Journal of Systematic Palaeontology Tree climbing - a ...

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Journal of Systematic Palaeontology

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Tree climbing - a fundamental avian adaptation

David A. Burnhama; Alan Feducciab; Larry D. Martina; Amanda R. Falkc a University of Kansas Natural History Museum and Biodiversity Institute, Lawrence, KS, USA b CB# 3280, Coker Hall, The University of North Carolina at Chapel Hill, Chapel Hill, NC, USA c Department of Geology, University of Kansas, Lawrence, KS, USA First published on: 16 December 2010

To cite this Article Burnham, David A. , Feduccia, Alan , Martin, Larry D. and Falk, Amanda R.(2010) 'Tree climbing - a

fundamental avian adaptation', Journal of Systematic Palaeontology,, First published on: 16 December 2010 (iFirst) To link to this Article: DOI: 10.1080/14772019.2010.522201 URL: http://dx.doi.org/10.1080/14772019.2010.522201

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Journal of Systematic Palaeontology, Vol. 00, Issue 0, 2010, 1–5

IN MEMORY OF CYRIL A. WALKER

Tree climbing – a fundamental avian adaptation David A. Burnhama∗, Alan Feducciab, Larry D. Martina and Amanda R. Falkc a

University of Kansas Natural History Museum and Biodiversity Institute, 1345 Jayhawk Boulevard, Lawrence, KS 66045, USA; b CB# 3280, Coker Hall, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-3280, USA; c Department of Geology, University of Kansas, 1475 Lawrence, KS 66045-7594, USA

Downloaded By: [Burnham, David] At: 22:16 16 December 2010

(Received 19 April 2010; accepted 4 May 2010) There have been a number of studies on the claws of Mesozoic birds, largely driven by interest in the habitat of Archaeopteryx. Many Mesozoic avians have large, well formed manual claws, largely absent in contemporary birds. Juvenile hoatzins are the only living birds with claws that are large enough to be generally functional, but not equivalent to those of Mesozoic birds. When birds developed an effective backstroke permitting easy ascent from flat surfaces, the need for manual claws disappeared, which would suggest that they were primarily used for climbing tree trunks and had little function in prey capture. This hypothesis has both phylogenetic and functional implications. The numerous claw studies to date are based primarily on measurements taken of the bony core, all that is usually preserved in fossils. Examination of contemporary birds shows that this is a poor estimator of the size and shape of the horny sheath that actually forms the functional claw. The discovery of vast numbers of exceptionally preserved fossil birds from the Late Jurassic and Early Cretaceous of China means that we now have an opportunity to compare actual horny claw data from the earliest birds with that of modern birds and test hypotheses on climbing, terrestrial activity, and predation. Keywords: claw morphology; avian evolution; arboreal; claw angle; Dromaeosauridae

Introduction Some of the most important differences between the primitive birds of the Mesozoic and those of the present day involve tree-trunk climbing. In modern birds with sophisticated flight, this behaviour is nearly always connected with specialized scansorial foraging (exceptions include juvenile hoatzins and owls). Because of this, living mammals may be more analogous functionally to some of the early birds than their closer modern relatives. This ability is partly reflected in the highly curved manual and pedal claws that are useful as grappling and climbing devices (Richardson 1942; Yalden 1985; Rose 1987), a point first argued for Archaeopteryx using modern analogues (Feduccia 1993). With the plethora of recent discoveries of Mesozoic Chinese birds, an even larger dataset within the context of early avian evolution can be considered. Even more importantly, the discovery of the basal dromaeosaurid Microraptor has provided the most extreme example of highly curved claws in a specialized, arboreal animal (Xu et al. 2003; Martin 2004; Burnham 2010). Previous workers have used claw morphology as the basis for determining lifestyle using the degree of curvature (Richardson 1942; Yalden 1985, 1997; Rose 1987; Peters & Görgner 1992; Feduccia 1993; Pike & Maitland 2004). We expand these studies of claw curvature by includ∗

Corresponding author. Email: [email protected]

ISSN 1477-2019 print / 1478-0941 online C 2010 The Natural History Museum Copyright DOI: 10.1080/14772019.2010.522201 http://www.informaworld.com

ing the horny sheath in these measurements from modern mammals, modern and fossil birds and dinosaurs. Fortunately, Early Cretaceous material from northeastern China and the Late Jurassic of southern Germany preserves numerous examples of the horny sheath around the claws in birds and dinosaurs. It is the shape of this horny sheath that provides information about the lifestyle of the animal. Unfortunately its shape cannot be predicted from that of the bony core and attempts to use the core have met with limited success (Ostrom 1974; Pike & Maitland 2004; Fowler et al. 2009; Chiappe 2007).

