The Rise and Fall of the Dinosaurs

by Steve Brusatte

  Weishampel’s book Transylvanian Dinosaurs is also the single best general reference on the Transylvanian dwarfed dinosaurs. For a more technical overview, there is a series of papers edited by Zoltán Csiki-Sava and Michael Benton, published as a special issue of Palaeogeography, Palaeoclimatology, Palaeoecology in 2010 (vol. 293). Helpful review papers have also been written by Weishampel and colleagues (National Geographic Research, 1991, 7: 196–215) and Dan Grigorescu (Comptes Rendus Paleovol, 2003, 2: 97–101). I was part of a team led by Csiki-Sava who wrote a broader review of European latest Cretaceous faunas—there were actually several islands that dinosaurs lived on during this time, the Transylvanian one being the best studied and most famous (ZooKeys, 2015, 469: 1–161).

  Mátyás Vremir, Zoltán Csiki-Sava, Mark Norell, and I published two papers on Balaur bondoc: a short initial description in which we named it (Csiki-Sava et al., Proceedings of the National Academy of Sciences USA, 2010, 107: 15357–61) and a longer monograph in which we figured and described each bone in detail (Brusatte et al., Bulletin of the American Museum of Natural History, 2013, 374: 1–100). With other colleagues, we also wrote a more expansive paper on the age and importance of the Transylvanian dinosaurs, with an emphasis on new discoveries (Csiki-Sava et al., Cretaceous Research, 2016, 57: 662–98).

  CHAPTER 8: DINOSAURS TAKE FLIGHT

  This chapter covers many of the themes that I wrote about in a Scientific American article (Jan. 2017, 316: 48–55), as well as in a technical review paper on early bird evolution (Brusatte, O’Connor, and Jarvis, Current Biology, 2015, 25: R888–R898) and a commentary piece in Science (2017, 355: 792–94). Much of the impetus for this chapter came from my PhD work, on the genealogy of birds and their closest relatives and on patterns and rates of evolution across the dinosaur-bird transition. I defended my PhD in 2012 (The Phylogeny of Basal Coelurosaurian Theropods and Large-Scale Patterns of Morphological Evolution During the Dinosaur-Bird Transition, Columbia University, New York) and published it in 2014 (Brusatte et al., Current Biology, 2014, 24: 2386–92).

  There is a huge literature on the origin of birds and their relationships with dinosaurs. The best general readable sources of information are three review papers, written by Kevin Padian and Luis Chiappe (Biological Reviews, 1998, 73: 1–42), Mark Norell and Xu Xing (Annual Review of Earth and Planetary Sciences, 2005, 33: 277–99), and Xu Xing and colleagues (Science, 2014, 346: 1253293). Mark Norell’s book Unearthing the Dragon (Pi Press, New York, 2005) is one of my all-time favorites—a romping journey through China to study feathered dinosaurs, enlivened with the photography of one of the best artists in the dinosaur business, my buddy Mick Ellison. More recently, Luis Chiappe and Meng Qingjin’s Birds of Stone (Johns Hopkins University Press, 2016) is a beautiful atlas of feathered dinosaurs and primitive birds from China.

  Pat Shipman’s Taking Wing (Trafalgar Square, 1998) tells the tale of how scientists first recognized the dinosaur-bird link and the sometimes fierce debates as this once controversial hypothesis became mainstream. Huxley, Darwin, Ostrom, and Bakker are all covered here. Huxley laid out his theory on the dinosaur-bird link in a series of papers, including important ones published in the Annals and Magazine of Natural History (1868, 2: 66–75) and Quarterly Journal of the Geological Society (1870, 26: 12–31). Debates about Archaeopteryx are chronicled in Paul Chambers’s book Bones of Contention (John Murray, 2002), which cites most of the relevant literature up to the early 2000s; the description of a new specimen of Archaeopteryx by Christian Foth and colleagues has recently taken the field much further (Nature, 2014, 511: 79–82). It is one of the papers that has advocated for a display “billboard” origin of theropod wings. The “Danish artist” is Gerhard Heilmann, and he made his arguments in his book The Origin of Birds (Witherby, 1926).

