira 2020, Robledo et al. 2018, Schachat et al. 2015, Schmidt et al. 2019, Wilf et al. 2006), as well as providing first and last appearance estimates for fossil- calibrated molecular phylogenies when trace fossils are attributable to specific lineages of herbivorous insects (ex. Doorenweerd et al. 2015, Labandeira et al. 1994, Labandeira et al. 2001, Lopez-Vaamonde et al. 2006, Wappler and Ben-Dov 2008, Winkler et al. 2009a). Although identification of the insect culprit is frequently impossible due to the unparalleled diversity of insect herbivores (Nielsen and Mound 2000), coupled with convergences in herbivore mouthparts (Labandeira 2019) and in feeding behaviors (Carvalho et al. 2014), the taxonomic identification of an insect herbivore to family, genus, or species is possible for some specialized types of feeding (ex. Jud and Sohn 2016, Sarzetti et al. 2008, Wilf et al. 2000, Winkler et al. 2010). Examples include the leaf margin removal by megachilid bees (Sarzetti et al. 2008, Wedmann et al. 2009), leaf mines of a Phytomyza leafmining fly (Winkler et al. 2009a), agromyzid fly leaf mines (Jud and Sohn 2016), scale impression marks and 12 9 covers by diaspidid scale insects (Wappler and Ben-Dov 2008), and possible hispine beetle (Cephaloleichnites strongi.) damage on Cretaceous gingers (Zingiberaceae) (Garc?a-Robledo and Staines 2008, Wilf et al. 2000). Recently, a blotch leaf mine with a distinctive frass trail was found on a fossil leaf from the Kaiparowits Formation, of Upper Cretaceous (Campanian) age, in southeastern Utah, USA. This leaf mine is structurally identical to those made by species in the genus Leucoptera, a clade of micro-moths that today are well known for their damage on agricultural crops (Bajec et al. 2009, Bradley and Carter 1982, Maciesiak 1999, Notley 1948, Schmitt et al. 1996). The fossil leaf mine is most similar to the mines of extant Leucoptera, such as the wildly polyphagous leaf miner species L. malifoliella O. Costa, 1836 (Bajec et al. 2009, Ellis 2018, USDA 2011). Here, we describe the leaf mine ichnofossil and discuss this ichnospecies within the phylogeny of the Lyonetiidae. Geological Setting The new ichnospecies was found on a fossil leaf from the Kaiparowits Formation is in the Grand Staircase-Escalante National Monument, Utah, USA (Figure 4.1). The formation is ~1,005 m thick and consists primarily of sandstone and mudstone beds derived from the Sevier Orogenic Belt immediately to the west (Beveridge et al. 2020, Roberts et al. 2005). These sediments were deposited in channel, lake, and floodplain settings on the western margin of the Western Interior Seaway coastal plain that extended from the Arctic to the Gulf of Mexico (Beveridge 13 0 Figure 4.1: (a) Map of the Grand Staircase?Escalante National Monument in Utah, USA, with the Kaiparowits Formation outcrop shown in green. Solid yellow denotes new monument boundaries (December 2017) and former monument boundaries are stippled in light yellow. DMNH loc. 4150, the Lost Valley locality, is denoted by a star. Map adapted from Crystal et al. (2019). (b) Stratigraphic column for the Kaiparowits Formation redrawn from Roberts (2007). Stratigraphic position of DMNH loc. 4150 is indicated. 13 1 et al. 2020, Roberts et al. 2005, Roberts et al. 2013). The Kaiparowits Formation is divided into informal lower, middle, and upper units comprising ~860 m of strata (Roberts 2007) and a new formal Upper Valley Member that adds ~255 m at the top of the formation (Beveridge et al. 2020). The middle unit produces the vast majority of fossil localities, including fossil plant localities (Miller et al. 2013, Roberts 2007). Based on 40Ar/39Ar dating of volcanic ashfall beds, the age of the informal lower to upper units in the Kaiparowits Formation (the traditionally recognized ~860 m of section) is 76.49 ? 0.14 to 74.69 ? 0.18 Ma (Roberts et al. 2013). The Upper Valley Member extends the top contact to ~72.8 Ma with a confidence interval of about one million years (Beveridge et al. 2020). The fossil floral and faunal composition, alongside evidence of depositional environments, suggests that the Kaiparowits Formation was deposited in a warm and humid palaeoclimate. Fossil leaves indicate a mean annual temperature of ~22 ?C and mean annual precipitation of ~180 cm per year (Miller et al. 2013). Oxygen and carbon isotopes, and palaeoclimate modeling, suggest possible monsoonal weather patterns (Sewall and Fricke 2013) and seasonal flooding (Crystal et al. 2019). Considering both depositional and fossil evidence, the palaeo-landscape of the Kaiparowits Formation arguably was similar to that of the present-day Gulf Coast in North America and certain areas of Southeast Asia (Crystal et al. 2019, Roberts 2007). The new ichnospecies was found on a fossil leaf collected from DMNH loc. 4150, known as the Lost Valley locality. The depositional environment and leaf preservation at DMNH loc. 4150 are described in Maccracken et al. (in review-a, 13 2 2019). Briefly, fossil leaves occur as compression?impression fossils in stacked 5?10 cm thick, fine-grained sandstone beds with minor mud partings. The depositional environment is interpreted as a medial to distal crevasse splay resulting from an event or events that infilled a perennial pond or small lake (Maccracken et al. in review-a). DMNH loc. 4150 occurs in the middle member of the Kaiparowits Formation about 415 ? 10 m above the base of the formation (Figure 4.1). Considering the stratigraphically nearest dated volcanic ash beds, using a depositional rate of 41 cm/1,000 years (Roberts et al. 2013), and assuming continuous deposition, the age of DMNH loc. 4150, and the new fossil ichnospecies, is 75.6 ? 0.18 Ma. Materials and Methods The discovery of the leaf mine was made while searching for evidence of insect damage on fossil leaves from DMNH loc. 4150. The leaf mine occurs on a single part-and-counterpart specimen (DMNH 47962a and DMNH 47962e). The specimen is housed in the palaeobotanical collections at the Denver Museum of Nature & Science. A Motic SMZ-161 stereoscopic microscope was used to view the fossil leaves. Detailed photographs were taken using a Canon EOS 5D Mark II camera with a Canon 65mm 1?5x macro lens. This assembly was mounted on StackShot hardware on a copy stand. Digital images were processed using Adobe Photoshop CC? (2017.01) and Zerene Stacker? focus-stacking software. Dimensions of the leaf mine were measured in Adobe Photoshop CC? (2017.01) and ImageJ (Schneider et al. 2012). 13 3 For the phylogenetic analysis, DNA barcodes were obtained from GENBANK (www.ncbi.nlm.nih.gov/genbank) for 15 species of extant Lyonetiidae (lyonet moths) and two out-groups of Gracillariidae (leaf blotch miner moths). Accession numbers of all these sequences are provided in Table 4.1. The collected DNA barcodes were aligned and edited using Geneious v. 11.1.4 (Biomatters Ltd.). Table 4.1: Accession numbers and base-pair (bp) lengths for the COI sequences in GENBANK (regular font) and the BOLD system (bold font). Family Genus Species Accession No. Seq. length (bp) Gracillariidae Caloptilia fidella JN272059.1 658 Gracillariidae Caloptilia azaleella HM405768.1 653 Lyonetiidae Lyonetia clerkella KX360270.1 658 Lyonetiidae Lyonetia prunifoliella MG470066.1 588 Lyonetiidae Lyonetia ledi KT147628.1 630 Lyonetiidae Lyonetia candida MG468023.1 588 Lyonetiidae Leucoptera lustratella JF853896.1 658 Lyonetiidae Paraleucoptera albella KR446906.1 581 Lyonetiidae Paraleucoptera sinuella HM873108.1 658 Lyonetiidae Perileucoptera coffeella LTOL915-08.COI-5P 658 Lyonetiidae Leucoptera sp. (KLM) MH417719.1 632 Lyonetiidae Leucoptera malifoliella KF367653.1 684 Lyonetiidae Leucoptera heringiella DEEUR1010-16.COI-5P 407 Lyonetiidae Leucoptera laburnella KR941504.1 576 Lyonetiidae Leucoptera orobi JF853767.1 658 Lyonetiidae Leucoptera lathyrifoliella KT782401.1 658 Lyonetiidae Leucoptera spartifoliella KR940230.1 588 A phylogenetic tree for the aligned DNA barcodes was constructed under the Maximum Likelihood (ML) criterion, using a default setting for RAxML-HPC Blackbox (Stamatakis 2014) through CIPRES Science Gateway website (www.phylo.org). Confidence was estimated by bootstrapping (BP), implemented in RAxML with 1000 resampling sets. The resulting trees were visualized using FigTree v.1.4.3 (Rambaut 2015), with a root at the divergence between in-groups and two species of Caloptilia. For comparison, the Neighbor-joining (NJ) tree was constructed 13 4 for the same DNA barcode data, using the Geneious tree builder in Geneious ver. 11.1.4. The genetic distance model was set as HKY with ?resampling tree? option (BP pseudoreplicates = 1,000). A formal description is forthcoming and all references to this ichnogenus and species should refer to that publication. Systematic Paleontology Phylum Arthropoda von Siebold, 1848 Subphylum Hexapoda Latreille, 1825 Class Insecta Linnaeus, 1758 Order Lepidoptera Linnaeus, 1758 Family Lyonetiidae Stainton, 1854 Ichnogenus Leucopteropsis Maccracken, Sohn, Miller & Labandeira, 2019, gen. nov. (Figure 4.2A?C) Type ichnospecies. Leucopteropsis spiralis Maccracken, Sohn, Miller & Labandeira, 2019, sp. nov., by monotypy Ichnogenus diagnosis.?Blotch mine large, circular to sub-circular in shape. Outer rim of mine thickened and dark in color. Oviposition site near center of mine on abaxial side of leaf, avoiding major leaf veins and leaf margin. Frass trail dark, continuous, thick, arcuate, and encircling in trajectory; starting near center of mine at 13 5 oviposition site; expanding in width and darkening in color as it concentrically spirals towards outer edge. Mine background light in colour, contrasting with a darker hued frass trail, and equally dark outermost rim of reaction tissue. Frass trails do not cross but do bifurcate and rejoin in their trajectories. No exit or pupation site is evident. Figure 4.2: Leucoptera fossil leaf mine: (a) The partially broken specimen includes the newly described leaf mine. (b) A close up of the leaf mine. (c) An overlay drawing of the leaf mine. 13 6 Etymology.?The ichnofossil resembles leaf mines are produced by extant Leucoptera malifoliella (Lepidoptera: Lyonetiidae) leaf miners. Derivation of the ichnogenus name is from the classical Greek words leukos, for "white"; pteron for "wing"; and ?psis for ?likeness?, or ?resemblance?). Material.?One part and counterpart specimen (DMNH 47962a and DMNH 47962e) occurs on plant morphotype KP90 (description below) from DMNH loc. 4150 located in the Upper Cretaceous Kaiparowits Formation of Utah, USA. Precise GPS locality information is available upon request. Description.?The mine is comprised of two distinct regions: a lighter inner circle of removed tissue with relatively even shading, and an outer portion with a concentric, spiral frass trail. The surface area of the preserved leaf mine covers 97.10 mm2 and our estimate for the full leaf mine is 105.96 mm2; 91.6% of the mine is estimated to be present. The mine is not perfectly circular; at the widest aspect, the mine is 11.49 mm in diameter, although the fossil leaf specimen containing the mine is broken, we estimate the full diameter close to 12.30 mm. The intact side has a radius of 7.42 mm at the greatest breadth and we estimate the radius of the broken-off portion to be 4.60 mm. This makes our reconstructed mine surface area estimate fairly conservative and the surface area of the full mine could have been greater than our approximation. As the larva moved within the leaf, it fed on internal leaf tissue and left a trail of frass that marked its precise trajectory. The movement of the larva inside the fossil leaf appears to start at the center of the mine and radiated in an arcuate trail that expanded outward with each concentric turn. The frass trails are between 0.25 mm 13 7 and 0.79 mm in width and the distance between frass trails is between 0 mm and 0.84 mm. Along the peripheral edge of the larval feeding zone is a thickened rim of reaction tissue produced by the plant in response to the herbivorized edge that is 0.16 mm to 0.73 mm in width. A pupation chamber is not present, and pupation site likely was external to the mine. Remarks.?We circumscribe Leucopteropsis to any leaf mine of fossil Cemiostominae that exhibit a spirally concentric fecal trajectory. This ichnogenus is indistinguishable from blotch leaf mines produced by moths in the extant genus Leucoptera. In general, Leucoptera mines are blotches that are circular in shape, with arcuate, approximately concentric frass trails. The closest morphology to Leucopteropsis spiralis mines is extant mines produced by Leucoptera, such as those produced by L. malifoliella, as the frass trails of each mine are indistinguishable from one another. Consequently, we are confident that the leaf miner of L. spiralis belongs within the family Lyonetiidae. We erect a new genus for this mine-type because we are unable to know the morphology, and therefore the taxonomy, of the moth specifically responsible for L. spiralis mines, and an ichnogenus for this mine-type has not been named previously. Ichnospecies L. spiralis Maccracken, Sohn, Miller & Labandeira, 2020 sp. nov. Specific diagnosis.?Same as the generic diagnosis. Etymology.? The specific name refers to the spiral pattern of the frass within the blotch mine; from classical Greek, derived from speira, meaning ?spiral?). 13 8 Type specimens.?Designated herein: holotype DMNH 47962a and DMNH 47962e, part and counterpart (Figure 4.2A?C). Damage type.?DT178. The Leucopteropsis spiralis mine is included in the amended version of the Guide to Insect (and Other) Damage Types on Compressed Plant Fossils (Labandeira et al. 2007c) as damage type DT178. Differential Diagnosis.?A blotch mine, identified as Tischeria sp. (Specimen no. IU15808-7545, Mine type KLm14) from the Maastrichtian of Tennessee (Ripley Formation) was illustrated by Stephenson (1992) (Sohn et al. 2012, Stephenson 1992) and the damage type was described as a medium to large blotch mine generally on the primary vein, with thickened outer walls and frass absent. The accompanying illustration of mine type KLm14 is similar to the Leucopteropsis mine, but close examination of the specimen revealed features inconsistent with a Leucopteropsis mine (Supplementary Figure 4.1 A,B in Appendix D). A second blotch leaf mine from the Miocene San Jos? Formation of Argentina was compared to extant Leucoptera malifoliella moths (Specimen no. CTES-IC 176, new damage type) (Robledo et al. 2018). The mine is circular, ca. 4 mm in diameter, with a smaller, circular patch of frass ca. 1.5 mm in diameter and bordered by a thick fringe of reaction tissue. As noted in the original paper, the frass does not form a spiral pattern within the mine, a characteristic of Leucoptera mines (Ellis 2018, Robledo et al. 2018, USDA 2011). We posit that this mine is more similar in morphology, although not necessarily related to, leaf mines made by the gracillariid moth species Phyllonorycter issikii Kumata, 1963 (Supplementary Figure 4.1 C, D). 13 9 Host Plant.?The Leucopteropsis spiralis mine occurs on a partial angiosperm leaf of unknown affinity. We provide a brief description of the host plant here; a full description of the leaf architecture of the host taxon is provided in the Supplementary Material (Appendix D). The taxon is provisionally designated as KP90 in the Kaiparowits Formation morphotype series. KP90 is pinnate, with somewhat irregularly spaced brochidodromous secondary venation, interspersed with frequent intersecondary veins. The primary vein is notably thicker than the secondary and higher order veins. The tertiary venation is mixed alternate and opposite percurrent, and quaternary venation appear irregular reticulate. KP90 is untoothed and exhibits a somewhat undulating margin; it is typically oblong and slightly asymmetrical in shape. The petiole is thick compared to the leaf area indicating a high leaf mass per area (Royer et al. 2007). Overall, many specimens of KP90 are generally well preserved and exhibit 4th and 5th order venation. We have identified 67 specimens of KP90 from DMNH loc. 4150. While a comprehensive examination of all plant localities in the Kaiparowits Formation has yet to be completed, KP90 appears minimally in three other localities within the formation. Although there is presently only one known instance of the Leucopteropsis mine, KP90 is heavily herbivorized and hosts a diverse suit of insect herbivore traces. Only twenty of the leaf specimens (29.85%) had no apparent damage while 47 specimens (70.15%) exhibited between one and four damage types. Among all KP90 specimens, there were a total of 25 damage types, grouped into seven functional feeding groups: margin feeding, hole feeding, skeletonization, surface feeding, piercing and sucking, mining, and galling (see Labandeira et al. 2007c for a 14 0 description of the damage spectra). Notably, there are other blotch-mine damage types found on KP90, which differ in shape and often lack frass as compared to the L. spiralis mine. The leaf specimen housing the L. spiralis mine (DMNH 47962a and DMNH 47962e) also contains margin feeding (DT15) and two types of hole feeding (DT01, DT02) (Labandeira et al. 2007c). Results and Discussion Evidence of lepidopterans during the Cretaceous, including the Leucopteropsis spiralis leaf mine described herein, is crucial to understand the diversity and evolution of Lepidoptera. Lepidopteran body fossils and ichnofossils are rare in Mesozoic deposits and are often difficult to identify to specific taxonomic groups (Schachat and Gibbs 2016, Sohn et al. 2015). The earliest known lepidopteran fossils are wing scales recovered from latest Triassic of Germany (ca. 212 Ma), and include scales of a glossatan moth (van Eldijk et al. 2018). Following this occurrence, the stem group lepidopteran Archaeolepis mane Whalley has been identified from the Lower Jurassic (ca. 195 Ma) of England (Sohn et al. 2015, Whalley 1986, Whalley 1985). While these body-fossil discoveries clearly indicate a Jurassic lepidopteran radiation, the diversity and abundance of lepidopteran specimens remain low throughout the Mesozoic Era (Zhang et al. 2013). A survey of lepidopteran fossil specimens from the Jurassic and Cretaceous Epochs found a total of 177 specimens (100 body fossils, 77 ichnofossils), which accounts for approximately 3% of all identified lepidopteran fossil specimens (Sohn et al. 2015). The discovery and description of Leucopteropsis spiralis contributes to that short list. 14 1 Identity of the leaf miner The morphology of leaf-mines often lacks phylogenetic characters that can be ranked above the species-level. Despite their usefulness for identification of mine makers (Jud and Sohn 2016, Winkler et al. 2009b), this issue has led to serious concerns about identifications of lepidopteran leaf-mine fossils based on extant analogs (Grimaldi and Engel 2005). Indeed, convergence in two major mine features, overall trajectories and frass patterns, is commonly found among multiple lepidopteran genera of higher taxonomic groups (Hering 1951). However, as an exception, some leaf miners within the lyonetiid subfamily Cemiostominae produce distinctive blotch mines that are unique and not found in other leaf mining clades (Dugdale et al. 1998). The mine maker of the leaf fossil in the present study is reliably identified as Cemiostominae, based on the characteristics described below. Larvae of Cemiostominae are miners in the leaves and bark of host plants and they pupate in a fusiform, silken cocoon outside of the leaf mine (Dugdale et al. 1998). Within the Lyonetiidae, the larvae of subfamily Cemiostominae principally produce blotch or linear-blotch mines that differ structurally from the typically narrow galleries of leaf-mines created by larvae in the subfamily Lyonetiinae (Dugdale et al. 1998). However, this distinction is not obvious, as some lyonetiids, e.g. Lyonetia prunifoliella, produce linear-blotch mines similar to Cemiostominae (Hering 1951). Phyllobrostis, which are leaf miners closely related to Lyonetia (Sohn 2013, Sohn et al. 2013), produce mines of dark blotches whose upper epidermis is consumed and deposited as larval fecal pellets (Mey 2006). However, the trajectory of this frass is serpentine and unlike that of L. spiralis. 14 2 Blotch mines with a concentric arrangement of frass rings that branch and rejoin are exclusively found in Cemiostominae (Mey 1994). Such a pattern is formed by deposition of frass on the underside of the upper epidermis of the host-plant foliage. These leaf mines can be found only in a few species of Leucoptera (Figure 4.3). In particular, the mines of Leucoptera malifoliella are most similar to the fossil leaf mine described herein (Figure 4.3A). While a small number of other taxa form leaf mines that superficially resemble those of Cemiostominae, none of these taxa fit all the characteristics of the leaf mines discussed here. Among all lepidopteran groups, leaf-mines of Tischeriidae may also exhibit a multiple-layered, concentric pattern that originated from progressive damage on foliar tissues by the larvae (Hering 1951) (Figure 4.3B). However, tischeriid leaf mines differ from those of Leucoptera by the absence of frass, as the larvae expel fecal pellets outside the leaf mines. Some species of Bucculatricidae also produce leaf-mines that often exhibit a frass pattern of concentric rings; however, these mines include both a linear segment in addition to a small blotch segment (Figure 4.3C). Some pathogenic marks on plant leaves made by ascomycotan epiphyllous fungi may also show concentric patterns, similar to Leucoptera leaf-mines (Figure 4.3D), but these necroses originate either as series of concentrically arrayed rings, circularly arranged pycnidia, or similar fructifications in one or multiple rings. Most common are the damage types DT66 (Xiao et al. in review), similar to Maple Tar Spot Disease; DT154 (Currano et al. 2008), resembling a leaf spot necrosis; and DT334 (Donovan et al. 2018), a different leaf spot necrosis. However, the circular patterns of fungal necroses are significantly different from the Leucopteropsis leaf mine. Overall, the frass patterns of the mine 14 3 described on the Kaiparowits fossil leaf morphotype KP90 (DMNH 47962a and DMNH 47962e) are indistinguishable to those of Leucoptera leaf-mines. Figure 4.3: Foliar mines and a pathogen with a concentric, multi-layered pattern. (a) Leaf-mine of Leucoptera scitella Zeller on Malus sp. (Rosaceae). (Photo by Gy?rgy Cs?ka.) (b) Leaf-mine of Bucculatrix firmianella Kuroko on Firmiana simplex (L.) W. F. Wight (Malvaceae). (Rearing no. K-557.) (c) A maturing leaf-mine of Tischeria sp. on Quercus mongolica Fisch. ex Ledeb. (Fagaceae). (Rearing no. K- 605.) (d) Phytopathogenic leaf blight spot on Commelina communis L. (Commelinaceae). Phylogeny of the Yponomeutoidea?Gracillarioidea Group Our fossil represents the second earliest record of the monophyletic Yponomeutoidea?Gracillarioidea (YG) group. The earliest fossil records of the group are Phyllocnistis leaf mines on fossilized leaves from the Early Cretaceous Dakota Formation (Davis 1994, Labandeira et al. 1994) at ca. 100?105 Ma. Although linear- 14 4 blotch mines are extremely common among leaf-mining lepidopterans (Grimaldi and Engel 2005), their phyllocnistine identity has been confirmed by Davis (1994) and Lopez-Vaamonde et al. (2006). The Leucopteropsis leaf-mine fossil described in this paper can be used as the reliable fossil calibration point for the subfamily Cemiostomiae within the YG group and consequently is an indicator for the antiquity of the most diverse lepidopteran group, Ditrysia. If the family Lyonetiidae is indeed monophyletic, Leucopteropsis spiralis also is an important calibration point for the moth family. However, for use of fossil Leucopteropsis as a calibration point within the YG group, the systematic position of the Cemiostominae must be better understood. The systematic relationships of Lyonetiidae and its putative subfamily, Cemiostominae, may not be straightforward because of two current issues. First is the absence of a robust phylogeny for Lyonetiidae and its relationship to other YG clades. Second, there is limited knowledge regarding detailed mine morphology of lepidopteran leaf-mining clades. The systematic position of Lyonetiidae remains uncertain, despite recent progress in lepidopteran phylogeny. There is broad consensus that Lyonetiidae belongs to a monophyletic clade within Yponomeutoidea and Gracillarioidea (Kawahara and Breinholt 2014, Regier et al. 2015, Sohn 2013, Sohn et al. 2013). However, the monophyly of Lyonetiidae has not been firmly established to date. The family currently includes two subfamilies, Lyonetiinae and Cemiostominae, and several genera whose subfamily affiliation remains undetermined. Two leaf-mining microlepidopteran groups, Bucculatricidae and Bedellidae, have sometimes been 14 5 treated as subfamily-level groups within Lyonetiidae (see a complete review in Baryshnikova 1999); however, the current consensus is that these two lineages belong to separate families (Kawahara et al. 2011, Sohn et al. 2013, van Nieukerken et al. 2011) (Figure 4.4). Figure 4.4: A working hypotheses as of mid 2020 of the phylogeny of Yponomeutoidea?Gracillarioidea group. At the left is Sohn et al. (2013) and at the right is Yang et al. (2019). Modified from original sources. The location of Lyonetiinae and Cemiostominnae within the larger Yponomeutoidea and Gracillarioidea is currently debated. Sohn et al. (2013) found that Lyonetiinae and Cemiostominae were placed, respectively, in the more distantly related clades of Yponomeutoidea and Gracillarioidea (Figure 4.4). In their phylogeny, only Lyonetiinae were placed within Yponomeutoidea as a basal lineage, while Cemiostominae were grouped with Gracillariidae and Bucculatricidae. These 14 6 relationships were, however, weakly supported or otherwise unstable. Interestingly, a molecular study (Yang et al. 2019) based on mitochondrial genomes resulted in grossly similar relationships (Figure 4.4), although the analysis lacked several important groups of Yponomeutoidea and Gracillarioidea in the analysis. Morphological characteristics also support the non-monophyly of Lyonetiidae, as Lyonetiinae and Cemiostominae show two major differences: the relative length of antenna to forewing and the presence/absence of spiniform setae on the abdominal terga. For these reasons, we believe that Cemiostominae are closer to Gracillariidae than to Yponomeutoidea, and likely represents one of the three basal lineages to the entire YG clade. Cemiostominae currently includes about 120 species in six genera (Sohn 2020). The majority (ca. 75%) of these species currently belong to Leucoptera, but a comprehensive generic revision may reveal several new genera. Host plants are documented for about 50% of Cemiostominae and data on their mine morphology is often lacking (Bradley and Carter 1982). Furthermore, the astonishingly high numbers of host plant species for each nominal leaf-miner species suggest that several species of Leucoptera are likely suites of cryptic species. This anomalously high level of host-plant breadth is suspect, given that the majority of leaf miners are monophagous (Prins et al. 2019). One example of this suspect polyphagy is the more than 25 host-plant species that are associated with the agricultural pest L. malifoliella Costa (Bajec et al. 2009, Ellis 2018, USDA 2011). Within the genus Leucoptera, not all members produce blotch mines with concentric frass layers. Searching available online libraries (e.g. 14 7 www.leafmines.co.uk; www.ukflymines.co.uk) and the entomological and agricultural literature (e.g. Cs?ka 2003, Hering 1951) of insect leaf-mines, we collected data on mine morphologies from 16 species of Leucoptera and found that blotch mines with concentric rings of frass occurred minimally on five species: L. heringiella Toll, L. laburnella Stainton, L. lotella Stainton, L. malifoliella Costa, and L. onobrychidella Klimesch. Frass patterns in some mines of Leucoptera coronillae Hering can appear concentric but in later stages, this pattern becomes disarrayed. Based on the divisions of Leucoptera proposed by Mey (1994), the above species are scattered in four species-groups. A COI-based phylogeny of 15 lyonetiids included three species whose larvae make blotch mines with a concentrically-ringed frass pattern. In the resulting Neighbor-Joining and Maximum Likelihood trees, these three species did not form a monophyletic group (Figure 4.5). In our COI phylogeny, the lustratella-group in Mey?s (1994) divisions was represented by only one species, Leucoptera lustratella, whereas the group from other analyses includes at least two species that produce blotch mines with concentric frass layers. Consequently, we conclude that the blotch mine with concentric rings of frass is very likely an ancestral form of mine type in the Leucoptera lineage. Nevertheless, it also is possible that the blotch mines with concentric frass rings have evolved multiple times independently. A denser sampling of the cemiostomine leaf-mines may help evaluate these two hypotheses. Because of the lack of a reliable phylogeny and a dense species-level tree for Lyonetiidae, divergence time estimation currently is not feasible. Our fossil 14 8 Figure 4.5: COI phylogeny of 15 lyonetiid and two gracillariid species. A: Maximum Likelihood Tree, B: Neighbor-joining tree. Numbers on nodes indicate percent bootstrapping support. Terminal label in the gray box represents the species producing blotch mines with a concentric, multi-layered frass pattern. 14 9 specimen of Leucopteropsis will become increasingly useful as a calibration point for the subfamily Cemiostominae once the uncertainty involving the gap between fossil age and actual divergence time is properly modeled. Conclusions The fossil leaf mine in the new ichnogenus and ichnospecies, Leucopteropsis spiralis (Lepidoptera: Lyonetiidea), from the Late Cretaceous Kaiparowits Formation (type locality age ca. 75.6 Ma) is herein described. The leaf-mining moth responsible for L. spiralis likely is an early member of the extant genus Leucoptera, a common agricultural pest genus. This trace fossil documents the earliest record of a cemiostomine leaf-mining moth, as well as the second oldest record of the Yponomeutoidea?Gracillarioidea clade. Despite the need for further phylogenetic work for the Lepidoptera, particularly the placement of the family Lyonetiidae and the subfamily Cemiostominae within the larger Yponomeutoidea?Gracillarioidea clade, this fossil provides an important Late Cretaceous calibration point for the age of the Yponomeutoidea?Gracillarioidea group. Acknowledgments We thank J. Shultz, D. Gruner, C. Delwiche, and C. Mitter for their guidance and support. We are grateful to the Denver Museum of Nature & Science?s (DMNS) Leaf Whackers for preparation of the Kaiparowits fossil specimens; K. MacKenzie, 15 0 G. Rossetto, and N. Neu-Yagle for their assistance in the collections; and J. Sertich for his leadership of the Kaiparowits fieldwork. DMNS provided financial support for the collections visit, R. Rissman and W. Rissman-Miller provided lodging and support, and The University of Maryland at College Park and the National Museum of Natural History provided the stipend for S. A. Maccracken. The second author (JCS) was supported by the ?Research Under Protection? subprogram of the Individual Research program on Basic Science and Engineering funded by the National Research Foundation of Korea (NRF-2017R1D1A2B05028793). Thanks go to M. Robledo for his assistance with the differential diagnosis and D. Davis, R. Eckert, P. Coffey, R. Gott, and C. Taylor for helping with the identification of the leaf mine. We are grateful to G. Motz and H. Wang for the loan of supplementary fossil materials. Finally, many thanks to the anonymous reviewers and editorial team. This is contribution 391 of the Evolution of Terrestrial Ecosystems at the National Museum of Natural History, in Washington, D.C. 15 1 Chapter 5: Late Cretaceous domatia reveal the antiquity of plant?mite mutualisms Abstract Mite houses, or acarodomatia, are found on the leaves of over 2,000 living species of flowering plants today. These structures facilitate tri-trophic interactions between the host plant, its fungi or herbivore adversaries, and fungivorous or predaceous mites by providing shelter for the mite consumers. Previously, the oldest acarodomatia were described on a Cenozoic Era fossil leaf dating to 49 million years in age. Here, we report the first occurrence of Mesozoic Era acarodomatia in the fossil record from leaves discovered in the Late Cretaceous Kaiparowits Formation (76.6?74.5 Ma) in southern Utah, USA. This discovery extends the origin of acarodomatia by >25 million years, and the antiquity of this plant?mite mutualism provides important constraints for the evolutionary history of acarodomatia on angiosperms. Background Mutualisms ? cooperative associations among species ? were key in the ecological ascendency of flowering plants (Eriksson et al. 2000, Grimaldi 1999). Pollination and seed dispersal, the two most common plant?animal mutualisms, are 15 2 widely recorded in modern and fossil communities. However, mutualisms between angiosperms and mites are less well known, despite the prominence of these interactions in modern ecosystems. Acarodomatia, or mite domiciles, located on the undersides of leaves, are thought to be the third most common plant?animal mutualism on earth today (Walter 2017) and likely contributed to the rise of flowering plants. Acarodomatia are pouches, pits, invaginations, or hair tufts located on the undersides of leaves at the axils of major vein branches (Nishida et al. 2006, O'Dowd and Willson 1989, 1991, Romero and Benson 2005, Walter 1996) (Figure 5.1). Inhabiting these minute structures are fungivorous or predaceous mites that provide protection to the host plant from fungi or herbivorous mites in exchange for refuge from other predators. At least 27 mite families in the superorders Acariformes and Parasitiformes (Karban et al. 1995, Pemberton and Turner 1989, Walter and O'Dowd 1992) are known to occupy acarodomatia (O'Dowd and Willson 1991). In particular, the shelter provided by the leaf is important for molting and oviposition for mutualistic mites, which otherwise would face desiccation or predation without the acarodomatia (Walter and Proctor 1999). This mutualism is facultative for both protected plants and beneficial mites, with no known specialization occurring between plant and mite species (Pemberton and Turner 1989). The generalized nature of this mutualism makes tracking the evolutionary history of acarodomatia particularly difficult, as compared to other tightly coevolved associations through time, such as certain specialist pollinators and their host plants (Winkler et al. 2009a). 