Material and methods Claw curvature was measured in 15 fossil specimens that were preserved with the horny sheath intact. We have examined most of the taxa ourselves, but in a few cases have relied on the literature. We also measured claws from the dermopteran Cynocephalus (KU 144596, 98144), the two-toed sloth Choloepus (Zool. 1228—KUVP Teaching Collection), and a bat, Pteropus (KU 2091, 157932), all housed at the University of Kansas Natural History Museum and Biodiversity Institute. All the pes measurements were taken from digit III. For most of the fossil forms, manual claws were also measured. Images of the specimens were

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D. A. Burnham et al. Table 1. List of species and respective claw arc measurements. Taxon name


Figure 1. UV photograph of the manual claws of a microraptor showing the keratinous sheath covering unguals III and IV.

either scanned (Epson Perfection 2450 Photo) from publications, or captured with close-up digital photography (Nikon D80 with an AF-S Micro-Nikkor 105 mm 1:2.8G ED lens). For cf. Microraptor sp. (LVH0026), a short wave ultraviolet lamp (Mineralight UVS-54) was used to enhance the horny sheath of the manual claw. Using Adobe Photoshop software, image files were created and best-fit circles were overlain onto the entire claw inclusive of the sheath. Lines were drawn from the tip of the horny sheath to the base of the ungual using Adobe Illustrator. The angle of inner claw curvature was measured by overlaying lines that touched both ends of the claw and ran as parallel to the base of the claw as possible. These lines met in the centre of the circle, creating the angle of inner claw curvature (Fig. 1). The degree of inner claw curvature was measured using a protractor. These results were added to a previously published dataset of modern birds generated by Feduccia (1993). All the data was plotted onto a graph of claw arc (degrees) versus species (see Table 1). Peters & Görgner (1992) also used horny sheath in their measurements, and had a more complicated method of measuring curvature; however, we used Richardson’s technique as this has been shown (Richardson 1942; Feduccia 1993) to be an accurate and easily repeatable method.

Results We used several comparative approaches beyond a duplication of Feduccia (1993). First, we compared manual to pedal claws on the same individual. We would predict that pedal claws should show some compromise between terrestrial locomotion and climbing. Manual claws should not show evidence of terrestrial locomotion and would be fully adapted for either climbing or predation. Terrestrial forms that did not climb might still retain a predatory function for the manual claws. Without a predatory function we would

Fossil specimens Juravenator Yanornis Pterodactylus Microraptor STM5–50 Jeholornis Confuciusornis Archaeopteryx Microraptor STM5–50 Jeholornis Confuciusornis Juravenator Archaeopteryx Cryptovolans Cryptovolans Confuciusornis Microraptor LVH 027 Microraptor LVH 028 Modern birds Apteryx australis Gallus varius Colinus virginianus Gallirallus australis Geococcyx californiana Numida meleagrides Geositta cunicularia Sturnella magna Neomorphus geoffroyi Cyanocitta cristata Myiarchus crinitus Coracias benghalensis Ramphococcyx calyorhynchus Coccyzus americanus Momotus momota Leptosomus discolor Pteroclossus frantzii Cuculus sparverioides Tockus fasciatus Sitta carolinensis Phoeniculus purpureus Certhia americana Trichodroma muraria Sphyrapicus varius Xiphorhynchus guttatus Picoides villosus Campethera carali Picus canus Dryocopus pileatus Modern mammals Choloepus Pteropus Choloepus Cynocephalus

Mans or pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Manus Manus Manus Pes Manus Manus Manus

Digit number

Claw angle

III IV III III III III III III III III III II (I) III (II) III I (II) II (III) III (IV)

75 95 96 138 139 141 137 138 139 141 153 154 159 165 172 180 180

Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes

III III III III III III III III III III III III III

52.2 60.5 61 64 65.6 66.8 70.2 70.9 77.6 101.8 112.2 113.3 113.8

Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes Pes

III III III III III III III III III III III III III III III III

115.9 116.2 118 122.9 124.1 125.3 129.5 138.3 142.9 141.1 149 153.7 154.4 156.4 160.9 161.1

Pes Pes Manus Pes

III? III? Ill III?