  Robert Bakker has written the story of the Dinosaur Renaissance in a way that only he can, both in his Scientific American article (1975, 232: 58–79) and his book The Dinosaur Heresies (William Morrow, 1986). John Ostrom published a litany of careful scientific papers on the dinosaur-bird link, most important his meticulous monographic description of Deinonychus (Bulletin of the Peabody Museum of Natural History, 1969, 30: 1–165), his essay in Nature (1973, 242: 136), his review paper in Annual Review of Earth and Planetary Sciences (1975, 3: 55–77), and his masterful manifesto in Biological Journal of the Linnean Society (1976, 8: 91–182). It is also essential here to note that the pioneering cladistic analyses by Jacques Gauthier in the 1980s firmly placed birds among the theropods (e.g., in Memoirs of the California Academy of Sciences, 1986, 8: 1–55).

  The first feathered dinosaur—Sinosauropteryx—was initially described by Qiang Ji and Shu’an Ji as a primitive bird (Chinese Geology, 1996, 10: 30–33). It was then reinterpreted as a feathered non-bird dinosaur by Pei-ji Chen et al. (Nature, 1998, 391: 147–52) and later described in detail by Phil Currie (Currie and Chen, Canadian Journal of Earth Sciences, 2001, 38: 705–27). Soon after the realization that Sinosauropteryx was a feathered dinosaur, an international team announced two additional feathered dinosaurs from China (Ji et al., Nature, 1998, 393: 753–61), and the floodgates opened from there. The vast majority of feathered dinosaurs discovered over the past two decades have been described by Xu Xing and his colleagues, and are well summarized in Norell’s Unearthing the Dragon, as well as more recent literature cited in the review papers listed above. The preservation of the feathered dinosaurs, and the role of volcanoes in fossilizing them, has been studied by many authors, most recently and comprehensively by Christopher Rogers and colleagues (Palaeogeography, Palaeoclimatology, Palaeoecology, 2015, 427: 89–99).

  The assembly of the bird body plan has been discussed by many authors. I’ve written about it in my PhD thesis and the Current Biology paper stemming from it (see above). Pete Makovicky and Lindsay Zanno covered it in their very readable chapter in the book Living Dinosaurs (Wiley, 2011). The American Museum Gobi expeditions are chronicled in one of my favorite pop-science dinosaur books: Dinosaurs of the Flaming Cliffs (Anchor, 1996) by Mark Norell’s New York colleague, expedition coleader, and fellow SoCal surfer dude, Mike Novacek. Some of the more important research papers on the Gobi fossils—illustrating their importance in understanding the assembly of modern bird biology—have been the description by Norell et al. of the brooding oviraptorosaur (Nature, 1995, 378: 774–76) and the study by Balanoff et al. on the evolution of the bird brain (Nature, 2013, 501: 93–96). Background references on flow-through lungs and dinosaur growth have been outlined above, in the bibliography for previous chapters. The spectacular fossil of a dinosaur from Liaoning preserved in a birdlike sleeping posture was described by Xu and Norell (Nature, 2004, 431: 838–41), and the birdlike eggshell tissue was first identified in a dinosaur by Mary Schweitzer and colleagues (Science, 2005, 308, no. 5727: 1456–60).

  Dinosaur feather evolution has been the subject of a great amount of research and an expansive literature. The review of Xu Xing and Yu Guo (Vertebrata PalAsiatica, 2009, 47: 311–29) is a good starting point. For a developmental biology perspective on feather evolution, the many excellent papers of Richard Prum should be consulted. Darla Zelenitsky and her colleagues described their feathered ornithomimosaurs in 2012 (Science, 338: 510–14), and I gleaned details of their fieldwork from an October 25, 2012, article in the Calgary Herald. Jakob Vinther first presented his methodology for determining the colors of fossil feathers in a 2008 paper (Biology Letters 4: 522–25), which unleashed a number of studies by Vinther and others on feathered dinosaurs. All of this excitement is reviewed by Jakob in a review paper in BioEssays (2015, 37: 643–56) and a first-person piece in Scientific American (Mar. 2017, 316: 50–57). The flamboyant colors of early winged dinosaurs have been worked out by a Chinese-led team (Li et al., Nature, 2014, 507: 350–53), and the display function of wings has been discussed in a Science perspective piece by Marie-Claire Koschowitz and collaborators (2014, 346: 416–18). The wacky Yi qi was described by Xu and his team (Nature, 2015, 5
21: 70–73).

  There has been an enormous—and often complex—literature on the flight abilities of early birds and feathered dinosaurs. A recent study by Alex Dececchi and colleagues—who found that Microraptor and Anchiornis were potentially capable of powered flight—is a good jumping-off point (PeerJ, 2016, 4: e2159). Engineering studies by Gareth Dyke and colleagues (Nature Communications, 2013, 4: 2489) and Dennis Evangelista and colleagues (PeerJ, 2014, 2: e632) deal with gliding in feathered theropods and review the most important previous work.

