Elsevier

Cretaceous Research

Volume 56, September–December 2015, Pages 53-59
Cretaceous Research

Did all theropods have chicken-like feet? First evidence of a non-avian dinosaur podotheca

https://doi.org/10.1016/j.cretres.2015.03.008Get rights and content

Highlights

  • We describe the first evidence of a podotheca in the dinosaur fossil record.

  • Concavenator supports the presence of the avian podotheca for the Theropoda clade.

  • The arthral condition is primitive in Theropoda.

  • The ichnological record could be interpreted based on the new evidence.

Abstract

The podotheca is the structure of scales covering the foot in extant birds. It is usually assumed that this structure is present in the whole clade of theropod dinosaurs; however, the knowledge of the origin of the podotheca is based on scarce direct evidence and its point of emergence within Theropoda is ambiguous. Here we discuss the relatively complete and well preserved podotheca of the basal tetanurae Concavenator corcovatus, which allows the description of its structure and its osteological correlation. We describe the skin pattern around the autopod of Concavenator and we compare it with available fossil skin impressions and the skin of extant crocodiles and birds. These scale impressions present a similar pattern to those observed in the autopod of avian theropods, so our results suggest that Concavenator have a bird-like podotheca. On the other hand, there is a current debate about the ichnological–osteological correlation in dinosaurs, derived from the lack of knowledge about the position of the phalanges in relation to the plantar pads of the podotheca. We describe, in Concavenator, an arthral condition of the position of the plantar pads. This condition would be the basal condition in the tetanurans and, thus, the ichnological record could be interpreted with an additional criterion. The autopod of Concavenator provides the first evidence of this type of structure in a non-avian theropod and it sheds light on the origin and distribution of this structure in the theropod large lineage.

Introduction

The pes of extant birds is covered, from the tibiotarsus to the end of the toes, by an integumentary structure that is a layer of scales known as podotheca. This structure is composed of three distinct types of scales (Stettenheim, 2000) showing a characteristic pattern of arrangement. Scutate and scutellate scales are the largest; mostly rectangular, and regularly arranged, situated on the anterior surface of the tarsometatarsus and the dorsal surface of the toes. In contrast, the smallest and irregular reticulate scales are located on the underside of toes and the posterior surface of the tarsus (Stettenheim, 2000). Traditionally, the presence of an avian podotheca has been inferred for the whole Theropoda clade (Hitchcock, 1836, Lull, 1904, Heilmann, 1926); however, the knowledge of the origin of this structure in non-avian theropods is conditioned by the limited fossil record of the skin covering the pes (Ji et al., 2001, Pu et al., 2013). In Dinosauria, skin impressions around the foot have been described in the hadrosaurids Saurolophus osborni, Saurolophus angustirostris and Corythosaurus casuaris (Brown, 1916, Bell, 2012, Bell, 2014). The anterior surface of the metatarsus of S. osborni is covered with scales like pebbles of 2 mm in diameter (Bell, 2012). Skin impressions over the digits are composed of slightly elongated hexagons of 7 mm and other smaller scales, randomly positioned (Bell, 2012, Bell, 2014). Saurolophus angustirostris present skin around the ankle joint and the dorsal surface of the pes. This skin is comparatively simpler than the skin of S. osborni, consisting of uniform pebbles 1–2 mm in diameter devoid of variation (Bell, 2012). Corythosaurus casuaris presents a similar pattern of the scales to other hadrosaurian (Brown, 1916, Bell, 2014). Moreover, skin impressions associated to pedal bones are also preserved in the basal ceratopsian Psittacosaurus (Mayr et al., 2002), with small (1–2 mm) and irregular tuberculate scales arranged in rosettes around and over metatarsals. Scales preserved over the metatarsal IV lack variation in size or shape. All of these impressions show a different pattern of size and arrangement from those observed in the avian podotheca. However, the recently described Kulindadromeus, a basal neornithischian, shows a skin patch around the tibia and the metatarsal area (Godefroit et al., 2014) that presents scales similar to those of birds.

Crocodiles, the extant sister group of birds, do not exhibit a bird-like podotheca. The pes is only covered by rectangular and ellipsoidal scales, presenting an oblique arrangement with respect to the axis of the toes (Alibardi and Thompson, 2000). The absence of a podotheca in the closest extant out-group of dinosaurs does not provide a strong support to the presence of this structure in non-avian theropod. Therefore, using the Extant Phylogenetic Bracketing (EPB: Witmer, 1995), the skin coverage of the autopod in Theropoda clade is reconstructed as Level II of inference.