15 3 Figure 5.1: Fossil acarodomatia from the Kaiparowits Formation, UT, USA, and modern acarodomatia for comparison. (a, b) Two modern pouch acarodomatia on Cinnamomum camphora (L.) J. Presl. (Lauraceae), shown in the abaxial (a) and adaxial (b) orientation, (c) two modern pit acarodomatia on Gardenia taitensis (DC) de Candolle (Rubiaceae), photograph by S. Zona, (d) modern pit acarodomatium on Coffea arabica (L.) Juss. (Rubiaceae), photograph by G. Romero, (e) two fossil (EPI.45456), (f, h) SEM images of acarodomatia from (d ) (EPI.45456), (g) fossil acarodomatium (EPI.40928) and (i) fossil acarodomatium dome (EPI.45427). Scale bars, 1.0 mm. 15 4 Acarodomatia presently are found exclusively on dicotyledonous angiosperms, especially woody arborescent species (Farmer 2014, Walter and Proctor 1999), with the exception of a single, unverified report of acarodomatia in the rolled leaf margins of one monocotyledonous angiosperm species (Burkill 1939). Acarodomatia are found on over 2,000 living species and 80 families ? ca. 28% of dicotyledonous families (Brouwer and Clifford 1990, Pemberton and Turner 1989, Walter 2017) ? of geographically widespread and taxonomically disparate angiosperms [5]. Plants have evolved acarodomatia multiple times, although the number of convergent evolutionary events is unknown (O'Dowd and Willson 1991). The percentage of trees with acarodomatia is greater than 15% in tropical forests (Brouwer and Clifford 1990, O'Dowd and Willson 1989, 1991) and range from 40% to 70% in temperate regions (O'Dowd and Pemberton 1994, 1998, Willson 1991). Despite the ecological prominence of modern acarodomatia, the fossil record of acarodomatia is sporadic and poorly understood. The unknown timing of origination and number of convergent evolutionary events, combined with widespread presence of acarodomatia among living woody dicotyledons and generalized nature of the association between mites and angiosperms, makes the fossil record of acarodomatia essential toward understanding the evolutionary history of this mutualism. Here, we describe fossil acarodomatia from the Upper Cretaceous Kaiparowits Formation, Utah, USA, which is the earliest documented occurrence of acarodomatia to date. 15 5 Materials and Methods Specimens were excavated from DMNH localities 3725 in 2009 and DMNH 4000 in 2010. These specimens currently are housed at the Denver Museum of Nature & Science (DMNS) in Denver, Colorado, USA. The leaves occur as compression- impression fossils on mudstone, siltstone, and fine-grained sandstone matrices (Locatelli et al. 2017) (see Supplementary Material in Appendix E for a detailed methodology). We used a Motic SMZ-161 steroscopic microscope to view the fossil leaves. Detailed photographs were taken with a Canon EOS 50D camera housing a Canon EF-D 60mm f/2.8 macro lens and an Olympus DP25 camera attached to an Olympus SZX12 microscope. Images were edited using Adobe Photoshop CC (19.1.3). For Scanning Electron Microscopy (SEM) images, we placed the fossil specimens in a low-temperature oven for 20 hours and used a Carl Zeiss EVO MA15 scanning electron microscope with a LAB6 electron source. Results Thirteen examples of the same type of acarodomatia were found on ten fossil leaf specimens from two localities of the Kaiparowits Formation (76.6?74.5 Ma), Utah, USA (Figure 5.1 E-I). Identification of acarodomatia of the Kaiparowits Formation is based on the location, size, and morphology of pore-like surface structures. The acarodomatia are located in primary-to-secondary and secondary-to- secondary vein axils and are embedded within vein tissue. These acarodomatia are classified as pouch acarodomatia, which comprise a cavity with a pore-like opening 15 6 on the abaxial side of the leaf (Figure 5.1 A, E-H) and a dome of foliar tissue on the adaxial side of the leaf (Figure 5.1I) (Jacobs 1966, O'Dowd and Willson 1989). This acarodomatium type generally is embedded within the vein tissue, as opposed to pit acarodomatia that generally occur in laminar tissues (Figure 5.1 C, D). There is substantial variation in acarodomatia classification schemes, but these fossil acarodomatia are morphologically similar to pouch domatia found on Cinnamomum camphora (L.) J. Presl. (Lauraceae) (Figure 5.1 A). The pores of the fossil acarodomatia are circular to rounded-triangular in shape. They are between 0.82 and 1.18 mm along the longest dimension, 0.71 and 1.06 mm in diameter along the shortest dimension, and cover an average of 1.02 mm2. These dimensions are consistent with modern pit and pouch acarodomatia, which are generally between ca. 0.5?3.0 mm in diameter (English?Loeb and Norton 2006). Additionally, the fossil acarodomatia are distinct from holes associated with herbivory because the structures exhibit smooth edges around the pore that lack plant reaction tissue, and are distinct from extrafloral nectaries, which tend to be bulbous and rarely occur in mid-laminar vein axils (Marazzi et al. 2013). All data and lines of evidence indicate that these foliar features are acarodomatia. The fossil acarodomatia occur sporadically, as they are not present at every major vein juncture on the fossil leaves. At most, we observed three acarodomatia per fossil leaf. However, most of the fossil leaf specimens examined are fragmentary, and the number of acarodomatia per fossil leaf may be greater. Ten of the 41 fossil leaf specimens (24%) from the acarodomatia-bearing plant taxon exhibiting acarodomatia display evidence of at least one acarodomatium. 15 7 The identity of the fossil leaf species remains unresolved. The very large size of this leaf taxon (exceeding 30 cm in length and 25 cm in width) likely led to pre- and post-depositional foliar fragmentation. Consequently, complete fossil leaves of this taxon have not been recovered. Without exception, all known specimens of this fossil leaf have intense hole and margin feeding insect damage. In particular, the hole feeding is occasionally so extensive that up to 80% of the lamina was consumed, which further obfuscates taxonomic identification. This hole feeding appears to be unrelated to the plant?mite mutualism involving acarodomatia; mites are an order of magnitude smaller than the average insect pest and likely outside the scope of a predaceous interaction. The vein fabric of this fossil leaf ? pinnate primary venation, brochidodromous secondary venation, alternate percurrent tertiary venation, and a thick, coalified, and thus likely woody petiole ? and overall size of the specimens indicate it is a woody dicotyledonous angiosperm (Hickey 1971) (Figure 5.2). A morphological description of the taxon, including photos, is provided in the Supplementary Material (Appendix E). Discussion Distribution of fossil and modern acarodomatia There are nine occurrences of domatia from the fossil record (Table 5.1), with the notable absence of ant domatia. Previously, the oldest known domatia were from the middle Eocene (ca. 49 Ma) of Victoria, Australia (O'Dowd et al. 1991). This 15 8 example is followed by late Eocene (ca. 42 Ma) acarodomatia from the same location (O'Dowd et al. 1991) and middle Eocene (ca. 44 Ma) acarodomatia from north- central Oregon, USA (Hanson 1996, Liu et al. 2014). Five younger examples of acarodomatia come from the Miocene of New Zealand (ca. 20 Ma) (Bannister et al. 2012, Conran et al. 2016, Kaulfuss 2012, Kaulfuss et al. 2015, Lee et al. 2010, Lee et al. 2012, Pole 1993, 1996), and the late Neogene to early Quaternary of Portugal (ca. 7 to 1.8 Ma) (G?is-Marques et al. 2018). The discovery of the Kaiparowits Formation acarodomatia (75.1 and 74.9 Ma, see Supplementary Material in Appendix E) is heretofore the oldest evidence of a plant?mite mutualism in the fossil record by more than 25 million years. It is also the oldest known domatia of any kind and extends the record of domatia into the Mesozoic Era. In contrast to acarodomatia, the evolutionary history of ant domatia (myrmecodomatia) is comparatively recent. Indirect evidence indicates that myrmecodomatia evolved during the Cenozoic (Nelsen et al. 2018), perhaps in the Early Miocene (ca. 19 Ma) (Chomicki and Renner 2015). However, no myrmecodomatia are known from the fossil record. It is possible that this is a result of poor preservation potential of myrmecodomatia structures or a sampling bias toward leaves. Myrmecodomatia differ from acarodomatia in several ways. Chiefly, myrmecodomatia are not located in the vein axils of plants due, in part, to the relatively large size of ant individuals, which often are larger than a single acarodomatium. Consequently, myrmecodomatia are located in hollow stems, swollen petioles, or enlarged thorns and therefore are less restricted to certain 15 9 Figure 5.2: Illustration depicting the hypothesized host plant leaf morphology, acarodomatia and mites of the Kaiparowits Formation plant?mite mutualism. Photograph specimen EPI.45456. Scale bar, 100 ?m. Illustration by M. Leggitt (Maccracken et al. 2019). 16 0 Table 5.1: Comparison of all acarodomatia reported from the fossil record. Age Site Location Host Plant Taxon Acarodoma- References tia Type Late Kaiparowits Utah, USA KP88 Pouch This study Cretaceous Formation (75.1 Ma) Middle Monier East South Elaeocarpaceae Tuft O?Dowd et Eocene Yatala Sand Australia, Lauraceae al. (1991) (ca. 49?42 Pit Australia (O'Dowd et Ma) al. 1991) Late Alcoa Coal Victoria, Elaeocarpaceae Tuft O?Dowd et Eocene mine Australia Lauraceae al. (1991) (ca. 42?37 (O'Dowd et Ma) al. 1991) Middle Clarno Oregon, USA Alnus clarnoensis ** Liu et al. Eocene Formation (Betulaceae) (2014) (ca. 44 Ma) (Liu et al. 2014) Early Manuherikia Otago, New Elaeocarpaceae ** Pole et al. Miocene group, Zealand (1993) (20 Ma)* Foulden (Pole 1993) Maar Early Foulden Otago, New Macaranga/Mallo ** Pole et al. Miocene Hills Zealand tus? (1996) (20 Ma)* Diatomite, (Euphorbiaceae) (Pole 1996) Foulden Maar Early Foulden Otago, New Euphorbiaceae Tuft Lee et al. Miocene Hills Zealand (2010, 2012) (20 Ma)* Diatomite, (Lee et al. Foulden 2010, Lee et Maar al. 2012) Early Foulden Otago, New Laurophyllum Tuft Bannister et Miocene Hills Zealand waipiata al. (2012) (20 Ma)* Diatomite, (Lauraceae) (Bannister et Foulden al. 2012) Maar Early Bannockburn Otago, New Malloranga Pocket Conran et al. Miocene Formation Zealand dentate (2016) (20?16 (Euphorbiaceae) (Conran et al. Ma) 2016) Mio- Middle Madeira Island, Ocotea foetens ** Gois- Pleistocene Volcanic Portugal (Lauraceae) Marques et (7?1.8 Complex; al. (2018) Ma) S?o Jorge (G?is- outcrop Marques et al. 2018) *Foulden Maar locality age is reported in Pole et al. (1996). **Domatia type not designated in publications. 16 1 morphological areas of the plant than acarodomatia. Myrmecodomatia also are found on a wider range of plant lineages, including monocotyledons, dicotyledons, and ferns. Nevertheless, myrmecodomatia are less common than acarodomatia, and are found on 700 plant species and 50 genera (Nelsen et al. 2018) despite the greater range of host-plant lineages. With the absence of fossil myrmecodomatia and their relatively recent evolution in the Miocene, the Kaiparowits Formation occurrences are the oldest known domatia of any kind to date. Antiquity of plant?arthropod associations and the evolution of acarodomatia Plant?animal mutualisms spurred, in part, the diversity of extant plants and animals (Bronstein et al. 2006, Heil et al. 2009, Ollerton 2017). Consequently, the evolution of plants coupled with plant?animal associations is a widely studied, important field within paleobiology and evolutionary biology (Kergoat et al. 2017, Labandeira 1998b, 2006b, Labandeira 2006c, Wheat et al. 2007). The most common, present-day plant?animal mutualism, pollination of seed plants by insects, originated during the Permian Period (299 to 252 Ma) (Labandeira 2010). Later, in the Mesozoic Era, the co-association of angiosperms and their insect pollinators fundamentally shaped the diversity and morphology of both groups (Bronstein et al. 2006, Ehrlich and Raven 1964). The second most common, modern plant?animal mutualism, the animal dispersal of seeds, also evolved during the Permian Period, as late Permian seeds are known from the gut cavities of tetrapods (Munk and Sues 1993, Tiffney 2004). Seed dispersal became widespread by the Mesozoic (Eriksson et al. 2000, Tiffney 2004) and increased exponentially into the Cenozoic (Tiffney 1984). In 16 2 contrast to pollination and seed dispersal, there is a substantial temporal lag between the origin of plant?mite associations and the evolution of plant?mite mutualisms. The earliest mites (Dunlop 2010, Hirst 1923, Kethley et al. 1989, Norton et al. 1988, Schaefer et al. 2010, Walter and Proctor 1999) appear during the Early to Middle Devonian (419 to 383 Ma), when they began to interact with primitive land plants (Kevan et al. 1975, Labandeira 2007, Labandeira et al. 2014). Both predatory and fungivorous mites lineages in the Acariformes that occupy acarodomatia (Kethley et al. 1989, Norton 1985, Walter 1988) appear in the fossil record during the Paleozoic at ca. 385 Ma (Walter and Proctor 1999). Parasitiformes, which also occupy acarodomatia, first appear in the mid-Cretaceous (ca. 99 Ma) (Klompen and Grimaldi 2001, Poinar and Brown 2003). Despite hundreds of millions of years of plant?mite associations and the prevalence of predaceous and fungivorous mites since the Paleozoic, the evolution of acarodomatia apparently was delayed until the Late Cretaceous. The origin of acarodomatia likely was spurred by the evolution of angiosperms during the Late Mesozoic?albeit the probability that domatia originated before the Cretaceous is difficult to evaluate (O'Dowd and Willson 1989). The Kaiparowits Formation acarodomatia pinpoint a minimum age of 75.5 Ma (see Supplementary Material in Appendix E) for the evolution of acarodomatia. Fossil acarodomatia are expected to occur in somewhat earlier Cretaceous floras, but the diminutive size, poor preservation of associated trichomes, and inconspicuousness associated with tufted acarodomatia might impede the detection of these structures. Given the almost exclusive occurrence of acarodomatia on living woody and arborescent dicotyledons, estimating the timing of woody and arborescent 16 3 growth forms in angiosperms arguably provides the best age constraint on the origin of acarodomatia. While the evolutionary origin of angiosperms has been dated to the Cretaceous (Magall?n et al. 2015), Jurassic (Wikstr?m et al. 2001), and even Triassic (Smith et al. 2010), the first widely accepted and abundant fossil evidence for angiosperms is palynological and dates to the mid Early Cretaceous, ca. 140 Ma (Crane et al. 1995, Herendeen et al. 2017, Hughes and McDougall 1994, Lupia et al. 1999). Herbaceous angiosperm mesofossils and macrofossils become diverse and abundant during the Barremian?Aptian transition (ca. 125 Ma) and unequivocal fossils of woody dicotyledons first appear near the Albian?Cenomanian boundary (ca. 100 Ma), although woodiness remains a rare growth habit at this time (Feild et al. 2011, Friis et al. 2011, Jud et al. 2018, Oakley and Falcon-Lang 2009, Philippe et al. 2008, Wheeler and Lehman 2009, Wheeler and Baas 1991). The first instances of woodiness around 100 Ma would suggest acarodomatia probably also evolved at this time (Barale et al. 2002, Philippe et al. 2008). This hypothesis is further supported by phylogenetically basal ANA (Amborellaceae, Nymphaeales and Austrobaileyaceae) grade angiosperms that completely lack acarodomatia, suggesting Early Cretaceous representatives of these linages also lacked acarodomatia. In contrast, some of the most basal woody lineages of magnoliid angiosperms including those in Piperales, Laurales and Magnoliales have acarodomatia (Zanella and Ferla 2013). While these clades evolved by about 125 Ma (Barale et al. 2002, Friis et al. 2011), they likely remained herbaceous until ca. 100 Ma, consistent with our hypothesis that acarodomatia evolved about 100 million year ago. 16 4 Acarodomatia arguably are a recent evolutionary innovation, much later than the pollination or seed dispersal plant?animal mutualisms, and well after the evolutionary history of other plant?mite associations (Walter 2017). Nevertheless, acarodomatia are the third-most common plant?animal mutualisms in modern ecosystems (Walter 2017). The Kaiparowits Formation acarodomatia, dated to 75.7 Ma, occur approximately 25 million years after the inferred evolution of these structures. While angiosperms are highly diverse by this time, their global rise to ecological dominance across most environments probably did not happen until the latest Cretaceous or Early Cenozoic (Johnson and Ellis 2002, Lidgard and Crane 1990, Wing et al. 1993). It is widely acknowledged that plant?animal mutualisms, specifically pollination and seed dispersal, played a seminal role in the ecological ascendency of angiosperms (Friis et al. 2011, van der Niet and Johnson 2012). Based on the function of modern acarodomatia, we suggest that plant?mite mutualisms may have contributed to the success of angiosperms in no small part by protecting these plants from elevated herbivore and fungal pressures during their evolutionary and ecological diversification. Acknowledgments We thank the DMNS Leaf Whackers, K. MacKenzie, N. Neu-Yagle, G. Rossetto, K. Hamby, E. Tielens, D. Gruner, S. Schachat, S. Whittaker, G. Romero, S. Zona and Y. Imada. We are also grateful to the two anonymous reviewers and the editorial board. 16 5 Chapter 6: Widespread biases in deep time plant?insect associational studies obscure potential patterns of insect preferences throughout the Age of Angiosperms Abstract Many recent studies have focused on discovering patterns of plant?insect interactions through deep time, but few have considered the empirical and analytical limits imposed by spatial, temporal, and sampling biases in the fossil record. Here we examine how host preferences by insect herbivores have changed throughout the Age of Angiosperms (Cretaceous Period?Quaternary Period) and with respect to floral diversity at each fossil locality. While we uncovered significant results suggesting that locality-specific insect herbivory stabilized during the last 28 million years and insect herbivory also is highly variable in diverse plant communities, these results are rendered uncertain due to inherent biases of the fossil record and differences in sampling regimes. Without consistent and accurate taxonomic information, we are not able to identify the underlying cause(s) for our significant results?they could either be real, biologically-meaningful patterns or simply artifacts of sampling. These results could (i) reflect plant communities changing through time, (ii) reflect certain clades having high or low instances of herbivory, (iii) exemplify the taxonomic bias in sampling methods that may overlook certain clades of plant hosts, or (iv) these results could reflect the difficulties of taxonomically identifying older angiosperm 16 6 plants and often implicit in the common practice of morphotyping a fossil flora. While our results do not explicitly answer our initial question of whether insect preference, as measured by richness of damage types, for host plants has occurred in deep time, it does provide avenues toward resolving this issue. Introduction Vascular plants and herbivorous insects are among the most biodiverse macroscopic clades of organisms and their ecological associations are a cornerstone of terrestrial ecosystems (Foottit and Adler 2009; Futuyma and Mitter 1996; Lewinsohn and Roslin 2008). The estimated global annual loss of foliage by insect herbivores is 5?18% (Coley and Barone 1996; Cyr and Pace 1993; Kozlov et al. 2015; Turcotte et al. 2014), which has profound, top-down effects on plant biomass, abundance, survival, reproduction, and diversity (Jia et al. 2018). Additionally, the diversity of ecological, biochemical, behavioral, physiological, genetic, and evolutionary underpinnings of plant?insect associations create an almost boundless prospective dataset (Strauss and Zangerl 2002) that extends to the Paleozoic Era (Labandeira 1998a; Labandeira 1998b; Labandeira 2002; Labandeira 2006; Labandeira et al. 2014). Insect herbivory has generally increased in diversity and specialization (Pinheiro et al. 2016), together with the diversification of vascular plants through time. A number of plant?insect associational studies also have documented significant changes in insect damage across particular geologic ages, regions, and relative to local plant diversities (e.g. Currano et al. 2010; Currano et al. 16 7 2008; Labandeira et al. 2002; Leckey and Smith 2017; Pinheiro et al. 2016; Wappler et al. 2009; Wappler and Gr?msson 2016; Wilf and Labandeira 1999; Wilf et al. 2001). However, relatively little attention has been paid to analyzing large-scale patterns of deep time plant?insect associations, specifically insect preference for particular plant hosts through time and in relation to plant community structure. Host plant preference by herbivorous insects, or the targeting of particular plants for herbivory, is subject to many factors, which include plant defense mechanisms (Bennett and Wallsgrove 1994; Ehrlich and Raven 1964; Kossel 1891), plant?insect coevolution (Ehrlich and Raven 1964; Farrell 1998; Janz 2011; McKenna et al. 2009; Mitter et al. 1988; Moreau et al. 2006), the degree of herbivore specialization on plant hosts (Forister et al. 2015; Jorge et al. 2017; Novotny et al. 2002a; Novotny et al. 2002b), the nutritional value of the plant (Minkenberg and Ottenheim 1990; Scheirs et al. 2003), the ability of the insect to find the plant in time and space (Feeny 1976; Miller and Strickler 1984), and the diversity of plant hosts within a particular habitat (Schallhart et al. 2012; Bach 1981). In particular, the higher the diversity of plant species in an area, as measured by the evenness and richness of plant species, the higher the productivity of that system (Huston 1997). Previous studies of deep time plant?insect associations have supported this theory to varying degrees (Currano et al. 2010; Wappler and Gr?msson 2016), except in cases of extreme habitat disturbance (Wilf et al. 2006). Insect preference is also known to have changed through time based on evidence of plant-host use across various herbivorous insect phylogenies (Bernays 1998; Eastop 1972; Eastop 1978; Wikler and Mitter 2008; Moran 1988), herbivorous 16 8 insect damage on fossil leaves (Winkler et al. 2009), and the presence of co-occurring herbivorous insect and plant lineages through time (Labandeira 2014). Notably, Labandeira (2014) compiled a list of insect families and their diet breadths across the rise and radiation of angiosperms during the Early Cretaceous Epoch and documented large-scale shifts from gymnosperm- and fern-feeders to angiosperm-feeders. Rigorous statistical methodologies to measure insect preference are now required to better quantify the role of insect preference in the fossil record through time. A novel method, which calculates the expected richness of insect damage for ancient plant hosts is used in this study to determine insect preference for, or aversion to, fossil plant hosts throughout the Age of Angiosperms. Using a dataset compiled from 19 publications of deep time plant?insect associations, we analyze insect preference for a total of 58,882 specimens, which document a considerable time interval during the Age of Angiosperms from ca. 76 to 2 Ma. The fossil localities used in this analysis represent a range of sampling regimes and inherent difficulties with fossil plant taxonomic identifications, as well as differences in geologic ages and paleobotanical diversities. Skewedness of insect preference for plant hosts, which is measured as higher or lower than expected, is distributed unevenly through time and in relation to plant host diversities, although we ultimately question how the nature of plant?insect association datasets may influence our ability to measure broad-scale patterns of insect preferences in the fossil record. 16 9 Methods Data Inclusion We analyzed the datasets of 151 previously published studies on plant?insect associations from the Age of Angiosperms and five previously unpublished locality datasets generated by the lead author Maccracken (Table 6.1). The earliest, undisputed fossil angiosperm material is dated to the Early Cretaceous (ca. 136 Ma) (Crane et al. 1995; Herendeen et al. 2017; Hughes and McDougall 1994; Lupia et al. 1999), so all plant?insect associational studies from this date and younger were considered, although the earliest suitable and available datasets were ca. 76 Ma, approaching the midpoint of the occurrence of fossil angiosperms. Geographically constrained localities were selected as the unit of comparison rather than datasets from entire geologic formations, disparate time intervals, or specific regions. We considered only localities with more than 50 leaves (as in Pinheiro et al. 2016) and with at least 20 specimens of the dominant host-plant taxon. Localities with repeat excavations (ex. Loc. 1a, Loc 1b, etc.) were combined unless the excavations were separated by distances greater than 50 m or from substantially different stratigraphic positions (ex. a locality with excavations straddling an extinction event). We surveyed over 100 published studies for potential inclusion in this study and used 19 of those datasets (Figure 6.1). We initially amassed a total of 58,882 fossil specimens from 106 localities (Table 6.1), which were selected based on four criteria: 1) a whole-flora approach was taken in each study, rather than analyzing insect damage on a single host plant species, a single instance or type of insect damage, or a small subset of specimens pulled from a larger fossil flora collection; 17 0 Table 6.1: Localities included in this study, with information on the publication, country, geologic formation, locality name, age of each locality, as well as the richness of plant hosts, specimens, and damage types. Publication Region/State, Geologic Locality Geologic Geologic Date Number Host Damage Country Deposit Name Age, Epoch Epoch Used of Plant Type in This Specimens Richness Richness Study* (Ma) Adroit et al. H?rault, Bernasso Bernasso Gelasian Pleistocene 2 535 20 40 (2016) France Th?ringen, Berga Berga Piacenzian Pliocene 2.8 534 33 25 Germany Adroit et al. (2018a) Lower- Willershausen Willershausen Piacenzian Pliocene 2.8 7491 209 83 Saxony, Germany Vesturland, Hre?avatn- Brekku? Messinian Miocene 6.5 184 13 12 Iceland Stafholt Vesturland, Hre?avatn- Hestabrekkur Messinian Miocene 6.5 89 8 11 Iceland Stafholt Vestfir?ir, Skar?sstr?nd- Fell Tortonian Miocene 8.5 58 7 4 Iceland M?kollsdalur Wappler & Vestfir?ir, Skar?sstr?nd- M?kollsdalur Tortonian Miocene 8.5 351 17 18 Gr?msson Iceland M?kollsdalur (2016) Vestfir?ir, Tr?llatunga- Tr?llatunga Tortonian Miocene 10 262 9 9 Iceland Gautshamar Vestfir?ir, Brj?nsl?kur- Brj?nsl?kur Serravallian Miocene 12 305 20 12 Iceland Selj? (Bar?astr?nd) Vestfir?ir, Sel?rdalur- S?l?rdalur Langhian Miocene 15 174 9 10 Iceland Botn M?ller et Otago, New Hindon Maar Hindon Maar Burdigalian Miocene 18.8 466 27 78 al. (2017) Zealand Crater North Most B?e??any Burdigalian Miocene 19.6 961 35 26 Bohemia, Czech 17 1 Knor et al. Republic (2012) North Most B?lina Burdigalian Miocene 19.6 2215 77 54 Bohemia, Czech Republic North Rhine- Rott Deposit Orsberg Chattian? Oligocene? 23 116 35 8 Westphalia, Aquitanian Miocene Wappler Germany (2010) North Rhine- Rott Deposit Rott Chattian? Oligocene? 23 2326 101 52 Westphalia, Aquitanian Miocene Germany Gunkel et Westerwald, Enspel Enspel Chattian Oligocene 24.8 1017 48 31 al. (2015) Germany Huesca, Sari?ena LV3 Chattian Oligocene 25.4 394 13 22 Spain Formation Dom?nguez Huesca, Sari?ena LV6 Chattian Oligocene 25.4 179 26 17 (2018) Spain Formation Huesca, Sari?ena LVNH Chattian Oligocene 25.4 138 11 17 Spain Formation Wappler North Rhine- Rott Deposit Quegstein Chattian Oligocene 25.8 371 37 12 (2010) Westphalia, Germany Amhara Chilga Basin CH72 Chattian Oligocene 27.5 195 23 18 Region, Ethiopia Currano et Amhara Chilga Basin CH90 Chattian Oligocene 27.5 126 15 9 al. (2011) Region, Ethiopia Amhara Chilga Basin CH92 Chattian Oligocene 27.5 155 14 17 Region, Ethiopia Currano et Amhara Chilga Basin CH40 Chattian Oligocene 27.5 208 14 21 al. (2011) Region, Ethiopia Amhara Chilga Basin CH41 Chattian Oligocene 27.5 93 25 13 Region, Ethiopia 17 2 Wappler & Spitsbergen, Renardodden Renardodden Priabonian Eocene 36 344 21 16 Denk Norway (2011) Wyoming, Green River 323 Lutetian Eocene 43 179 15 11 Wilf et al. USA Formation (2001) Wyoming, Green River 1732 Lutetian Eocene 43 638 27 26 USA Formation Spitsbergen, Aspelintoppen Nathorstfjellet Lutetian Eocene 44 283 14 17 Wappler & Norway Denk Spitsbergen, Aspelintoppen Nordenski?ldfjellet Lutetian Eocene 44 277 14 18 (2011) Norway Rhineland- Eckfeld Maar Eckfeld Lutetian Eocene 44.3 3816 33 64 Palatinate, Wappler et Germany al. (2012) Hesse, Messel Messel Yrpesian? Eocene 47.8 5499 93 97 Germany Lutetian Wyoming, Aycross EPWR1601 Ypresian Eocene 49.1 292 22 21 USA Wyoming, Aycross EPWR1602 Ypresian Eocene 49.1 186 17 16 USA Currano et Wyoming, Aycross EPWR1603 Ypresian Eocene 49.1 270 15 13 al. (2019) USA Wyoming, Aycross EPWR1604 Ypresian Eocene 49.1 160 17 17 USA Wyoming, Wind River DMNH5098 Ypresian Eocene 52.4 231 21 23 USA Wyoming, Wind River DMNH5100 Ypresian Eocene 52.4 373 7 29 USA Currano et Wyoming, Wind River DMNH5102 Ypresian Eocene 52.4 370 21 18 al. (2019) USA Wyoming, Wind River DMNH5104 Ypresian Eocene 52.4 175 19 13 USA Wyoming, Willwood 42400 Ypresian Eocene 52.7 492 19 60 USA Wyoming, Willwood 42401 Ypresian Eocene 52.7 106 10 17 USA Wyoming, Willwood 42402 Ypresian Eocene 52.7 100 6 16 Currano et USA al. (2010) Wyoming, Willwood 42403 Ypresian Eocene 52.7 476 19 57 17 3 USA Wyoming, Willwood 42404 Ypresian Eocene 52.7 102 8 16 USA Wyoming, Willwood 42405 Ypresian Eocene 52.7 495 15 54 USA Utah, USA Wasatch 41342 Ypresian Eocene 53 343 13 15 Wilf et al. Formation (2001) Utah, USA Wasatch 41352 Ypresian Eocene 53 438 16 20 Formation Wyoming, Willwood 37560 Ypresian Eocene 53.4 693 15 56 Currano et USA al. (2010) Wyoming, Willwood 37654 Ypresian Eocene 54.2 250 13 17 USA Schmidt et Wyoming, Hanna E Ypresian Eocene 54.5 323 17 18 al. (2019) USA Wyoming, Willwood 42384 Ypresian Eocene 55.8 995 28 38 Currano et USA al. (2008) Wyoming, Fort Union 41643 Ypresian Eocene 55.9 767 15 12 USA Wilf et al. Wyoming, Fort Union 41270 Thanetian? Paleocene? 