Chapter 10 Methods of studying early theropod flight

The study of early theropod flight involves avialans as well as other pennaraptorans. It requires the study of anatomy that is familiar to the modern ornithologist, but also very different and alien. Early theropod flight therefore necessitates study methods that can incorporate what we know about sophisticated powered and unpowered flight in living birds while being mindful of the differences between them and the earliest theropod flyers. In this chapter we will survey key methods and approaches, covering their best-practice applications along the timeline of early theropod flight evolution and priorities for future method development. 1 Vertebrate Palaeontology Laboratory, Division of Earth and Planetary Science, the University of Hong Kong, Hong Kong. 2 College of Natural and Social Sciences, California State University, Los Angeles. 3 Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles; and Real Academia Ciencias Exactas, Físicas y Naturales, Madrid. 4 Department of Earth Sciences, University of Cambridge, Cambridge. 5 Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles. 6 Division of Natural Sciences, Mount Marty College, Yankton, SD. 7 Foundation for Scientific Advancement, Sierra Vista, AZ. 8 Redpath Museum, McGill University, Montreal. INTRODUCTION Locomotion plays a central role in the lives of most vertebrates, and reconstructing locomotor behaviors of extinct taxa is key to understanding some major evolutionary transitions—for example, the origin of walking tetrapods or swimming whales. But how do we reconstruct locomotion in extinct taxa when it is very difficult to compare them to modern forms? When trying to decipher early theropod flight, researchers are faced with substantial anatomical differences between modern flying birds like pigeons and early birds like Archaeopteryx as well as their closely related nonavialan relatives. In particular, extant volant birds have a large keel on the sternum, which anchors two main flight muscles, the pectoralis for downstroke and the supracoracoideus for upstroke (George and Berger, 1966). Though the supracoracoideus is in a ventral position, it is 278 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY NO. 440 few anatomical features, such as feathers and/or wings (e.g., Burgers and Chiappe, 1999; Nudds and Dyke, 2010; Chiappe et al. 2019), tails (e.g., Gatesy and Dial, 1996; Gatesy, 2001; Pittman et al., 2013), the shoulder (e.g., Jenkins, 1993; Baier et al., 2007; Navalón et al., 2018), or the supracoracoideus muscle (e.g., Poore et al., 1997b). Recent efforts to leverage the locomotor variation among nearly 11,000 living species (Prum et al., 2015; Gill and Donsker, 2017) using large-scale datasets to characterize aspects of the avian flight apparatus have begun to bear fruit. New analytical techniques are showing that yet more high-fidelity flight-related soft-tissue details are hidden in the very best preserved pennaraptorans, especially those from China (Falk et al., 2016; Wang et al., 2017; see Serrano et al., chap. 13). Advancements in early flight studies have greatly benefited from the evolutionary context provided by a range of detailed phylogenetic analyses, the details of which are provided by Pittman et al. in chapter 2. Large-scale Avian Anatomical Datasets: Seminal datasets like those by Greenewalt (1975) or Hartman (1961) have been extremely helpful in informing our understanding of early theropod flight (e.g., Dececchi et al., 2016; Pei et al., in press), but their use has generally fallen out of favor in recent times. The reason for this may be that these datasets are often created from amalgamations of other datasets or sources, so that specific specimens are rarely scored for all relevant measurements (Hartman, 1961; Greenewalt, 1975). A new generation of studies has begun to broach this data gap to quantify anatomical variation for key modules of the flight apparatus by using large comparative samples that draw on the majority of avian higher-order subclades. These studies have begun to yield form-function relationships that may provide new lines of investigation into early flight. This includes work on the furcula (Close and Rayfield, 2012) as well as on flight feathers (Feo et al., 2015) and skeletal proportions (Field et al., 2013; Serrano et al., 2015). Feathers are among the most characteristic avian specializations, but quantitative compariable to elevate and supinate (Poore et al., 1997a; Tobalske and Biewener, 2008) the wing because it loops through a donut-shaped triosseal canal and attaches to the dorsal surface of the humerus, similar to a pulley. Archaeopteryx, in contrast, has no triosseal canal and no ossified sternum, but some early avialans and possibly volant nonavialan pennaraptorans have either feature or both in an incipient form (Zhou and Zhang, 2002; Xu et al., 2003; Baier et al., 2007; Dyke et al., 2013; Zheng et al., 2014; Pei et al., in press). Consequently, at least some of the flight muscles of many early avialans and suspected volant nonavialan pennaraptorans were probably not very large, and would have had different configurations compared with extant birds. What does that mean in terms of the locomotor capacity of early birds and some nonavialan pennaraptorans? The study of early theropod flight engages tailored methodologies with their own emphases to address the spectrum of form-function differences along the line of descent from the first theropod flyers to modern living ones. Theropod aerial locomotion seems to have multiple origins, the study of which involves anatomy that is very different to modern birds. At the other end of the theropod flight timeline, the origin of avian flight involves looking at a much more refined set of flight-related avian features that allowed birds to adopt different flight styles, but not the sophisticated powered flight of living birds. In this chapter we will survey key methods and approaches adopted in studying early theropod flight, detailing their best practice applications to the facets of this iconic field of pennaraptoran paleontology. FORM-FUNCTION RELATIONSHIPS Substantial efforts to characterize the morphology of early pennaraptoran theropods and investigate their relationship with flight function continue to greatly advance our knowledge of early theropod flight. This ranges from numerous studies assessing the functional morphology of single taxa (Navalón et al., 2015; Xu et al., 2015; Wang et al., 2017) to work focusing on one or a 2020 PITTMAN ET AL.: METHODS OF STUDYING EARLY THEROPOD FLIGHT 279 sons between flight-feather morphology in living and extinct total-clade birds are hampered by the rarity of intact fossil feathers and the preservation difficulty posed by their flexible feather vanes. A large comparative dataset examining feather-barb geometry was successfully generated and used to characterize macroevolutionary patterns in barb arrangement across the crown bird tree of life (Feo et al., 2015). Among other observations, this study observed that crown birds exhibit characteristic barb-to-rachis attachment angles on the leading and trailing edges of flight feathers (Feo et al., 2015). Primary feather barbs on a wing’s leading edge that cut into the air during flight connect to the rachis at narrow attachment angles, providing a relatively inflexible airfoil for stability during flight, whereas barbs on the trailing edge of flight feathers connect to the rachis at broad angles of attachment, providing a more flexible vane in order to maintain a coherent wing surface through feather-tofeather contact. These patterns are generally conserved across crown birds. In contrast to this pattern, deinonychosaurians, like Microraptor, and early-diverging volant avialans, like Archaeopteryx, Confuciusornis, and Sapeornis, exhibit trailing edge barbs with angles of attachment indistinguishable from the narrow angles of FIG. 1. Flight feather morphology across paravian phylogeny (modified from Feo et al., 2015). Early-diverging taxa (indicated by dashed pink lines) exhibit flight feather trailing edges characterized by narrow angles of barb-to-rachis attachment. The crownlike condition (broad angles of barb-to-rachis trailing edge attachment; blue dashed lines) arose on the internode subtending Ornithothoraces, and may have conferred a more flexible trailing edge of the wing during flight in order to increase feather-to-feather contact and maintenance of a coherent wing surface in flight during active downstrokes. Silhouettes from phylopic.org. Microraptor Archaeopteryx Sapeornis Confuciusornis Eopengornis Aves