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The inner : and Darren Naisha a School of Earth & Environmental Sciences University of Portsmouth, Portsmouth, UK

First published on: 23 November 2010

To cite this Article Naish, Darren(2010) 'The inner bird: anatomy and evolution', Historical Biology,, First published on: 23 November 2010 (iFirst) To link to this Article: DOI: 10.1080/08912963.2010.506741 URL: http://dx.doi.org/10.1080/08912963.2010.506741

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BOOK REVIEW

The inner bird: anatomy and evolution, by Gary W. The anatomy and function of , their evolution- Kaiser, University of British Columbia, 2007, 386 pp., ary origins and their distribution in form the ISBN 978-0-7748-1344-0 subject of the third and final section. Kaiser uses his knowledge of modern bird aerodynamics and flight Good, non-technical books on anatomy are rare; good, behaviour to look anew at , confuciusor- non-technical books on avian anatomy are just about non- nithids, enantiornithines (‘ball-shouldered ’ of his existent. Gary Kaiser’s The Inner Bird: Anatomy and usage) and other birds, and the final chapter in this Evolution stands out as one of a kind – it is not brand new section – that on the structure and function of marine (having been published in 2007), but still has yet to be birds – is one of the best in the book. A glossary and widely recognised as the valuable piece of scholarship that numerous graphs, tables and diagrams are included, and it is. I will state here at the outset that I cannot recommend the text is fully referenced. it highly enough. The volume takes its title from one of Kaiser’s most Containing a wealth of information that ranges from profound intellectual proposals: the notion that neor- the Mesozoic ancestry of birds to neornithine phylogeny, nithine birds are ‘puppeteers that hide behind a screen of flight dynamics, functional and ecology, it feathers’; creatures that have evolved a highly novel body should be sought out and consulted avidly by anyone plan for . Neornithines are, generally speaking, seriously interested in avian anatomy and evolution. small, fragile, thin-limbed , protected and covered Kaiser’s volume not only serves as both a wide-ranging by an extensive ‘environmental suit’ formed from their introduction and review but also includes new data and integument and with only a few of their extremities truly several interesting new hypotheses. The author also exposed to the elements. This is the ‘inner bird’ body challenges widely held ideas where appropriate and brings plan, and it has enabled some birds to make a living from attention to the fact that erroneous, highly dated views on freezing cold oceans, to live for months on end on the avian anatomy and function are still being promoted. The and to become one of the most successful Inner Bird is also eminently readable: it is not a textbook. clades in a multitude of terrestrial and aquatic habitats. The book begins with an introduction to avian anatomy As Kaiser puts it, neornithines have come a long way (covering both structure in general, and the many from their ancestors. Extensive hands-on experience of north Pacific skeletal and soft tissue peculiarities of the different bird , and others provide Kaiser with a groups) and then compares and contrasts modern practical, grounded perspective. Among the best bits of (neornithine) birds with their dinosaurian ancestors. the book are those on the ecomorphology, behaviour and There is a huge amount of information here that has not breeding biology of the birds that frequent the Pacific been distilled before. Kaiser’s discussions of such areas as

Downloaded By: [Naish, Darren W] At: 20:56 23 November 2010 northwest, among them sea and . Unless you sesamoid distribution and function, neck mobility, the are a specialist on these birds, much of what Kaiser says form of the lumbar–synsacrum junction, chewing will be novel. He writes of bald eagles Haliaeetus behaviour and bill morphology in and , leucocephalus that have learnt to prowl about on the forest the possible role of the glycogen body and the massive floor at night in quest of auks returning to their nests and variation seen in furcular anatomy among neornithines are alludes briefly to humanity’s many disgusting abuses of extremely welcome. seabirds for artillery practise, pet food and leather. An A second section begins with a review of the history of explosion of research on the biology of the marbled avian classification and is then devoted to a discussion of murrelet Brachyramphus marmoratus during the 1990s avian phylogeny. Kaiser spends a lot of time on demonstrated – contrarily to received wisdom – that and focuses on ambiguity and murrelets and other small auks were far from weak-flying disagreement more than their opposites. He also uses this ‘proto-’, but extremely fast, powerful, highly as an opportunity to examine the wonderful but always mobile exploiters of the marine prey that they rely on. annoying Opisthocomus hoazin. The amazing Kaiser makes the argument that they are in fact among the anatomy and controversial phylogenetic position of this most specialised of birds and that we should marvel at their South American bird evidently fascinate the author and he ‘exploitation of power and seemingly extravagant returns to it many times over, also featuring it and its expenditures of energy’ (p. 324). In similar vein, he on the cover. argues that and divers should not be dismissed as