56 345 9 23 (2001) USA Ypresian Eocene Currano et Wyoming, Willwood 42411 Thanetian Paleocene 56.4 1015 19 30 al. (2010) USA Currano et Wyoming, Fort Union 42042 Thanetian Paleocene 57.5 1298 14 26 al. (2008) USA Schmidt et Wyoming, Hanna C Thanetian Paleocene 58.0 304 13 21 al. (2019) USA Currano et Wyoming, Fort Union 42041 Thanetian Paleocene 58.9 907 7 19 al. (2008) USA Schmidt et Wyoming, Hanna A Selandian Paleocene 59.5 92 13 9 al. (2019) USA Wappler et Menat, Menat Menat Pit Selandian Paleocene 60.5 791 74 37 al. (2009) France Lagerstatte Wappler & Spitsbergen, Firkanten Kolfjellet Selandian Paleocene 61.0 335 17 19 Denk Norway (2011) Patagonian Pe?as LF Danian Paleocene 62.4 568 29 42 Argentina Coloradas Donovan et Patagonian Salamanca PL1 Danian Paleocene 64.1 1089 29 48 17 4 al. (2018) Argentina Patagonian Salamanca PL2 Danian Paleocene 65.2 1137 31 54 Argentina North Fort Union 441 Danian Paleocene 65.6 90 10 9 Dakota, USA North Fort Union 562 Danian Paleocene 65.6 78 7 13 Dakota, USA North Fort Union 898 Danian Paleocene 65.6 173 9 12 Dakota, USA North Fort Union 2217 Danian Paleocene 65.6 296 23 13 Labandeira Dakota, USA et al. North Fort Union 86107 Danian Paleocene 65.6 457 17 14 (2002a) Dakota, USA North Fort Union 86110 Danian Paleocene 65.6 297 12 17 Dakota, USA North Fort Union 87150 Danian Paleocene 65.6 544 11 8 Dakota, USA North Fort Union 88103 Danian Paleocene 65.6 86 11 6 Dakota, USA North Fort Union KJ8403 Danian Paleocene 65.6 67 8 8 Dakota, USA North Fort Union 2212 Maastrichtian Late 66.5 67 12 9 Dakota, USA Cretaceous North Fort Union 86100 Maastrichtian Late 66.5 508 21 17 Dakota, USA Cretaceous North Fort Union 86102 Maastrichtian Late 66.5 190 18 11 Dakota, USA Cretaceous North Fort Union 86153 Maastrichtian Late 66.5 155 13 13 Dakota, USA Cretaceous North Fort Union 87110 Maastrichtian Late 66.5 62 8 10 Dakota, USA Cretaceous North Fort Union 87129 Maastrichtian Late 66.5 104 15 8 Dakota, USA Cretaceous Labandeira North Fort Union 87134 Maastrichtian Late 66.5 172 14 17 et al. Dakota, USA Cretaceous (2002a) North Fort Union 88111 Maastrichtian Late 66.5 70 11 3 Dakota, USA Cretaceous North Hell Creek 1489 Maastrichtian Late 66.5 102 26 16 Dakota, USA Cretaceous 17 5 North Hell Creek 1491 Maastrichtian Late 66.5 269 17 23 Dakota, USA Cretaceous North Hell Creek 1781 Maastrichtian Late 66.5 117 18 14 Dakota, USA Cretaceous North Hell Creek 1855 Maastrichtian Late 66.5 123 10 21 Dakota, USA Cretaceous North Hell Creek 2087 Maastrichtian Late 66.5 349 33 14 Dakota, USA Cretaceous North Hell Creek 2097 Maastrichtian Late 66.5 245 15 18 Dakota, USA Cretaceous North Hell Creek 2098 Maastrichtian Late 66.5 123 17 15 Dakota, USA Cretaceous North Hell Creek 2099 Maastrichtian Late 66.5 76 15 8 Dakota, USA Cretaceous North Hell Creek 2203 Maastrichtian Late 66.5 392 17 18 Dakota, USA Cretaceous North Hell Creek 428 Maastrichtian Late 66.5 708 67 32 Dakota, USA Cretaceous North Hell Creek 517 Maastrichtian Late 66.5 134 16 9 Dakota, USA Cretaceous North Hell Creek 566 Maastrichtian Late 66.5 114 20 8 Dakota, USA Cretaceous Labandeira North Hell Creek 567 Maastrichtian Late 66.5 373 24 21 et al. Dakota, USA Cretaceous (2002a) North Hell Creek 568 Maastrichtian Late 66.5 139 21 22 Dakota, USA Cretaceous North Hell Creek 571 Maastrichtian Late 66.5 279 21 24 Dakota, USA Cretaceous North Hell Creek 897 Maastrichtian Late 66.5 123 16 18 Dakota, USA Cretaceous North Hell Creek 900 Maastrichtian Late 66.5 470 44 31 Dakota, USA Cretaceous Patagonian Lefip?n LefE Maastrichtian Late 66.5 606 41 45 Argentina Cretaceous Patagonian Lefip?n LefL Maastrichtian Late 66.5 108 26 28 Donovan et Argentina Cretaceous al. (2018) Patagonian Lefip?n LefW Maastrichtian Late 66.5 140 30 28 Argentina Cretaceous New Mexico, Fruitland/ 302 Campanian Late 74.3 66 15 7 17 6 USA Kirtland Cretaceous New Mexico, Fruitland/ 9726 Campanian Late 74.3 189 42 20 USA Kirtland Cretaceous This study Utah, USA Kaiparowits Lost Valley Campanian Late 75.6 3918 79 78 Cretaceous Utah, USA Kaiparowits Caveat Friendship Campanian Late 75.6 502 55 34 Cretaceous Utah, USA Kaiparowits JARS Campanian Late 75.7 719 70 51 Cretaceous *Dates for each locality were obtained from the original publications. When a geologic interval or range of dates was given, we calculated the mean, using the Geological Society of America?s Geological Time Scale v. 5.0 when necessary (Walker et al. 2018). 17 7 Figure 6.1: Map of localities analyzed in this study. Circles represent approximate number of localities per region. 17 8 2) the study used the damage type schema from the Guide to Insect (and Other) Damage Types on Compressed Plant Fossils (Labandeira et al. 2007); 3) the sites were from either the Mesozoic or Cenozoic Eras, in which angiosperms were typically a dominant component of the floras; and 4) data were publicly available or authors shared their data via personal correspondence. We attempted to incorporate all relevant studies in the analysis, but some studies may have been unintentionally overlooked. Additionally, not all authors responded to our request for data, consented to share data from previously published studies, or provided datasets that were setup in such a way that they could not be incorporated into this study. We obtained the geologic age for each locality from the original publications. In cases where a range of dates was given, we calculated the mean from the geological time interval provided. Furthermore, when only a geologic stage was provided, we used the midpoint date of the stage range. Occasionally, dates were estimated from locality placement on stratigraphic columns or external stratigraphic publications. Geologic dating across these localities varied in accuracy, attributable to poor stratigraphic context of the floras, obsolete dating methods or studies, and excessively large error estimates. The variability of the geologic dating was inherent in a study of this scale and we assumed that this variability did not alter the results in a meaningful way. We used the assigned plant-host taxonomic identifications from the publications, but attempted to correct all misspelled specimen data within reason and based on the species already present in a particular dataset (ex. ?Alus sp.? to ?Alnus sp.?). Indeterminate leaves that could not be morphotyped (ex. ?indeterminate sp.?) 17 9 were excluded from the analyses and subspecies identifications were lumped back into their respective species. Data were otherwise unaltered and we did not check damage type analyses for accuracy. Statistics reported in the publications occasionally differed from the datasets, such as differences in number of specimens or number of plant-host species. In these cases we used the datasets because it was impossible to identify the inconsistencies. Taxonomy (family, order) of each plant host was compiled using the package ?taxize? for R statistical software (Chamberlain et al. 2017; R Development Core Team 2013). Plant hosts that could not be identified by ?taxize? were added by hand, which frequently happened for extinct genera. We obtained taxonomic information for extinct taxa from the peer-reviewed publications, Fossilworks (Alroy 2016), or academic institution websites. We also compiled the clade of each plant host (fern, gymnosperm, magnoliid angiosperm, monocotyledonous angiosperm, or eudicotyledonous angiosperm). However, the category of ?dicotyledonous angiosperm? was not used as it creates a paraphyly stemming from the exclusion of the monocots (Soltis and Soltis 2004). Additionally, we did not compile taxonomic information for a number of morphotyped plant hosts, such as ?monocot sp.?, ?conifer 1?, etc., although the relevant clade was sometimes evident based on the morphotype labels. We noted the presence of nitrogen-fixing plant species, which are known to influence the level of insect herbivory due to higher leaf Nitrogen : Carbon ratios (Currano et al. 2016), in the dataset. Legumes (Fabaceae) are well known for their symbiotic mutualism with soil-dwelling rhizobia to fix atmospheric nitrogen (Duggar 18 0 and Davis 1916; Russell 1894). However, not all legumes possess the ability to fix nitrogen, with early diverging lineages having low percentages of nitrogen fixing species compared to more recently diverging lineages (Bryan et al. 1996). A recent reclassification of Fabaceae sinks the mimosoid clade within the subfamily Caesalpiniodeae (LPWG 2017), meaning that the Caesalp clade has a greater number of nitrogen fixing species. Formerly, the Mimosoid clade had ~90% nitrogen fixing species (~2700 species), while the Caesalp clade had ~23% nitrogen fixing species (~460 species). In this study, we categorized the legume taxa identified to the Caesalp clade as being non-nitrogen fixing because many of the identifications were made before the Mimosoid clade was sunk into the Caesalp clade, and therefore the likelihood of those taxa being non-nitrogen fixing members of the clade was high. Some non-legume plant clades also have evolved the ability to form symbiotic relationships with microbes to fix nitrogen: including cycads, Gunnera (Gunneraceae) (Bergman et al. 1996; Bergman et al. 2007; Santi et al. 2013), Azolla (Salviniaceae), Alnus (Betulaceae), Rubus (Roseaceae), and approximately twenty other less common genera (Bond 1983; Sprent and Parsons 2000). Data Analyses To assess if there was a general relationship between insect herbivory and time, we regressed an index of damage-type diversity against the geologic age of all localities. Within each of the 164 localities, we then ranked plant hosts by abundance from the most abundant to least abundant plant host. A cutoff of a 20 specimen minimum for the most abundant plant host was implemented and 106 localities met this cutoff (Table 6.1). This helped to eliminate heavily cherry-picked fossil floras 18 1 that underrepresented the most common taxon. Next, skewed levels of herbivory, or those that fell outside of an expected range, were calculated for each plant host at each locality. For each locality, we produced a vector comprising each plant host specimen, either a taxonomically identified species or morphotype, and an adjacent matrix of the presence or absence of damage types for that specimen. To generate the p-value, we then randomly shuffled the vector (plant host specimens) 50,000 times to determine what proportion of the time we found more herbivory or less herbivory per plant host, as measured by the richness of damage types in the matrix, than that of the original data. This allowed us to only compare levels of herbivory for a plant host in relation to the other plant hosts for their particular locality, since heterogeneity of ecological and evolutionary factors among the localities would render whole-dataset comparisons meaningless. Taxa represented by 5 or fewer specimens were removed from the dataset due to insufficient sample sizes for plant-host analyses. To calculate the expected proportion of type I errors, a False Discovery Rate was used on the data (Garc?a 2004; Verhoeven et al. 2005) and significance was reached at p ? 0.0111. After plant hosts with significantly skewed levels of herbivory were found, localities were categorized as either having at least one plant host with skewed levels of herbivory or having no plant hosts with skewed levels of herbivory. Two empirical cumulative distributions were then calculated: one for the localities that have plant hosts with significantly skewed levels of herbivory and one for the localities without plant hosts that have significantly skewed levels of herbivory. To test for differences between the two distributions, and because we are comparing distributions with 18 2 continuous measures, a Wilcox rank sum test with continuity correction was calculated for the ages of these two distributions. Three diversity indices were calculated for the diversity of plant hosts at each fossil locality (Table 6.2). These were chosen because they are commonly used in neontological ecology studies. Once the diversity of each locality was calculated, a Wilcox rank sum test with continuity correction was calculated for the diversity index and the distribution of localities that included plant hosts with significantly skewed levels of insect herbivory. Finally, a linear regression was calculated for the geologic ages and diversity indices for subsampled localities to determine if these variables were strongly correlated with one another. All plots were was produced with the R package ?ggplot2? (R Development Core Team 2013). Table 6.2: Diversity metrics calculated in this study. Diversity Metric Equation Variables s is the number of plant hosts at Simpson?s Index (D) ! a locality, pi is the proportion of 1/ ?!! individuals of the ith plant host !!! ! s is the number of plant hosts at ? ?!ln?! a locality, pi is the proportion of Shannon?s Index (H?) !!! individuals of the ith plant host ! !/(!!!) s is the number of plant hosts at ?! a locality, pi is the proportion of ! Hill numbers (qD or qH ) !!! individuals of the ith plant host, and q is the ?order? of the diversity metric 18 3 Results There was no correlation (R2=0.004, p=0.51) between the overall damage-type diversity and geologic age of all subsampled localities, which span from ca. 76?2 Ma. We next conducted analyses within each locality to better understand general patterns of plant?insect associations in deep time. There was a total of 291 plant hosts, from 79 localities, which had significantly skewed (higher or lower) levels of herbivory based on random chance (Figure 6.2; Supplementary Tables 6.1, 6.2). The majority of these significant results were for plant hosts with lower than expected herbivory (255 plant hosts), while only 36 plant hosts exhibited higher than expected levels of herbivory. Overall, the majority of plant hosts with significantly lower levels of herbivory than expected were the more abundant taxa at the localities, whereas those with significantly higher levels of herbivory were often the relatively rarer taxa (Supplementary Figure 6.1). Several plant lineages were disproportionately likely to have skewed herbivory that was lower than expected (Supplementary Table 6.2), including those in the gymnosperm order Pinales, the extinct Lauraceae genus Daphnogene, the extinct Magnoliidae morphogenus Laurophyllum, several monocot plant hosts, and a seemingly random assortment of eudicotyledons. Only 23% of the total plant hosts with low levels of herbivory for which we had taxonomic information belonged to the taxa listed above. Alternatively, plant hosts belonging to the asterid order Cornales were significantly more likely to be the target of herbivory (Supplementary Table 6.1); over 10% of Cornales specimens had elevated levels of herbivory, yet only 27% 18 4 Figure 6.2: Abundance rank of plant hosts that have significantly less (blue dot) and/or significantly more (red triangle) through time (Ma). Note non-linear x- and y-axes. 18 5 of highly herbivorized plants for which we have taxonomic information belong to Cornales. Interestingly, nitrogen-fixing species were not found to have significantly higher or lower than expected levels of insect herbivory. The majority of plant hosts with skewed levels of herbivory were not taxonomically identified; of all 79 sites for which we obtained significant results for at least one taxon, 56 lacked plant-host taxonomic information and only 23 included taxonomic information. There was a significant difference of the distributions through time between the localities that include plant hosts with skewed levels of herbivory and the distribution of localities that do not have plant hosts with skewed levels of herbivory (Wilcox Rank Sum Test with continuity correction, p=0.02) (Figure 6.3). The older localities, those between ca. 76?28 Ma, had a greater proportion of localities that include plant hosts with skewed levels of herbivory, whereas the younger localities had many fewer of these localities. For the localities over 50 Ma for which we get significant results for at least one taxon, 46 localities lack plant host taxonomic information and a scant 12 include taxonomic information. Localities with greater plant host diversity, as calculated by the Simpson?s Index (D), were also significantly more likely to contain plant hosts with significantly skewed levels of herbivory (p = 0.01955) (Figure 6.4). This result was also found when employing Shannon?s Index (H?) (p = 0.009044). Both D and H? can be converted to an ?effective number of species?: the number of species that would produce the empirical value of the diversity index if all species were equally abundant (Hill, 1973). Many ecologists prefer the effective number of species over diversity 18 6 16 12 20 Figure 6.3: Distributions of localities through time (Ma) for localities with significantly skewed plant hosts (purple line) and localities without significantly skewed plant hosts (gray line). Note non-linear y-axis. indices because the effective number of species has a linear relationship with total species diversity (Jost, 2006). When D and H? are converted to effective numbers of species, the p-values that relate diversity to the presence of plant hosts with significantly skewed levels of herbivory remain unchanged. This is because the Wilcox rank sum test generates p-values from the rank of each locality rather than its raw D, H?, or effective number of species, and the rank of each locality does not change when a diversity index is converted to an effective number of species. However, geologic age and plant diversity per locality were not strongly correlated (R2=0.005288; p = 0.45883) (Figure 6.5), meaning that these variables are largely independent of one another. 18 7 Proportion of localities Figure 6.4: Distributions of localities by plant community diversity (Simpson?s D) for localities with significantly skewed plant hosts (purple line) and localities without significantly skewed plant hosts (gray line). 18 8 Proportion of localities Figure 6.5: Regression of plant community diversity (Simpson?s D) for each locality through time (Ma) with 95% confidence intervals (R2=0.005288; p = 0.45883). Localities with significantly skewed plant hosts are represented by purple dots and localities without significantly skewed plant hosts are represented by gray dots. 18 9 Discussion A broadly-held assumption in the field of plant?insect associations is that there has been widespread changes from the Cretaceous to the present-day in the diversities of angiosperms, their insect herbivores, insect damage, and insect plant- host preference, changes attributable to a coevolutionary arms race (Ehrlich and Raven 1964; Farrell 1998; Janz 2011; McKenna et al. 2009; Mitter et al. 1988; Moreau et al. 2006). We did not find a meaningful correlation between geologic age and the diversity of insect herbivory. Instead, we found that levels of insect herbivory were increasingly skewed for plant hosts at localities with older geologic ages and also for localities with higher plant-host diversities. However, these results are not necessarily clear-cut and this is a cautionary anecdote for the analyses of deep time plant?insect associations. Fossil Record Quality and Sampling Biases as a Function of Age Paleobotanical datasets invariably introduce difficult to control, and often problematic, variables (DiMichele and Gastaldo 2008), including paleolatitude, temperature, precipitation levels, ecosystem type, seasonality, atmospheric carbon dioxide, depositional environment, areal extent of the fossil deposit, time averaging, taphonomic setting, preservational quality of the plant specimens, and evolutionary histories (ex. Behrensmeyer et al. 2000; Locatelli 2014). These conditions almost certainly differ among each of the localities and make comparisons increasingly problematic, but may be analyzed in further studies as predictor models. Moreover, the probability of an organism becoming preserved as a fossil is ?vanishingly small? (Raup 1979), although the fossil record tends to increase in completeness, quality, 19 0 and our ability to identify specimens taxonomically towards the Recent (Kidwell and Holland 2002; Raup 1979; Raup 1972). This phenomenon, known as the Pull of the Recent, explains the factors that lead to an often-artificial increase in diversity of organisms through time approaching the Recent (Raup 1979), which are pertinent to the paleobotanical datasets analyzed in this study. Factors contributing to the Pull of the Recent include the more fully developed taxonomy of extant taxa (Raup 1979). Plant hosts in younger floras often closely resemble and may indeed be closely related to extant taxa and are more easily identified and characterized by paleobotanists (Niklas and Tiffney 1994), especially in the case of angiosperm plant hosts. For example, the datasets analyzed in this study substantially increase in the proportion of identified taxa from older to younger studies. Human error and sampling biases are also of great concern. Beyond inherent differences in data collection among researchers (judgment calls, access to various equipment, etc.) there are substantial differences in how plant-host specimens are analyzed. Museum paleobotanical collections are often fraught with sampling biases, as researchers typically over-collect the rare plant taxa and underrepresent common plant taxa, commonly referred to as ?cherry picking? (Labandeira et al. 2002). Within paleobotanical collections and sampling regimes, there also may also be preference to analyze particular clades of host plants. For instance, some researchers prioritize eudicotyledonous and magnoliid angiosperms, but exclude monocotyledonous angiosperms and non-angiosperms, in order to keep analyses as consistent with other such studies and constrained as possible (ex. Adroit et al. 2016; Wappler and Gr?msson 2016; Wilf et al. 2006). Although this sampling regime is practical, it does 19 1 make comparisons with studies that include all plant host clades tenuous, and more troublingly, not all publications have explicitly disclosed this sampling bias. Finally, morphotyping, which is often implemented for older floras, limits our ability to compare such localities to those with extensive taxonomic identifications. Although species richness of morphotyped floras can be assessed, more fine scale analyses involving specific clades of plants are often not feasible. Our results show a greater proportion of localities with skewed levels of herbivory from ca. 75?28 Ma, and that the younger localities from ca. 28?2 Ma have more stable levels of herbivory. The fundamental question we ask is: why do we see this change in insect preference through time? Because of issues with sampling, such as that the majority of plant hosts with skewed levels of herbivory were not taxonomically identified especially for sites over 50 Ma and the proportion of disproportionate herbivory for identified plant hosts also was relatively low (23% for disproportionately unherbivorized taxa and 27% for disproportionately herbivorized taxa), it is impossible to differentiate between potential explanations for our results. These explanations may be: 1) older localities include more of the plant hosts with skewed levels of insect herbivory, i.e. those belonging to Pinales, Daphnogene, Laurophyllum, and/or monocotyledons; 2) older localities were more likely to have the particular eudicotyledon plant hosts with skewed levels of herbivory due purely to random chance; or 3) researchers involving younger localities were more likely to exclude non-eudicotyledonous plant hosts, eliminating a large portion of the plant hosts that often had significant results. We cannot affirm that the increased variability of insect herbivory at older localities was the result of insect preferences for or 19 2 against particular plant taxa, as it may be the result of sampling biases and/or increasing taxonomic uncertainties with geologic age. Plant Community Diversity and Insect Herbivory The relationship between ecological productivity and species richness is studied widely in modern ecosystems (ex. Cardinale et al. 2011; Waide et al. 1999). Arguments for why, in general, as species richness increases the productivity also increases focus on resource complementarity and the ?selection probability effect? (Huston 1997). Resource complementarity is the differentiated resource use between species in higher diversity systems leading to greater productivity per species than if that system were less diverse, whereas ?selection probability effect?, or sampling effect, is the increased probability of an exceptionally productive species occurring in a diverse system (Huston 1997). Waide et al. (1999) only found empirical evidence for the ?selection probability effect?, although resource complementarity is still widely discussed in ecological literature (ex. Ashton et al. 2010; Barry et al. 2019; Peralta et al. 2014; Poisot et al. 2013). We asked if there was also a positive relationship between plant host richness and insect herbivory in deep time and found that increasingly diverse localities were more likely to contain plant hosts with disproportionate levels of herbivory. There was a significant difference between the distributions of localities with and without plant hosts having disproportionate levels of herbivory and plant host diversity (Simpson?s D). These results might at first glance support the idea that as plant host diversity increases, the probability of including a plant species with skewed levels of herbivory also increases. However, these results are unsubstantiated; localities with 19 3 significant results were over two times as likely to omit taxonomic identifications of plant hosts, and the majority of the significant results occurred in localities over 50 Ma, which were four times as likely to omit taxonomic identifications of plant hosts. Despite plant-host diversity at these localities staying relatively constant through time, the distribution and lack of taxonomic resolution of plant hosts through time again poses an insurmountable problem. We cannot differentiate between several explanations, which are similar to those posed above: 1) localities with higher plant diversity were more likely to contain the plant hosts with skewed levels of insect herbivory, i.e. those belonging to Pinales, Daphnogene, Laurophyllum, and/or monocotyledons; 2) localities with higher plant diversity were more likely to have the particular eudicotyledon plant hosts with skewed levels of herbivory due purely to random chance; or 3) researchers that excluded non-eudicotyledonous plant hosts both eliminated many of the plant hosts that were found to have skewed levels of herbivory and also artificially skewed the plant-host diversities at each locality, potentially rendering this comparison meaningless. Patterns of Insect Herbivory at Finer Temporal and Spatial Scales Multiple studies have found significant relationships between plant?insect associations and floral diversity or geologic age, and in conjunction with other abiotic and biotic factors that are linked with geologic age (ex. Currano et al. 2010; Currano et al. 2008; Labandeira et al. 2002; Leckey and Smith 2017; Pinheiro et al. 2016; Wappler et al. 2009; Wappler and Gr?msson 2016; Wilf and Labandeira 1999; Wilf et al. 2001). This study, which drew from datasets collected across many regions and time intervals, could not detect significant relationships that have been detected at 19 4 finer temporal and spatial scales, or for those which used different methodologies. For example, Pinheiro et al. (2016) found that herbivory frequency increased through time from the Devonian until the Paleocene?Eocene boundary, then decreased during the Eocene (Pinheiro et al. 2016). That study postulated that herbivory was associated with changes in global temperature, atmospheric CO2, and O2 availability (Pinheiro et al. 2016), not simply an increase of herbivory from the Paleozoic to the Cenozoic. Indeed, many studies have looked at plant?interactions through time, but as a function of insect herbivory in response to abiotic and biotic factors instead of insect herbivore preference through time (ex. Currano et al. 2010; Currano et al. 2008; Labandeira et al. 2002; Leckey and Smith 2017; Wappler et al. 2009; Wappler and Gr?msson 2016; Wilf and Labandeira 1999; Wilf et al. 2001). Previous studies that explicitly tested the relationships between insect herbivory and plant community diversity have produced varying results. Wappler and Gr?msson (2016) found that in Icelandic Neogene deposits, plant diversity and the number of damage types were positively related (r=0.76; p= 0.0001), and that the plant diversity changed through time in response to long-term global cooling in the Neogene. In particular, they found that the structural complexity of diverse herbaceous localities increased insect herbivory, even when the patterns of global cooling led the authors to predict otherwise (Wappler and Gr?msson 2016). Another study, Currano et al. (2010), measured insect damage richness against floral diversity for the Paleocene-Eocene Thermal Maximum (PETM) in the Bighorn Basin of Wyoming, USA. They found that insect herbivory was influenced by mean annual temperature (MAT) (R2=0.89; p<0.01) more so than floral diversity (R2=0.38; 19 5 p=0.08) (Currano et al. 2010). A later study by Currano et al. (2019) found that the low-diversity Big Horn Basin flora had a higher diversity of damage types compared to the two, more diverse Wind River Floras (Currano et al. 2019). Currano et al. (2019) hypothesized that this was most likely attributable to microhabitat differences between the sites or endemism of populations that were bisected by high altitude mountain passes (Currano et al. 2019). Perhaps the most striking example of insect herbivory and plant diversity occurs in early Paleocene localities 1 to 2 Ma after the Cretaceous/Paleogene extinction event (Wilf et al. 2006). Wilf et al. (2006) found unbalanced food webs at the Castle Rock and Mexican Hat Floras; there was a positive relationship between insect damage and plant diversity for the Cretaceous through Paleocene floras, except the Castle Rock Flora was exceptionally diverse and had extremely low levels of insect herbivory, while conversely, the Mexican Hat Flora had a relatively depauperate floral diversity, but exceedingly high levels of insect herbivory (Wilf et al. 2006). It is likely that at finer-grained regional and temporal scales, plant diversity is indeed a driver in the diversity of insect damage, although this can be greatly influenced by climatic factors, ecological disturbance, and depositional environment. Guidelines for the Study of Ancient Deep Time Plant?Insect Associations The results of this study are only useful if we evaluate best practices for the study of deep time plant?insect associations. Best practices include: ? Measuring the surface area of each leaf specimen and herbivorized area. Foliar surface area measurements not only documents the intensity of insect 19 6 herbivory, which has been found not to necessarily correlate with damage- type diversity (Schachat et al. 2018), but it will also standardize the differences in leaf size. The larger the leaf, the greater the potential for more herbivory, including a greater number of damage types. For example, comparing a palm frond to a legume leaflet in terms of damage-type diversity is grossly imbalanced, but using surface areas for each species allows greater equivalency. ? Additional plant?insect associational studies of Mesozoic Era deposits will be necessary in future meta-analyses (Xiao et al. in review) to achieve significant understanding of the plant?insect fossil record. ? Identifications of fossil angiosperm species or well-resolved morphotypes should include the lowest taxonomic rank possible. We suggest that even when morphotyping, instead of a designation like ?Leaf Type 1?, if possible and judicious, record with clade- or order-level taxonomic information, (ex. ?Magnoliid 1?, ?Pinales 1?, ?Malvaceae 1?) Conclusions Insight into how insect herbivore preferences for plant hosts have changed throughout the age of angiosperms is important to better understand the diversity of plant?insect associations we see today. Although we found that insect preference has changed through geologic time over the past 76 Ma, and in response to the diversity of plants at each locality, these results may instead be indicative of sampling regime 19 7 and taxonomic uncertainties rather than broad scale patterns of resource use. These results underscore the need to standardize data collection methods and more carefully consider the results of meta-analyses of plant?insect associations. Acknowledgments Thanks to my coauthors, S. Schachat and C. Labandeira, as well as all the authors that shared their datasets. This would not have been possible without the decades of hard work and expertise that provided the building blocks for the study. Thanks also to J. Shultz, for carefully editing this chapter. 19 8 Chapter 7: Conclusions Insects are the most diverse and speciose organisms on earth, and a keystone of modern ecosystems due to the ecological services they provide, including pollination, predation, prey, detritivory, and herbivory. Herbivory in particular has been an important driver of terrestrial ecosystems for hundreds of millions of years and understanding the dynamics of past herbivory will be important in the study of conservation paleobiology (Barnosky et al. 2017, Dietl and Flessa 2011, Dietl et al. 2015, Rick and Lockwood 2013), as well as reconstructing ancient food webs and ecosystems, the end goal for many ongoing collaborative paleontological research projects. The research presented in this dissertation includes the first quantification of plant?insect associations during the Campanian Age, and is among the relatively few analyses of insect herbivory for the Cretaceous Period. The goals of the dissertation were to document the diversity of insect damage on fossil leaves from the Kaiparowits Formation Flora, describe new plant host species, novel insect damage types, important plant?arthropod associations, and analyze datasets of plant?insect associations during the Age of Angiosperms to better understand large-scale patterns of insect preference of plant hosts. In total, this dissertation documents traces of insect behavior in the Kaiparowits Formation, which has yet to yield recognizable insect body fossils, and explores the role of insect herbivores in ecosystems during the Age of Angiosperms. 