  My colleagues and I presented our case for rapid rates of morphological evolution in early birds in a joint paper (Current Biology, 2014, 24: 2386–92). The methods we used in that paper were developed with Graeme Lloyd and Steve Wang and described in an earlier work (Lloyd et al., Evolution, 2012, 66: 330–48). Roger Benson and Jonah Choiniere also demonstrated a burst of speciation and limb evolution around the dinosaur-bird transition (Proceedings of the Royal Society Series B, 2013, 280: 20131780), and Roger Benson’s dinosaur body-size study (cited above) found the big decrease in size around this same point in the family tree. Many other recent studies have also looked at rates of evolution around the transition, and these are cited and discussed in the two above papers.

  Jingmai O’Connor has named a copious number of new fossil birds from China. Two of her most important works are her genealogy of early birds (O’Connor and Zhonghe Zhou, Journal of Systematic Palaeontology, 2013, 11: 889–906) and her chapter (with Alyssa Bell and Luis Chiappe) in the book Living Birds (cited above). Her PhD advisor, Luis Chiappe, has also published a number of important papers on early birds over the last quarter century.

  CHAPTER 9: DINOSAURS DIE OUT

  I wrote about the dinosaur extinction for Scientific American, where I first told some of the stories in this chapter (Dec. 2015, 312: 54–59). After Richard Butler and I gathered our group of international colleagues to sit down and try to come to a consensus on the dinosaur extinction, we published a status report in Biological Reviews (2015, 90: 628–42). Joining Richard and me were Paul Barrett, Matt Carrano, David Evans, Graeme Lloyd, Phil Mannion, Mark Norell, Dan Peppe, Paul Upchurch, and Tom Williamson. Additionally, Richard and I worked with Albert Prieto-Márquez and Mark Norell on our 2012 study of morphological disparity leading up to the extinction (Nature Communications, 3: 804).

  My contribution to the dinosaur extinction debate, however, has been tiny. There have been hundreds, maybe thousands, of studies published on this greatest of dinosaur mysteries. There is no way I can do justice to all of them here, so instead I’ll point inquisitive readers in the direction of Walter Alvarez’s book T. rex and the Crater of Doom (Princeton University Press, 1997). It is a readable, entertaining, and scrupulous first-person view of how Walter and his colleagues solved the riddle of the end-Cretaceous extinction. It cites all of the most important papers on the subject, including those that lay out the evidence for impact, those that identified and dated the Chicxulub crater, and various dissenting views. The story that I tell at the beginning of the chapter, although full of artistic license, is based on the sequence of impact events Alvarez describes and the evidence that he outlines.

  Much more work has been published since then, and much of this has been cited and discussed in our 2015 Biological Reviews paper. Some of the most exciting recent work—too recent to be discussed in our paper—is research by Paul Renne, Mark Richards, and their Berkeley colleagues that dates the Deccan Traps (the remnants of the big volcanoes in India), shows that most of the eruptions occurred right around the Cretaceous-Paleogene boundary, and argues that the asteroid impact may have kicked the volcanic system into overdrive (Renne et al., Science, 2015, 350: 76–78; and Richards et al., Geological Society of America Bulletin, 2015, 127: 1507–20). The timing of the Deccan eruptions and their relationship with the impact are still being debated as I write this.

  Of course, anyone who’s interested in the history of science and loves primary sources should check out the original paper in which the Alvarez team presented the asteroid theory (Luis Alvarez et al., Science, 1980, 208: 1095–1108), along with other papers from their team, and from Jan Smit and his colleagues around the same time.

  Many independent studies have tracked dinosaur evolution during the Mesozoic, and many of them focus particularly on the latest Cretaceous. In addition to the new data set we presented in our Biological Reviews paper, the other key recent studies were published by Barrett et al. (Proceedings of the Royal Society of London Series B, 2009, 276: 2667–74) and Upchurch et al. (Geological Society of London Special Publication, 2011, 358: 209–40). Modern studies try to correct for sampling bias, but this is an issue that wasn’t seriously recognized until a very important—but oddly, largely forgotten—paper by Dale Russell in 1984 (Nature, 307: 360–61). David Fastovsky, Peter Sheehan, and their colleagues grasped the lesson from this paper and published a very important study of latest Cretaceous dinosaur diversity in the mid-2000s (Geology, 2004, 32: 877–80). Jonathan Mitchell’s ecological food-web study was presented in a 2012 paper (Proceedings of the National Academy of Sciences USA, 109: 18857–61).