ISSN 0891-2963 print/ISSN 1029-2381 online DOI: 10.1080/08912963.2010.506741 http://www.informaworld.com 2 Book Review

poor fliers (as textbooks and tradition would have it), but Greg Paul, now argue that bird-like maniraptorans are that they might be considered the avian equivalents of flightless birds. They continue to argue, however, that this Boeing 747s and other avionic workhorses: able to carry ‘expanded Avialae/Aves’ is nothing to do with Dino- large payloads for great distances at high speeds, despite sauria!). Accordingly, a reasonable interpretation of the an energetically costly take-off. fossil record is that birds were, originally, only one Kaiser is convinced by the evidence for the maniraptoran lineage among many: nothing special and not dinosaurian , and long sections of the obviously destined for phenomenal success. book are devoted to discussing the similarities and Worth noting is that Kaiser is a bit out of date in saying differences seen between birds and their non-avian that Archaeopteryx is older than all of its closest non-avian relatives. The notion that birds cannot be dinosaurs is relatives. Even prior to 2007, numerous (admittedly heavily promoted in the ornithological literature – most scrappy) remains demonstrated the presence of non-avian notably in ’s The Origin and Evolution of maniraptorans older than Archaeopteryx. Pedopenna –a Birds (Feduccia 1996). Because Feduccia’s book is one of Middle bird-like maniraptoran with long hindlimb the most visible of volumes on bird evolution, audiences feathers – was described in 2005 (Xu and Zhang 2005). can be forgiven for thinking that ornithologists as a whole Several additional, recently described feathered manir- reject the hypothesis of a dinosaurian ancestry for birds. aptorans can now be said to pre-date Archaeopteryx, This is absolutely not true, and those interested should take including Anchiornis, Epidendrosaurus and Epidexipteryx. every opportunity to note that all of Feduccia (et al.’s) While I am extremely happy that Kaiser tackled criticisms are invalid or erroneous (e.g. that non-avian Mesozoic birds and other dinosaurs so extensively (and theropods are too big to be ancestral to birds, that they while his insights and hypotheses are excellent, insightful occur too late in the fossil record, that their anatomy bars and thought provoking), his work would definitely have them from avian ancestry and that other Mesozoic reptiles benefited from a check by a worker who specialises on make better potential bird ancestors). It is also worth these animals. In one section, the four-winged dromaeo- noting that many of Feduccia’s proposals about the saur is repeatedly referred to as Eoraptor: the phylogeny of neornithines are idiosyncratic and that his latter is an early predatory from the of volume does not accurately represent current thinking on Argentina; it is not closely associated with avian ancestry. avian evolutionary history. The Inner Bird helps provide Protoavis (a highly controversial fossil from the Triassic part of the antidote, bringing home the point that the of Texas thought by its describer to be a bird more closely dinosaurian origin of birds is well supported and robust related to neornithines than is Archaeopteryx) is wrongly and widely adopted by many ornithologists interested in and consistently called ‘Protavis’, and quite a few palaeontology. other names are spelt incorrectly too. The reference to Indeed, if anything is clear from the explosion of Rahonavis from Madagascar as a close relative of recently described feathered maniraptoran theropods Archaeopteryx ignores recent evidence showing that it is (virtually all of which are from Province in more likely one of the unenlagiine dromaeosaurs. Kaiser is China), it is that the early members of several of the key incorrect in suggesting that Archaeovolans (see below) groups (oviraptorosaurs, epidendrosaurs, troodontids and might be synonymous with Arctosaurus: the former is a