19 9 Descriptions of fossil plant?insect associations range from ichnotaxonomic descriptions of damage types, to documentation of the earliest known acarodomatia as evidence for a mutualism between plants and mites, and systematic analyses of all types of insect herbivory on Catula gettyi, a newly described species of Lauraceae. In addition, a comprehensive analysis of the intensity and diversity of insect herbivores at a single locality within the Kaiparowits Formation details the primary consumption of plants in a Campanian habitat, the JARS locality, and provides a baseline of comparison for future Cretaceous plant?insect associational studies. Finally, deep time plant?insect association datasets are used to test several modern ecological theories of the role that plant?insect associations have on ecosystem productivity. It is anticipated that the results will aid future meta-analyses in our field of study. Avoidable and unavoidable biases in datasets from deep time may complicate even significant results from meta-analyses of ancient ecological datasets, and we need to reevaluate the methodologies we use in this field. In total, the discoveries and analyses presented in this dissertation allow a better reconstruction of ancient ecosystems of the Kaiparowits Formation, recognize some of the first documented plant?insect associations from a Campanian-aged deposit, and trace the evolutionary trajectories of modern insect lineages and ecological associations back in time to the Late Cretaceous. Future Directions After surveying plant?insect associational studies covering a wide range of time periods and geographic localities, I am consistently reminded of the general trends within the field and gaps in our knowledge. There are major unstudied periods 20 0 of time in the fossil record where plant?insect associations would benefit from analysis. These include additional, systematic studies on floras that likely contain the earliest evidences of insect herbivory, the Permian/Triassic Extinction Event, and most importantly, a full survey of the Mesozoic. Capturing plant?insect associations before, during, and preceding the rise and radiation of angiosperms is of great importance when studying the coevolution of angiosperms and herbivorous insects. Indeed, several workers are currently researching mid-Cretaceous insect herbivory, but there remains much more work to be done in the broader Mesozoic. The work may be hampered by the relatively small number of known Jurassic and Early to mid- Cretaceous floras, but this is an opportune time to support international paleontological teams that may discover, and control access to, new and important fossiliferous deposits. Furthermore, much of the literature on herbivory studies is from the Northern Hemisphere, notably the Western Interior of North America (i.e. this dissertation) and Europe. Studies from the Southern Hemisphere are disproportionately important (ex. Currano et al. 2011, Donovan et al. 2016, Donovan et al. 2018, Fern?ndez and Chiesa 2020, Liu et al. 2020, Ma et al. 2020, McDonald et al. 2007, M?ller et al. 2017, Prevec et al. 2009, Scott et al. 2004, Srivastava and Srivastava 2016, Zhang et al. 2018), and more are needed to counterbalance the Northern Hemisphere biases. Additionally, for all plant?insect associational studies, sampling regimes should be carefully considered and explicitly stated. If we can create reproducible, comparable datasets, future meta-analyses will be both successful and informative. This includes examination of plant?insect associations for entire floras and trying to 20 1 determination of the taxonomic identities of plant hosts. Here I outline goals for my future research and the entire field of study: 1. Collect fossils in a systematic and unbiased way (i.e. census collecting, collecting all plant taxa present). 2. Increase sample sizes if possible. No matter the sample size, subsample and rarefy the data to make comparisons less biased. 3. Use the Labandeira et al. (2007c) Guide to insect (and other) damage types on compressed plant fossils (version 3.01) and the forthcoming Version 4, to describe insect damage on fossil leaves and contribute to the guide with new damage types. This is a communal resource that is constantly updated by researchers from across the globe. Ichnotaxonomic descriptions of damage type can be useful (see Chapter 3), but these descriptions are best undertaken when the damage is identifiable to a particular insect herbivore lineage. 4. Measure surface area of leaves and insect damage. This methodology takes a great deal of time, but it standardizes data to account for differences in leaf size. For example, a palm leaf and a legume leaflet have different potentials for the intensities and diversities of insect damage. Moreover, diversity of herbivory and intensity of herbivory are not necessarily correlated, so surface area measurements capture an important metric of insect herbivory that leaf count and damage type diversity cannot. 5. Publish datasets and consider publishing data on your own if the journal does not support data publication. 20 2 6. Try to publish in open access journals, and if not feasible, use online platforms to make research available and/or be responsive to online requests for publications. 7. Test hypotheses regarding how land plants became herbivorized during the past 400 million years, and describe the modes, mechanisms, and consequences of the evolution of insect herbivory. I greatly look forward to the future of research on deep time plant?insect associations, hopefully produced by an even more diverse pool of scientists, studying new time periods, geographic areas, and implementing novel and visionary analyses. 20 3 Appendices A. Letter to the Dean of the Graduate School 20 4 B. Chapter 2 Supplementary Information Modern Insect Herbivory on Lauraceae Although all herbivore functional feeding groups provide a variety of damage types on extant members of the Lauraceae, there are some notable patterns of herbivory within the family. The DTs inflicted by hole, margin and surface feeders, as well as skeletonizers, are at typical levels of diversity expected for a moderately diverse host-plant family such as Lauraceae. However, a considerable proliferation of associations exists between the broad taxonomic varieties of scale insects and particular host species of Lauraceae. By contrast, the frequency of leaf miners on Lauraceae are minimal (Spencer 2012), while gallers are very diverse, particularly in the Neotropics (Maia et al. 2014). Seed predation is overwhelmingly accomplished by small vertebrates rather than insects (Martins et al. 2015, Myster 1997). Several ant? plant associations, such as between the sweetwood hosts Ocotea dendrodaphne Mez and O. atirrensis Mez & Donn that house the ant symbiont Myrmelachista flavocotea Longino, have been documented (McNett et al. 2010). Another ant?plant association is between Ocotea pedalifolia Mez and the ant Myrmelachista sp. as before, but involving a third mutualist member, the mealy bugs Dysmicoccus brevipes (Cockerell) and D. cryptus (Hempel) that also live in the hollowed-out stems (Stout 1979). Hole Feeding. ? The polyphagous beet armyworm Spodoptera exigua Hubner (Lepidoptera: Noctuidae) is a prominent hole feeder on Lindera benzoin L. (spicebush) in the Southeastern United States. This generalist herbivore, however, 20 5 lessens its levels of hole feeding under conditions of induced response in which its plant host responds to herbivore attack by producing feeding-deterrent substances and structural defenses in foliar tissues (Mooney et al. 2009). Margin Feeding. ? The specialist herbivore, Epimecis hortaria F. (Lepidoptera: Geometridae) is a major margin feeder on Lindera benzoin L. and Sassafras albidum (Nuttall) Nees. This relationship is particularly striking, as elevated levels of photoprotective phenolic compounds occur in sun leaves where higher temperatures increase photosynthesis (Niesenbaum and Kluger 2006), resulting in decreased nitrogen levels. Feeding E. hortaria larvae respond by increasing significantly their level of herbivory (Mooney and Niesenbaum 2012). By contrast, shade leaves on the same plant display decreased levels of E. hortaria margin feeding. although this pattern is not true for all herbivores (Niesenbaum 1992). The Promethea Silkmoth, Callosamia promethea (Lepidoptera: Saturniidae), is a large caterpillar that feeds on Sassafras albidum as one of its primary hosts, also preferring sun leaves over shade leaves (Osier and Jennings 2007). Skeletonization. ? Although recently introduced from Japan, the highly polyphagous Japanese beetle Popillia japonica (Coleoptera: Scarabaeidae) is probably the most prolific skeletonizer of lauraceous sassafras, Sassafras albidum, native to Eastern North America (Potter and Held 2002). Other than the Japanese beetle, there are few native skeletonizing insects on Lauraceae. Surface Feeding. ? Several species of the specialist skipper genus Venada (Lepidoptera: Hesperiidae) are apparently obligate surface feeders of several species 20 6 of the aromatic, lauraceous Ocotea (sweetwood) (Burns et al. 2013). The feeding damage of Venada produces light-colored, polygonal patches of removed epidermal leaf tissue. The most conspicuous obligate surface feeder on Lauraceae is the Spicebush Swallowtail, Papilio troilus L. (Lepidoptera: Papilionidae), that feeds on members of Lauraceae in Eastern North America such as Lindera benzoin, Sassafras albidum, its two primary hosts, and Cinnamomum camphora L. J. Presl. (camphor), Persea borbonia L. (Spreng.) (Redbay), and occasionally members of more distantly related Magnoliaceae (Nitao et al. 1991). Piercing and Sucking. ? The numerous relationships between piercing-and-sucking scale insects and planthoppers on modern Lauraceae hosts indicate that piercing and sucking harbors the single most diverse functional feeding group for Lauraceae. Almost all of these common hemipteran associations are polyphagous and target vascular phloem tissue, such as the black scale, Saissetia oleae (Bernard) (Coccidae), on California bay Umbellaria californica (Hook. & Arn.) Nutt. in California. The similarly polyphagous cottony cushiony scale, Iceyra purchasi Maskell (Monophlebidae), is found on bay laurel Laurus nobilis L., as is the planthopper, Metcalfa pruinosa (Say) (Flatidae), also occurring on L. nobilis. The palm fiorina scale, Fiorinia fioriniae Targioni-Tozzetti (Diaspididae), is a worldwide pest on species of Persea, particularly avocados, in California and Florida, although palms are the preferred host. Piercing-and-sucking insects produce damage on their host plants characterized as cratered punctures and circular, elliptical or ovoidal impressions on surface tissues (Johnson and Lyon 1991). 20 7 Oviposition. ? Many Lepidoptera, such as papilionid butterflies, oviposit on the leaf surfaces of a variety of lauraceous hosts that often are food plants for their larvae (Carter and Feeny 1999, Frankfater and Scriber 1999). However, these oviposition events do not leave detectible damage on epidermal tissue and would not enter the fossil record. There are few instances of documented oviposition that produce recognizable scar tissue on extant Lauraceae. One example is the damselfly Palaemnema desiderata Selys (Odonata: Platystictidae) ovipositing on the twigs, branches and leaf petioles of the lauraceous Licaria sp. in Panama (Soriano et al. 1982). Mining. ? Lauraceae hosts are poorly represented among leaf-mining insects. The most prominent leaf-miner family on Lauraceae (Labandeira et al. 2002a, Labandeira et al. 2002b) are the gracillariid genera Acrocercops, Caloptila, Gracillaria, Lithocolletis and Phyllocnistis that occur on Cinnamomum, Laurus, Lindera, Litsea, Persea, Sassafras and Umbellaria (Fletcher 1920, 1933, Hering 1957, Kumata 1982, Kumata et al. 1988, Needham et al. 1928, Yuan and Robinson 1993). Documented occurrences of the Yellow Poplar Weevil, Odontopus calceatus, also termed the Yellow Poplar Weevil and Sassafras Weevil (Coleoptera: Curculionidae), mines Liriodendron tulipifera L., its primary host, but also mines less commonly Sassafras albidum (Nuttall) Nees and introduced Laurus nobilis L. in Florida (Buss 2006). The apple leaf miner, Lyonetia clerkella L. (Lepidoptera: Lyonettidae), occasionally occurs on Laurus nobilis, although its primary host are Rosaceae and birch across Eurasia and Northern Africa (Berg 1960). Although no leafmining flies (Diptera: 20 8 Agromyzidae) are miners of Lauraceae, at least 13 genera of Lauraceae host at least four Phytobia species of cambium miners in stems and trunks (Spencer 2012). Galling. ? The most notable, described gall association is the avocado psyllid Trioza anceps Tuthill (Hemiptera: Psyllidae) on avocado, Persea americana L., in the southeastern United States. The incidence of this leaf-curl gall is dependent on the specific chemical profile of its host plant, preferring the variety drymifolia within populations of P. americana (Torres-Gurrola et al. 2011). Another Trioza induced gall occurs on Nectandra salicina in Costa Rica, resulting in malformation of a pedunculated fruit that becomes enlarged and is sessilely positioned at the base of a twig (Blackmer and Hanson 1997). One of several Cecidomyiidae (gall midge) galls on Lauraceae is Pseudasphondylia neolitseae (Diptera: Cecidomyiidae), a conical foliar gall on Neolitsea seriacea (Blume) Koidz. in southern Kyushu, Japan (Yukawa and Akimoto 2006). Nevertheless, the greatest diversity of galls on Lauraceae are present in the Neotropics (Maia et al. 2014). Hosts include Cinnamomum (cinnamon), Cryptocarya (mountain laurel), Nectandra (sweetwood), Ocotea and probably unaffiliated genera (Juli?o et al. 2014, Maia et al. 2014, Medianero et al. 2014). Seed Predation. ? Seeds of Lauraceae are overwhelmingly large and typically are dispersed and occasionally predated by birds and small mammals (Holl and Lulow 1997, Martins et al. 2015). Insect predation on seeds of Lauraceae is rare and typically affect species with smaller seeds. One example is loblolly sweetwood Ocotea leucoxylon (Sw.) Laness. occurring on landslides within forests in Puerto Rico, that are predated by undisclosed insects (Myster 1997). The large, robust fruits of many species of Persea (bay, avocado) that are distributed in the Neotropics have a 20 9 dispersal syndrome favoring intact consumption and dispersal of the large seeds by mammal megaherbivores that became extinct during the end of the Pleistocene Epoch (Wolstenholme and Whiley 1999). The extinction of browsing and seed-dispersing megaherbivores such as litopterns, ground sloths, gompotheres and New World horses rendered many modern species of Persea as ?neotropical anachronisms? that presently lack the facility of seed dispersal (Janzen and Martin 1982). 5.2.10. Pathogens. ? Laurel wilt is a vascular disease that invades the xylem of many species of Lauraceae. The disease caused by Raffaelea lauricola T.C. Harr (Ascomycetes: Ophiostomataceae) and is vectored by the ambrosia beetle Xyleborus glabratus Eichoff (Coleoptera: Curculionidae), which is especially harmful to Persea borbonia of the Southeastern United States (Hughes et al. 2015). Tritrophic Interactions. ? When generalist (polyphagous) lepidopteran larvae of Arctiidae and Megalopytidae that consumed secondary compounds of Necandra hypoleuca and N. latifolia, respectively, were in turn consumed by the adult ant Paraponera clavata, there was a minimal rejection rate of the larval prey items (Dyer 1995). However, when specialist (monophagous) lepidopteran larvae of Lasiocampidae, Nymphalidae and Saturniidae consumed N. hypoleuca, Ocotea meziana and Ocotea sp., respectively, there was an elevated rejection rate of the larval prey items. This study indicates that specialist lepidopteran larvae feeding on certain species of Lauraceae can sequester and concentrate secondary compounds to the detriment of predators such as an ant. 21 0 Antiherbivore Resistance in Modern Lauraceae Modern Lauraceae contain significant levels of secondary compounds. For example, Persea americana Mill. (avocado) foliage is especially rich in monoterpenes, sesquiterpenes and similar compounds (Niogret et al. 2013) in the Southeastern United States. In Eastern North America Lindera benzoin has low levels of herbivory particularly in sun rather than shade environments due to production of the phenols of vanillic, chlorogenic, p-coumaric and ferulic acids (Ingersoll et al. 2010). Monoterpenes occur at modest levels at all developmental stages of California bay, Umbullaria californica (Hook. & Arn.) Nutt, where it apparently is a deterrent to folivorous insects and blacktail deer (Goralka and Langenheim 1996), but prized as adding flavor and aroma to cooked foods. However, at the Miyazaki Experimental Forest in Japan, foliar extracts of 16 lauraceous species of Actinodaphne, Cinnamomum, Laurus, Lindera, Litsea and Machilus proved to have negative consequences when fed to insects (Gonz?lez-Coloma et al. 1994a, Gonz?lez-Coloma et al. 1994b). The outcomes of these extracts ranged from subtle antifeedent effects to toxins causing death (Gonz?lez-Coloma et al. 1994a, Gonz?lez-Coloma et al. 1994b). An interesting occurrence in the Canary Islands of Spain features a highly defended laurel forest, where Appolonia barbusana, Laurus azorica, Ocotea foetens and Persea indica exhibit elevated levels of cyanoid diterpenes that have varying levels of insecticidal properties (Gonz?lez-Coloma et al. 1994a, Gonz?lez-Coloma et al. 1994b). Cyanoid dipertene plant extracts of cyandol, cyanoids and cinnceylanol from the four lauraceous genera exhibited modest antifeedent properties to strong growth inhibition when fed to larvae of the lepidopteran tobacco cutworm Spodoptera 21 1 litura F. (Noctuidae), cotton bollworm Heliothis armigera H?bner (Noctuidae) and tussock moth Calliteara fortunata Rogenhofer (Erebidae), as well as the Japanese termite Reticulitermes speratus (Kolbe) (Isoptera: Rhinotermitidae) (Gonz?lez- Coloma et al. 1994a, Gonz?lez-Coloma et al. 1994b). The moderate to strong insecticidal properties of extracts from these four lauraceous species suggest a collective response to insect herbivory in a geographically constrained, insular environment. Interestingly, in a DNA?bar-coding study of a rainforest dominated by Dipterocarpaceae and from the much larger island of Borneo, species of the leaf beetle Anadimonia that were specialized on two species of Lauraceae displayed low levels of feeding, indicating high levels of chemically-defended lauraceous foliage (Kishimoto-Yamada et al. 2013). In addition to chemical defenses, Lauraceae possess considerable structural defenses. Features frequently found in Lauraceae indicate mechanical impediments to insect herbivory principally involve leaf toughness (Grubb 1986). Elements contributing to leaf toughness are thickened epidermis layers, cell-wall rigidity in hypodermis layers, and the presence of robust, girdling fiber strands (Grubb 1986). Recently, the report of cork warts on the leaves of six species of Mezilaurus indicates a novel type structural defense in Lauraceae (Vaz et al. 2018). Cork warts are accumulations of suberized, thickened cells surrounding smaller, radially arranged epidermal cells (Vaz et al. 2018), and provide an additional level of antiherbivore structural defense. 21 2 Supplementary Table 2.1: Comparable species to Catula gettyi. Species epithet Cinnamomum palaciosii Cinnamomum hatschbahii Cinnamomum litsaeaefolium Cinnamomum halmaheirae Cinnamomum pedatineruium Cinnamomum australe Cinnamomum glaziovii Cinnamomum tomentulosum Cinnamomum chana Cinnamomum camphora Cinnamomum montanum Cinnamomum zapatae Cinnamomum erythropus Cinnamomum taubertianum Cinnamomum pedunculatum syn. japonicum 21 3 a b c d e f g Supplementary Figure 2.1: Paratypes of Catula gettyi showing the range of leaf architecture exhibited by this taxon. (a) DMNH 41570. (b) DMNH 54371. (c) DMNH 54379. (d) DMNH 54370. (e) DMNH 41584. (f) DMNH 41567. (g) DMNH 54380. Scale bars = 1.0 cm. 21 4 Supplementary Figure 2.2: Hell Creek species: (a) Marmarthia pearsonii, (b) M. trivialis (c) ?Artocarpus? lessigiana, and (d) ?Ficus? planicostata. Black scale bars= 10 mm; white scale bar= 10 mm. Photographs by R. Wicker, DMNS. 21 5 C. Chapter 3 Supplementary Information Supplementary Figure 3.1: Herbivory index for individual plant hosts in the JARS locality. Center line represents the herbivory index and the upper/lower boundaries represent the 95% confidence interval range. 21 6 D. Chapter 4 Supplementary Information Locality Description of Fossil Leaf Morphotype KP90 that bears Leucopteropsis spiralis The leaf morphotype KP90 occurs as isolated leaves. Leaf attachment petiolate; leaf organization presumed simple. Petiole terete, flanked with a thin wing of laminar tissue extending from the blade, wing width ~0.2 mm or less; petiole base slightly swollen with a C-shaped base interpreted as an abscission scar. Blade attachment marginal. Laminar size notophyll to mesophyll; laminar length 6.5 to 13 cm; laminar width 1.2 to 3.1 cm; laminar length to width ratio 4:1 to 6:1. Laminar shape oblong, or slightly elliptic in smaller specimens; medial symmetry typically symmetrical, slight asymmetry in ~25% of the specimens. Laminar base asymmetrical, with an asymmetrical basal insertion; base angle acute; base shape rounded to convex. Laminar apex angle acute; apex shape convex to rounded; laminar apex without specialized features. Leaf margin entire, unlobed, and with a slight marginal undulation in most specimens; laminar edge otherwise appearing unremarkable. Laminar surface texture appearing smooth. Primary venation pinnate; course of primary vein straight; primary vein much thicker (> 10x) than secondary veins. Secondary vein organization simple brochidodromous; agrophic veins absent; naked basal veins absent; spacing of secondary veins on primary vein varies between regular and irregular; angle of secondary vein departure from primary vein acute and uniform; attachment excurrent; major secondary veins occasionally anastomose as they approach the leaf margin. Minor secondary veins absent. Intersecondary veins present; extending < 50% of the length of the subjacent secondary vein; proximal 21 7 course parallel to major secondary veins, distal course reticulating; frequency of < 1 intersecondary vein per intercostal area. Intercostal tertiary vein organization opposite percurrent and sinuous; tertiary vein course angle with respect to the primary vein obtuse; tertiary vein angle variability with respect to the primary vein inconsistent. Epimedial tertiary veins reticulate; proximal course parallel to the subjacent secondary vein; distal course parallel to the intercostal tertiary vein. Exterior tertiary course looped. Quaternary vein fabric irregular reticulate. Quinternary vein fabric irregular reticulate. Areolation appearing to exhibit poor development, however, higher order venation generally not preserved; freely-ending veinlets not observed. Marginal ultimate venation exhibiting incomplete loops. No cuticular or fertile material recovered or associated with these leaf fossils. 21 8 A B C D Supplementary Figure 4.1: (a) Photograph of Tischeria sp. leaf mine (Specimen no. IU15808-7545, Mine type KLm14) from the Maastrichtian of the Tennessee (Ripley Formation) and (b) redrawn illustration from Stephenson (1992) (Sohn et al. 2012, Stephenson 1992). (c) A blotch leaf mine from the Miocene San Jos? Formation of Argentina (Specimen no. CTES-IC 176, new damage type) and (d) close up, used with permission from Robledo (Robledo et al. 2018). 21 9 E. Chapter 5 Supplementary Information Locality Description During the past 10 years of field exploration, more than 100 megafloral localities have been found and collected in the ca. 860 m thick, Campanian-aged Kaiparowits Formation (76.6 ? 74.5 Ma) (Roberts et al. 2013) in southern Utah, USA (Supplementary Figure 5.1). Most of these localities occur in the middle member (ca. 90-110 to ca. 550 m) (Roberts 2007) of the formation. Within the middle member, the majority of megafloral localities are further restricted to the stratigraphic zone between ca. 300 and 450 m. The fossil leaf species presented in Maccracken et al. (main text) that hosts the mite domatia is designated as plant morphotype ?KP88? (the morphotype number is an abbreviation for the Kaiparowits Formation [KP] and a sequential listing of the number of morphotypes in the formation (see Miller et al. 2013)). The host taxon, KP88, occurs at only two localities: DMNH Loc. 3725 (JARS) and 4000 (Talk Radio), which occur at ca. 365 ? 20 m and ca. 440 ? 10 m above the base of the formation, respectively (Supplementary Figure 5.2). A depositional rate of 41 cm/1,000 years was obtained by calculating 40Ar/39Ar ages on sanidine crystals from volcanic ash beds (Roberts et al. 2013) and informs our dating of the acarodomatia. Considering only the error associated with the stratigraphic position of the localities, we estimate the age of DMNH locality 3725 at 75.7 ? 0.05 Ma and DMNH locality 4000 at 75.5 ? 0.02 Ma. These dates are equivalent to a late Campanian age (Walker et al. 2013). The two localities at which morphotype KP88 occurs represent different depositional environments. In the facies association (FA) classification of Roberts 22 0 (2007) for the Kaiparowits Formation, DMNH locality 3725 (Roberts et al. 2013) occurs in FA6, which is finely laminated, calcareous silt- and mudstone. This facies association is interpreted as forming in lacustrine settings (Roberts 2007). In contrast, DMNH locality 4000 occurs in FA5, which is minor tabular and lenticular sandstone, immediately above FA9, which is carbonaceous mudstone. FA5 is interpreted as forming in crevasse splays and crevasse channels, and FA9 is interpreted as forming in swamps and oxbow lakes (Roberts 2007). Currently, KP88 is represented by 41 partial specimens: 34 from DMNH locality 3725, and 7 from DMNH locality 4000. Acarodomatia (13 total) are found on ten specimens: EPI. 40928, 40929, 40930, 40931, 40932, 40933, 45427, 45455, 45456, and 47132. The very large size of this fossil leaf morphotype, exceeding 30 cm in length and 25 cm in width, likely led to pre- and post-depositional lamina fragmentation and the omnipresence of partial specimens in the settings for which it is found. Until more complete material is recovered, we elect to describe KP88 while retaining its informal morphotype designation. Leaf Description The following terminology used follows Ellis et al. (2009) (Ellis et al. 2009). Leaves likely simple. Leaf attachment appearing petiolate; arrangement with other leaves unknown. Petiole exhibiting a pronounced corrugated texture; up to 1 cm thick; alternatively, leaves could be nearly sessile and attached to a woody and corrugately textured branch. Blade attachment marginal. Lamina of megaphylly size; length exceeding 30 cm; width exceeding 25 cm; and a lamina length to width ratio 22 1 ca. 1.2:1. The lamina shape appearing ovate; medial lamina slightly asymmetrical. Laminar base appearing symmetrical; base angle reflexed; base shape cordate. Lamina apex not observed. Leaf margin entire (untoothed), unlobed; laminar surface texture appearing smooth (small raised bumps on the compression/impression surface are interpreted as mineral deposits). Primary venation pinnate; thickness of primary vein up to ca. 0.5 cm; course of primary vein more or less straight; primary vein decreases in width toward apex after giving rise to major secondary veins; on some specimens it appears that laminar tissue partially covers the primary vein, particularly near the leaf base. Secondary vein organization appearing simple brochidodromous; agrophic veins present, simple; seven basal veins present including both primary and secondary veins; naked basal veins absent; secondary veins immediately crowded at the leaf base but otherwise regularly spaced along the primary vein; angle of secondary vein departure from primary vein acute and constant; secondary vein course appearing to arch towards the leaf apex, decurrent on the primary vein; minor secondary veins absent (with the exception of the agrophic veins); interior secondary veins and intersecondary veins absent. Intercostal tertiary vein organization preserved in small portions of the recovered leaf material; where observed, alternate percurrent and sinuous; tertiary vein course angle with regard to the primary vein obtuse; tertiary vein angle variability unknown. Epimedial tertiary veins appearing alternate percurrent; proximal course perpendicular to the midvien, distal course unknown. Exterior tertiary course unknown. Quaternary and higher vein fabric unknown. Highest order veins observed along marginal venation, appearing looped. No cuticular or fertile material has been recovered or associated with these leaf fossils. 22 2 Morphotype Exemplar. DMNH EPI.47131 (Supplementary Figure 5.3 A?C). Referred Specimens (not figured). DMNH 40928, 40929, 40930, 40931, 40932, 40933, 45427, 45455, 45456. Damage Type (DT) Assignment. This acarodomatium is assigned to DT339 in an addendum to the most recent version of the Damage Guide (Labandeira et al. 2007c). 22 3 DMNH Loc. 4000 DMNH Loc. 3925 Supplementary Figure 5.1: Map showing major roads, towns and land designation boundaries in southern Utah, USA. The exposures of the Upper Cretaceous Kaiparowits Formation are shown in green. Stars indicate the approximate locations of DMNH localities 3725 and 4000 where KP88 was found. Figure modified from Lyson et al. (2017). 22 4 900 800 upper unit 700 600 500 DMNH Loc. 4000 ~440 ? 10 m 400 middle DMNH Loc. 3725 unit ~365 ? 20 m 300 200 100 lower unit 0 m Supplementary Figure 5.2: Representative stratigraphic column for the Kaiparowits Formation redrawn from Roberts (2007) showing major sedimentary modes. The stratigraphic positions are shown of DMNH localities 3725 and 4000 where examples of KP88 were recovered. 22 5 Wahweap Kaiparowits Formation Canaan Formation Peak Fm. Meandering Tidally infl./ Anastomosing Meandering estuarine and meandering A B C Supplementary Figure 5.3: Morphotype exemplar specimen DMNH 47132 of KP88 described in Maccracken et al. (2019) from DMNH locality 4000. (a) The most complete specimen of KP88. Specimen shows about 75% of the lamina. (b) Detail showing the lower right-hand section of the leaf with alternate percurrent tertiary vein fabric. The large veins at top and bottom of the image are secondary veins. (c) Detail showing corrugated surface on petiole or stem. White scale bar = 1.0 cm; black scale bars = 0.5 cm. 22 6 G. Chapter 6 Supplementary Information The Fruitland and Kirtland Formations The Fruitland and Kirtland (F/K) Formations are located in the northwest corner of New Mexico, USA, at approximate paleolatitude of 44.2oN (Miller et al. 2013). These formations are among the upper units within the San Juan Basin, bounded by the older Pictured Cliffs Sandstone and a massive uncomformity that separates the Cretaceous strata from the overlaying Tertiary Ojo Alamo Sandstone (Fassett and Steiner 1997, Hunt and Lucas 1992). Radiometric dating of volcanic ash by Fassett and Steiner (1997) found the Fruitland/Kirtland Formations to be middle Campanian in age (ca. 73?75.5 Ma). The F/K Formations are well-known for fossils of vertebrates, invertebrates, and plant macrofossils (Davies-Vollum et al. 2011, Hunt 1991, Hutchinson and Kues 1985, Longrich 2011, Sullivan 1999, Sullivan and Lucas 2006, Sullivan and Lucas 2000, Sullivan and Williamson 1999, Williamson 2000, Williamson and Weil 2008). The Kirtland Formation overlies the older Fruitland Formation, but they are often grouped together owing to similar depositional environments (Fassett and Steiner 1997, Hunt and Lucas 1992). In general, fossils are found in fine-grained and organic deposits, which are interpreted as floodplains and overbank deposits or in slightly coarser-grained rocks that were likely channel systems (Davies-Vollum et al. 2011, Hunt and Lucas 1992). Fossil leaves in the F/K Formations are found in fine-grained mudstones and sandstones. Formal descriptions of all localities will be made available in future paleobotanical publications. 22 7 Fruitland/Kirtland Formations specimens are housed at the National Museum of Natural History in Washington, DC. This flora was collected by Dr. Lisa Boucher and colleagues from 1999?2004. 