  The most important studies of Hell Creek dinosaurs and how they were changing in the lead-up to the asteroid impact include those by Peter Sheehan and David Fastovsky’s team (Science, 1991, 254: 835–39; Geology, 2000, 28: 523–26), Tyler Lyson and his colleagues (Biology Letters, 2011, 7: 925–28), and the meticulous fossil catalogs of Dean Pearson and his collaborators, who include Kirk Johnson and the late Doug Nichols (Geology, 2001, 29: 39–42; and Geological Society of America Special Papers, 2002, 361: 145–67).

  Fastovsky’s undergraduate textbook, the subject of my praise in passing, is the excellent Evolution and Extinction of the Dinosaurs (Cambridge University Press), which was coauthored with David Weishampel. The book has gone through several editions, and is also available in a shorter and punchier version for younger students, called Dinosaurs: A Concise Natural History.

  Bernat Vila and Albert Sellés have written many papers on the latest Cretaceous dinosaurs of the Pyrenees. The most general of these is a study of how dinosaur diversity changed in this region during the latest Cretaceous, a project that they generously invited me to contribute to (Vila, Sellés, and Brusatte, Cretaceous Research, 2016, 57: 552–64). Other important papers include Vila et al., PLoS ONE, 2013, 8, no. 9: e72579, and Riera et al., Palaeogeography, Palaeoclimatology, Palaeoecology, 283: 160–71. When it comes to Romania, the end-Cretaceous story is covered in the papers cited for chapter 7 above. Finally, Roberto Candeiro, Felipe Simbras, and I have written a paper summarizing the latest Cretaceous dinosaurs of Brazil (Annals of the Brazilian Academy of Sciences 2017, 89: 1465–85).

  The question of why non-bird dinosaurs died, while other animals survived remains an active subject of debate. To my mind, the most important insights have been articulated by Peter Sheehan and his colleagues on the subject of plant- versus detritus-based food chains and land versus freshwater environments (e.g., Geology, 1986, 14: 868–70; and Geology, 1992, 20: 556–60); by Derek Larson, Caleb Brown, and David Evans on the subject of seed-eating (Current Biology, 2016, 26: 1325–33); by Greg Erickson and his team on the issue of egg incubation and growth (Proceedings of the National Academy of Sciences USA, 2017, 114: 540–45); and by Greg Wilson and his mentor Bill Clemens regarding mammal survivorship and the importance of small body size and generalist diets (e.g., Wilson’s papers in Journal of Mammalian Evolution, 2005, 12: 53–76; and Paleobiology, 2013, 39: 429–69). An important paper by Norman MacLeod and colleagues is a good review of what lived and what died at the end of the Cretaceous, and what that may mean for kill mechanisms ( Journal of the Geological Society of London, 1997, 154: 265–92).

  I love the analogy of dinosaurs holding a “dead man’s hand.” I wish I could say I came up with it myself, but it was Greg Erickson who (as far as I know) first used it, in a quote in Carolyn Gramling’s news article on his egg incubation study (“Dinosaur Babies Took a Long T
ime to Break Out of Their Shells,” Science online, News, Jan. 2, 2017).

  One further important caveat is necessary. The dinosaur extinction is probably the most controversial subject in the history of dinosaur research—at least judging by the number of hypotheses, research papers, debates, and arguments. The scenario that I present in this chapter—that the extinction happened suddenly and was primarily caused by the asteroid—stems from my own deep reading on the subject, my own primary research on latest Cretaceous dinosaurs, and in particular from the big communal consensus that we outlined in our Biological Reviews paper. I firmly believe that this scenario is most consistent with the evidence that we have, both in terms of the geological record (the evidence for a catastrophic impact is undeniable) and the fossil record (studies showing that dinosaurs were still quite diverse right up until the end).

  There are, however, those with alternative views. The point of this chapter is not to dissect each and every theory on the dinosaur extinction—that could easily be the subject of an entire book—but it is worth giving some directions to literature that argues against my version of the extinction. For many decades, David Archibald and William Clemens have argued for a more gradual extinction, caused by changes in temperature and/or sea level; Gerta Keller and her colleagues have argued that the Deccan eruptions were the primary culprit; and more recently, my friend Manabu Sakamoto has used complex statistical models to make the iconoclastic claim that dinosaurs were in a long-term decline, in which they were producing fewer and fewer species over time. Dive into this literature to learn more, and decide for yourself where the preponderance of evidence lies. There are other skeptical or dissenting views as well, but that’s all I’ll have to say about that.