Downloaded By: [Naish, Darren W] At: 20:56 23 November 2010 dromaeosaurids) were all extremely similar to the earliest Chinese bird from the , while the latter is an birds. All were small, feathered, leggy omnivores or indeterminate archosauromorph named for a single neck predators with long arm and tail feathers and delicate, from the Triassic of Canada; they have never been toothed . In fact these little maniraptorans are so linked to my knowledge. similar that the members of the different lineages are Greg Paul’s proposal that deinonychosaurs and other sometimes wrongly allocated. The early troodontids non-avian maniraptorans may have been secondarily Anchiornis and Jinfengopteryx, for example, were flightless is not, as Kaiser implies, the same as the ‘birds originally described as birds, and it has proven increasingly come first’ hypothesis. The latter notion, developed by difficult to find reliable characters that distinguish writer–researcher George Olshevsky, proposes that small Archaeopteryx from non-avian maniraptorans. Analyses size and a scansorial lifestyle evolved early on in that incorporate good taxonomic and character sampling , that all dinosaurs are the direct descendants still find Archaeopteryx to be part of the bird branch within of such ancestors and that one dinosaur lineage – Aves – (e.g. Norell et al. 2001), but it is far from is unique in retaining these ancestral features. inconceivable that Archaeopteryx could prove to be on the It is also rather misleading to imply or state that deinonychosaur branch or that deinonychosaurs could be ‘Archaeoraptor’ (a faked composite specimen, showcased on the bird branch. This makes a mockery of the idea that in 1999 by National Geographic as a new intermediate in deinonychosaurs are somehow fundamentally different Mesozoic bird evolution) ‘took the professional commu- from birds (this is what Feduccia and colleagues argued nity by surprise’ (p. 221). The authenticity of this fossil until recently. They have since rescinded this and, like was in fact doubted from the start: I mentioned these Historical Biology 3

doubts to the fossil’s describer (Stephan Czerkas of The might be predictable that any book published in 2007 will Dinosaur Museum in Utah) on the very day of its debut, be woefully out of date on this subject. That is not but was reassured that any concerns were unwarranted! obviously true (though read on): Kaiser promotes the view Czerkas later described one half of ‘Archaeoraptor’ (as throughout that palaeognaths are outside a clade that Archaeovolans repatriatus) in his 2002 volume Feathered includes all neognaths and that neognaths consist of Dinosaurs and the Origin of , ostensibly volume 1 of Galloanserae (waterfowl and game birds) and everything a peer-reviewed publication emanating from The Dinosaur else (properly termed ). This is the ‘consensus Museum (Archaeovolans is now thought to be synon- view’ on neornithine phylogeny, and it is well supported. ymous with martini, named in 2001). Kaiser is The relationships within Neoaves have proved more highly critical of this volume, noting that its contents ‘read problematic. Kaiser is partial to the (new at the time of his somewhat like the technical discussions posted on the writing) proposal that Neoaves might consist of a Internet, and they lack a tone of detached objectivity paucispecific, mostly Southern Hemisphere and characteristic of publications with a longer history’ a much larger Coronaves (Fain and Houde 2004). Some (pp. 221–222). These views very much echo those made additional support for a group something like Metaves was elsewhere in the technical research community and, in my provided by Hackett et al. (2008). However, Morgan- opinion at least, it is good to have them on record. Richards et al. (2008) argued that the data used to support These minor quibbles aside, one aspect of Kaiser’s the monophyly of Metaves were suspect and that its approach to the dinosaurian ancestry of birds is constituents (, pigeons, , flamingos, problematic, namely, his implication that ‘birds’ and swifts, , , , grebes and ‘dinosaurs’ can and should be clearly differentiated. He ) were scattered about the neoavian . notes at the start (p. 1) that he opts to restrict the term Interestingly, Kaiser is slightly critical of Livezey and ‘bird’ to those feathered animals that fly, and the term Zusi’s enormous morphological analysis (Livezey and ‘dinosaur’ to those non-flying forms that may or may not Zusi 2007), in part, because this study supported the have feathers. I can understand that this convention seems monophyly of alleged groupings that seem hard to accept. to make life simpler if you are only worrying about literary Ironically, these are mostly ‘traditional’ and Livezey and style, but it is misleading. Zusi’s results are conservative compared to several other For one, it implies that birds are fundamentally recently published phylogenies. Divers and grebes are different from other dinosaurs. Those many little feathered perhaps the most notorious of the alleged groupings they theropods and the anatomy of birds and other theropods in supported: it is difficult not to assume from the outset general, show that birds are dinosaurs no matter how (as Kaiser does) that any similarities seen between these offensive this might seem to traditional usage of those two are the result of convergence, and that some of the terms. As noted above, early birds – archaeopterygids and more profound differences between the two reveal distinct other archaic, long-tailed forms, in particular – can no origins. Some other ornithologists have expressed a longer be rightfully regarded as unusual compared to other similar dissatisfaction with Livezey and Zusi (2007): Mayr maniraptorans. Birds are different from other dinosaurs, (2008) argued that, for all its size, the conclusions of this but the peculiarities that we have in mind when we say analysis were misled by a low ‘signal-to-noise’ ratio.