22 8 Supplementary Table 6.1: Plant hosts with significantly higher levels of insect herbivory than expected and all relevant associated data. Abun Angi ANA Mag Species/ - p- o- - - Eu- N- Age Morphotyp Publicatio dance valu Pterido Gymno sper Grad nolii Mono dico Fixe (Ma e Locality n Rank e -sperm -sperm m e d -cot t r ) Adroit et 0.00 Vitis sp. Bernasso al. (2016) 12 6 0 0 1 0 0 0 1 0 2 Tilia Willershause Adroit et 0.00 saportae n al. (2018) 51 1 0 0 1 0 0 0 1 0 2.8 Fraxinus Willershause Adroit et 0.00 ornus n al. (2018) 78 3 0 0 1 0 0 0 1 0 2.8 Wappler & Betula M?kollsdalu Gr?msson 0.00 cristata r (2016) 2 9 0 0 1 0 0 0 1 0 8.5 Quercus Knor et al. 0.00 rhenana B?e??any (2012) 8 0 0 0 1 0 0 0 1 0 19.6 Populus Knor et al. 0.00 zaddachii B?lina (2012) 20 0 0 0 1 0 0 0 1 0 19.6 cf. Berberis Dom?ngue 0.00 sp. Level NH z (2018) 4 7 0 0 1 0 0 0 1 0 25.4 Currano et 0.00 Type K1 CH72 al. (2011) 2 3 NA NA NA NA NA NA NA NA 27.5 Plant Host Wilf et al. 0.00 19 323 (2001) 3 6 NA NA NA NA NA NA NA NA 43 Plant Host Wilf et al. 0.00 12 1732 (2001) 4 5 NA NA NA NA NA NA NA NA 43 Plant Host Wilf et al. 0.00 15 1732 (2001) 9 1 NA NA NA NA NA NA NA NA 43 Wappler et 0.00 Laura Sp. Eckfeld al. (2012) 10 0 0 0 1 0 0 0 0 0 44.3 Wappler et 0.00 Ulma Sp. Eckfeld al. (2012) 22 1 0 0 1 0 0 0 1 0 44.3 Wappler et 0.00 Ruta Sp. Eckfeld al. (2012) 29 0 0 0 1 0 0 0 1 0 44.3 Rhodomyrto phyllum Wappler et 0.00 sinuatum Messel al. (2012) 17 0 0 0 1 0 0 0 1 0 47.8 22 9 Symplocos Currano et 0.00 incondita EPWR1601 al. (2019) 10 0 0 0 1 0 0 0 1 0 49.1 Dicot sp. Currano et 0.00 WW053 42403 al. (2010) 8 5 0 0 1 0 0 0 1 0 52.7 Wilf et al. 0.00 Plant Host 1 41352 (2001) 2 5 NA NA NA NA NA NA NA NA 53 Dicot sp. Currano et 0.00 WW003 42384 al. (2008) 9 1 0 0 1 0 0 0 1 0 55.8 Browniea 42042 Currano et 0.00serrata al. (2008) 3 0 0 0 1 0 1 0 0 0 57.5 Davidia 42041 Currano et 0.00antiqua al. (2008) 5 2 0 0 1 0 0 0 1 0 58.9 Wappler & Corylites Kolfjellet Denk 0.01 hebridicus (2011) 6 0 0 0 1 0 0 0 1 0 61 Labandeira et al. 0.00 FU7 441 (2002) 1 0 NA NA NA NA NA NA NA NA 65.6 Labandeira et al. 0.00 FU16 87150 (2002) 4 0 NA NA NA NA NA NA NA NA 65.6 Labandeira et al. 0.00 HC43 517 (2002) 2 2 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC212 567 (2002) 5 1 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC212 1491 (2002) 3 0 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC200 1781 (2002) 4 0 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC212 2203 (2002) 5 8 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC73 86102 (2002) 3 1 NA NA NA NA NA NA NA NA 66.5 23 0 Labandeira et al. 0.00 HC66 86153 (2002) 4 3 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC36 87129 (2002) 4 9 NA NA NA NA NA NA NA NA 66.5 Labandeira et al. 0.00 HC57 88111 (2002) 3 0 NA NA NA NA NA NA NA NA 66.5 0.00 D80 302 This study 3 3 NA NA NA NA NA NA NA NA 74.3 0.00 F10 9726 This study 10 3 NA NA NA NA NA NA NA NA 74.3 0.00 sp25.1 Lost Valley This study 7 1 NA NA NA NA NA NA NA NA 75.6 23 1 Supplementary Table 6.2: Plant hosts with significantly lower levels of insect herbivory than expected and all relevant associated data. Abun - Angi ANA Mag Species/ danc p- o- - - Eu- N- Age Morpho- Pub- e valu Pterido Gymno sper Grad nolii Mon dico Fi (Ma type Locality lication Rank e -sperm -sperm m e d o-cot t x ) Sorbus Adroit et 0.00 domestica Bernasso al. (2016) 7 0 0 0 1 0 0 0 1 0 2 Acer opulifoliu Adroit et 0.00 m Bernasso al. (2016) 11 0 0 0 1 0 0 0 1 0 2 Adroit et 0.00 Acer sp. Bernasso al. (2016) 15 0 0 0 1 0 0 0 1 0 2 Fagus Adroit et 0.00 attenuata Berga al. (2018) 1 4 0 0 1 0 0 0 1 0 2.8 Zelkova Willershau Adroit et 0.00 ungeri sen al. (2018) 1 0 0 0 1 0 0 0 1 0 2.8 Carpinus Willershau Adroit et 0.00 betulus sen al. (2018) 9 0 0 0 1 0 0 0 1 0 2.8 Willershau Adroit et 0.00 Oleaceae sen al. (2018) 18 6 0 0 1 0 0 0 1 0 2.8 Betula Willershau Adroit et 0.00 lenta sen al. (2018) 30 2 0 0 1 0 0 0 1 0 2.8 Willershau Adroit et 0.00 Ericaceae sen al. (2018) 76 0 0 0 1 0 0 0 1 0 2.8 Betulacea Willershau Adroit et 0.00 e sen al. (2018) 102 2 0 0 1 0 0 0 1 0 2.8 Willershau Adroit et 0.00 Buxaceae sen al. (2018) 105 0 0 0 1 0 0 0 1 0 2.8 Potamoge Willershau Adroit et 0.00 to sp. sen al. (2018) 109 0 0 0 1 0 0 1 0 0 2.8 Potamoge ton Willershau Adroit et 0.00 crispus sen al. (2018) 115 0 0 0 1 0 0 0 0 0 2.8 Acer Wappler askelssoni & 0.00 i Brekku? Gr?msson 3 0 0 0 1 0 0 0 1 0 6.5 23 2 (2016) Wappler Acer & askelssoni M?kollsda Gr?msson 0.00 i lur (2016) 7 0 0 0 1 0 0 0 1 0 8.5 Wappler Acer & islandicu M?kollsda Gr?msson 0.00 m lur (2016) 8 0 0 0 1 0 0 0 1 0 8.5 Wappler & M?kollsda Gr?msson 0.00 Ulmus sp. lur (2016) 9 0 0 0 1 0 0 0 1 0 8.5 Wappler & Tr?llatung Gr?msson 0.00 Acer sp. a (2016) 4 0 0 0 1 0 0 0 1 0 10 Wappler & Juglandac Tr?llatung Gr?msson 0.00 eae sp. a (2016) 5 0 0 0 1 0 0 0 1 0 10 Brj?nsl?k Wappler Acer ur & askelssoni (Bar?astr? Gr?msson 0.00 i nd) (2016) 3 0 0 0 1 0 0 0 1 0 12 Hindon M?ller et 0.00 N Morph 10 Maar al. (2017) 7 0 NA NA NA NA NA NA NA A 18.8 Ripogonu Hindon M?ller et 0.00 m Maar al. (2017) 12 1 0 0 1 0 0 1 0 0 18.8 Hindon M?ller et 0.00 N Morph 6 Maar al. (2017) 15 9 NA NA NA NA NA NA NA A 18.8 Hindon M?ller et 0.00 Monocot Maar al. (2017) 16 1 0 0 1 0 0 1 0 0 18.8 Daphnoge ne polymorp Knor et 0.00 ha B?e??any al. (2012) 2 4 0 0 1 0 1 0 0 0 19.6 Nyssa Knor et 0.00 haidingeri B?e??any al. (2012) 6 5 0 0 1 0 0 0 1 0 19.6 23 3 Zelkova zelkovifoli Knor et 0.00 a B?e??any al. (2012) 17 0 0 0 1 0 0 0 1 0 19.6 Knor et 0.00 Carya sp. B?e??any al. (2012) 20 0 0 0 1 0 0 0 1 0 19.6 Ulmus pyramidal Knor et 0.00 is B?lina al. (2012) 2 3 0 0 1 0 0 0 1 0 19.6 Comptoni a Knor et 0.00 difformis B?lina al. (2012) 15 0 0 0 1 0 0 0 1 1 19.6 Rosa Knor et 0.00 europaea B?lina al. (2012) 30 8 0 0 1 0 0 0 1 0 19.6 Crataegus Knor et 0.00 sp. B?lina al. (2012) 59 0 0 0 1 0 0 0 1 0 19.6 Magnolio psida sp. Wappler Orsberg 0.00 2 (2010) 6 0 0 0 1 0 0 0 0 0 23 Magnolio psida sp. Wappler 0.00 2 (2010) Rott 1 0 0 0 1 0 0 0 0 0 23 Daphnoge ne cinnamom Wappler 0.00 ifolia (2010) Rott 4 0 0 0 1 0 1 0 0 0 23 Ailanthus ailanthifol Wappler 0.00 ia (2010) Rott 19 8 0 0 1 0 0 0 1 0 23 Juglandac Wappler 0.00 eae (2010) Rott 31 0 0 0 1 0 0 0 1 0 23 Laurus Wappler 0.00 obovata (2010) Rott 36 0 0 0 1 0 0 0 0 0 23 Trigonob alanopsis rhamnoid Wappler 0.00 es (2010) Rott 37 0 0 0 1 0 0 0 1 0 23 Eotrigono balanus furcinervi Wappler 0.00 s (2010) Rott 47 0 0 0 1 0 0 0 1 0 23 23 4 Fagus deucalion Wappler 0.00 is (2010) Rott 54 0 0 0 1 0 0 0 1 0 23 Vacciniu Wappler 0.00 m rottense (2010) Rott 59 0 0 0 1 0 0 0 1 0 23 Daphnoge Gunkel et 0.01 ne sp. Enspel al. (2015) 6 0 0 0 1 0 1 0 0 0 24.8 Daphnoge ne cinnamom Gunkel et 0.00 ifolia Enspel al. (2015) 17 0 0 0 1 0 1 0 0 0 24.8 Cupressac Dom?ngue 0.00 eae z (2018) Level NH 2 0 0 1 0 0 0 0 0 0 25.4 Liquidam bar Quegstein Wappler 0.00 europaea (2010) 6 0 0 0 1 0 0 0 1 0 25.8 Magnolia attenuata Quegstein Wappler 0.00 (2010) 7 0 0 0 1 0 0 0 0 0 25.8 Laurophyl lum sp. Quegstein Wappler 0.00 (2010) 8 0 0 0 1 0 0 0 0 0 25.8 Currano et al. 0.00 Albizia CH72 (2011) 1 1 0 0 1 0 0 0 1 1 27.5 Mildbrae Currano diodendro et al. 0.00 n CH72 (2011) 9 0 0 0 1 0 0 0 1 1 27.5 Morphoty Wilf et al. 0.00 N pe 13 323 (2001) 1 0 NA NA NA NA NA NA NA A 43 Morphoty Wilf et al. 0.00 N pe 13 1732 (2001) 1 0 NA NA NA NA NA NA NA A 43 Morphoty Wilf et al. 0.00 N pe 5 1732 (2001) 6 0 NA NA NA NA NA NA NA A 43 Morphoty Wilf et al. 0.00 N pe 28 1732 (2001) 11 0 NA NA NA NA NA NA NA A 43 Wappler Fagales Nathorstfjellet & Denk 0.00sp. (2011) 9 0 0 0 1 0 0 0 1 0 44 Trochode Nathorstfj Wappler 0.00 ndroides ellet & Denk 11 0 0 0 1 0 0 0 1 0 44 23 5 crenulata (2011) Wappler Apocy et al. 0.00 Sp. Eckfeld (2012) 2 0 0 0 1 0 0 0 1 0 44.3 Wappler Tern. et al. 0.00 N Dent. Eckfeld (2012) 3 0 NA NA NA NA NA NA NA A 44.3 Wappler Pungi. et al. 0.00 Walt. Eckfeld (2012) 4 0 0 0 1 0 1 0 0 0 44.3 Wappler Dicot et al. 0.00 Ulmo Eckfeld (2012) 5 0 0 0 1 0 0 0 1 0 44.3 Wappler et al. 0.00 Carp. Sp. Eckfeld (2012) 7 0 0 0 1 0 0 0 1 0 44.3 Wappler Faba et al. 0.00 Typ1 Eckfeld (2012) 8 0 0 0 1 0 0 0 1 1 44.3 Wappler Compt et al. 0.00 Sp. Eckfeld (2012) 12 0 0 0 1 0 0 0 1 1 44.3 Wappler et al. 0.00 Cerci Sp. Eckfeld (2012) 15 4 0 0 1 0 0 0 1 0 44.3 Wappler Myricac et al. 0.00 Sp. Eckfeld (2012) 16 6 0 0 1 0 0 0 1 1 44.3 Wappler et al. 0.00 Poly Sp. Eckfeld (2012) 21 0 0 0 1 0 0 0 1 0 44.3 Wappler Ulmus et al. 0.00 Sp. Eckfeld (2012) 23 0 0 0 1 0 0 0 1 0 44.3 Wappler et al. 0.00 Zelko Sp. Eckfeld (2012) 25 0 0 0 1 0 0 0 1 0 44.3 Wappler 0.00 Thea Sp. Eckfeld et al. 28 0 0 0 1 0 0 0 1 0 44.3 23 6 (2012) Wappler et al. 0.00 Daph Sp. Eckfeld (2012) 31 0 0 0 1 0 1 0 0 0 44.3 Wappler et al. 0.00 Myri Sp. Eckfeld (2012) 32 0 0 0 1 0 0 0 1 1 44.3 Laurophyl lum Wappler lanigeroid et al. 0.00 es Messel (2012) 2 0 0 0 1 0 0 0 0 0 47.8 Daphnoge ne Wappler crebrigra et al. 0.00 nosa Messel (2012) 8 0 0 0 1 0 1 0 0 0 47.8 Wappler Daphnoge et al. 0.01 ne sp. Messel (2012) 9 1 0 0 1 0 1 0 0 0 47.8 Wappler Ulmaceae et al. 0.00 sp. Messel (2012) 11 4 0 0 1 0 0 0 1 0 47.8 Wappler Daphnoge et al. 0.00 ne sp1 Messel (2012) 13 0 0 0 1 0 1 0 0 0 47.8 Wappler Dicot et al. 0.00 spGM002 Messel (2012) 14 0 0 0 1 0 0 0 1 0 47.8 Laurophyl Wappler lum et al. 0.00 hirsutum Messel (2012) 16 2 0 0 1 0 0 0 0 0 47.8 Wappler Nymphae et al. 0.00 aceae sp. Messel (2012) 19 0 0 0 1 0 0 0 0 0 47.8 Ulmoidea e Wappler Formenkr et al. 0.00 eis 1 Messel (2012) 21 0 0 0 1 0 0 0 1 0 47.8 Laurophyl Wappler 0.00 lum sp2 Messel et al. 23 0 0 0 1 0 0 0 0 0 47.8 23 7 (2012) Wappler Cercidiph et al. 0.00 yllum sp Messel (2012) 28 0 0 0 1 0 0 0 1 0 47.8 Wappler et al. 0.00 Hedera sp Messel (2012) 34 0 0 0 1 0 0 0 1 0 47.8 Juglandac eae Wappler Formenkr et al. 0.00 eis 3 Messel (2012) 35 0 0 0 1 0 0 0 1 0 47.8 Laurophyl lum Wappler natistomu et al. 0.00 m Messel (2012) 37 0 0 0 1 0 0 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 tertiarium Messel (2012) 38 0 0 0 1 0 0 0 0 0 47.8 Wappler Menisper et al. 0.00 maceae sp Messel (2012) 39 0 0 0 1 0 0 0 1 0 47.8 Wappler Sloanea et al. 0.00 sp Messel (2012) 40 1 0 0 1 0 0 0 1 0 47.8 Ternstroe Wappler mites et al. 0.00 dentaus Messel (2012) 41 3 0 0 1 0 0 0 1 0 47.8 Wappler Cabomba et al. 0.00 sp Messel (2012) 48 0 0 0 1 1 0 0 0 0 47.8 Wappler Comptoni et al. 0.00 a sp Messel (2012) 49 0 0 0 1 0 0 0 1 1 47.8 Daphnoge ne Wappler cryptosto et al. 0.00 ma Messel (2012) 50 0 0 0 1 0 1 0 0 0 47.8 Daphnoge Wappler 0.00 ne Messel et al. 51 0 0 0 1 0 1 0 0 0 47.8 23 8 leptohuep (2012) he Daphnoge Wappler ne et al. 0.00 multipora Messel (2012) 52 0 0 0 1 0 1 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 glaphyre Messel (2012) 53 0 0 0 1 0 0 0 0 0 47.8 Wappler Laurophyl et al. 0.00 lum sp1 Messel (2012) 54 0 0 0 1 0 0 0 0 0 47.8 Wappler Polyspora et al. 0.00 hassiaca Messel (2012) 55 0 0 0 1 0 0 0 1 0 47.8 Wappler Symploco et al. 0.00 s sp Messel (2012) 56 0 0 0 1 0 0 0 1 0 47.8 Wappler Ampelops et al. 0.00 is sp Messel (2012) 59 0 0 0 1 0 0 0 1 0 47.8 Byttnerio phyllum Wappler tiliaefoliu et al. 0.00 m Messel (2012) 66 0 0 0 1 0 0 0 1 0 47.8 Daphnoge Wappler ne et al. 0.00 eocaenica Messel (2012) 67 0 0 0 1 0 1 0 0 0 47.8 Wappler Daphnoge et al. 0.00 ne sp3 Messel (2012) 68 0 0 0 1 0 1 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 alatum Messel (2012) 70 0 0 0 1 0 0 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 ebenoides Messel (2012) 71 0 0 0 1 0 0 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 lutetium Messel (2012) 72 0 0 0 1 0 0 0 0 0 47.8 23 9 Laurophyl Wappler lum et al. 0.00 schottleri Messel (2012) 74 0 0 0 1 0 0 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 streble Messel (2012) 75 0 0 0 1 0 0 0 0 0 47.8 Laurophyl Wappler lum et al. 0.00 weylandii Messel (2012) 76 0 0 0 1 0 0 0 0 0 47.8 Wappler Legumino et al. 0.00 sae sp2 Messel (2012) 78 0 0 0 1 0 0 0 1 1 47.8 Wappler Legumino et al. 0.00 sae sp3 Messel (2012) 79 0 0 0 1 0 0 0 1 1 47.8 Wappler Legumino et al. 0.00 sae sp4 Messel (2012) 80 0 0 0 1 0 0 0 1 1 47.8 Platanus Wappler fraxinifoli et al. 0.00 a Messel (2012) 81 0 0 0 1 0 0 0 1 0 47.8 Viscophyl Wappler lum et al. 0.00 pinnatum Messel (2012) 84 0 0 0 1 0 0 0 1 0 47.8 Viscophyl lum Wappler septemner et al. 0.00 vium Messel (2012) 85 0 0 0 1 0 0 0 1 0 47.8 Currano Dicot sp. EPWR160 et al. 0.00 AY004 1 (2019) 5 0 0 0 1 0 0 0 1 0 49.1 Currano Platanites EPWR160 et al. 0.00 raynoldsii 1 (2019) 9 0 0 0 1 0 0 0 1 0 49.1 Aleurites Currano fremonten EPWR160 et al. 0.00 sis 1 (2019) 11 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY008 1 (2019) 12 0 0 0 1 0 0 0 1 0 49.1 24 0 Aleurites Currano fremonten EPWR160 et al. 0.00 sis 2 (2019) 6 0 0 0 1 0 0 0 1 0 49.1 Currano Platanites EPWR160 et al. 0.00 raynoldsii 2 (2019) 7 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY005 2 (2019) 8 0 0 0 1 0 0 0 1 0 49.1 Symploco Currano s EPWR160 et al. 0.00 incondita 2 (2019) 10 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY009 3 (2019) 2 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY005 3 (2019) 8 0 0 0 1 0 0 0 1 0 49.1 Currano Platanites EPWR160 et al. 0.00 raynoldsii 3 (2019) 9 0 0 0 1 0 0 0 1 0 49.1 Aleurites Currano fremonten EPWR160 et al. 0.00 sis 3 (2019) 11 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY009 4 (2019) 4 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 WR007 4 (2019) 7 0 0 0 1 0 0 0 1 0 49.1 Currano Dicot sp. EPWR160 et al. 0.00 AY004 4 (2019) 8 0 0 0 1 0 0 0 1 0 49.1 Symploco Currano s DMNH51 et al. 0.00 incondita 02 (2019) 1 0 0 0 1 0 0 0 1 0 52.4 Currano Dicot sp. DMNH51 et al. 0.00 WR007 02 (2019) 8 0 0 0 1 0 0 0 1 0 52.4 24 1 Currano Dicot sp. et al. 0.00 WW052 42402 (2010) 3 1 0 0 1 0 0 0 1 0 52.7 "Dombey Currano a" novi- et al. 0.00 mundi 42403 (2010) 4 5 0 0 1 0 0 0 1 0 52.7 Morphoty Wilf et al. 0.00 N pe 18 41342 (2001) 2 4 NA NA NA NA NA NA NA A 53 Morphoty Wilf et al. 0.00 N pe 3 41352 (2001) 1 0 NA NA NA NA NA NA NA A 53 Fabaceae Currano sp. et al. 0.00 WW040 37560 (2010) 2 0 0 0 1 0 0 0 1 1 53.4 Fabaceae Currano sp. et al. 0.00 WW042 37560 (2010) 5 8 0 0 1 0 0 0 1 1 53.4 Currano dicot sp. et al. 0.00 WW001 42384 (2008) 1 0 0 0 1 0 0 0 1 0 55.8 Currano Platanus et al. 0.00 raynoldsi 41643 (2008) 4 0 0 0 1 0 0 0 1 0 55.9 Morphoty Wilf et al. 0.00 N pe 8 41270 (2001) 1 7 NA NA NA NA NA NA NA A 56 Currano Platanus et al. 0.00 raynoldsi 42411 (2010) 5 0 0 0 1 0 0 0 1 0 56.4 Currano Persites et al. 0.00 argutus 42042 (2008) 1 0 0 0 1 0 1 0 0 0 57.5 Currano Browniea et al. 0.00 serrata 42041 (2008) 2 8 0 0 1 0 1 0 0 0 58.9 Currano Platanus et al. 0.00 raynoldsi 42041 (2008) 3 1 0 0 1 0 0 0 1 0 58.9 Schmidt et al. 0.00 N HB182 A (2019) 2 0 NA NA NA NA NA NA NA A 59.5 24 2 Schmidt et al. 0.00 N HB178 A (2019) 5 0 NA NA NA NA NA NA NA A 59.5 "Cinnamo Wappler mum" et al. 0.01 martyi Menat (2009) 7 0 0 0 1 0 1 0 0 0 60.5 Wappler "Corylus" et al. 0.00 sp. Menat (2009) 12 0 0 0 1 0 0 0 1 0 60.5 Wappler "Atriplex" et al. 0.00 borealis Menat (2009) 22 0 0 0 1 0 0 0 1 0 60.5 Wappler Acer Kolfjellet & Denk 0.00 arcticum (2011) 10 0 0 0 1 0 0 0 1 0 61 Donovan et al. 0.00 N SA73 LF (2018) 2 8 NA NA NA NA NA NA NA A 62.4 Donovan et al. 0.00 N SA43 PL2 (2018) 6 8 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.00 N SA47 PL2 (2018) 8 0 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.01 N SA16 PL2 (2018) 9 0 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.00 N SA8 PL2 (2018) 14 1 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.00 N SA58 PL2 (2018) 18 4 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.00 N SA50 PL2 (2018) 19 4 NA NA NA NA NA NA NA A 64.1 Donovan et al. 0.00 N 65.2 SA44 PL1 (2018) 6 0 NA NA NA NA NA NA NA A 2 24 3 Donovan et al. 0.00 N 65.2 SA8 PL1 (2018) 9 0 NA NA NA NA NA NA NA A 2 Donovan et al. 0.00 N 65.2 SA5 PL1 (2018) 14 3 NA NA NA NA NA NA NA A 2 Labandeir a et al. 0.00 N FU7 562 (2002) 4 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU2 2217 (2002) 3 3 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N HC123 2217 (2002) 8 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU38 86107 (2002) 3 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU35 86107 (2002) 8 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU3 86110 (2002) 2 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU4 86110 (2002) 3 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU4 87150 (2002) 1 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU26 87150 (2002) 2 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU51 87150 (2002) 5 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU3 88103 (2002) 1 0 NA NA NA NA NA NA NA A 65.6 24 4 Labandeir a et al. 0.00 N FU26 88103 (2002) 2 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU1 88103 (2002) 6 0 NA NA NA NA NA NA NA A 65.6 Labandeir a et al. 0.00 N FU4 KJ8403 (2002) 2 0 NA NA NA NA NA NA NA A 65.6 Donovan Morphoty et al. 0.01 N pe 20 LefE (2018) 9 0 NA NA NA NA NA NA NA A 66.5 Donovan Morphoty et al. 0.00 N pe 36 LefE (2018) 16 5 NA NA NA NA NA NA NA A 66.5 Donovan Morphoty et al. 0.00 N pe 61 LefE (2018) 20 3 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC166 428 (2002) 1 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC165 428 (2002) 10 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC180 428 (2002) 16 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 428 (2002) 21 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC62 517 (2002) 4 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC165 517 (2002) 6 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC200 517 (2002) 7 0 NA NA NA NA NA NA NA A 66.5 24 5 Labandeir a et al. 0.00 N HC44 517 (2002) 8 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC32 566 (2002) 2 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC103 566 (2002) 4 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC80 567 (2002) 2 2 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC137 567 (2002) 8 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 567 (2002) 9 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC225 567 (2002) 11 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC70 567 (2002) 12 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC103 568 (2002) 3 2 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 571 (2002) 3 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N FU4 571 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC71 571 (2002) 7 4 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC71 897 (2002) 3 0 NA NA NA NA NA NA NA A 66.5 24 6 Labandeir a et al. 0.00 N FU37 900 (2002) 6 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC111 900 (2002) 17 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC135 1491 (2002) 1 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC211 1491 (2002) 4 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC90 1491 (2002) 6 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 1491 (2002) 7 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC165 1781 (2002) 1 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC70 1781 (2002) 6 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC49 1855 (2002) 2 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC241 2087 (2002) 2 1 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N Morph-E 2087 (2002) 10 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 2097 (2002) 6 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC266 2098 (2002) 1 1 NA NA NA NA NA NA NA A 66.5 24 7 Labandeir a et al. 0.00 N FU2 2098 (2002) 2 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC81 86100 (2002) 1 6 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.01 N HC80 86100 (2002) 2 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC35 86100 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC90 86100 (2002) 9 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 86100 (2002) 11 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC71 86102 (2002) 4 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC70 86102 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N FU37 86102 (2002) 9 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC1 87110 (2002) 3 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC44 87110 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC57 87129 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 87134 (2002) 4 0 0 1 0 0 0 0 0 0 66.5 24 8 Labandeir a et al. 0.00 N FU3 87134 (2002) 5 0 NA NA NA NA NA NA NA A 66.5 Labandeir Taxodiace a et al. 0.00 ae 88111 (2002) 1 0 0 1 0 0 0 0 0 0 66.5 Labandeir a et al. 0.00 N HC114 88111 (2002) 2 0 NA NA NA NA NA NA NA A 66.5 Labandeir a et al. 0.00 N HC32 88111 (2002) 4 0 NA NA NA NA NA NA NA A 66.5 This 0.00 N D2 302 study 1 0 NA NA NA NA NA NA NA A 74.3 This 0.00 N C10 9726 study 1 0 NA NA NA NA NA NA NA A 74.3 This 0.00 N D45 9726 study 4 0 NA NA NA NA NA NA NA A 74.3 This 0.00 N D29 9726 study 6 0 NA NA NA NA NA NA NA A 74.3 This 0.00 N M3 9726 study 9 0 NA NA NA NA NA NA NA A 74.3 Morphoty Caveat This 0.01 N pe 33.2 Friendship study 1 1 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 17.1 Friendship study 3 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 12.1 Friendship study 5 1 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 7.1 Friendship study 9 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 10.2 Friendship study 11 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 10.3 Friendship study 12 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 24.2 Friendship study 14 5 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 11.1 Friendship study 15 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 19 0.00 NA NA NA NA NA NA NA N 75.6 24 9 pe 10.4 Friendship study 0 A Morphoty Caveat This 0.00 N pe 29.1 Friendship study 20 0 NA NA NA NA NA NA NA A 75.6 Morphoty Caveat This 0.00 N pe 31.1 Friendship study 21 0 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp35.1 Valley study 5 3 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp31.4 Valley study 6 2 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp31.2 Valley study 8 0 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp11.2 Valley study 15 1 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp30.2 Valley study 20 2 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp7.6 Valley study 24 0 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp7.4 Valley study 28 0 NA NA NA NA NA NA NA A 75.6 Lost This 0.00 N sp5.1 Valley study 33 0 NA NA NA NA NA NA NA A 75.6 This 0.00 N sp39.1 JARS study 2 1 NA NA NA NA NA NA NA A 75.7 This 0.00 N sp7.1 JARS study 4 0 NA NA NA NA NA NA NA A 75.7 This 0.00 N sp12.1 JARS study 5 8 NA NA NA NA NA NA NA A 75.7 This 0.00 N sp5.1 JARS study 13 1 NA NA NA NA NA NA NA A 75.7 25 0 Bibliography Adams, J. M., Brusa, A., Soyeong, A., & Ainuddin, A. (2010). Present-day testing of a paleoecological pattern: Is there really a latitudinal difference in leaf-feeding insect-damage diversity? Review of Palaeobotany and Palynology, 162(1), 63?70. Adler, P., & Foottit, R. (2009). Introduction to Insect Biodiversity. In Footit, R. G. & P. H. Adler (Eds.) Insect Biodiversity: Science and Society (pp. 1?6). West Sussex, England: Wiley-Blackwell Publishing. Adroit, B., Girard, V., Kunzmann, L., Terral, J.-F., & Wappler, T. (2018a). Plant? insect interactions patterns in three European paleoforests of the late- Neogene? early-Quaternary. PeerJ, 6, e5075. Adroit, B., Malekhosseini, M., Girard, V., Abedi, M., Rajaei, H., Terral, J.-F., & Wappler, T. (2018b). Changes in pattern of plant?insect interactions on the Persian ironwood (Parrotia persica, Hamamelidaceae) over the last 3 million years. Review of Palaeobotany and Palynology, 258, 22?35. Adroit, B., Wappler, T., Terral, J.-F., Ali, A. A., & Girard, V. (2016). Bernasso, a paleoforest from the early Pleistocene: New input from plant?insect interactions (H?rault, France). Palaeogeography, Palaeoclimatology, Palaeoecology, 446, 78?84. Akai, S. (1950). Studies on the pathological anatomy of fungus galls of plants. Memoirs of the College of Agriculture, Kyoto University, 58, 1?60. Ali, J. G., & Agrawal, A. A. (2012). Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science, 17(5), 293?302. Alroy, J. (2016). Fossilworks: gateway to the paleobiology database. http://fossilworks.org/. Arens, N. C., & Gleason, J. P. (2016). Insect folivory in an angiosperm-dominated flora from the Mid-Cretaceous of Utah, USA. Palaios, 31(3), 71?80. 25 1 Ashton, I. W., Miller, A. E., Bowman, W. D., & Suding, K. N. (2010). Niche complementarity due to plasticity in resource use: Plant partitioning of chemical N forms. Ecology, 91(11), 3252?3260. Bach, C. E. (1981). Host plant growth form and diversity: effects on abundance and feeding preference of a specialist herbivore, Acalymma vittata (Coleoptera: Chrysomelidae). Oecologia, 50(3), 370-375. Bagchi, R., Gallery, R. E., Gripenberg, S., Gurr, S. J., Narayan, L., Addis, C. E., . . . Lewis, O. T. (2014). Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature, 506(7486), 85?88. Bairstow, K. A., Clarke, K. L., McGeoch, M. A., & Andrew, N. R. (2010). Leaf miner and plant galler species richness on Acacia: Relative importance of plant traits and climate. Oecologia, 163(2), 437?448. Bajec, D., Rodi?, K., & Peterlin, A. (2009). Wide range of host plants of pear leaf blister moth (Leucoptera malifoliella [O. Costa]). Zbornik predavanj in referatov 9. Slovenskega Posvetovanja o Varstvu Rastlin, Nova Gorica, Slovenije, 431?434. Bannister, J. M., Conran, J. G., & Lee, D. E. (2012). Lauraceae from rainforest surrounding an early Miocene maar lake, Otago, southern New Zealand. Review of Palaeobotany and Palynology, 178, 13?34. Barale, G., Barbacka, M., & Philippe, M. (2002). Early Cretaceous flora of Hungary and its palaeoecological significance. Acta Palaeobotanica, 42(1), 13?27. Barnosky, A. D., Hadly, E. A., Gonzalez, P., Head, J., Polly, P. D., Lawing, A. M., . . . Zhang, Z. (2017). Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems. Science, 355(6325), 594?604. Barry, K. E., Mommer, L., van Ruijven, J., Wirth, C., Wright, A. J., Bai, Y., . . . Isbell, F. (2019). The future of complementarity: Disentangling causes from consequences. Trends in Ecology & Evolution, 34(2), 167?180. 25 2 Baryshnikova, S. (1999). Review of Leaf Miners (Lepidoptera, Lyonetiidae) of the Fauna of Russia: I. Subfamily Cerniostominae. Entomological Review, 79(2), 191?199. Bascompte, J., & Jordano, P. (2007). Plant?animal mutualistic networks: The architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38, 567?593. Basset, Y., & Novotny, V. (1999). Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biological Journal of the Linnean Society, 67(4), 477?499. Beck, A. L., & Labandeira, C. C. (1998). Early Permian insect folivory on a gigantopterid-dominated riparian flora from north-central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology, 142(3), 139?173. Behrensmeyer, A. K., Kidwell, S. M., & Gastaldo, R. A. (2000). Taphonomy and paleobiology. Paleobiology, 26(4), 103?147. Bennett, R. N., & Wallsgrove, R. M. (1994). Secondary metabolites in plant defence mechanisms. New Phytologist, 127(4), 617?633. Bentley, B. L. (1979). Longevity of individual leaves in a tropical rainforest under- story. Annals of Botany, 43(1), 119?121. Berendse, F., & Scheffer, M. (2009). The angiosperm radiation revisited, an ecological explanation for Darwin?s ?abominable mystery?. Ecology Letters, 12(9), 865?872. Berg, W. (1960). Zur Kenntnis der Obstbaumminiermotte Lyonetia clerkella L. unter besonderer Ber?cksichtigung des Massenwechsels w?hrend der Jahre 1951 bis 1953. Zeitschrift f?r Angewandte Entomologie, 45(3), 268?303. Bergman, B., Matveyev, A., & Rasmussen, U. (1996). Chemical signalling in cyanobacterial?plant symbioses. Trends in Plant Science, 1(6), 191?197. 25 3 Bergman, B., Rai, A., Rasmussen, U., Elmerich, C., & Newton, W. (2007). In Associative and Endophytic Nitrogen-Fixing Bacteria and Cyanobacterial Associations. (Vol. 5, pp. 323). Netherlans: Springer Netherlands. Bernays, E. A. (1998). Evolution of feeding behavior in insect herbivores. Bioscience, 48(1), 35?44. Berry, E. W. (1909). Pleistocene swamp deposits in Virginia. The American Naturalist, 43(511), 432?436. Berry, E. W. (1925). The Flora of the Ripley Formation, USGS Special Papers 136, 1?94. Beveridge, T. L., Roberts, E. M., & Titus, A. L. (2020). Volcaniclastic member of the richly fossiliferous Kaiparowits Formation reveals new insights for regional correlation and tectonics in southern Utah during the latest Campanian. Cretaceous Research, 114, 104527. Blackmer, J., & Hanson, P. (1997). Abundance and life history of two gall-inducing homopterans on Nectandra salicina (Lauraceae) in Monteverde, Costa Rica. Revista de Biolog?a Tropical, 1131?1137. Blake, K. S. (2017). Zane Grey, Wild Horse Mesa, and the Kaiparowits Plateau. Zane Grey Explorer, 2(2), 16-23. Blakey, R. (2011). Colorado Plateau Geosystems. Inc., Western North America Series: http://www.cpgeosystems.com/paleomaps.html. Bodnaryk, R. P. (1992). Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard. Phytochemistry, 31(8), 2671?2677. Bond, G. (1983). Taxonomy and distribution of non-legume nitrogen-fixing systems. In Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications (pp. 55?87). Boston, MA: Springer. 25 4 Bradley, J., & Carter, D. (1982). A new lyonetiid moth, a pest of winged?bean. Systematic Entomology, 7(1), 1?9. Brinkman, D., Aquillon-Martinez, M. C., De Leon D?vila, C., Jamniczky, H., Eberth, D. A., & Colbert, M. (2009). Euclastes coahuilaensis sp. nov., a basal cheloniid turtle from the late Campanian Cerro del Pueblo Formation of Coahuila State, Mexico. PaleoBios, 28(3), 76?88. Brinkman, D. B., Newbrey, M. G., Neuman, A. G., & Eaton, J. G. (2013). Freshwater osteichthyes from the Cenomanian to late Campanian of Grand Staircase? Escalante National Monument, Utah. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase The Late Cretaceous of Southern Utah. Edited by AL Titus and MA Loewen (pp. 195?236). Bloomington, Indiana: Indiana University Press. Bronstein, J. L., Alarcon, R., & Geber, M. (2006). The evolution of plant?insect mutualisms. New Phytologist, 172(3), 412?428. Brooks, H. (1955). Healed wounds and galls on fossil leaves from the Wilcox deposits (Eocene) of western Tennessee. Psyche: A Journal of Entomology, 62(1), 1?9. Brouwer, Y. M., & Clifford, H. T. (1990). An annotated list of domatia-bearing species. Notes from the Jodrell Laboratory (12), 1?33. Brown, R. W. (1962). Paleocene Flora of the Rocky Mountains and Great Plains (pp. 375): US Government Printing Office. Brues, C. T. (1910). The parasitic Hymenoptera of the tertiary of Florissant, Colorado. Bulletin of Museum of Comparative Zoology, Harvard, 54, 1?125. Brues, C. T. (1924). The specificity of food-plants in the evolution of phytophagous insects. The American Naturalist, 58(655), 127?144. Brues, C. T. (1936). Evidences of insect activity preserved in fossil wood. Journal of Paleontology, 637?643. 25 5 Bryan, J. A., Berlyn, G. P., & Gordon, J. C. (1996). Toward a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae. In Current Issues in Symbiotic Nitrogen Fixation (pp. 151?159): Springer. Buatois, L. A., & M?ngano, M. G. (2011). Ichnology: Organism-Substrate Interactions in Space and Time (pp. 370): Cambridge University Press. Burkill, I. H. (1939). Two notes on Dioscoreas in the Congo: (1) The acarodomatia of D. minutflora Engl. and D. smilaciflora De Wild., and (2) Twining in both directions in D. baya De Wild. Proceedings of the Linnean Society of London, 151(2), 57?61. Burns, J. M., Janzen, D. H., Hallwachs, W., & Hajibabaei, M. (2013). DNA barcodes reveal yet another new species of Venada (Lepidoptera: Hesperiidae) in northwestern Costa Rica. Proceedings of the Entomological Society of Washington, 115(1), 37?48. Buss, E. (2006). Leafminers on ornamental plants. The Institute of Food and Agricultural Sciences, University of Florida, 1?4. https://ufdcimages.uflib.ufl.edu/IR/00/00/28/84/00001/MG00600.pdf. Calvillo-Canadell, L., & Cevallos-Ferriz, S. R. (2007). Reproductive structures of Rhamnaceae from the Cerro del Pueblo (Late Cretaceous, Coahuila) and Coatzingo (Oligocene, Puebla) Formations, Mexico. American Journal of Botany, 94(10), 1658?1669. Cardinale, B. J., Matulich, K. L., Hooper, D. U., Byrnes, J. E., Duffy, E., Gamfeldt, L., . . . Gonzalez, A. (2011). The functional role of producer diversity in ecosystems. American Journal of Botany, 98(3), 572?592. Carpenter, F. M., Folsom, J., Essig, E., Kinsey, A., Brues, C., Boesel, M., & Ewing, H. (1937). In Insects and Arachnids from Canadian Amber (Vol. 40, pp. 1061?1082). Toronto, Canada: University of Toronto. Carr, T. D., Williamson, T. E., Britt, B. B., & Stadtman, K. (2011). Evidence for high taxonomic and morphologic tyrannosauroid diversity in the Late Cretaceous (Late Campanian) of the American Southwest and a new short-skulled 25 6 tyrannosaurid from the Kaiparowits Formation of Utah. Naturwissenschaften, 98(3), 241?246. Carter, M., & Feeny, P. (1999). Host-plant chemistry influences oviposition choice of the spicebush swallowtail butterfly. Journal of Chemical Ecology, 25(9), 1999?2009. Carvalho, M. R., Wilf, P., Barrios, H., Windsor, D. M., Currano, E. D., Labandeira, C. C., & Jaramillo, C. A. (2014). Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests. PLoS ONE, 9(5), e94950. Cenci, R., & Adami-Rodrigues, K. (2017). Record of gall abundance as a possible episode of radiation and speciation of galling insects, Triassic, southern Brazil. Revista Brasileira de Paleontologia, 20(3), 279?286. Cevallos-Ferriz, S. R., Estrada-Ruiz, E., & P?rez-Hern?ndez, B. R. (2008). Phytolaccaceae infructescence from Cerro del Pueblo Formation, Upper Cretaceous (late Campanian), Coahuila, Mexico. American Journal of Botany, 95(1), 77?83. Chamberlain, S., Szoecs, E., Foster, Z., Boettiger, C., Ram, K., Bartomeus, I., ... & Oksanen, J. (2017). Package ?taxize?. Taxonomic Information from Around the Web. Chanderbali, A. S., van der Werff, H., & Renner, S. S. (2001). Phylogeny and historical biogeography of Lauraceae: Evidence from the chloroplast and nuclear genomes. Annals of the Missouri Botanical Garden, 88(1), 104?134. Chaney, R. W. (1920). The flora of the Eagle Creek Formation. Contributions of the Walker Museum, 2(2), 115?181. Chomicki, G., & Renner, S. S. (2015). Phylogenetics and molecular clocks reveal the repeated evolution of ant?plants after the late Miocene in Africa and the early Miocene in Australasia and the Neotropics. New Phytologist, 207(2), 411? 424. 25 7 Christenhusz, M. J., & Byng, J. W. (2016). The number of known plants species in the world and its annual increase. Phytotaxa, 261(3), 201?217. Cifelli, R. L. (1990a). Cretaceous mammals of southern Utah. I. Marsupials from the Kaiparowits Formation (Judithian). Journal of Vertebrate Paleontology, 10(3), 295?319. Cifelli, R. L. (1990b). Cretaceous mammals of southern Utah. IV. Eutherian mammals from the Wahweap (Aquilan) and Kaiparowits (Judithian) Formations. Journal of Vertebrate Paleontology, 10(3), 346?360. Cifuentes-Ruiz, P., Vrsansky, P., Vega, F. J., Cevallos-Ferriz, S. R., Gonzalez- Soriano, E., & de Jes?s, C. D. (2006). Campanian terrestrial arthropods from the Cerro del Pueblo Formation, Difunta Group in northeastern Mexico. Geologica Carpathica-Bratislava, 57(5), 347?354. Cockerell, T. (1910). A Fossil Fig. Torreya, 10(10), 222?224. Cohen, K. M., Finney, S. C., Gibbard, P. L., & Fan, J.-X. (2013). The ICS International Chronostratigraphic Chart. Episodes, 36(3), 199?204. Coiffard, C., Gomez, B., Daviero-Gomez, V., & Dilcher, D. L. (2012). Rise to dominance of angiosperm pioneers in European Cretaceous environments. Proceedings of the National Acadademy of Sciences, 109(51), 20955?20959. Coley, P. (1988). Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia, 74(4), 531?536. Coley, P. D., & Barone, J. (1996). Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27(1), 305?335. Coley, P. D., Bryant, J. P., & Chapin, F. S. (1985). Resource availability and plant antiherbivore defense. Science, 230(4728), 895?899. 25 8 Conran, J. G., Lee, D. E., & Reichgelt, T. (2016). Malloranga dentata (Euphorbiaceae: Acalyphoideae): A new fossil species from the Miocene of New Zealand. Review of Palaeobotany and Palynology, 226, 58?64. Cornell, H. V., & Hawkins, B. A. (2003). Herbivore responses to plant secondary compounds: A test of phytochemical coevolution theory. The American Naturalist, 161(4), 507?522. Crabtree, D. R. (1987). Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Annals of the Missouri Botanical Garden, 707?747. Crabtree, D. R. (1989). The early Campanian flora of the Two Medicine Formation, northcentral Montana. Dissertation, University of Montana. Crane, P. R. (1987). Vegetational consequences of the angiosperm diversification. (pp. 358): Cambridge University Press, Cambridge, UK. Crane, P., & Jarzembowski, E. (1980). Insect leaf mines from the Palaeocene of southern England. Journal of Natural History, 14(5), 629?636. Crane, P. R., Friis, E. M., & Pedersen, K. R. (1995). The origin and early diversification of angiosperms. Nature, 374(6517), 27?33. Cruaud, A., R?nsted, N., Chantarasuwan, B., Chou, L. S., Clement, W. L., Couloux, A., . . . Hanson, P. E. (2012). An extreme case of plant?insect codiversification: Figs and fig-pollinating wasps. Systematic Biology, 61(6), 1029?1047. Crystal, V. F., Evans, E. S., Fricke, H., Miller, I. M., & Sertich, J. J. (2019). Late Cretaceous fluvial hydrology and dinosaur behavior in southern Utah, USA: Insights from stable isotopes of biogenic carbonate. Palaeogeography, Palaeoclimatology, Palaeoecology, 516, 152?165. Cs?ka, G. (2003). Leaf mines and leaf miners. Agroinform Kiad?, Budapest. 25 9 Currano, E. D. (2009). Patchiness and long-term change in early Eocene insect feeding damage. Paleobiology, 35(4), 484?498. Currano, E. D., Jacobs, B. F., Pan, A. D., & Tabor, N. J. (2011). Inferring ecological disturbance in the fossil record: A case study from the late Oligocene of Ethiopia. Palaeogeography, Palaeoclimatology, Palaeoecology, 309(3?4), 242?252. Currano, E. D., Labandeira, C. C., & Wilf, P. (2010). Fossil insect folivory tracks paleotemperature for six million years. Ecological Monographs, 80(4), 547? 567. Currano, E. D., Laker, R., Flynn, A. G., Fogt, K. K., Stradtman, H., & Wing, S. L. (2016). Consequences of elevated temperature and pCO 2 on insect folivory at the ecosystem level: perspectives from the fossil record. Ecology and Evolution, 6(13), 4318?4331. Currano, E. D., Pinheiro, E. R., Buchwaldt, R., Clyde, W. C., & Miller, I. M. (2019). Endemism in Wyoming plant and insect herbivore communities during the early Eocene hothouse. Paleobiology, 1?19. Currano, E. D., Wilf, P., Wing, S. L., Labandeira, C. C., Lovelock, E. C., & Royer, D. L. (2008). Sharply increased insect herbivory during the Paleocene?Eocene Thermal Maximum. Proceedings of the National Academy of Sciences, 105(6), 1960?1964. Cyr, H., & Pace, M. L. (1993). Allometric theory: Extrapolations from individuals to communities. Ecology, 74(4), 1234?1245. Darwin, C., & Seward, A. C. (1903). More Letters of Charles Darwin (Vol. 2): Murray London. Davies-Vollum, K. S., Boucher, L. D., Hudson, P., & Proskurowski, A. Y. (2011). A Late Cretaceous coniferous woodland from the San Juan Basin, New Mexico. Palaios, 26(2), 89?98. 26 0 Davis, D. R. (1994). New leaf-mining moths from Chile, with remarks on the history and composition of Phyllocnistinae (Lepidoptera: Gracillariidae). Neotropical Lepidoptera, 5(1), 65?75. de Boer, H. J., Eppinga, M. B., Wassen, M. J., & Dekker, S. C. (2012). A critical transition in leaf evolution facilitated the Cretaceous Angiosperm Revolution. Nature Communications, 3, 1221. Decourten, F. L., & Russell, D. A. (1985). A specimen of Ornithomimus velox (Theropoda, Ornithomimidae) from the terminal Cretaceous Kaiparowits Formation of southern Utah. Journal of Paleontology, 59(5), 1091?1099. Delwiche, C. F., & Cooper, E. D. (2015). The evolutionary origin of a terrestrial flora. Current Biology, 25(19), R899?R910. Denver Museum of Nature Science (DMNS): Guide to morphotyping fossil floras. http://www.paleobotanyproject.org/morphotyping.aspx. Dietl, G. P., & Flessa, K. W. (2011). Conservation paleobiology: Putting the dead to work. Trends in Ecology and Evolution, 26(1), 30?37. Dietl, G. P., Kidwell, S. M., Brenner, M., Burney, D. A., Flessa, K. W., Jackson, S. T., & Koch, P. L. (2015). Conservation paleobiology: Leveraging knowledge of the past to inform conservation and restoration. Annual Review of Earth and Planetary Sciences, 43. Dilcher, D. L. (2001). Paleobotany: Some aspects of non-flowering and flowering plant evolution. Taxon, 697?711. DiMichele, W. A., & Gastaldo, R. A. (2008). Plant paleoecology in Deep Time. Annals of the Missouri Botanical Garden, 95(1), 144?198. Ding, Q.-H., Zhang, L.-D., Guo, S.-Z., Zhangg, C., Peng, Y.-D., Jia, B., . . . Xing, D.- H. (2003). Study on the paleoecology of Yixian Formation in Beipiao area, western Liaoning Province, China. Journal of Precious Metallic Geology, 12(1), 9?18. 26 1 Dom?nguez, RM (2018). First plant-insect interactions from the Oligocene of the Iberian Peninsula. Journal of the Geological Society of Spain , 31 (1), 19-28. Donovan, M. P., Iglesias, A., Wilf, P., Labandeira, C. C., & C?neo, N. R. (2016). Rapid recovery of Patagonian plant?insect associations after the end- Cretaceous extinction. Nature Ecology & Evolution, 1(1), 1?5. Donovan, M. P., Iglesias, A., Wilf, P., Labandeira, C. C., & C?neo, N. R. (2018). Diverse plant?insect associations from the latest Cretaceous and early Paleocene of Patagonia, Argentina. Ameghiniana, 55(3), 303?338. Donovan, M. P., Wilf, P., Labandeira, C. C., Johnson, K. R., & Peppe, D. J. (2014). Novel insect leaf-mining after the end?Cretaceous extinction and the demise of Cretaceous leaf miners, Great Plains, USA. PLoS ONE, 9(7), e103542. Doorenweerd, C., Van Nieukerken, E. J., Sohn, J.-C., & Labandeira, C. C. (2015). A revised checklist of Nepticulidae fossils (Lepidoptera) indicates an Early Cretaceous origin. Zootaxa, 3963(3), 295?334. Doyle, J. A., Scott, L., Cadman, A., & Verhoeven, R. (1999). The rise of angiosperms as seen in the African Cretaceous pollen record. Palaeoecology of Africa and the surrounding islands, 26, 3?29. Dugdale, J. S., Kristensen, N. P., Robinson, G. S., & Scoble, M. J. (1998). The Yponomeutoidea. Lepidoptera, Moths and Butterflies, 1, 119?130. Duggar, B. M., & Davis, A. R. (1916). Studies in the physiology of the fungi. I. Nitrogen fixation. Annals of the Missouri Botanical Garden, 3(4), 413?437. Dunlop, J. A. (2010). Geological history and phylogeny of Chelicerata. Arthropod Structure & Development, 39(2?3), 124?142. Dunne, J. A., Labandeira, C. C., & Williams, R. J. (2014). Highly resolved early Eocene food webs show development of modern trophic structure after the end-Cretaceous extinction. Proceedings of the Royal Society B: Biological Sciences, 281(1782), 20133280. 26 2 Dyer, L. A. (1995). Tasty generalists and nasty specialists? Antipredator mechanisms in tropical lepidopteran larvae. Ecology, 76(5), 1483?1496. Eastop, V. (1972). Deductions from the present day host plants of aphids and related insects. Paper presented at the Royal Entomological Society of London Symposium, 157?178. Eastop, V. (1978). Evolution of aphid/plant relationships. In Insect/Plant Relationships (pp. 157?178): Oxford, Blackwell. Eaton, J. G., & Cifelli, R. L. (1988). Preliminary report on Late Cretaceous mammals of the Kaiparowits Plateau, southern Utah. University of Wyoming, Contributions to Geology 26(2), 45?55. Eaton, J. G., Cifelli, R. L., Hutchison, J. H., Kirkland, J. I., & Parrish, J. M. (1999). Cretaceous vertebrate faunas from the Kaiparowits Plateau, south-central Utah. Vertebrate Paleontology in Utah, Utah Geological Survey, 99(1), 345. Eberth, D. A., Delgado, C. R., Lerbekmo, J. F., Brinkman, D. B., Rodr?guez, R. A., & Sampson, S. D. (2004). Cerro del Pueblo Fm (Difunta Group, Upper Cretaceous), Parras Basin, southern Coahuila, Mexico: Reference sections, age, and correlation. Revista Mexicana de Ciencias Geol?gicas, 21(3), 335? 352. Ehrlich, P. R., & Raven, P. H. (1964). Butterflies and plants: A study in coevolution. Evolution, 18(4), 586?608. Eilperin, J. (2017). Trump to Cut Bears Ears National Monument by 85?Percent, Grand Staircase-Escalante by Half, Documents Show. The Washington Post. Eklund, H., & Kva?ek, J. (1998). Lauraceous inflorescences and flowers from the Cenomanian of Bohemia (Czech Republic, central Europe). International Journal of Plant Sciences, 159(4), 668?686. Ellis, B., Daly, D. C., Hickey, L. J., Johnson, K. R., Mitchell, J. D., Wilf, P., & Wing, S. L. (2009). Manual of Leaf Architecture (pp. 190): Cornell University Press, Ithaca, NY. 26 3 Ellis, W. (2018). Plant parasites of Europe: Leaf miners, gallers, and fungi. https://bladmineerders.nl/ English?Loeb, G., & Norton, A. (2006). Lack of trade?off between direct and indirect defence against grape powdery mildew in riverbank grape. Ecological Entomology, 31(5), 415?422. Eriksson, O., Friis, E. M., & L?fgren, P. (2000). Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. The American Naturalist, 156(1), 47?58. Est?vez-Gallardo, P., Sender, L. M., Mayoral, E., & Diez, J. B. (2019). First evidence of insect herbivory on Albian aquatic angiosperms of the NE Iberian Peninsula. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 108(4), 429?435. Estrada?Ruiz, E., & Cevallos?Ferriz, S. R. S. (2007). Infructescences from the Cerro del Pueblo Formation (Late Campanian), Coahuila, and El Cien Formation (Oligocene?Miocene), Baja California Sur, Mexico. International Journal of Plant Sciences, 168(4), 507?519. Fagua, G., Condamine, F. L., Horak, M., Zwick, A., & Sperling, F. A. (2017). Diversification shifts in leafroller moths linked to continental colonization and the rise of angiosperms. Cladistics, 33(5), 449?466. Farke, A. A., Henn, M. M., Woodward, S. J., & Xu, H. A. (2014). Leidyosuchus (Crocodylia: Alligatoroidea) from the Upper Cretaceous Kaiparowits Formation (late Campanian) of Utah, USA. PaleoBios, 30(3), 72?88. Farke, A. A., & Patel, P. P. (2012). An enantiornithine bird from the Campanian Kaiparowits Formation of Utah, USA. Cretaceous Research, 37, 227?230. Farke, A. A., & Wilridge, C. A. (2013). A possible pterosaur wing phalanx from the Kaiparowits Formation (late Campanian) of Southern Utah, USA. PalArch's Journal of Vertebrate Palaeontology, 10(2), 1?6. Farmer, E. E. (2014). Leaf Defence. (pp. 224): Oxford University Press, Oxford, UK. 26 4 Farrell, B. D. (1998). "Inordinate fondness" explained: Why are there so many beetles? Science, 281(5376), 555?559. Fassett, J. E., & Steiner, M. B. (1997). Precise age of C33N-C32R magnetic-polarity reversal, San Juan Basin, New Mexico and Colorado. New Mexico Geological Society Guidebook, 48, 239?247. Feeny, P. (1976). Plant Apparency and Chemical Defense. In J. W. Wallace & R. L. Mansell (Eds.), Biochemical Interaction Between Plants and Insects (pp. 1? 40): Springer US, Boston, MA. Feild, T. S., Brodribb, T. J., Iglesias, A., Chatelet, D. S., Baresch, A., Upchurch, G. R., . . . Kvacek, J. (2011). Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, 108(20), 8363?8366. Fern?ndez, J. A., & Chiesa, J. O. (2020). Plant?insect interactions in the fossil flora of the Bajo de Veliz Formation (Gzhelian-Asselian): San Luis, Argentina. Ichnos, 27(2), 156?166. Feng, Z., Wang, J., R??ler, R., ?lipi?ski, A., & Labandeira, C. (2017). Late Permian wood-borings reveal an intricate network of ecological relationships. Nature communications, 8(1), 1?6. Filho, E. B. d. S., Adami-Rodrigues, K., Lima, F. J. d., Bantim, R. A. M., Wappler, T., & Saraiva, A. ?. F. (2019). Evidence of plant?insect interaction in the Early Cretaceous Flora from the Crato Formation, Araripe Basin, Northeast Brazil. Historical Biology, 31(7), 926?937. Fiorillo, A. R. (2008). Dinosaurs of Alaska: implications for the Cretaceous origin of Beringia. Geological Society of America Special Papers, 442, 313?326. Fletcher, T. B. (1920). Life-histories of Indian Insects: Microlepidoptera. Memoirs of the Department of Agriculture, India, 6, 1?217. 26 5 Fletcher, T. B. (1933). Life-histories of Indian Microlepidoptera (Second Series) Cosmopterygidae to Neopseustidae (pp. 85): The Imperial Council of Agricultual Research, Delhi, India. Foldi, I., & Watson, G. W. (2001). A new pest scale insect on avocado trees in Colombia, Laurencella colombiana, sp. n.(Hemiptera: Coccoidea: Margarodidae). Paper presented at the Annales de la Soci?t? entomologique de France. Foottit, R. G., & Adler, P. H. (2009). Insect Biodiversity (pp. 904): Wiley Online Library. Forister, M. L., Novotny, V., Panorska, A. K., Baje, L., Basset, Y., Butterill, P. T., . . . Diniz, I. R. (2015). The global distribution of diet breadth in insect herbivores. Proceedings of the National Academy of Sciences, 112(2), 442?447. Frankfater, C. R., & Scriber, J. M. (1999). Florida red bay (Persea borbonia) leaf extracts deter oviposition of a sympatric generalist herbivore, Papilio glaucus (Lepidoptera: Papilionidae). Chemoecology, 9(3), 127?132. Friis, E.M., Chaloner, W.G., & Crane, P.R. (Eds.) Origins of Angiosperms and Their Biological Consequences (pp. 107?144): Cambridge University Press, Cambridge, UK. Friis, E. M., Crane, P. R., & Pedersen, K. R. (2011). pp. 350, Early Flowers and Angiosperm Evolution. New York: Cambridge University Press. Futuyma, D. J., & Mitter, C. (1996). Insect?plant interactions: The evolution of component communities. Philosophical Transactions of the Royal Society B: Biological Sciences, 351(1345), 1361?1366. Gale, A. S. (2000). The Cretaceous World. In S. J. Culver & P. F. Rawson (Eds.), Biotic Response to Global Change: The Last 145 Million Years (Vol. 145, pp. 4?19): Cambridge University Press. 26 6 Gangwere, S. (2017). Relationships between the mandibles, feeding behavior, and damage inflicted on plants by the feeding of certain acridids (Orthoptera). The Great Lakes Entomologist, 1(1), 13?16. Garc?a, L. V. (2004). Escaping the Bonferroni iron claw in ecological studies. Oikos, 105(3), 657?663. Garc?a-Robledo, C., & Staines, C. L. (2008). Herbivory in gingers from latest Cretaceous to present: is the ichnogenus Cephaloleichnites (Hispinae, Coleoptera) a rolled-leaf beetle? Journal of Paleontology, 82(5), 1035?1037. Gardner, J. D., & DeMar, D. G. (2013). Mesozoic and Palaeocene lissamphibian assemblages of North America: A comprehensive review. Palaeobiodiversity and Palaeoenvironments, 93(4), 459?515. Gaston, K. J. (1991). The magnitude of global insect species richness. Conservation Biology, 5(3), 283?296. Gates, T. A., Prieto-M?rquez, A., & Zanno, L. E. (2012). Mountain building triggered Late Cretaceous North American megaherbivore dinosaur radiation. PLoS ONE, 7(8). Gates, T. A., & Sampson, S. D. (2007). A new species of Gryposaurus (Dinosauria: Hadrosauridae) from the late Campanian Kaiparowits Formation, southern Utah, USA. Zoological Journal of the Linnean Society, 151(2), 351?376. Gates, T. A., Sampson, S. D., Delgado de Jesus, C. R., Zanno, L. E., Eberth, D., Hernandez-Rivera, R., . . . Kirkland, J. I. (2007). Velafrons coahuilensis, a new lambeosaurine hadrosaurid (Dinosauria: Ornithopoda) from the late Campanian Cerro del Pueblo Formation, Coahuila, Mexico. Journal of Vertebrate Paleontology, 27(4), 917?930. Gnaedinger, S. C., Adami-Rodrigues, K., & Gallego, O. F. (2014). Endophytic oviposition on leaves from the Late Triassic of northern Chile: Ichnotaxonomic, palaeobiogeographic and palaeoenvironment considerations. Geobios, 47(4), 221?236. 26 7 G?is-Marques, C. A., Madeira, J., & Menezes de Sequeira, M. (2018). Inventory and review of the Mio?Pleistocene S?o Jorge flora (Madeira Island, Portugal): Palaeoecological and biogeographical implications. Journal of Systematic Palaeontology, 16(2), 159?177. Golovneva, L., Sun, G., & Bugdaeva, E. (2008). Campanian flora of the Bureya River basin (Late Cretaceous of the Amur region). Paleontological Journal, 42(5), 554?567. Golovneva, L. B. (2000). Aquatic plant communities at the Cretaceous-Palaeogene boundary in north-eastern Russia. Acta Palaeobotanica, 40(2), 139?151. Gonz?lez-Coloma, A., Escoubas, P., Lljide, L., & Mizutan, J. (1994a). Insecticidal activity screening of Japanese Lauraceae. Applied Entomology and Zoology, 29(2), 289?292. Gonz?lez-Coloma, A., Escoubas, P., Reina, M., & Mizutani, J. (1994b). Antifeedant and insecticidal activity of endemic Canarian Lauraceae. Applied Entomology and Zoology, 29(2), 292?296. Goralka, R. J., & Langenheim, J. H. (1996). Implications of foliar monoterpenoid variation among ontogenetic stages of the California bay tree (Umbellularia californica) for deer herbivory. Biochemical Systematics and Ecology, 24(1), 13?23. Gray, J., Massa, D., & Boucot, A. (1982). Caradocian land plant microfossils from Libya. Geology, 10(4), 197?201. Gray, J., & Shear, W. (1992). Early life on land. American Scientist, 80, 444?456. Green, E. E. (1917). A list of Coccidae affecting various genera of plants. Annals of Applied Biology, 4(1?2), 75?89. Grimaldi, D. (1999). The co-radiations of pollinating insects and angiosperms in the Cretaceous. Annals of the Missouri Botanical Garden, 373?406. 26 8 Grimaldi, D., & Agosti, D. (2000). A formicine in New Jersey Cretaceous amber (Hymenoptera: Formicidae) and early evolution of the ants. Proceedings of the National Academy of Sciences, 97(25), 13678?13683. Grimaldi, D., & Engel, M. S. (2005). Evolution of the Insects. (pp. 755): Cambridge University Press, New York. Grimaldi, D. A., Nascimbene, P. C., & Penney, D. (2010). Raritan (New Jersey) Amber. In D. Penney (Ed.), Biodiversity of Fossils in Amber from the Major World Deposits (pp. 167?191). Manchester, UK: Siri Scientific Press. Grubb, P. (1986). Sclerophylls, pachyphylls, and pycnophylls: The nature and significance of hard leaf surface. Insects and the Plant Surface, 137?150. Gunkel, S., & Wappler, T. (2015). Plant?insect interactions in the upper Oligocene of Enspel (Westerwald, Germany), including an extended mathematical framework for rarefaction. Palaeobiodiversity and Palaeoenvironments, 95(1), 55?75. Hancock, J., & Kauffman, E. (1979). The great transgressions of the Late Cretaceous. Journal of the Geological Society, 136(2), 175?186. Hanson, C. B. (1996). Stratigraphy and Vertebrate Faunas of the Bridgerian? Duchesnean Clarno Formation, North-Central Oregon. In D. R. Prothero & R. J. Emry (Eds.), The Terrestrial Eocene-Oligocene Transition in North America (pp. 206?239). New York: Cambridge University Press. Hartman, J. H., Johnson, K. R., & Nichols, D. J. (2002). The Hell Creek Formation and the Cretaceous-Tertiary Boundary in the Northern Great Plains: An Integrated Continental Record of the End of the Cretaceous (Vol. 361): Geological Society of America. Heil, M., Gonz?lez-Teuber, M., Clement, L. W., Kautz, S., Verhaagh, M., & Bueno, J. C. S. (2009). Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proceedings of the National Academy of Sciences, 106(43), 18091?18096. 26 9 Heimhofer, U., Hochuli, P., Burla, S., Dinis, J., & Weissert, H. (2005). Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology, 33(2), 141?144. Hellmund, M., & Hellmund, W. (1996). Zum Fortpflanzungsmodus fossiler Kleinlibellen (Insecta, Odonata, Zygoptera). Pal?ontologische Zeitschrift, 70(1), 153?170. Herendeen, P. S., Crepet, W. L., & Nixon, K. C. (1994). Fossil flowers and pollen of Lauraceae from the Upper Cretaceous of New Jersey. Plant Systematics and Evolution, 189(1?2), 29?40. Herendeen, P. S., Friis, E. M., Pedersen, K. R., & Crane, P. R. (2017). Palaeobotanical redux: Revisiting the age of the angiosperms. Nature Plants, 3(3), 1?8. Hering, E. (1951). Biology of Leaf Miners.?s-Gravenhage (pp. 420): Springer Netherlands. Hering, E. (1957). Bestimmungstabellen der Blattminen von Europa, band I. (pp. 306?309) In W. Junk, s? Gravenage. Springer Netherlands. Hering, E. M. (2013). Biology of the leaf miners: Springer Science & Business Media. Herman, A., & Kva?ek, J. (2007). Early Campanian Gr?nbach flora of Austria. Paleontological Journal, 41(11), 1068?1076. Hernandez, F. G. L. (1997). On Cinnamomum (Lauraceae) in Mexico. Acta Bot?nica Mexicana(40), 1?18. Heron, H. (2003). Tortoise beetles (Chrysomelidae: Cassidinae) and their feeding patterns from the North Park Nature Reserve, Durban, KwaZulu-Natal, South Africa. Durban Museum Novitates, 28(1), 31?44. Hickey, L. (1971). Evolutionary significance of leaf architectural features in the woody dicots. American Journal of Botany, 58, 469. 27 0 Hickey, L., Klise, L., & Green, W. (2006). The Yale?Princeton Compendium Index of North American Mesozoic and Cenozoic Type Fossil Plants [electronic database]. Release 1.0.[2006 Jan 11]. New Haven, CT: Peabody Museum of Natural History, Yale University. In: Peabody Museum of Natural History, Yale University New Haven. Hickey, L. J. (2001). On the nomenclatural status of the morphogenera, Quereuxia and Trapago. Taxon, 50(4), 1119?1124. Hickey, L. J., & Doyle, J. A. (1977). Early Cretaceous fossil evidence for angiosperm evolution. The Botanical Review, 43(1), 3?104. Hickey, L. J., & Hodges, R. W. (1975). Lepidopteran leaf mine from the early Eocene Wind River Formation of northwestern Wyoming. Science, 189(4204), 718? 720. Hill, M. O. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology, 54(2), 427-432. Hillaire-Marcel, C., McKellar, R. C., Wolfe, A. P., Tappert, R., & Muehlenbachs, K. (2008). Correlation of Grassy Lake and Cedar Lake ambers using infrared spectroscopy, stable isotopes, and palaeoentomology. Canadian Journal of Earth Sciences, 45(9), 1061?1082. Hirst, S. (1923). XLVI.?On some Arachnid remains from the Old Red Sandstone (Rhynie Chert Bed, Aberdeenshire). Annuals and Magazine of Natural History, 12(70), 455?474. Hoffman, A. D. (1932). Miocene insect gall impressions. Botanical Gazette, 93(3), 341?342. Holl, K. D., & Lulow, M. E. (1997). Effects of species, habitat, and distance from edge on post?dispersal seed predation in a tropical rainforest. Biotropica, 29(4), 459?468. Hughes, M. A., Smith, J., Ploetz, R., Kendra, P., Mayfield, A., Hanula, J., . . . Riggins, J. (2015). Recovery plan for laurel wilt on redbay and other forest 27 1 species caused by Raffaelea lauricola and disseminated by Xyleborus glabratus. Plant Health Progress, 16(4), 173?210. Hughes, N. F., & McDougall, A. B. (1994). Search for antecedents of Early Cretaceous monosulcate columellate pollen. Review of Palaeobotany and Palynology, 83(1?3), 175?183. Hunt, A. P. (1991). Integrated vertebrate, invertebrate and plant taphonomy of the Fossil Forest area (Fruitland and Kirtland Formations: Late Cretaceous, San Juan County, New Mexico, USA. Palaeogeography, Palaeoclimatology, Palaeoecology, 88(1?2), 85?107. Hunt, A. P., & Lucas, S. G. (1992). Stratigraphy, paleontology and age of the Fruitland and Kirtland formations (Upper Cretaceous), San Juan Basin, New Mexico. New Mexico Geological Society Guidebook, 43, 217?239. Huston, M. A. (1997). Hidden treatments in ecological experiments: Re-evaluating the ecosystem function of biodiversity. Oecologia, 110(4), 449?460. Hutchinson, P. J., & Kues, B. S. (1985). Depositional environments and paleontology of Lewis Shale to lower Kirtland shale sequence (Upper Cretaceous), Bisti area, northwestern New Mexico. New Mexico Bureau of Mines and Mineral Resources Circular, 195, 25?54. Hutton, Y. Y. (1997). Laurel scale, Aonidia lauri (Bouch?) (Homoptera: Coccoidea, Diaspididae), a pest of bay laurel, new to Britain. Entomologist's Gazette, 48, 195?198. Iannuzzi, R., & Labandeira, C. (2008). The oldest record of external foliage feeding and the expansion of insect folivory on land. Annals of the Entomological Society of America, 101(1), 79?94. Ingersoll, C. M., Niesenbaum, R. A., Weigle, C. E., & Lehman, J. H. (2010). Total phenolics and individual phenolic acids vary with light environment in Lindera benzoin. Botany, 88(11), 1007?1010. 27 2 Irmis, R. B., Hutchinson, H., Sertich, J. J. W., & Titus, A. L. (2013). Crocodyliforms from the Late Cretaceous of Grand Staircase?Escalante Notional Monument and vicinity, southern Utah, U.S.A. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah (pp. 424?444). Bloomington, Indiana: Indiana University Press. Jacobs, M. (1966). On domatia-the viewpoints and some facts. Paper presented at the Proceedings van de Koninklijke Nederlandse Akademie van Wetenschappen Section C. Janz, N. (2011). Ehrlich and Raven revisited: Mechanisms underlying codiversification of plants and enemies. Annual Review of Ecology, Evolution, and Systematics, 42, 71?89. Janzen, D. H., & Martin, P. S. (1982). Neotropical anachronisms: The fruits the gomphotheres ate. Science, 215(4528), 19?27. Jarzembowski, E. (1995). Early Cretaceous insect faunas and palaeoenvironment. Cretaceous Research, 16(6), 681?693. Jarzembowski, E., & Ross, A. (1996). Insect origination and extinction in the Phanerozoic. Geological Society, London, Special Publications, 102(1), 65? 78. Jia, S., Wang, X., Yuan, Z., Lin, F., Ye, J., Hao, Z., & Luskin, M. S. (2018). Global signal of top-down control of terrestrial plant communities by herbivores. Proceedings of the National Academy of Sciences, 115(24), 6237?6242. Johnson, K. R. (1996). Description of seven common fossil leaf species from the Hell Creek Formation (Upper Cretaceous: Upper Maastrichtian), North Dakota, South Dakota, and Montana. Proceedings of the Denver Museum of Natural History, 3(12), 1?47. Johnson, K. R. (2002). Megaflora of the Hell Creek and lower Fort Union Formations in the western Dakotas: Vegetational response to climate change, the Cretaceous?Tertiary boundary event, and rapid marine transgression. In J. H. Hartman, K. R. Johnson, & D. J. Nichols (Eds.), The Hell Creek Formation and the Cretaceous-Tertiary Boundary in the Northern Great Plains: An 27 3 Integrated Continental Record of the End of the Cretaceous (Vol. 361, pp. 329?391): Geological Society of America Special Paper. Johnson, K. R., & Ellis, B. (2002). A tropical rainforest in Colorado 1.4 million years after the Cretaceous?Tertiary boundary. Science, 296(5577), 2379?2383. Johnson, K. R., Nichols, D. J., Attrep, M., & Orth, C. J. (1989). High-resolution leaf- fossil record spanning the Cretaceous/Tertiary boundary. Nature, 340(6236), 708?711. Johnson, W. T., & Lyon, H. H. (1991). Insects that Feed on Trees and Shrubs (pp. 560): Comstock Publishing Associates, Ithaca. NY. Jorge, L. R., Novotny, V., Segar, S. T., Weiblen, G. D., Miller, S. E., Basset, Y., & Lewinsohn, T. M. (2017). Phylogenetic trophic specialization: A robust comparison of herbivorous guilds. Oecologia, 185(4), 551?559. Jost, L. (2006). Entropy and diversity. Oikos, 113(2), 363-375. Jud, N. A., Michael, D., Williams, S. A., Mathews, J. C., Tremaine, K. M., & Bhattacharya, J. (2018). A new fossil assemblage shows that large angiosperm trees grew in North America by the Turonian (Late Cretaceous). Science Advances, 4(9), eaar8568. Jud, N. A., & Sohn, J.-C. (2016). Evidence for an ancient association between leaf mining flies and herbaceous eudicot angiosperms. Cretaceous Research, 63, 113?121. Juli?o, G. R., Almada, E. D., & Fernandes, G. W. (2014). Galling Insects in the Pantanal Wetland and Amazonian Rainforest. In Neotropical Insect Galls (pp. 377?403): Springer. Karban, R., & Baldwin, I. T. (2007). Induced Responses to Herbivory: (pp. 330) University of Chicago Press. 27 4 Karban, R., English-Loeb, G., Walker, M. A., & Thaler, J. (1995). Abundance of phytoseiid mites on Vitis species: Effects of leaf hairs, domatia, prey abundance and plant phylogeny. Experimental & Applied Acarology, 19(4), 189?197. Kaulfuss, U. (2012). Fossil microorganisms, plants and animals from the Early Miocene Foulden Maar, Otago, New Zealand. Paper presented at the Geoscience Society of New Zealand Miscellaneous Publication 131A: Abstract Volume of the Fourth International Maar Conference A Multidisciplinary Congress on Monogenetic Volcanism, Auckland, New Zealand. Kaulfuss, U., Lee, D. E., Barratt, B. I., Leschen, R. A., Larivi?re, M. C., Dlussky, G. M., . . . Harris, A. C. (2015). A diverse fossil terrestrial arthropod fauna from New Zealand: Evidence from the early Miocene Foulden Maar fossil lagerst?tte. Lethaia, 48(3), 299?308. Kawahara, A. Y., & Breinholt, J. W. (2014). Phylogenomics provides strong evidence for relationships of butterflies and moths. Proceedings of the Royal Society B: Biological Sciences, 281(1788), 20140970. Kawahara, A. Y., Ohshima, I., Kawakita, A., Regier, J. C., Mitter, C., Cummings, M. P., . . . Lopez-Vaamonde, C. (2011). Increased gene sampling strengthens support for higher-level groups within leaf-mining moths and relatives (Lepidoptera: Gracillariidae). BMC Evolutionary Biology, 11(1), 182. Kawahara, A. Y., Plotkin, D., Espeland, M., Meusemann, K., Toussaint, E. F., Donath, A., . . . dos Reis, M. (2019). Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proceedings of the National Academy of Sciences, 116(45), 22657?22663. Kazakova, I. (1985). The character of damage to plants by Orthoptera (Insecta) linked to the structure of their mouthparts (on the example of Novosibirsk Akademgorodok fauna). Anthropogenic Influences on Insect Communities. Nauka, Novosibirsk, Russia, 122?127. Keen, F. P. (1952). Insect Enemies of Western Forests: US Department of Agriculture Misc. Publications. 27 5 Kennedy, C., & Southwood, T. (1984). The number of species of insects associated with British trees: A re-analysis. The Journal of Animal Ecology, 53(2), 455? 478. Kergoat, G., Meseguer, A., & Jousselin, E. (2017). Evolution of Plant?Insect Interactions: Insights From Macroevolutionary Approaches in Plants and Herbivorous Insects. In N. Sauvion, D. Thi?ry, & P.