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Integrative and Comparative Biology Integrative and Comparative Biology, volume 56, number 5, pp. 1044–1046 doi:10.1093/icb/icw115 Society for Integrative and Comparative Biology Book Review On the Wing: Insects, Pterosaurs, Birds, Bats and the Evolution of Animal Flight David E. Alexander. New York, NY: Oxford University Press, 2015. 210 pp. ISBN 978-0-19-999677-3 (hardcover), $29.95 Introduction Flying animals have captivated public attention for at least as long as there have been written records. Powered flapping flight is one of the most energetically costly behaviors in the animal kingdom, yet due to the low cost of transport of flight relative to running and walking, it can be an efficient way to move (Schmidt-Nielson 1972). Evolutionarily, flapping flight has evolved four times: in bats, birds, pterosaurs, and insects. Many animal flight experts are only peripherally aware of the flying taxa they do not study; thus, it is nice to see all four groups being treated together in the same book. On the Wing: Insects, Pterosaurs, Birds, Bats and the Evolution of Animal Flight, by David E. Alexander, is composed of 10 chapters—three introductory chapters on flight and then one chapter apiece on gliding animals, each of the four taxa that have evolved powered flapping flight, and secondarily flightless animals, plus a conclusion. It is aimed at the general public and does an excellent job of explaining difficult concepts such as phylogenetics and induced drag in layman’s terms; however, it has enough ‘‘depth’’ to be required reading for any individual who wishes to learn more about animal flight—whether for personal or professional reasons. For some flight researchers, the enjoyment of this book will hinge on the fact that it argues for a gliding origin of powered flapping flight in all four lineages. Many scientists, particularly ornithologists and entomologists, disagree (e.g., Medved et al. 2015; Heers et al. 2016). Alexander uses results from studies of theoretical modeling and flapping robots to suggest that gliding and flapping may be opposite ends of a continuum rather than two completely separate modes of flight. Furthermore, bats and pterosaurs are widely accepted to have evolved from gliding ancestors, and there have long been gliding-origin hypotheses for birds (e.g., ‘trees-down’) and insects. With the discovery of Microraptor gui, a gliding dromaesaurid, and increasing evidence that flight evolved in terrestrial, not aquatic, insects, Alexander concludes that powered flapping flight has always evolved from gliding. He does point out that any such argument is controversial, because all modern animals are either pure gliders or powered flappers (which, if large enough, also have the ability to glide). The lack of any extant animal that flaps just a little bit to help control its primarily gliding behavior is a problem with this hypothesis—but, to be fair, there are counterarguments for all of the current hypotheses regarding the origin of powered flapping flight. The book does present these alternatives, particularly the wing-assisted incline running (WAIR) hypothesis for birds and the surfaceskimming hypothesis for insects, although each of these arguments is dismissed in favor of a gliding to flapping transition. However, if one is openminded enough to at least consider the possibility that powered flapping flight always evolves from gliding, this book is up-to-date and informative. In terms of the book’s readability, members of the general public may have to look up a few words to thoroughly understand it; while scientific jargon involving flight is mostly avoided (‘parasite drag’) and explained when it cannot be avoided (‘lift:drag ratio’), a few overly scientific terms (‘extant’) do slip through. However, someone with an undergraduate degree in science should have no trouble with the text. Moreover, Alexander has a clear and comfortable writing style that draws the reader in and makes them want to continue reading. Section 1: flying, flapping, and gliding Although the book itself is not divided into sections, there is a natural division between the first three chapters and the next six chapters plus the conclusion. The book starts by exploring the ‘‘wow’’ factor of flight: what animals fly fastest, furthest and highest. Chapter 2 briefly discusses the physiology of flight and then provides an in-depth description of the wing structure of the four lineages with powered flapping flight. The third chapter examines the physics of flight, including lift, drag, camber and wing Advanced Access publication August 31, 2016 ß The Author 2016. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Book Review stroke kinematics. It also includes a section on gliding flight that sets up the argument that powered flapping flight always evolves from gliding. The introductory section is unique because Alexander does not just rely on examples of one or two flying lineages. For example, ornithologists who know exactly which animal is going to win the ‘how far?’ section can still be impressed by the feats of honeybee workers making foraging flights. It is clear from the outset that Alexander plans to discuss all four groups of powered flapping flyers equally, and he does an admirable job, both in the introductory section and later in the book. Several arguments are, however, overstated in the introductory section, such as that ‘‘air properties do change a bit with size but are fundamentally the same for all animals.’’ In the book’s defense, these arguments are softened later in the book; in the chapter on insects, for example, Alexander discusses the wings of tiny insects and why they do not look anything like the wings of larger insects. Another issue with this section is that a few aspects of Chapter 2’s discussion of muscles are inaccurate. Lactic acid is not a harmful waste product, as we once thought; in fact, it can actually be a substrate for aerobic metabolism (Mann 2007). Furthermore, both carbohydrates and fats can be broken down to provide the molecules that the body uses for aerobic and anaerobic metabolism. It is thus misleading to state that aerobic metabolism depends on fat and anaerobic metabolism relies on carbohydrates. Chapter 3 explains how animals fly and glide. From clear diagrams showing that animals do not just flap their wings straight up and down (as many students think) to a strong, understandable argument that camber is not the be-all and end-all of flight (thus explaining why Bernoulli’s equations do not tell the whole story of flight), this chapter is a home run. People who know almost nothing about physics will be able to understand how flight works through Alexander’s use of well-chosen metaphors and examples. For example, readers are invited to ‘‘fly’’ their hand out of a car window the next time they are a passenger, and change the angle of attack to feel changes in lift and drag. Section 2: flighted (and flightless) animals Section 2 contains separate chapters for gliding animals, each of the four lineages with powered flapping flight, and flightless animals. The gliding chapter has just a few minor issues; in particular, it is relatively heavy on herpetofauna and light on mammals. 