Downloaded By: [Naish, Darren W] At: 20:56 23 November 2010 such things are almost entirely unique to neornithines: it is Kaiser proclaims early on in the book that molecular wiser to say, then, that it is not that birds are different from techniques have failed to produce a good phylogeny for other dinosaurs; it is that neornithines are different from modern birds, and he also notes that the results of such other dinosaurs. studies have proved contradictory. These assertions are Second, the idea of differentiating ‘birds’ and arguable, though one might say that ‘convincing’ ‘dinosaurs’ based on flight ability does not work given molecular phylogenies for Neornithes have only appeared that some of the animals on the ‘dinosaur side’ of the since Kaiser’s book was published (e.g. Hackett et al. divide were almost certainly capable of flight (examples 2008). Anyway, given this strong criticism, it is somewhat include the dromaeosaurs Microraptor and Rahonavis). surprising that Kaiser leans heavily in places on Sibley and ‘Non-avian dinosaur’ and/or ‘non-avian theropod’ are, no Ahlquist’s phylogenetic proposals of the 1980s and 1990s doubt, annoying, verbose terms to some, but – if we are (e.g. Sibley and Ahlquist 1990), even sometimes treating interested in precision – they are necessary and their ‘tapestry’ as if it were the one true phylogeny. While inoffensive. Perhaps those objecting to these terms should it is widely recognised that Sibley and Ahlquist got a lot of see how frequent the terms ‘non-human ’ and ‘non- stuff right, the overall shape of their ‘tapestry’ has not human primate’ are used in the behavioural and stood the test of time, and it has also been argued that the primatological literature. phylogeny they depicted was not supported by the genetic Long sections of The Inner Bird are devoted to data they compiled. phylogeny. Given the uncertainty and disagreement that Kaiser’s frequent reference to ‘Paleognathae’ is has surrounded certain sections of the neornithine tree, it slightly irksome and he frequently refers to Galloanserae 4 Book Review