-A. Calatayud (Eds.), Advances in Botanical Research (Vol. 81, pp. 25?53): Elsevier. Kethley, J. B., Norton, R. A., Bonamo, P. M., & Shear, W. A. (1989). A terrestrial alicorhagiid mite (Acari: Acariformes) from the Devonian of New York. Micropaleontology, 35(4), 367?373. Kevan, P., Chaloner, W., & Savile, D. (1975). Interrelationships or early terrestrial arthropods and plants. Palaeontology, 18(2), 391?417. Khan, M. A., Spicer, R. A., Spicer, T. E., & Bera, S. (2014). Fossil evidence of insect folivory in the eastern Himalayan Neogene Siwalik forests. Palaeogeography, Palaeoclimatology, Palaeoecology, 410, 264?277. Kidwell, S. M., & Holland, S. M. (2002). The quality of the fossil record: Implications for evolutionary analyses. Annual Review of Ecology and Systematics, 33(1), 561?588. Kirkland, J., Hern?ndez-Rivera, R., Aguill?n Mart?nez, M., Delgado de Jes?s, C., G?mez-Nu?ez, R., & Vallejo, I. (2000). The Late Cretaceous Difunta Group of the Parras Basin, Coahuila, Mexico, and its vertebrate fauna. Paper presented at the Society of Vertebrate Paleontology Annual Meeting. Kirkland, J. I., Eaton, J. G., & Brinkman, D. B. (2013). Elasmobranchs from Upper Cretaceous freshwater facies in southern Utah. In At the Top of the Grand Staircase: the Late Cretaceous of Southern Utah. Indiana University Press, Bloomington (pp. 153?194). Bloomington, Indiana: Indiana University Press. Kishimoto-Yamada, K., Kamiya, K., Meleng, P., Diway, B., Kaliang, H., Chong, L., . . . Ito, M. (2013). Wide host ranges of herbivorous beetles? Insights from DNA bar coding. PLoS ONE, 8(9), e74426. 27 6 Klompen, H., & Grimaldi, D. (2001). First Mesozoic record of a parasitiform mite: A larval argasid tick in Cretaceous amber (Acari: Ixodida: Argasidae). Annals of the Entomological Society of America, 94(1), 10?15. Klucking, E. P. (1987). Leaf venation patterns: Lauraceae (Vol. 2, pp. 261). Berlin: J. Cramer. Knor, S., Prokop, J., Kva?ek, Z., Janovsk?, Z., & Wappler, T. (2012). Plant? arthropod associations from the Early Miocene of the Most Basin in North Bohemia?palaeoecological and palaeoclimatological implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 321, 102?112. Knowlton, F. H. (1900). The Flora of the Montana Formation (Vol. 163, pp. 181) USGS Bulletin. Knowlton, F. H. (1917). Geology and paleontology of the Raton Mesa and other regions in Colorado and New Mexico. U.S. Geological Survey Professional Paper, 101, 323?455. Kodrul, T., Krassilov, V., & Vasilenko, D. (2009). Campanian aquatic and wetland biota from Kundar, Amur Region, Russian Far East. Paper presented at the Tenth International Symposium on Mesozoic Ecosystems. Kolbert, E. (2018). The Damage Done by Trump?s Department of the Interior. New Yorker, 22. Kossel, A. (1891). Ueber die chemische Zusammensetzung der Zelle. Du Bois- Reymond?s Archiv/Arch Anat Physiol Physiol Abt, 181?186. Kozlov, M. (1988). Paleontology of lepidopterans and problems in the phylogeny of the order Papilionida. The Cretaceous Biocoenotic Crisis in the Evolution of Insects. Nauka, Moscow, 16?69. Kozlov, M. V., Lanta, V., Zverev, V., & Zvereva, E. L. (2015). Global patterns in background losses of woody plant foliage to insects. Global Ecology and Biogeography, 24(10), 1126?1135. 27 7 Krassilov, V. (2007). Mines and galls on fossil leaves from the Late Cretaceous of southern Negev, Israel. African Invertebrates, 48(1), 13?22. Krassilov, V., & Karasev, E. (2008). First evidence of plant?arthropod interaction at the Permian?Triassic boundary in the Volga Basin, European Russia. Alavesia, 2, 247?252. Krassilov, V., & Shuklina, S. (2008). Arthropod trace diversity on fossil leaves from the mid-Cretaceous of Negev, Israel. Alavesia, 2, 239?245. Krassilov, V. A. (2008a). Evidence of temporary mining in the Cretaceous fossil mine assemblage of Negev, Israel. Insect Science, 15(3), 285?290. Krassilov, V. A. (2008b). Mine and gall predation as top down regulation in the plant?insect systems from the Cretaceous of Negev, Israel. Palaeogeography, Palaeoclimatology, Palaeoecology, 261(3), 261?269. Kumata, T. (1982). A taxonomic revision of the Gracillaria Group occurring in Japan (Lepidoptera: Incurvarioidea). Insecta Matsumurana, 26, 1?186. Kumata, T., Kuroko, H., & Ermolaev, V. (1988). Japanese species of the Acrocercops Group (Lepidoptera: Gracillariidae) Part 2. Insecta Matsumurana, 40, 1?133. Kva?ek, J., & Herman, A. (2004). The Campanian Gr?nbach flora of Lower Austria: Palaeoecological interpretations. Annalen des Naturhistorischen Museums in Wien. Serie A f?r Mineralogie und Petrographie, Geologie und Pal?ontologie, Anthropologie und Pr?historie, 91?101. Laa?, M., & Hoff, C. (2015). The earliest evidence of damselfly-like endophytic oviposition in the fossil record. Lethaia, 48(1), 115?124. Labandeira, C. C. (1994). A compendium of fossil insect families. Milwaukee Public Museum Contributions in Biology and Geology, 1?87. Labandeira, C. C. (1998a). Early history of arthropod and vascular plant associations. Annual Review of Earth and Planetary Sciences, 26(1), 329?377. 27 8 Labandeira, C. C. (1998b). Plant?insect associations from the fossil record. Geotimes, 43, 18?24. Labandeira, C. C. (1998c). The Role of Insects in Late Jurassic to Middle Cretaceous Ecosystems. In S. G. Lucas, J. I. Kirkland, & J. W. Estep (Eds.), Lower and Middle Cretaceous Terrestrial Ecosystems (pp. 105?124). New Mexico: New Mexico Museum of Natural History and Science. Labandeira, C. C. (2001). The rise and diversification of insects. In Briggs, D. E. G. & Crowther, P. R. (Eds.) Palaeobiology II (pp. 82?88): Oxford: Blackwell Science. Labandeira, C. C. (2002a). The history of associations between plants and animals. In C Herrera, O Pellmyr (Eds.) Plant?Animal Interactions: An Evolutionary Approach (pp. 26?74) Oxford, UK: Blackwell. Labandeira, C. C. (2002b). Paleobiology of predators, parasitoids, and parasites: Death and accomodation in the fossil record of continental invertebrates. The Paleontological Society Papers, 8, 211?250. Labandeira, C. C. (2005). The fossil record of insect extinction: New approaches and future directions. American Entomologist, 51(1), 14?29. Labandeira, C. C. (2006a). Assessing the fossil record of plant?insect associations: Ichnodata versus body-fossil data. In R. Bromley, L. Buatois, J. Genise, M. G.Ma?ngano, & R. Melchor (Eds.), Ichnology at the Crossroads: A Multidimensional Approach to the Science of Organism?Substrate Interactions (Vol. 88, pp. 9?26). Tulsa, Oklahoma. Labandeira, C. C. (2006b). The four phases of plant?arthropod associations in deep time. Geologica Acta, 4(4), 405?438. Labandeira, C. C. (2006c). Silurian to Triassic plant and hexapod clades and their associations: New data, a review, and interpretations. Arthropod Systematics & Phylogeny, 64(1), 53?94. 27 9 Labandeira, C. C. (2007). The origin of herbivory on land: Initial patterns of plant tissue consumption by arthropods. Insect Science, 14(4), 259?275. Labandeira, C. C. (2010). The pollination of mid Mesozoic seed plants and the early history of long-proboscid insects. Annals of the Missouri Botanical Garden, 97(4), 469?513. Labandeira, C. C. (2012). Evidence for outbreaks from the fossil record of insect herbivory. Insect Outbreaks Revisited. Wiley-Blackwell, 269?290. Labandeira, C. C. (2014). Why Did Terrestrial Insect Diversity Not Increase During the Angiosperm Radiation? Mid-Mesozoic, Plant?Associated Insect Lineages Harbor Clues. In P. Pontarotti (Ed.), Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life (pp. 261?299). Switzerland: Springer. Labandeira, C. C. (2019). The Fossil Record of Insect Mouthparts: Innovation, Functional Convergence, and Associations with Other Organisms. In H. Krenn (Ed.), Insect Mouthparts (Vol. 5, pp. 567?671): Springer. Labandeira, C. C., & Anderson, J. (2005). Insect leaf-mining in Late Triassic gymnospermous floras from the Molteno Formation of South Africa. Paper presented at the Geological Society of America Abstracts with Programs. Labandeira, C. C., Dilcher, D. L., Davis, D. R., & Wagner, D. L. (1994). Ninety- seven million years of angiosperm?insect association: Paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Sciences, 91(25), 12278?12282. Labandeira, C. C., & Eble, G. J. (2005). The Fossil Record of Insect Diversity and Disparity. In J. Anderson, F. Thackeray, B. V. Wyk, & M. D. Wit (Eds.), Gondwana Alive: Biodiversity and the Evolving Biosphere. South Africa: Witwatersrand University Press. Labandeira, C. C., Ellis, B., Johnson, K., & Wilf, P. (2007a). Patterns of plant?insect associations from the Cretaceous?Paleogene interval of the Denver Basin. Paper presented at the Geological Society of America Annual Meeting Abstracts with Programs. 28 0 Labandeira, C. C., Johnson, K. R., & Lang, P. (2002a). Preliminary assessment of insect herbivory across the Cretaceous?Tertiary boundary: Major extinction and minimum rebound. Geological Society of America Special Paper, 361, 297?327. Labandeira, C. C., Johnson, K. R., & Wilf, P. (2002b). Impact of the terminal Cretaceous event on plant?insect associations. Proceedings of the National Academy of Sciences, 99(4), 2061?2066. Labandeira, C. C., Kustatscher, E., & Wappler, T. (2016). Floral assemblages and patterns of insect herbivory during the Permian to Triassic of Northeastern Italy. PLoS ONE, 11(11), e0165205. Labandeira, C. C., Kva?ek, J., & Mostovski, M. B. (2007b). Pollination drops, pollen, and insect pollination of Mesozoic gymnosperms. Taxon, 56(3), 663?695. Labandeira, C. C., LePage, B. A., & Johnson, A. H. (2001). A Dendroctonus bark engraving (Coleoptera: Scolytidae) from a middle Eocene Larix (Coniferales: Pinaceae): Early or delayed colonization? American Journal of Botany, 88(11), 2026?2039. Labandeira, C. C., Nufio, C., Wing, S., & Davis, D. (1995). Insect feeding strategies from the Late Cretaceous Big Cedar Ridge flora: Comparing the diversity and intensity of Mesozoic herbivory with the present. Paper presented at the Geological Society of America, Abstracts with Programs. Labandeira, C. C., & Sepkoski, J. J. (1993). Insect diversity in the fossil record. Science, 261(5119), 310?315. Labandeira, C. C., Tremblay, S. L., Bartowski, K. E., & VanAller Hernick, L. (2014). Middle Devonian liverwort herbivory and antiherbivore defence. New Phytologist, 202(1), 247?258. Labandeira, C. C., Wilf, P., Johnson, K. R., & Marsh, F. (2007c). Guide to insect (and other) damage types on compressed plant fossils. Smithsonian Institution, National Museum of Natural History, Department of Paleobiology, Washington, DC. 28 1 Leaf Architecture Working Group (1999). Manual of Leaf Architecture: Morphological description and categorization of dicotyledonous and net- Veined Monocotyledonous Angiosperms. Smithsonian Institute: Washington, DC. 67 pp. In (Vol. 581): Jodrell. Leckey, E. H., & Smith, D. M. (2017). Individual host taxa may resist the climate- mediated trend in herbivory: Cenozoic herbivory patterns in western North American oaks. Palaeogeography, Palaeoclimatology, Palaeoecology, 487, 15?24. Lee, D. E., Bannister, J. M., Raine, J. I., & Conran, J. G. (2010). Euphorbiaceae: Acalyphoideae fossils from early Miocene New Zealand: Mallotus? Macaranga leaves, fruits, and inflorescence with in situ Nyssapollenites endobalteus pollen. Review of Palaeobotany and Palynology, 163(1?2), 127? 138. Lee, D. E., Conran, J. G., Lindqvist, J. K., Bannister, J. M., & Mildenhall, D. C. (2012). New Zealand Eocene, Oligocene and Miocene macrofossil and pollen records and modern plant distributions in the Southern Hemisphere. The Botanical Review, 78(3), 235?260. Legume Phylogeny Working Group (2017). A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66(1), 44?77. LePage, B. A., Yang, H., & Matsumoto, M. (2005). The Evolution and Biogeographic History of Metasequoia. In The geobiology and ecology of Metasequoia (pp. 3?114): Springer. Lesquereux, L. (1878). Contributions to the fossil flora of the Western Territories; Part II: The Tertiary Flora (Vol. 7): US Government Printing Office. Lesquereux, L. (1892). The Flora of the Dakota Group: A Posthumous Work (Vol. 17): US Government Printing Office. Lewinsohn, T. M., & Roslin, T. (2008). Four ways towards tropical herbivore megadiversity. Ecology Letters, 11(4), 398?416. 28 2 Lidgard, S., & Crane, P. R. (1990). Angiosperm diversification and Cretaceous floristic trends: A comparison of palynofloras and leaf macrofloras. Paleobiology, 16(1), 77?93. Liebhold, A., Volney, W., & Schorn, H. (1982). An unidentified leaf mine in fossil Mahonia reticulata (Berberidaceae). The Canadian Entomologist, 114(5), 455?456. Light, A., & Hale, B. (2018). Year one of Donald Trump?s presidency on climate and the environment. In: Taylor & Francis. Lin, X., Labandeira, C. C., Ding, Q., Meng, Q., & Ren, D. (2019). Exploiting nondietary resources in deep time: Patterns of oviposition on mid-Mesozoic plants from northeastern China. International Journal of Plant Sciences, 180(5), 411?457. Liu, H.-Y., Wei, H.-B., Chen, J., Guo, Y., Zhou, Y., Gou, X.-D., . . . Feng, Z. (2020). A latitudinal gradient of plant?insect interactions during the late Permian in terrestrial ecosystems? New evidence from Southwest China. Global and Planetary Change, 103248. Liu, X., Manchester, S. R., & Jin, J. (2014). Alnus subgenus Alnus in the Eocene of western North America based on leaves, associated catkins, pollen, and fruits. American Journal of Botany, 101(11), 1925?1943. Lively, J. R. (2015). A new species of baenid turtle from the Kaiparowits Formation (Upper Cretaceous, Campanian) of southern Utah. Journal of Vertebrate Paleontology, 35(6), e1009084. Lively, J. R. (2016). Baenid turtles of the Kaiparowits Formation (Upper Cretaceous: Campanian) of southern Utah, USA. Journal of Systematic Palaeontology, 35(6), 16. Locatelli, E. R. (2014). The exceptional preservation of plant fossils: A review of taphonomic pathways and biases in the fossil record. The Paleontological Society Papers, 20, 237?258. 28 3 Locatelli, E. R., McMahon, S., & Bilger, H. (2017). Biofilms mediate the preservation of leaf adpression fossils by clays. Palaios, 32(11), 708?724. Loewen, M. A., Irmis, R. B., Sertich, J. J., Currie, P. J., & Sampson, S. D. (2013). Tyrant dinosaur evolution tracks the rise and fall of Late Cretaceous oceans. PLoS ONE, 8(11), e79420. Loewen, M. A., Sampson, S. D., Lund, E. K., Farke, A. A., Aguill?n-Mart?nez, M. C., de Leon, C. A., . . . Eberth, D. A. (2010). Horned dinosaurs (Ornithischia: Ceratopsidae) from the Upper Cretaceous (Campanian) Cerro del Pueblo Formation, Coahuila, Mexico. Paper presented at the New perspectives on horned dinosaurs: The Royal Tyrrell Museum Ceratopsian Symposium. Longrich, N. R. (2011). Titanoceratops ouranos, a giant horned dinosaur from the late Campanian of New Mexico. Cretaceous Research, 32(3), 264?276. Lopez-Vaamonde, C., Wikstrom, N., Labandeira, C., Godfray, H. C., Goodman, S. J., & Cook, J. M. (2006). Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants. Journal of Evolutionary Biology, 19(4), 1314?1326. Lorea-Hernandez, F. G. (1997). A systematic revision of the Neotropical species of Cinnamomum Schaeffer (Lauraceae), Thesis, University of St. Louis, MO. Lund, E. K., Sampson, S. D., & Loewen, M. A. (2016). Nasutoceratops titusi (Ornithischia, Ceratopsidae), a basal centrosaurine ceratopsid from the Kaiparowits Formation, southern Utah. Journal of Vertebrate Paleontology, 36(2), 26. Lupia, R., Lidgard, S., & Crane, P. R. (1999). Comparing palynological abundance and diversity: Implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology, 25(3), 305?340. Lyson, T. R., Joyce, W. G., & Sertich, J. J. (2017). A new chelydroid turtle, Lutemys warreni, gen. et sp. nov., from the Upper Cretaceous (Campanian) Kaiparowits Formation of southern Utah. Journal of Vertebrate Paleontology, 37(6), e1390672. 28 4 Ma, F.-J., Ling, C.-C., Ou-Yang, M.-S., Yang, G.-M., Shen, X.-P., & Wang, Q.-J. (2020). Plant?insect interactions from the Miocene (Burdigalian?Langhian) of Jiangxi, China. Review of Palaeobotany and Palynology, 275, 104176. Maccracken, S. A., & Labandeira, C. C. (2020). The Middle Permian South Ash Pasture assemblage of north-central Texas: Coniferophyte and gigantopterid herbivory and longer-term herbivory trends. International Journal of Plant Sciences, 181(3), 342?362. Maccracken, S. A., Miller, I. M., Johnson, K. R., Sertich, J. J. W., & Labandeira, C. C. (in review). Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA). PLoS ONE. Maccracken, S. A., Miller, I. M., & Labandeira, C. C. (2019). Late Cretaceous domatia reveal the antiquity of plant?mite mutualisms in flowering plants. Biology Letters, 15(11), 20190657. Maccracken, S. A., Sohn, J.-C., Miller, I. M., & Labandeira, C. C. (in review). A new Late Cretaceous leaf mine Leucopteropsis spiralis gen. et sp. nov. (Lepidoptera: Lyonetiidae) and the deep time origin of a common agricultural pest. Journal of Systematic Palaeontology. Maciesiak, A. (1999). Pear leaf blister moth (Leucoptera scitella Zell.) appearance and control. Progress in Plant Protection, 39(2), 444?447. MacKerron, D. (1976). Wind damage to the surface of strawberry leaves. Annals of Botany, 40(2), 351?354. Magall?n, S., G?mez?Acevedo, S., S?nchez?Reyes, L. L., & Hern?ndez?Hern?ndez, T. (2015). A metacalibrated time?tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, 207(2), 437?453. Maia, V. C., Carvalho-Fernandes, S. P., Rodrigues, A. R., & Ascendino, S. (2014). Galls in the Brazilian Coastal Vegetation. In Neotropical Insect Galls (pp. 295?361): Springer. 28 5 Manchester, S. R. (2014). Revisions to Roland Brown's North American Paleocene flora. Acta Musei Nationalis Pragae, Series B-Historia Naturalis, 70(3?4), 153?210. Mani, M. (1964). Gall-bearing plants and gall-inducing organisms. In Ecology of Plant Galls (pp. 12?34): Springer. Marazzi, B., Bronstein, J. L., & Koptur, S. (2013). The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Annals of Botany, 111(6), 1243?1250. Martinez, M. C. A. (2010). Fossil vertebrates from the Cerro del Pueblo Formation, Coahuila, Mexico, and the distribution of late Campanian (Cretaceous) terrestrial vertebrate faunas. Dissertation, Southern Methodist University. Martins, A. M., Abilio, F. M., de Oliveira, P. G., Feltrin, R. P., de Lima, F. S. A., Antonelli, P. d. O., . . . Hamel, P. (2015). Pondberry (Lindera melissifolia, Lauraceae) seed and seedling dispersers and predators. Global Ecology and Conservation, 4, 358?368. McAlpine, J., & Martin, J. (1969). Canadian amber?a paleontological treasure-chest. The Canadian Entomologist, 101(8), 819?838. McBride, E. F. (1974). Significance of color in red, green, purple, olive, brown, and gray beds of Difunta Group, northeastern Mexico. Journal of Sedimentary Research, 44(3), 760?773. McCoy, V., Wappler, T., & Labandeira, C. (in press). Exceptional fossilization of ecological interactions: Plant defenses during the four major expansions of arthropod herbivory in the fossil record. In C. Gee, M. Sander, & V. McCoy (Eds.), Fossilization: The Material Nature of Ancient Plants and Animals in the Paleontological Record: Johns Hopkins University Press. McDonald, C., Francis, J., Compton, S., Haywood, A., Ashworth, A., Hinojosa, L. F., & Smellie, J. (2007). Herbivory in Antarctic fossil forests: Evolutionary and palaeoclimatic significance. U.S.Geological Survey and The National Academies, USGS OF-2007-1047, Extended Abstract 059. 28 6 McKellar, R. C., & Wolfe, A. P. (2010). Canadian amber. Biodiversity of fossils in amber from the major world deposits, 149?166. McKenna, D. D., Sequeira, A. S., Marvaldi, A. E., & Farrell, B. D. (2009). Temporal lags and overlap in the diversification of weevils and flowering plants. Proceedings of the National Academy of Sciences, 106(17), 7083?7088. McKenna, D. D., Wild, A. L., Kanda, K., Bellamy, C. L., Beutel, R. G., Caterino, M. S., . . . Jameson, M. L. (2015). The beetle tree of life reveals that Coleoptera survived end?Permian mass extinction to diversify during the Cretaceous terrestrial revolution. Systematic Entomology, 40(4), 835?880. McMahon, S., Anderson, R. P., Saupe, E. E., & Briggs, D. E. (2016). Experimental evidence that clay inhibits bacterial decomposers: Implications for preservation of organic fossils. Geology, 44(10), 867?870. McNett, K., Longino, J., Barriga, P., Vargas, O., Phillips, K., & Sagers, C. L. (2010). Stable isotope investigation of a cryptic ant?plant association: Myrmelachista flavocotea (Hymenoptera, Formicidae) and Ocotea spp.(Lauraceae). Insectes Sociaux, 57(1), 67?72. Medianero, E., Barrios, H., & Nieves-Aldrey, J. L. (2014). Gall-inducing insects and their associated parasitoid assemblages in the forests of Panama. In Neotropical Insect Galls (pp. 465?496): Springer. Meng, Q. M., Labandeira, C. C., Ding, Q. L., & Ren, D. (2019). The natural history of oviposition on a ginkgophyte fruit from the Middle Jurassic of northeastern China. Insect Science, 26(1), 171?179. Mey, W. (1994). Taxonomische Bearbeitung der westpal?arktischen Arten der Gattung Leucoptera H?bner,?1825?, s. 1.(Lepidoptera, Lyonetiidae) ?Taxonomic revision of the westpalaearctic species of the genus Leucoptera H?bner,?1825?, s. I.(Lepidoptera, Lyonetiidae)?. Deutsche entomologische Zeitschrift, 41(1), 173?234. Mey, W. (2006). Revision of the genus Phyllobrostis Staudinger, 1859 (Lepidoptera, Lyonetiidae). Deutsche Entomologische Zeitschrift, 53(1), 114?147. 28 7 Meyer, J. (1987). Plant galls and gall inducers. Stuttgart: Gebr?der Borntraeger. Michalak, I., Zhang, L. B., & Renner, S. S. (2010). Trans?Atlantic, trans?Pacific and trans?Indian Ocean dispersal in the small Gondwanan Laurales family Hernandiaceae. Journal of Biogeography, 37(7), 1214?1226. Miller, C. J. (2018). For a Lump of Coal & a Drop of Oil: An Environmentalist?s Critique of the Trump Administration?s First Year of Energy Policies. Virginia Environmental Law Journal, 36(2), 185?274. Miller, D. R., & Davidson, J. A. (2005). Armored Scale Insect Pests of Trees and Shrubs (Hemiptera: Diaspididae): Cornell University Press. Miller, I. M., Johnson, K. R., Kline, D. E., Nichols, D. J., & Barclay, R. S. (2013). A Late Campanian flora from the Kaiparowits. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah (pp. 107?131). Bloomington, Indiana: Indiana University Press. Miller, J. R., & Strickler, K. L. (1984). Finding and accepting host plants. In Chemical Ecology of Insects (pp. 127?157): Springer. Minkenberg, O. P., & Ottenheim, J. J. (1990). Effect of leaf nitrogen content of tomato plants on preference and performance of a leafmining fly. Oecologia, 83(3), 291?298. Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., . . . Zhou, X. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346(6210), 763?767. Mitter, C., Farrell, B., & Wiegmann, B. (1988). The phylogenetic study of adaptive zones: Has phytophagy promoted insect diversification? The American Naturalist, 132(1), 107?128. Moisan, P., Labandeira, C. C., Matushkina, N. A., Wappler, T., Voigt, S., & Kerp, H. (2012). Lycopsid?arthropod associations and odonatopteran oviposition on Triassic herbaceous Isoetites. Palaeogeography, Palaeoclimatology, Palaeoecology, 344?345, 6?15. 28 8 M?ller, A. L., Kaulfuss, U., Lee, D. E., & Wappler, T. (2017). High richness of insect herbivory from the early Miocene Hindon Maar crater, Otago, New Zealand. PeerJ, 5, e2985. Mooney, E., & Niesenbaum, R. (2012). Population?specific responses to light influence herbivory in the understory shrub Lindera benzoin. Ecology, 93(12), 2683?2692. Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G., & Worm, B. (2011). How many species are there on Earth and in the ocean?. PLoS Biology, 9(8), e1001127. Moran, N. A. (1988). The evolution of host-plant alternation in aphids: Evidence for specialization as a dead end. The American Naturalist, 132(5), 681?706. Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B., & Pierce, N. E. (2006). Phylogeny of the ants: Diversification in the age of angiosperms. Science, 312(5770), 101?104. Moreau, J.-D., Gomez, B., Daviero-Gomez, V., N?raudeau, D., & Tafforeau, P. (2016). Inflorescences of Mauldinia sp. (Lauraceae) and associated fruits from the Cenomanian of Languedoc Roussillon, France. Cretaceous Research, 59, 18?29. M?ller, R. T., de Ara?jo-J?nior, H. I., Aires, A. S. S., Roberto-da-Silva, L., & Dias- da-Silva, S. (2015). Biogenic control on the origin of a vertebrate monotypic accumulation from the Late Triassic of southern Brazil. Geobios, 48(4), 331? 340. Munk, W., & Sues, H. (1993). Gut contents of Parasaurus (Pareiasauria) and Protorosaurus (Archosauromorpha) from the Kupferschiefer (Upper Permian) of Hessen, Germany. Pal?ontologische Zeitschrift, 67, 169?176. Murray, G. E., Weidie Jr, A., Boyd, D., Forde, R., & Lewis Jr, P. (1962). Formational divisions of Difunta Group, Parras Basin, Coahuila and Nuevo Leon, Mexico. AAPG Bulletin, 46(3), 374?383. 28 9 Myster, R. W. (1997). Seed predation, disease and germination on landslides in Neotropical lower montane wet forest. Journal of Vegetation Science, 8(1), 55?64. Needham, J. G., Frost, S. W., & Tothill, B. H. (1928). Leaf-mining insects. Baltimore, Maryland: The Williams & Wilkins Co. Nelsen, M. P., Ree, R. H., & Moreau, C. S. (2018). Ant?plant interactions evolved through increasing interdependence. Proceedings of the National Academy of Sciences 115(48), 12253?12258. Nielsen, E. S., & Mound, L. A. (2000). Global diversity of insects: The problems of estimating numbers. Nature and Human Society: The Quest for a Sustainable World, 213?222. Niesenbaum, R. A. (1992). The effects of light environment on herbivory and growth in the dioecious shrub Lindera benzoin (Lauraceae). American Midland Naturalist, 270?275. Niesenbaum, R. A., & Kluger, E. C. (2006). When studying the effects of light on herbivory, should one consider temperature? The case of Epimecis hortaria F.(Lepidoptera: Geometridae) feeding on Lindera benzoin L.(Lauraceae). Environmental Entomology, 35(3), 600?606. Niklas, K. J., & Tiffney, B. H. (1994). The quantification of plant biodiversity through time. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 345(1311), 35?44. Niogret, J., Epsky, N. D., Schnell, R. J., Boza, E. J., Kendra, P. E., & Heath, R. R. (2013). Terpenoid variations within and among half-sibling avocado trees, Persea americana Mill. (Lauraceae). PLoS ONE, 8(9), e73601. Nishida, R. (2002). Sequestration of defensive substances from plants by Lepidoptera. Annual Review of Entomology, 47(1), 57?92. 29 0 Nishida, S., Tsukaya, H., Nagamasu, H., & Nozaki, M. (2006). A comparative study on the anatomy and development of different shapes of domatia in Cinnamomum camphora (Lauraceae). Annals of Botany, 97(4), 601?610. Nitao, J. K., Ayres, M. P., Lederhouse, R. C., & Scriber, J. M. (1991). Larval adaptation to lauraceous hosts: Geographic divergence in the spicebush swallowtail butterfly. Ecology, 72(4), 1428?1435. Norton, R. (1985). Aspects of the biology and systematics of soil arachnids, particularly saprophagous and mycophagous mites. Quaestiones Entomologicae, 21, 523?541. Norton, R. A., Bonamo, P. M., Grierson, J. D., & Shear, W. A. (1988). Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York. Journal of Paleontology, 62(2), 259?269. Notley, F. (1948). The Leucoptera leaf miners of coffee on Kilimanjaro. I.? Leucoptera coffeella, Gu?r. Bulletin of Entomological Research, 39(3), 399? 416. Novotny, V., Basset, Y., Miller, S. E., Drozd, P., & Cizek, L. (2002a). Host specialization of leaf-chewing insects in a New Guinea rainforest. Journal of Animal Ecology, 400?412. Novotny, V., Basset, Y., Miller, S. E., Weiblen, G. D., Bremer, B., Cizek, L., & Drozd, P. (2002b). Low host specificity of herbivorous insects in a tropical forest. Nature, 416(6883), 841?844. Novotny, V., Drozd, P., Miller, S. E., Kulfan, M., Janda, M., Basset, Y., & Weiblen, G. D. (2006). Why are there so many species of herbivorous insects in tropical rainforests? Science, 313(5790), 1115?1118. Nydam, R. L. (2013). Lizards and Snakes from the Cenomanian through Campanian of Southern Utah: Filling the Gap in the. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah (pp. 370?423). Bloomington, Indiana: Indiana University Press. 29 1 O'Dowd, D. J., Brew, C. R., Christophel, D. C., & Norton, R. A. (1991). Mite?plant associations from the Eocene of southern Australia. Science, 252(5002), 99? 101. O'Dowd, D. J., & Pemberton, R. W. (1994). Leaf domatia in Korean plants: Floristics, frequency, and biogeography. Vegetatio, 114(2), 137?148. O'Dowd, D. J., & Pemberton, R. W. (1998). Leaf domatia and foliar mite abundance in broadleaf deciduous forest of north Asia. American Journal of Botany, 85(1), 70?78. O'Dowd, D. J., & Willson, M. F. (1989). Leaf domatia and mites on Australasian plants: ecological and evolutionary implications. Biological Journal of the Linnean Society, 37(3), 191?236. O'Dowd, D. J., & Willson, M. F. (1991). Associations between mites and leaf domatia. Trends in Ecology & Evolution, 6(6), 179?182. Oakley, D., & Falcon-Lang, H. J. (2009). Morphometric analysis of Cretaceous (Cenomanian) angiosperm woods from the Czech Republic. Review of Palaeobotany and Palynology, 153(3?4), 375?385. Ollerton, J. (2017). Pollinator diversity: Distribution, ecological function, and conservation. Annual Review of Ecology, Evolution, and Systematics, 48, 353? 376. Opler, P. A. (1973). Fossil lepidopterous leaf mines demonstrate the age of some insect?plant relationships. Science, 179(4080), 1321?1323. Opler, P. A. (1982). Fossil leaf-mines of Bucculatrix(Lyonetiidae) on Zelkova(Ulmaceae) from Florissant, Colorado. Journal of the Lepidopterists Society, 36(2), 145?147. Osier, T., & Jennings, S. (2007). Variability in host?plant quality for the larvae of a polyphagous insect folivore in midseason: The impact of light on three deciduous sapling species. Entomologia Experimentalis et Applicata, 123(2), 159?166. 29 2 Palmer, J. D., Soltis, D. E., & Chase, M. W. (2004). The plant tree of life: An overview and some points of view. American Journal of Botany, 91(10), 1437?1445. Parrish, J. T., & Spicer, R. A. (1988). Late Cretaceous terrestrial vegetation: A near- polar temperature curve. Geology, 16(1), 22?25. Pemberton, R. W., & Turner, C. E. (1989). Occurrence of predatory and fungivorous mites in leaf domatia. American Journal of Botany, 76, 105?112. Penn-Roco, A. (2018). Trump's Dismantling of the National Monuments: Sacrificing Native American Interests on the Altar of Business. National Law Guild Review, 75, 35. Pennisi, E. (2009). How Angiosperms Took Over the World. Sciencemag. https://www.sciencemag.org/news/2009/12/how-angiosperms-took-over- world. Peralta, G., Frost, C. M., Rand, T. A., Didham, R. K., & Tylianakis, J. M. (2014). Complementarity and redundancy of interactions enhance attack rates and spatial stability in host?parasitoid food webs. Ecology, 95(7), 1888?1896. Perez-Hernandez, B., Rodriguez-de la Rosa, R., & Cevallos-Ferriz, S. (1997). Permineralized infructescence from the Cerro del Pueblo Formation (Campanian), near Saltillo, Coahuila, Mexico: Phytolaccaceae. American Journal of Botany, 84, 139. Peris, D., Perez-de la Fuente, R., Penalver, E., Delclos, X., Barron, E., & Labandeira, C. C. (2017). False blister beetles and the expansion of gymnosperm?insect pollination modes before angiosperm dominance. Current Biology, 27(6), 897?904. Philippe, M., Gomez, B., Girard, V., Coiffard, C., Daviero-Gomez, V., Thevenard, F., . . . N?raudeau, D. (2008). Woody or not woody? Evidence for early angiosperm habit from the Early Cretaceous fossil wood record of Europe. Palaeoworld, 17(2), 142?152. 29 3 Pike, E. M. (1994). Historical changes in insect community structure as indicated by hexapods of Upper Cretaceous Alberta (Grassy Lake) amber. The Canadian Entomologist, 126(3), 695?702. Pike, E. M. (1995). Amber taphonomy and the Grassy Lake, Alberta, amber fauna. Dissertation, University of Calgary. Pinheiro, E., Tybusch, G., & Iannuzzi, R. (2012). New evidence of plant?insect interactions in the Lower Permian from Western Gondwana. The Paleobotanist 61, 67?74. Pinheiro, E. R., Iannuzzi, R., & Duarte, L. D. (2016). Insect herbivory fluctuations through geological time. Ecology, 97(9), 2501?2510. Poinar, G., & Brown, A. E. (2003). A new genus of hard ticks in Cretaceous Burmese amber (Acari: Ixodida: Ixodidae). Systematic Parasitology, 54(3), 199?205. Poisot, T., Mouquet, N., & Gravel, D. (2013). Trophic complementarity drives the biodiversity?ecosystem functioning relationship in food webs. Ecology Letters, 16(7), 853?861. Pole, M. (1993). Early Miocene flora of the Manuherikia Group, New Zealand. 5. Smilacaceae, Polygonaceae, Elaeocarpaceae. Journal of the Royal Society of New Zealand, 23(4), 289?302. Pole, M. (1996). Plant macrofossils from the Foulden Hills Diatomite (Miocene), Central Otago, New Zealand. Journal of the Royal Society of New Zealand, 26(1), 1?39. Potoni?, H. (1893). Die Flora des Rotliegenden von Th?ringen-Abh. K?n. Preuss. Geologie Landesanst, NF, 9. Potter, D. A., & Held, D. W. (2002). Biology and management of the Japanese beetle. Annual Review of Entomology, 47(1), 175?205. 