Ichnological evidence is an alternative source of information about the skin coverage of the pes of dinosaurs. Based on this evidence, it is known that the skin pattern on the pes of some sauropods is different from the crocodilian-like structure and from the avian podotheca. Preserved scale impressions in sauropod footprints have a polygonal contour and are arranged in rosettes, where each polygon is separated by grooves (Platt and Hasiotis, 2006). These data are also consistent with the distribution of scales interpreted on sauropod embryos (Coria and Chiappe, 2007). Furthermore, a similar pattern of scale impressions in rosettes is also observed in footprints attributed to Stegosaurus and Ankylosaurus (McCrea et al., 2001, Mateus et al., 2011). Available ornithopods footprints show a unique large pad beneath the digits (Langston, 1960, Currie et al., 1991), unlike the multipads of the avian podotheca. This isolated digital pad is observed in a preserved foot of Mantellisaurus from Las Hoyas (Llandres-Serrano et al., 2013). Furthermore, the paleoichnological records of other archosauriforms have been also compared. The footprints of ichnofamily Chirotheriidae were associated to several members of the crurotarsi (Avanzini, 2000, Avanzini et al., 2007). In the skin impressions of its digits some of them show millimetre-sized ellipsoidal and rectangular scales. These scales are arranged in irregular rows crossing obliquely the digit axis and forming a checkerboard pattern (Avanzini, 2000, Avanzini and Mietto, 2008, Avanzini et al., 2011, Díaz-Martínez and Pérez-García, 2012).

Therefore, neither direct nor indirect evidence provided by out-groups of Theropoda provide unambiguous information on the coverage of skin neither on the feet of basal theropod groups nor on the origin of extant bird podotheca.

We test herein the presence of an avian podotheca in the Tetanurae clade, analyzing the holotype specimen of Concavenator corcovatusOrtega et al., 2010 (MCCM-LH 6666). This specimen partially preserves the skin covering the pes. The analysis of its integumentary impressions enables a description of the first evidence of this structure in non-avian theropods.

Section snippets

Material and methods

The integumentary impressions analysed belong to MCCM-LH 6666, the holotype of Concavenator corcovatus (Ortega et al., 2010), a well-preserved, nearly complete and articulated skeleton from the Lower Cretaceous (Barremian stage) in Las Hoyas fossil site (Cuenca, Spain). The current study focus on the delicate integumentary structures located under the pedal digits and in the metatarsal area of the right pes of Concavenator. This autopod is almost complete and the metatarsals and phalanges are

Geological setting

Las Hoyas fossil site (Fig. 1) is situated 30 Km NE from the city of Cuenca, in the Cuenca Province (Spain), within Las Hoyas subbasin in the Serranía de Cuenca. The latter is part of the Iberian Ranges, which runs NW-SE in the East Central part of the Iberian Peninsula.

Las Hoyas subbasin was filled mainly with deposits of the La Huérguina Fm, with almost 400 m of distal alluvial and palustrine-lacustrine deposits from Barremian age (Fregenal-Martínez and Meléndez, 2000). Las Hoyas fossil site

Skin impressions of metatarsal area

The preserved skin impressions are located in the lateral side of metatarsal IV and around metatarsal V (Fig. 2). The soft-tissue mainly consists of skin impressions with different rate of preservation, resulting from the distinct mineralization associated to the authigenic early mineralization (Briggs et al., 1993, Briggs et al., 1997). This differentiation has been also observed in Pelecanimimus polyodon (Briggs et al., 1997), where the outlines of the tissues are associated to the

Discussion

Due to their location, arrangement and shape, the impressions observed around the autopod of MCCM-LH 6666 are interpreted as the skin around the ankle area, the plantar pads and the ungual sheaths; as suggested by Ortega et al. (2010).

The scale impressions have been compared with the skin of the pes in certain taxa (eg Alligator mississippiensis, Struthio camelus, Gallus gallus domestic). Concavenator has the same arrangement of the integumentary structure as the podotheca of extant birds

Conclusion

Historically, the reconstruction of the pes of theropod dinosaurs was based on an accelerated optimization of the ambiguous rise of the avian podotheca in the evolution of the group. Concavenator provides evidence of the presence of an avian podotheca structure in a non-avian theropod, supporting the presence of this condition for, at least, the Avetheropoda clade. Moreover, the reconstruction of the complete structure allows the establishment of the arthral disposition of the plantar pads as

Acknowledgments

We thank R. Fuertes for manuscript revision and S. Torralba for photography in Fig. 4A. We would like to thank two anonymous reviewers whose comments and suggestions have greatly improved the manuscript. We acknowledge the Museo de las Ciencias de Castilla-La Mancha for access to the specimen. Elena Cuesta research is financed by FPU subprogram of the Spanish Ministerio de Educación, Cultura y Deportes (ref. AP2010-0816). IgnacioDíaz-Martínez research is supported by the projects IT834-13 of

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