120 124 131 170

expect the manual claws to be progressively reduced and lost, with improved ability to take off from flat surfaces. In other words, the development of a keeled sternum may


Tree climbing – a fundamental avian adaptation

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Figure 2. Graph from Feduccia (1993) with our Table 1 data.

be reflected in the reduction and loss of the manual claws. The earliest ornithurine birds resemble modern shorebirds and presumably occupied an ecological niche with few trees, necessitating perfection adaptations such as the sternal keel for take-off from the ground. All early ornithurines have reduced manual claws, mostly lost in modern birds. Vestigial manual claws are found in a large array of extant juvenile birds, and Fisher (1940) was unable to discover vestigial manual claws in only six living orders of birds. The only modern birds with large functional manual claws are juvenile hoatzins, which use such claws in climbing; not trunk climbing, but rather climbing and clambering about in the branches. The manual claws of Microraptor showed the highest degree of known claw curvature, exceeding all values from previously published data (Peters & Görgner 1992; Feduccia 1993; Fowler et al. 2009). These claws are transversely compressed, highly recurved, with pointed, needle-like tips. Trunk climbing birds had higher claw curvatures than other locomotory types. Microraptor scores higher than even the most accomplished modern avian climbers, above the trunk-climbing morphology described by Feduccia (1993) (Fig. 2). Cryptovolans ( = Microraptor) and Confuciusornis also scored above modern birds in the climbing category. The high similarity between the curvature of the manual and pedal claws in Microraptor and Cryptovolans indicates a common function: tree-climbing (Rose 1987). The manual claws of Archaeopteryx and Juravenator scored within the range of Feduccia’s climbing category. However, in Juravenator, the pes claw scored low at 75◦ , reflecting a terrestrial lifestyle. However, it is often

quite difficult to ascertain the critical parameter of lateral compression for fossil claws adapted for trunk climbing; in predatory claws there is typically a lateral expansion, especially at the claw base. Regardless, there is an obvious gap in the new data between 100 and 140◦ that corresponds to the gap in Feduccia’s (1993) graph; however, the gap in Feduccia’s graph represents a clear break between ground birds and perching birds. The break in the graph of fossil bird claw curvature represents a similar break, but falls in the overlap range between ground birds and perching birds. This probably reflects the more diverse assemblage of modern birds, or suggests that more advanced grounddwelling birds were not present during the late Mesozoic. The data may also represent that the Jehol birds are mostly arboreal forms.

Discussion Claws designed for predatory grasping may not be distinguishable from climbing claws by claw angle alone, but are easily distinguished by a thicker base that tapers towards the tip (Yalden 1997). The manual claws of Microraptor correspond to the tree climbing morphology and were surely only used for climbing, as prey held at the tips of the long fingers could not be reached by the mouth. Manual claw III, which is the largest, has a curvature of 180◦ , placing it beyond the observed range for predatory birds and within the range for the pedal claws of the most advanced modern climbers, such as woodpeckers (Peters & Görgner 1992; Feduccia 1993; Fowler et al. 2009), and slightly


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D. A. Burnham et al.