1045 Unfortunately, it also gives flying fish relatively short shrift, citing a paper from 1995 instead of a more recent analysis of lift:drag ratios of the pectoral fins (wings) in these animals (Park and Choi 2010). In terms of the chapter on insects (Chapter 5), non-entomologists will likely wish the relevant phylogeny (Figure 5.4) was presented earlier, when the different taxa are first referenced. It may also be difficult for non-entomologists to tell the difference between the historical ‘‘gill theory’’ hypothesis described here and Marden’s surface-skimming hypothesis; the latter seems to be an updated version of the former, albeit with a more plausible mechanism for how a gill could evolve into a wing. Aside from these two minor issues, however, this chapter is easily one of the best discussions of insect flight and its evolution available. Given how controversial the evolution of bird flight is, it is no surprise that Alexander’s chapter on birds (Chapter 6) contains a few controversial statements. For example, the WAIR hypothesis is quickly dismissed, without reference to more recent discussions (e.g., Heers and Dial 2012). Also, a key part of the book’s argument for a gliding origin of avian flight is that a dromaesaurid (Microraptor gui) was a glider; according to Alexander, it is thus inappropriate to say that all theropods (including any direct ancestors of birds) were cursorial so birds must have evolved from cursorial ancestors. While this is true, it is still fair to say that the vast majority of described theropods were cursorial, making it more likely (although not certain) that avian flight evolved in cursorial, and not arboreal, animals. (Full disclosure: this reviewer feels that the WAIR hypothesis best explains the evolution of avian flight.) Chapter 7 discusses the origin of flight in bats. Here, few scientists question a gliding origin for flight. Several common misconceptions about bats are corrected in this chapter, such as that ‘‘microbats’’ and ‘‘megabats’’ evolved flight (and other features) separately. At the end of the chapter, Alexander provides a stimulating discussion of echolocation and its interaction with flight in bats. Unfortunately, a study published after Alexander’s book showed that the story of echolocation and flight in bats may not be as clear-cut as the book describes because of the rapid expansion of bats following their initial evolution (Hahn and Nakhleh 2016). The pterosaur chapter (Chapter 8) is fascinating, although Alexander shows Soemmerring’s bat-like reconstruction of a pterosaur—odd, given that, as he argues, it has long misled scientists into thinking pterosaurs were bat-like; why perpetuate the 1046 image? It would perhaps have been preferable to show images of fossils with the wing membranes clearly preserved as well as fossils of pterosaur trackways showing them walking on all fours. Chosen figures aside, Alexander does an excellent job of calling attention to areas of pterosaur flight that need additional study, such as the enormous range of body size within this lineage (and within species). The final two chapters are on secondary flightlessness and unifying themes. The first of the two chapters is (arguably) missing a short discussion of vampire bats’ secondarily-gained ability to ‘‘run’’ (Riskin and Hermanson 2005), but is an enjoyable read nevertheless. In the final chapter is a wellreasoned argument why bats and pterosaurs are generally accepted to represent gliding-to-flying transitions: they look like typical gliding animals, with a membrane stretched in between their limbs on either side. Birds and insects, conversely, have wings that do not look as if they arose from a gliding membrane, which is likely one reason why there is more controversy surrounding the origin of flight in these taxa. At the very end of this chapter, Alexander takes the opportunity to point new (and old) animal flight researchers in interesting and productive new directions. Overview Minor quibbles aside, On the Wing: Insects, Pterosaurs, Birds, Bats and the Evolution of Animal Flight, is an excellent book. It is extremely well-written, and balances discussion of all four taxa like no Book Review other published treatise on animal flight. Moreover, it is accessible to the general public while still providing enough depth (and appropriate references) for anyone who wants to further examine the evolution of flight. This book is a must-read for all graduate students who plan to work on the evolution or biomechanics of flight, regardless of what lineage(s) they study. Melissa S. Bowlin Department of Natural Sciences, University of Michigan-Dearborn E-mail: [email protected] References Hahn MW, Nakhleh L. 2016. Irrational exuberance for resolved species trees. Evol 70:7–17. Heers AM, Dial KP. 2012. From extant to extinct: locomotor ontogeny and the evolution of animal flight. TREE 27:296– 305. Heers AM, Baier DB, Jackson BE, Dial KP. 2016. Flapping before flight: high resolution, three-dimensional skeletal kinematics of wings and legs during avian development. PLoS ONE 11:e0153446. Medved V, Marden JH, Fescemyer HW, Der JP, Liu J, Mahfooz N, Popadić A. 2015. Origin and diversification of wings: insights from a neopteran insect. PNAS 112:15946–51. Mann T. 2007. Sporting myths: the REAL role of lactate during exercise. SAJSM 19:114–16. Park H, Choi H. 2010. Aerodynamic characteristics of flying fish in gliding flight. J Exp Biol 213:3269–79. Riskin DK, Hermanson JW. 2005. Biomechanics: independent evolution of running in vampire bats. Nature 434:292. Schmidt-Nielsen K. 1972. Locomotion: energy cost of swimming, flying, and running. Science 177:222–8.