as Galloanserinae and even as Galloanseriformes. And original thought, data collation and hypothesis formation. I because the same topic is visited on a few different am certainly impressed by his novel discussions of topics occasions (see below), I was left somewhat confused by that have not previously been discussed outside of the his position on the affinities of New World vultures technical literature, if at all: the role moisture droplets (cathartids) and . In places he does seem to consider might have on the flight abilities of various birds, the them close kin. Recent work establishes that cathartids are influence bone cross section has on flight style, the close relatives of accipitrids and that the once mooted evolutionary correlation between size and body shape, cathartid– link is erroneous, but one still sees it the role long tails may play in reducing turbulence and so trotted out as a well-supported ‘counter-intuitive’ proposal on. Kaiser has also made efforts to make his data available: (ironically, often by people hoping to show how up-to-date some of it is tabulated in the book, but much more is made they are on avian phylogeny!). available in online appendices (http://innerbird.com). A few interesting similarities shared by the Hoatzin Uniquely, The Inner Bird is both an excellent popular, and some enantiornithines (the anterior part of the sternum readable account and a major contribution to the scientific lacks a and the hypocleidium extends far posteriorly literature. It, and its author, deserve great accolade. on the sternum’s ventral surface) give Kaiser pause for thought and he suggests that they had similar lifestyles. Previous authors have hinted at the possibility of hoatzin- like specialisation for a folivorous diet in some References enantiornithines (Feduccia 1996), though this has been Chiappe LM. 2007. Glorified dinosaurs: The origin and early . London: Wiley. contested as none of the other features seen in the Fain MG, Houde P. 2004. Parallel radiations in the primary clades of enantiornithine skeleton are consistent with it (Chiappe birds. Evolution. 58:2558–2573. 2007). Note, however, that Kaiser specifically does not say Feduccia A. 1996. The origin and evolution of birds. New Haven & London: Yale University Press. that the hoatzin is a living enantiornithine (he actually says Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, ‘I am itching to suggest that the Hoatzin might be a Cjojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, surviving member of the ball-shouldered birds but, sadly, it Marks B, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T. 2008. A phylogenomic study of birds reveals their is not so’ (p. 263)). evolutionary history. Science. 320:1763–1768. Incidentally, Kaiser has avian tarsometatarsal fusion Livezey BC, Zusi RL. 2007. Higher- phylogeny of modern birds the wrong way round: He notes that neornithines fuse the (, Aves: Neornithes) based on . II. Analysis and discussion. Zoolog J Linnean Soc. 149:1–95. at its proximal end and that enantior- Mayr G. 2008. Avian higher- level phylogeny: Well-supported clades and nithines fused the distal end first. In fact, neornithines what we can learn from a phylogenetic analysis of 2954 begin their fusion distally, enantiornithines proximally. morphological characters. J Zoolog Syst Evol Res. 46:63–72. Morgan-Richards M, Trewick SA, Bartosch-Ha¨rlid A, Kardailsky O, My main complaint about the book is that it does not Phillips MJ, McLenachan PA, Penny D. 2008. Bird evolution: seem that well organised. The reader finds themselves Testing the Metaves clade with six new mitochondrial genomes. covering what seems like the same ground on more than BMC Evol Biol. 8:20, doi:10.1186/1471-2148-8-20. Norell MA, Clark JM, Makovicky PJ. 2001. Phylogenetic relationships one occasion (albeit from different angles), and some of among coelurosaurian theropods. In: Gauthier J, Gall LF, editors. the different sections overlap substantially. Those brief New perspectives on the origin and early evolution of birds:

Downloaded By: [Naish, Darren W] At: 20:56 23 November 2010 introductory sections on bone and tendon anatomy make Proceedings of the International Symposium in Honor of John H. Ostrom. Yale University (New Haven): Peabody Museum of very familiar reading, but I can understand that they were Natural History. p. 49–67. needed for the more in-depth anatomical discussions that Sibley CG, Ahlquist JA. 1990. Phylogeny and classification of birds. New follow. Illustrations and black and white photos appear Haven: Yale University Press. Xu X, Zhang F. 2005. A new maniraptoran dinosaur from China with long throughout: they are mostly very good, but it is unfortunate feathers on the metatarsus. Naturwissenschaften. 92:173–177. there are not enough of them. As is hopefully made clear in this review, The Inner Darren Naish Bird is a significant volume that will hopefully inspire School of Earth & Environmental Sciences many people – palaeontologists, ornithologists and even University of Portsmouth, Burnaby Building interested amateur birders and biology students – to look Burnaby Rd, Portsmouth PO1 3QL, UK at avian anatomy with new, or renewed, interest and Email: [email protected] appreciation. I reiterate the point that Kaiser’s book is not q 2010, Darren Naish an invaluable review but also that it includes a great deal of