29 4 Prevec, R., Labandeira, C. C., Neveling, J., Gastaldo, R. A., Looy, C. V., & Bamford, M. (2009). Portrait of a Gondwanan ecosystem: A new late Permian fossil locality from KwaZulu-Natal, South Africa. Review of Palaeobotany and Palynology, 156(3), 454?493. Prins, J. D., Ar?valo-Maldonado, H. A., Davis, D. R., Landry, B., Vargas, H. A., Davis, M. M., . . . Moreira, G. R. P. (2019). An illustrated catalogue of the Neotropical Gracillariidae (Lepidoptera) with new data on primary types. Zootaxa, 4574(1), 1?110. Prokop, J., Wappler, T., Knor, S., & Kva?ek, Z. (2010). Plant?arthropod associations from the Lower Miocene of the Most Basin in Northern Bohemia (Czech Republic): A preliminary report. Acta Geologica Sinica?English Edition, 84(4), 903?914. R Development Core Team. (2013). R: A language and environment for statistical computing. Rambaut, A. (2015). FigTree, v1.4.3. . In. Available at: https://github.com/rambaut/figtree/releases/tag/1.4.3pre. Rasband, W. (2012). ImageJ: Image processing and analysis in Java. Astrophysics Source Code Library. Rasnitsyn, A. (1988). An outline of evolution of the hymenopterous insects (order Vespida). Oriental Insects, 22(1), 115?145. Raup, D. (1979). Biases in the fossil record of species and genera. Carnegie Museum of Natural History Bulletin, 13, 85?91. Raup, D. M. (1972). Taxonomic diversity during the Phanerozoic. Science, 177(4054), 1065?1071. Ravindran, P., Nirmal-Babu, K., & Shylaja, M. (2003). Cinnamon and cassia: the genus Cinnamomum: CRC press. 29 5 Regier, J. C., Mitter, C., Davis, D. R., Harrison, T. L., Sohn, J. C., Cummings, M. P., . . . Mitter, K. T. (2015). A molecular phylogeny and revised classification for the oldest ditrysian moth lineages (Lepidoptera: Tineoidea), with implications for ancestral feeding habits of the mega?diverse Ditrysia. Systematic Entomology, 40(2), 409?432. Reis-Avila, G., & Oliveira, J. M. (2017). Lauraceae: A promising family for the advance of neotropical dendrochronology. Dendrochronologia, 44, 103?116. Rhoades, D. F., & Cates, R. G. (1976). Toward a general theory of plant antiherbivore chemistry. In Biochemical interaction between plants and insects (Vol. 10, pp. 168?213). New York: Plenam Press. Rick, T. C., & Lockwood, R. (2013). Integrating paleobiology, archeology, and history to inform biological conservation. Conservation Biology, 27(1), 45? 54. Rivera-Sylva, H. E., Frey, E., & Guzm?n-Guti?rrez, J. R. (2009). Evidence of predation on the vertebra of a hadrosaurid dinosaur from the Upper Cretaceous (Campanian) of Coahuila, Mexico. Carnets de Geologi? (L02), 1? 6. Roberts, E. M. (2007). Facies architecture and depositional environments of the Upper Cretaceous Kaiparowits Formation, southern Utah. Sedimentary Geology, 197(3?4), 207?233. Roberts, E. M., Deino, A. L., & Chan, M. A. (2005). 40 Ar/39 Ar age of the Kaiparowits Formation, southern Utah, and correlation of contemporaneous Campanian strata and vertebrate faunas along the margin of the Western Interior Basin. Cretaceous Research, 26(2), 307?318. Roberts, E. M., Rogers, R. R., & Foreman, B. Z. (2007). Continental insect borings in dinosaur bone: Examples from the Late Cretaceous of Madagascar and Utah. Journal of Paleontology, 81(1), 201?208. Roberts, E. M., Sampson, S. D., Deino, A. L., Bowring, S. A., & Buchwaldt, R. (2013). The Kaiparowits Formation: A remarkable record of Late Cretaceous terrestrial environments, ecosystems, and evolution in western North America. 29 6 In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah (pp. 85?106). Bloomington, Indiana: Indiana University Press. Roberts, E. M., & Tapanila, L. (2006). A new social insect nest from the Upper Cretaceous Kaiparowits Formation of southern Utah. Journal of Paleontology, 80(4), 768?774. Roberts, E. M., Tapanila, L., & Mijal, B. (2008). Taphonomy and sedimentology of storm-generated continental shell beds: A case example from the Cretaceous Western Interior Basin. The Journal of Geology, 116(5), 462?479. Robledo, J. M., Pinheiro, E. R., Gnaedinger, S. C., & Wappler, T. (2018). Plant? insect interactions on dicots and ferns from the Miocene of Argentina. Palaios, 33(7), 338?352. Ro?ek, Z., Gardner, J. D., Eaton, J. G., & Prikryl, T. (2013). Anuran ilia from the Upper Cretaceous of Utah?diversity and stratigraphic patterns. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah. Indiana University Press, Bloomington, Indiana (pp. 273?294). Bloomington, Indiana: Indiana University Press. Rohwer, J. (1993a). Lauraceae. In K. Kubitzki, J. G. Rohwer, & V. Bittrich (Eds.), The Families and Genera of Vascular Plants (Vol. II; Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families, pp. 366?391). Berlin: Springer? Verlag. Rohwer, J. G. (1993b). Lauraceae. In Flowering Plants? Dicotyledons (pp. 366?391): Springer. Romero, G. Q., & Benson, W. W. (2005). Biotic interactions of mites, plants and leaf domatia. Current Opinion in Plant Biology, 8(4), 436?440. de la Rosa, R. A. R.., & Cevallos-Ferriz, S. R. S. (1998). Vertebrates of the El Pelillal locality (Campanian, Cerro Del Pueblo Formation), southeastern Coahuila, Mexico. Journal of Vertebrate Paleontology, 18(4), 751?764. 29 7 de la Rosa, D. B., & Rodriguez, R. (2006). Nonmarine Turtles from the Cerro del Pueblo Formation (Campanian), Coahuila State, Mexico. Late Cretaceous Vertebrates from the Western Interior: Bulletin 35, 229?234. Rosenthal, G. A., & Berenbaum, M. R. (2012). Herbivores: Their Interactions with Secondary Plant Metabolites. In Ecological and Evolutionary Processes (Vol. 2): Academic Press. Ross, A. (2015). Insects in Burmese amber. Paper presented at the Entomologentagung 02.?05.03.2015 Frankfurt/M. Programm und Abstracts. (Frankfurt: Deutsche Gesellschaft f?r allgemeine und angewandte Entomologie e.V., 2015). Ross, A. (2018). The remarkable palaeodiversity in Burmese amber. Paper presented at the AMBERIF 2018: Interantional Fair of Amber, Jewellery and Gemstones. International Symposium Amber. Science and Art Abstracts. International Fair Co, Gda?sk, Poland, pp. 12?17. Ross, A., & Jarzembowski, E. (1993). Arthropoda (Hexapoda; Insecta). The Fossil Record, 2, 363?426. Ross, A. J., Jarzembowski, E., & Brooks, S. J. (2000). The Cretaceous and Cenozoic record of insects (Hexapoda) with regard to global change. In S. J. Culver & P. F. Rawson (Eds.), Biotic Response to Global Change: The Last 145 Million Years (Vol. 145, pp. 288?302): Cambridge, MA, Cambridge University Press. Royer, D. L., Sack, L., Wilf, P., Lusk, C. H., Jordan, G. J., Niinemets, ?., . . . Coley, P. D. (2007). Fossil leaf economics quantified: Calibration, Eocene case study, and implications. Paleobiology, 33(4), 574?589. Rozefelds, A. C., & Sobbe, I. (1987). Problematic insect leaf mines from the Upper Triassic Ipswich Coal Measures of southeastern Queensland, Australia. Alcheringa, 11(1), 51?57. Russell, H. (1894). The fixation of free nitrogen by plants. Botanical Gazette, 19(7), 284?293. 29 8 Sampson, S., Loewen, M., Ryan, M., Chinnery-Allgeier, B., & Eberth, D. (2010a). Paper presented at the New Perspectives on Horned Dinosaurs: The Royal Tyrrell Museum Ceratopsian Symposium. Sampson, S. D., Loewen, M. A., Farke, A. A., Roberts, E. M., Forster, C. A., Smith, J. A., & Titus, A. L. (2010b). New horned dinosaurs from Utah provide evidence for intracontinental dinosaur endemism. PLoS ONE, 5(9), e12292. Sampson, S. D., Lund, E. K., Loewen, M. A., Farke, A. A., & Clayton, K. E. (2013). A remarkable short-snouted horned dinosaur from the Late Cretaceous (late Campanian) of southern Laramidia. Proceedings of the Royal Society B: Biological Sciences, 280(1766), 1?7. Santi, C., Bogusz, D., & Franche, C. (2013). Biological nitrogen fixation in non- legume plants. Annals of Botany, 111(5), 743?767. Sarzetti, L. C., Labandeira, C. C., & Genise, J. F. (2008). A leafcutter bee trace fossil from the middle Eocene of Patagonia, Argentina, and a review of megachilid (Hymenoptera) ichnology. Palaeontology, 51(4), 933?941. Schachat, S., & Labandeira, C. (in press). Are insects heading toward their first mass extinction? Distinguishing turnover from crises in the fossil record. Annals of the Entomological Society of America, 113. Schachat, S. R., & Gibbs, G. W. (2016). Variable wing venation in Agathiphaga (Lepidoptera: Agathiphagidae) is key to understanding the evolution of basal moths. Royal Society Open Science, 3(10), 160453. Schachat, S. R., Labandeira, C. C., & Chaney, D. S. (2015). Insect herbivory from early Permian Mitchell Creek Flats of north-central Texas: Opportunism in a balanced component community. Palaeogeography, Palaeoclimatology, Palaeoecology, 440, 830?847. Schachat, S. R., Labandeira, C. C., Clapham, M. E., & Payne, J. L. (2019). A Cretaceous peak in family-level insect diversity estimated with mark? recapture methodology. Proceedings of the Royal Society B: Biological Sciences, 286(1917), 20192054. 29 9 Schachat, S. R., Labandeira, C. C., Gordon, J., Chaney, D., Levi, S., Halthore, M. N., & Alvarez, J. (2014). Plant?insect interactions from early Permian (Kungurian) Colwell Creek Pond, north-central Texas: The early spread of herbivory in riparian environments. International Journal of Plant Sciences, 175(8), 855?890. Schachat, S. R., Labandeira, C. C., & Maccracken, S. A. (2018). The importance of sampling standardization for comparisons of insect herbivory in deep time: A case study from the late Palaeozoic. Royal Society Open Science, 5(3), 171991. Schachat, S. R., Maccracken, S. A., & Labandeira, C. C. (2020). Sampling fossil floras for the study of insect herbivory: How many leaves is enough? Mitteilungen aus dem Museum f?r Naturkunde in Berlin. Fossil Record, 23(1), 15?32. Schaefer, I., Norton, R. A., Scheu, S., & Maraun, M. (2010). Arthropod colonization of land? Linking molecules and fossils in oribatid mites (Acari, Oribatida). Molecular Phylogenetics and Evolution, 57(1), 113?121. Schallhart, N., Tusch, M. J., Wallinger, C., Staudacher, K., & Traugott, M. (2012). Effects of plant identity and diversity on the dietary choice of a soil?living insect herbivore. Ecology, 93(12), 2650-2657. Scheirs, J., De Bruyn, L., & Verhagen, R. (2003). Host nutritive quality and host plant choice in two grass miners: Primary roles for primary compounds? Journal of Chemical Ecology, 29(6), 1373?1389. Schmidt, L. E. A., Dunn, R. E., Mercer, J., Dechesne, M., & Currano, E. D. (2019). Plant and insect herbivore community variation across the Paleocene?Eocene boundary in the Hanna Basin, southeastern Wyoming. PeerJ, 7, e7798. Schmitt, J., Brown, M., & Davis, D. (1996). Taxonomy, morphology, and biology of Lyonetia prunifoliella (Lepidoptera: Lyonetiidae), a leafminer of apple. Annals of the Entomological Society of America, 89(3), 334?345. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671?675. 30 0 Schneider, H., Schuettpelz, E., Pryer, K. M., Cranfill, R., Magall?n, S., & Lupia, R. (2004). Ferns diversified in the shadow of angiosperms. Nature, 428(6982), 553. Scott, A., Chaloner, W., & Paterson, S. (1985). Evidence of pteridophyte?arthropod interactions in the fossil record. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences, 86, 133?140. Scott, A. C., Anderson, J. M., & Anderson, H. M. (2004). Evidence of plant?insect interactions in the Upper Triassic Molteno Formation of South Africa. Journal of the Geological Society, 161(3), 401?410. Scott, A. C., & Paterson, S. (1984). Techniques for the study of plant/arthropod interactions in the fossil record. Geobios, 17, 449?457. Scott, A. C., & Taylor, T. N. (1983). Plant/animal interactions during the Upper Carboniferous. The Botanical Review, 49(3), 259?307. Scudder, S. H. (1886). Systematic Review of our Present Knowledge of Fossil Insects, Including Myridpods and Arachnids (Vol. 31, pp. 136): Charleston, SC, Nabu Publishers. Serrano-Bra?as, C. I., Espinosa-Ch?vez, B., & Maccracken, S. A. (2018a). Gastrochaenolites Leymerie in dinosaur bones from the Upper Cretaceous of Coahuila, north-central Mexico: Taphonomic implications for isolated bone fragments. Cretaceous Research, 92, 18?25. Serrano-Bra?as, C. I., Espinosa-Ch?vez, B., & Maccracken, S. A. (2018b). Insect damage in dinosaur bones from the Cerro del Pueblo Formation (Late Cretaceous, Campanian) Coahuila, Mexico. Journal of South American Earth Sciences, 86, 353?365. Sessa, E. B., Banks, J. A., Barker, M. S., Der, J. P., Duffy, A. M., Graham, S. W., . . . Marchant, D. B. (2014). Between two fern genomes. GigaScience, 3(1), 15. 30 1 Sewall, J. O., & Fricke, H. C. (2013). Andean-scale highlands in the Late Cretaceous Cordillera of the North American western margin. Earth and Planetary Science Letters, 362, 88?98. Shear, W. A., Bonamo, P. M., Grierson, J. D., Rolfe, W. I., Smith, E. L., & Norton, R. A. (1984). Early land animals in North America: Evidence from Devonian age arthropods from Gilboa, New York. Science, 224(4648), 492?494. Signor, P. W., Lipps, J. H., Silver, L., & Schultz, P. (1982). Sampling bias, gradual extinction patterns, and catastrophes in the fossil record. Geological Implications of Impacts of Large Asteroids and Comets on the Earth, 190, 291?296. Sinclair, R. J., & Hughes, L. (2010). Leaf miners: The hidden herbivores. Austral Ecology, 35(3), 300?313. Smith, D. M. (2012). Exceptional preservation of insects in lacustrine environments. Palaios, 27(5), 346?353. Smith, D. M., Cook, A., & Nufio, C. R. (2006). How physical characteristics of beetles affect their fossil preservation. Palaios, 21(3), 305?310. Smith, S. A., Beaulieu, J. M., & Donoghue, M. J. (2010). An uncorrelated relaxed- clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences, 107(13), 5897?5902. Sohn, J.-C. (2013). Molecular phylogenetics, biodiversity and life history evolution of Yponomeutoidea (Lepidoptera: Ditrysia), with a catalog and an overview of the lepidopteran fossils. Dissertation, University of Maryland, College Park. Sohn, J.-C. (2020). unpublished data. Sohn, J.-C., Doorenweerd, C., Nam, K. S., & Choi, S.-W. (2019a). New leaf-mine fossil from the Geumgwangdong Formation, Pohang Basin, South Korea, associates pygmy moths (Lepidoptera, Nepticulidae) with beech trees (Fagaceae, Fagus) in the Miocene. Journal of Paleontology, 93(2), 337?342. 30 2 Sohn, J.-C., Kim, N.-H., & Choi, S.-W. (2019b). Effect of elevation on the insect herbivory of Mongolian oaks in the high mountains of southern South Korea. Journal of Asia-Pacific Entomology 22(3), 957?962. Sohn, J.-C., Labandeira, C., Davis, D., & Mitter, C. (2012). An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa, 3286(1), 1?132. Sohn, J.-C., Labandeira, C. C., & Davis, D. R. (2015). The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): Implications for evolutionary diversity and divergence-time estimates. BMC Evolutionary Biology, 15(1), 1?12. Sohn, J.-C., Regier, J. C., Mitter, C., Davis, D., Landry, J.-F., Zwick, A., & Cummings, M. P. (2013). A molecular phylogeny for Yponomeutoidea (Insecta, Lepidoptera, Ditrysia) and its implications for classification, biogeography and the evolution of host plant use. PLoS ONE, 8(1), e55066. Soltis, P. S., & Soltis, D. E. (2004). The origin and diversification of angiosperms. American Journal of Botany, 91(10), 1614?1626. Soriano, E. G., Gutierrez, R. N., & Garza, M. V. (1982). Reproductive behavior of Palaemnema desiderata Selys (Odonata: Platystictidae). Advances in Odonatology, 1(1), 55?62. Spencer, K. A. (2012). Host specialization in the world Agromyzidae (Diptera) (Vol. 45, pp. 444): Netherlands, Springer Netherlands. Spicer, R. A., & Parrish, J. (1987). Plant megafossils, vertebrate remains, and paleoclimate of the Kogosukruk tongue (Late Cretaceous), North Slope, Alaska. US Geological Survey Circular, 998, 47?48. Sprent, J. I., & Parsons, R. (2000). Nitrogen fixation in legume and non-legume trees. Field Crops Research, 65(2?3), 183?196. 30 3 Spurr, K., Geib, P. R., & Collette, J. H. (2004). Patterns of human activity in "The Heart of the Desert Wild": Archeological Survey and Testing on the Kaiparowits Plateau, Grand Staircase-Escalante National Monument. The Colorado Plateau: Cultural, Biological, and Physical Research, 19. Srivastava, R., & Srivastava, A. (2016). Insect herbivory in Gondwana plants. The Palaeobotanist 65(1): 131?137. Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post- analysis of large phylogenies. Bioinformatics, 30(9), 1312?1313. Stephenson, J. (1992). Evidence of plant insect interactions in the late Cretaceous and early Tertiary. Dissertation, Royal Holloway, University of London. Stevens, P. F., & Davis, H. (2001). Angiosperm phylogeny website. http://www.mobot.org/MOBOT/research/APweb/ Stork, N. E. (1988). Insect diversity: Facts, fiction and speculation. Biological Journal of the Linnean Society, 35(4), 321?337. Stout, J. (1979). An association of an ant, a mealy bug, and an understory tree from a Costa Rican rain forest. Biotropica, 11(4), 309?311. Strauss, S. Y., & Zangerl, A. R. (2002). Plant?insect interactions in terrestrial ecosystems. Plant?Animal Interactions: An Evolutionary Approach, 2002, 77?106. Su, T., Adams, J. M., Wappler, T., Huang, Y.-J., Jacques, F. M., Liu, Y.-S. C., & Zhou, Z.-K. (2015). Resilience of plant?insect interactions in an oak lineage through Quaternary climate change. Paleobiology, 41(1), 174?186. Sullivan, R. M. (1999). Nodocephalosaurus kirtlandensis, gen. et sp. nov., a new ankylosaurid dinosaur (Ornithischia: Ankylosauria) from the Upper Cretaceous Kirtland Formation (Upper Campanian), San Juan Basin, New Mexico. Journal of Vertebrate Paleontology, 19(1), 126?139. 30 4 Sullivan, R. M., & Lucas, S. (2006). Saurornitholestes robustus n. sp.(Theropoda: Dromaeosauridae) from the Upper Cretaceous Kirtland Formation (De-na-zin Member), San Juan Basin, New Mexico. Late Cretaceous Vertebrates from the Western Interior: New Mexico Museum of Natural History and Science Bulletin, 35, 253?256. Sullivan, R. M., & Lucas, S. G. (2000). Alamosaurus (Dinosauria: Sauropoda) from the late Campanian of New Mexico and its significance. Journal of Vertebrate Paleontology, 20(2), 400?403. Sullivan, R. M., & Williamson, T. E. (1999). A New Skull of Parasaurolophus (Dinosauria: Hadrosauridae) from the Kirtland Formation of New Mexico and a Revision of the Genus. New Mexico Museum of Natural History and Science Bulletin, 15,1?52. Szwedo, J., & Nel, A. (2015). The Cretaceous insects: A promising state of the art. Cretaceous Research, 52, 628?630. Tallamy, D. W. (1986). Behavioral Adaptations in Insects to Plant Allelochemicals. In Brattsten L.B., & Ahmad S. (eds), Molecular Aspects of Insect-Plant Associations (pp. 273?300): Boston, MA, Springer. Tank, D. C., Eastman, J. M., Pennell, M. W., Soltis, P. S., Soltis, D. E., Hinchliff, C. E., . . . Harmon, L. J. (2015). Nested radiations and the pulse of angiosperm diversification: Increased diversification rates often follow whole genome duplications. New Phytologist, 207(2), 454?467. Tapanila, L., & Roberts, E. M. (2013). Continental Invertebrates and Trace Fossils from the Campanian Kaiparowits Formation, Utah. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah (pp. 132?152). Bloomington, Indiana: Indiana University Press. Taylor, T. N., & Taylor, E. L. (1993). The Biology and Evolution of Fossil Plants: Englewood Cliffs, N.J., Prentice Hall. 30 5 Tiffney, B. H. (1984). Seed size, dispersal syndromes, and the rise of the angiosperms: Evidence and hypothesis. Annals of the Missouri Botanical Garden, 71(2), 551?576. Tiffney, B. H. (2004). Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics, 35, 1?29. Titus, A., Eaton, J., & Sertich, J. (2016). Late Cretaceous stratigraphy and vertebrate faunas of the Markagunt, Paunsaugunt, and Kaiparowits plateaus, southern Utah. Geology of the Intermountain West, 3, 229?291. Titus, A. L., & Loewen, M. A. (2013). At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah. Bloomington, Indiana: Indiana University Press. Torres-Gurrola, G., Delgado-Lamas, G., & Espinosa-Garc?a, F. J. (2011). The foliar chemical profile of criollo avocado, Persea americana var. drymifolia (Lauraceae), and its relationship with the incidence of a gall-forming insect, Trioza anceps (Triozidae). Biochemical Systematics and Ecology, 39(2), 102? 111. Turcotte, M. M., Davies, T. J., Thomsen, C. J., & Johnson, M. T. (2014). Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proceedings of the Royal Society B: Biological Sciences, 281(1787), 20140555. Turland, N. J., Wiersema, J. H., Barrie, F. R., Greuter, W., Hawksworth, D., Herendeen, P. S., . . . Marhold, K. (2018). International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017: Koeltz Botanical Books. Underwood, E. (2017). Why fossil scientists are suing Trump over monuments move. In: American Association for the Advancement of Science. Upchurch, G. R., & Dilcher, D. L. (1990). Cenomanian angiosperm leaf megafossils, Dakota Formation, Rose Creek locality, Jefferson County, southeastern Nebraska. Geological Survey Bulletin Series 1915, 126. 30 6 USDA. (2011). Pear Leaf Blister Moth Leucoptera malifoliella. Stone Fruit Commodity-Based Pest Survey. Retrieved from http://download.ceris.purdue.edu/file/1081 van der Niet, T., & Johnson, S. D. (2012). Phylogenetic evidence for pollinator- driven diversification of angiosperms. Trends in Ecology & Evolution, 27(6), 353?361. van der Werff, H., & Richter, H. (1996). Toward an improved classification of Lauraceae. Annals of the Missouri Botanical Garden, 409?418. van Eldijk, T. J., Wappler, T., Strother, P. K., van der Weijst, C. M., Rajaei, H., Visscher, H., & van de Schootbrugge, B. (2018). A Triassic?Jurassic window into the evolution of Lepidoptera. Science Advances, 4(1), e1701568. van Nieukerken, E. J., Kaila, L., Kitching, I. J., Kristensen, N. P., Lees, D. C., Minet, J., . . . Simonsen, T. J. (2011). Order Lepidoptera Linnaeus, 1758. In: Zhang, Z.-Q.(Ed.) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148(1), 212?221. Vasilenko, D. V. (2008). Insect ovipositions on aquatic plant leaves Quereuxia from the Upper Cretaceous of the Amur region. Paleontological Journal, 42(5), 514?521. Vavrek, M. J., Hills, L. V., & Currie, P. J. (2014). A hadrosaurid (Dinosauria: Ornithischia) from the Late Cretaceous (Campanian) Kanguk Formation of Axel Heiberg Island, Nunavut, Canada, and its ecological and geographical implications. Arctic, 67, 1?9. Vaz, P. P., de Souza, P. R., Alves, F. M., & Arruda, R. d. C. d. O. (2018). Cork-warts on leaves of Lauraceae: Confirming a suspicion. Plant Systematics and Evolution, 304, 723?729. Verhoeven, K. J., Simonsen, K. L., & McIntyre, L. M. (2005). Implementing false discovery rate control: Increasing your power. Oikos, 108(3), 643?647. 30 7 Vincent, C., De Oliveira, D., & B?langer, A. (1990). The management of insect pollinators and pests in Quebec strawberry plantations. In N. J. Bostanian, L. T. Wilson, & T. J. Dennehy (Eds.), Monitoring and integrated management of arthropod pests of small fruit crops (pp. 177?192). St.-Jean-sur-Richelieu, Quebec, Canada: Research Station, Agriculture Canada. von Balthazar, M., Pedersen, K. R., Crane, P. R., Stampanoni, M., & Friis, E. M. (2007). Potamacanthus lobatus gen. et sp. nov., a new flower of probable Lauraceae from the Early Cretaceous (Early to Middle Albian) of eastern North America. American Journal of Botany, 94(12), 2041?2053. Wahlberg, N., Wheat, C. W., & Pe?a, C. (2013). Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS ONE, 8(11), e80875. Waide, R., Willig, M., Steiner, C., Mittelbach, G., Gough, L., Dodson, S., . . . Parmenter, R. (1999). The relationship between productivity and species richness. Annual Review of Ecology and Systematics, 30(1), 257?300. Walker, J. D., Geissman, J. W., Bowring, S., & Babcock, L. (2018). The Geological Society of America Geologic Time Scale v. 5.0. Geological Society of America. Walter, D. (2017). Little houses in big trees: An Aesop's fable with plants. Wildlife Australia, 54(1), 26?31. Walter, D. E. (1988). Predation and mycophagy by endeostigmatid mites (Acariformes: Prostigmata). Experimental & Applied Acarology, 4(2), 159? 166. Walter, D. E. (1996). Living on leaves: mites, tomenta, and leaf domatia. Annual Review of Entomology, 41(1), 101?114. Walter, D. E., & O'Dowd, D. J. (1992). Leaf morphology and predators: Effect of leaf domatia on the abundance of predatory mites (Acari: Phytoseiidae). Environmental Entomology, 21(3), 478?484. 30 8 Walter, D. E., & Proctor, H. C. (1999). Mites: Ecology, Evolution and Behaviour. Wallingford, UK CABI Publishing. Wang, H., & Dilcher, D. L. (2018). Early Cretaceous angiosperm leaves from the Dakota Formation, Hoisington III locality, Kansas, USA. Palaeontologia Electronica, 21, 1?49. Wang, X. (2017). A Biased, Misleading Review on Early Angiosperms. Natural Science, 9(12), 399?405. Wang, Y., Labandeira, C. C., Shih, C., Ding, Q., Wang, C., Zhao, Y., & Ren, D. (2012). Jurassic mimicry between a hangingfly and a ginkgo from China. Proceedings of the National Academy of Sciences, 109(50), 20514?20519. Wappler, T. (2010). Insect herbivory close to the Oligocene?Miocene transition?a quantitative analysis. Palaeogeography, Palaeoclimatology, Palaeoecology, 292(3?4), 540?550. Wappler, T., & Ben-Dov, Y. (2008). Preservation of armoured scale insects on angiosperm leaves from the Eocene of Germany. Acta Palaeontologica Polonica, 53(4), 627?634. Wappler, T., Currano, E. D., Wilf, P., Rust, J., & Labandeira, C. C. (2009). No post- Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants, Menat, France. Proceedings of the Royal Society B: Biological Sciences, 276(1677), 4271?4277. Wappler, T., & Denk, T. (2011). Herbivory in early Tertiary Arctic forests. Palaeogeography, Palaeoclimatology, Palaeoecology, 310(3-4), 283-295. Wappler, T., & Gr?msson, F. (2016). Before the ?Big Chill?: Patterns of plant?insect associations from the Neogene of Iceland. Global and Planetary Change, 142, 73?86. Wappler, T., Kustatscher, E., & Dellantonio, E. (2015a). Plant?insect interactions from Middle Triassic (late Ladinian) of Monte Agnello (Dolomites, N- 30 9 Italy)?Initial pattern and response to abiotic environmental perturbations. PeerJ, 3, e921. Wappler, T., Labandeira, C. C., Engel, M. S., Zetter, R., & Grimsson, F. (2015b). Specialized and Generalized Pollen-Collection Strategies in an Ancient Bee Lineage. Current Biology, 25(23), 3092?3098. Wappler, T., Labandeira, C. C., Rust, J., Frankenh?user, H., & Wilde, V. (2012). Testing for the effects and consequences of mid Paleogene climate change on insect herbivory. PLoS ONE, 7(7), e40744. Weber, J. Z. (1981). A taxonomic revision of Cassytha (Lauraceae) in Australia. Journal of the Adelaide Botanic Garden, 187?262. Wedmann, S., Wappler, T., & Engel, M. S. (2009). Direct and indirect fossil records of megachilid bees from the Paleogene of Central Europe (Hymenoptera: Megachilidae). Naturwissenschaften, 96(6), 703?712. Whalley, P., & Jarzembowski, E. A. (1981). A new assessment of Rhyniella, the earliest known insect, from the Devonian of Rhynie Scotland. Nature, 291(5813), 317-317 Whalley, P. (1986). A review of the current fossil evidence of Lepidoptera in the Mesozoic. Biological Journal of the Linnean Society, 28(3), 253?271. Whalley, P. S. (1985). The systematics and palaeogeography of the Lower Jurassic insects of Dorset, England. Bulletin of the British Museum, Natural History. Geology, 39(3), 107?189. Wheat, C. W., Vogel, H., Wittstock, U., Braby, M. F., Underwood, D., & Mitchell- Olds, T. (2007). The genetic basis of a plant?insect coevolutionary key innovation. Proceedings of the National Academy of Sciences, 104(51), 20427?20431. Wheeler, E., & Lehman, T. (2009). New Late Cretaceous and Paleocene dicot woods of Big Bend National Park, Texas and review of Cretacous wood characteristics. IAWA Journal, 30(3), 293?318. 31 0 Wheeler, E. A., & Baas, P. (1991). A survey of the fossil record for dicotiledonous wood and its significance for evolutionary and ecological wood anatomy. IAWA Journal, 12(3), 275?318. Wiens, J. J., Lapoint, R. T., & Whiteman, N. K. (2015). Herbivory increases diversification across insect clades. Nature Communications, 6, 8370. Wikstr?m, N., Savolainen, V., & Chase, M. W. (2001). Evolution of the angiosperms: Calibrating the family tree. Proceedings of the Royal Society B: Biological Sciences, 268(1482), 2211?2220. Wilf, P. (2008). Insect?damaged fossil leaves record food web response to ancient climate change and extinction. New Phytologist, 178(3), 486?502. Wilf, P., & Labandeira, C. C. (1999). Response of plant?insect associations to Paleocene?Eocene warming. Science, 284(5423), 2153?2156. Wilf, P., Labandeira, C. C., Johnson, K. R., Coley, P. D., & Cutter, A. D. (2001). Insect herbivory, plant defense, and early Cenozoic climate change. Proceedings of the National Academy of Sciences, 98(11), 6221?6226. Wilf, P., Labandeira, C. C., Johnson, K. R., & Ellis, B. (2006). Decoupled plant and insect diversity after the end-Cretaceous extinction. Science, 313(5790), 1112?1115. Wilf, P., Labandeira, C. C., Kress, W. J., Staines, C. L., Windsor, D. M., Allen, A. L., & Johnson, K. R. (2000). Timing the radiations of leaf beetles: Hispines on gingers from latest Cretaceous to recent. Science, 289(5477), 291?294. Williamson, T. E. (2000). Review of Hadrosauridae (Dinosauria, Ornithischia) from the San Juan Basin, New Mexico. Dinosaurs of New Mexico: New Mexico Museum of Natural History and Science, Bulletin, 17, 191?213. Williamson, T. E., & Weil, A. (2008). Metatherian mammals from the Naashoibito Member, Kirtland Formation, San Juan Basin, New Mexico and their biochronologic and paleobiogeographic significance. Journal of Vertebrate Paleontology, 28(3), 803?815. 31 1 Willis, K., & McElwain, J. (2014). The Evolution of Plants: Oxford University Press. Willis, K. J. (2017). State of the World?s Plants 2017. Kew Royal Botanic Gardens. Willson, M. F. (1991). Foliar shelters for mites in the eastern deciduous forest. American Midland Naturalist, 126, 111?117. Wing, S. L., Hickey, L. J., & Swisher, C. C. (1993). Implications of an exceptional fossil flora for Late Cretaceous vegetation. Nature, 363(6427), 342?344. Winkler, I. S., Labandeira, C. C., Wappler, T., & Wilf, P. (2010). Distinguishing Agromyzidae (Diptera) leaf mines in the fossil record: New taxa from the Paleogene of North America and Germany and their evolutionary implications. Journal of Paleontology, 84(5), 935?954. Winkler, I. S., & Mitter, C. (2008). The phylogenetic dimension of insect-plant interactions: a review of recent evidence. Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects, 240-263 Winkler, I. S., Mitter, C., & Scheffer, S. J. (2009). Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies. Proceedings of the National Academy of Sciences, 106(43), 18103?18108. Winkler, I. S., Scheffer, S. J., & Mitter, C. (2009). Molecular phylogeny and systematics of leaf?mining flies (Diptera: Agromyzidae): Delimitation of Phytomyza Fall?n sensu lato and included species groups, with new insights on morphological and host?use evolution. Systematic Entomology, 34(2), 260? 292. Wolfe, J. A. (1975). Some aspects of plant geography of the Northern Hemisphere during the late Cretaceous and Tertiary. Annals of the Missouri Botanical Garden, 264?279. Wolstenholme, B., & Whiley, A. (1999). Ecophysiology of the avocado (Persea americana Mill.) tree as a basis for pre-harvest management. Revista Chapingo Serie Horticultura, 5, 77?88. 31 2 Woolley, C. H., Smith, N. D., & Sertich, J. J. (2020). New fossil lizard specimens from a poorly-known squamate assemblage in the Upper Cretaceous (Campanian) San Juan Basin, New Mexico, USA. PeerJ, 8, e8846. Xiao, L. F., Labandeira, C. C., Dilcher, D. L., & Ren, D. (in review). Insect herbivory at the dawn of the angiosperm radiation. International Journal of Plant Sciences. Xu, Q., Jin, H., & Labandeira, C. C. (2018). Williamson Drive: Herbivory on a north- central Texas flora of latest Pennsylvanian age shows discrete component community structure, early expansion of piercing and sucking, and plant counterdefenses. Review of Palaeobotany and Palynology, 251, 28?72. Yang, M., Hu, B., Zhou, L., Liu, X., Shi, Y., Song, L., . . . Cao, J. (2019). First mitochondrial genome from Yponomeutidae (Lepidoptera, Yponomeutoidea) and the phylogenetic analysis for Lepidoptera. ZooKeys, 879, 137?156. Yuan, D., & Robinson, G. S. (1993). Caloptilia leaf-miner moths (Gracillariidae) of south-east Asia. Bulletin of the British Museum (Natural History), Entomology Series, 62(1), 1?37. Yukawa, J., & Akimoto, K. (2006). Influence of synchronization between adult emergence and host plant phenology on the population density of Pseudasphondylia neolitseae (Diptera: Cecidomyiidae) inducing leaf galls on Neolitsea sericea (Lauraceae). Population Ecology, 48(1), 13?21. Zanella, J., & Ferla, N. J. (2013). Influ?ncia das estruturas na abund?ncia de fitose?deos em plantas de ambiente natural do litoral norte do Rio Grande do Sul, Brasil. Revista Destaques Acad?micos, 5(3), 19?26. Zanno, L. E., Loewen, M. A., Farke, A. A., Kim, G.-S., Claessens, L., & McGarrity, C. T. (2013). Late Cretaceous theropod dinosaurs of southern Utah. In A. L. Titus & M. A. Loewen (Eds.), At the Top of the Grand Staircase: The Late Cretaceous of Southern Utah. Edited by AL Titus and MA Loewen. (pp. 504? 525). Bloomington, Indiana: Indiana University Press. Zhang, Q., & Wang, B. (2017). Evolution of lower Brachyceran flies (Diptera) and their adaptive radiation with angiosperms. Fronteirs in Plant Science, 8, 631. 31 3 Zhang, S.-H., Chen, T.-Y., Zeng, X., Yu, Y., Zhang, Y., & Xie, S.-P. (2018). Plant? insect associations from the upper Miocene of Lincang, Yunnan, China. Review of Palaeobotany and Palynology, 259, 55?62. Zhang, W., Shih, C., Labandeira, C. C., Sohn, J.-C., Davis, D. R., Santiago-Blay, J. A., . . . Ren, D. (2013). New fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of northeastern China. PLoS ONE, 8(11), e79500. 31 4