above the manual claws of Archaeopteryx. In Microraptor, the pedal claw for digit III measures 138◦ , placing it well above the highest range for modern perching birds and also above the range of modern trunk climbing birds. This claw curvature exceeds that measured for any known animal in both manual and pedal unguals. The extreme lateral compression seen in the claws of Microraptor is only matched by modern trunk climbing mammals and birds, such as squirrels, dermopterans, fruit bats and woodpeckers (Yalden 1985). Needle-point tips are also characteristic for these claws and are unlike terrestrial archosaurs such as the Upper Jurassic Compsognathus and Juravenator, in which flattened pedal claws resemble those of terrestrial birds, being broader than deep, giving a distinctly hooflike impression (Yalden 1985). Since the manual and pedal claws of Microraptor score nearly the same, this indicates it was a specialized arborealist. If Microraptor could fly or walk these claw measurements would skew the graph in opposite directions. The horny sheaths of modern birds and mammals have a subungual groove formed by ventral keels that merge distally towards the tips of the claws (Manning et al. 2009). It is likely that this is the primitive condition and was apparently modified only in a few groups, such as owls and possibly cursorial dromaeosaurs, to function as a killing claw (Manning et al. 2009). Deinonychosaurs are characterized, in part, by an enlarged claw on the second pedal digit. A stout, truncated penultimate phalanx permits this claw to be retracted. In later forms, this is thought to be part of a unique predatory complex, although it has been argued recently that they functioned for grasping rather than as a killing instrument (Senter 2006). Microraptor has such a claw, and the holotype of M. gui preserves the horny sheath in anatomical position (Xu et al. 2003) showing that it was enormously elongated and recurved (152◦ ). However, it also shows the extreme lateral compression found in trunk climbing birds and mammals and the subapical constriction and needle like tip unique to trunk climbing birds (Yalden 1985). The bony core has dorsal and ventral tubercles, suggesting this ungual was capable of powerful flexion and retraction. However, in later dromaeosaurs, the dorsal tuber is reduced. This suggests that it was not a predatory device in Microraptor but was used in climbing. It may have opposed the claw on the first digit (reduced but with an enlarged claw sheath) and perhaps also the fourth digit which is able to swing laterally and is often preserved in that position in the specimens so that the foot could firmly grip branches. The predatory functions of this complex probably evolved after the loss of flight in this lineage. Microraptor provides a salient endpoint for claw curvature, since it has been widely documented as an arboreal animal (Xu et al. 2003; Martin 2004) and any further increase in claw curvature beyond 180◦ would be maladaptive and non-functional. Furthermore, it is obvious from the extremely elongate hindlimb flight feathers that the

hindlimbs were unavailable for cursorial locomotion. This alone suggests that highly curved claws evolved for climbing. Even more importantly, our data show a lack of intermediate forms, indicating that modern birds have diversified further ecologically. Important aboreal behaviours include vertical tree trunk climbing and scansorial foraging, perching or resting, pendant-hanging, and transversing across gaps between branches (limb grasping). These behaviours are more easily facilitated with possession of certain osteological features such as transversely compressed and sharply curved claws on the manus and pes (Yalden 1985), long arms that can supinate in unison (Nudds & Dyke 2009), mobility in the hindlimb joints (especially the ankles), and a tail modified for balance or support (Ostrom 1969). More interesting than the curvature evidence that Microraptor is a claw-climbing arborealist are some features consistent with arboreal positional behaviour: bowed limbs and phalanges (Jungers et al. 1997), and powerful forelimbs (humerus, radial tuberosity indicating strong flexion and large sternals) (Rose 1987; Bloch & Doyer 2007). The posteriorly bent pubis also lowers the centre of gravity while tree-trunk climbing (Burnham 2010), and the animal is able to support itself vertically on the trunk with a stiff tail (Chatterjee & Templin 2004; Manning et al. 2009). Given that current evidence supports the view that Microraptor is a basal dromaeosaur, this new data suggest that large, curved claws evolved first for arboreal behaviour, as hypothesized elsewhere (Zani 2000). Dromaeosaurids are suggested to have possessed a locking mechanism for their claws similar to that in modern birds and mammals (Manning et al. 2005), and therefore may have engaged in suspensory behaviours such as climbing, clinging, perching and even perhaps hanging. These behaviours were later modified, as arboreal forms diversified and more terrestrial forms emerged. It may also suggest that predatory or other functions of manual claws in deinonychosaurs may be secondary (Manning et al. 2009).

Acknowledgements We graciously thank E. Gong (Northeastern University) for access to specimens and providing support, and R. Timm for access to modern specimens under his care. We dedicate this manuscript to the memory of Cyril Walker, who realized the unique characters of enantiornithurine birds, and thank Gareth Dyke for organizing this symposium in his honour.

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