This blogpost was modified June 22, 2015 with the addition of the red text and two cladograms pulled from Cau et al. 2015 along with a third from Brusatte et al. 2013.
Another change July 9 after new data on Archaeopteryx and Aurornis shift Balaur to nest with Velociraptor.
Balaur bondoc (Figs. 1-6; EME PV.313, Csiki et al. 2010, Latest Cretaceous), is a mid-sized theropod dinosaur with not one, but two raised scythe claws on pedal digits 1 and 2 (Fig. 1). More typical forms of similar size, like Deinonychus and Velociraptor (Fig. 4), have only a single scythe claw.
Figure 1. The right foot of Balaur bondoc, a raptor-like theropod dinosaur known chiefly from its limbs and pelvis. Note the two scythe claws here. Yellow phalanges are raised off the substrate during terrestrial locomotion. At left from Cau et al. 2015. Middle derived from that drawing. Right, traced from photo in Cau et al. 2015).
(Cziski et al. 2010) and later (Brusatte et al. 2013) Balaur nested with velociraptorine dromaeosaurids, based on the Theropod Working Group (TWiG) matrix. However, Cau et al (2015) noted that Balaur had a suite of autapomorphies not present in dromaeosaurids, nor in most other non-avialan theropods. These unique traits include a fused carpometacarpus, loss of a functional third manual digit, proximal fusion of the tarsometatarsus, and an enlarged first pedal digit.
By contrast to the original nesting,
Cau et al. (2015) recovered Balaur more derived than Archaeopteryx among the birds. They used two prior theropod matrices in their study: Brusatte et al. (2014) and Lee et al. (2014). Cau et al. concluded, “Our reinterpretation of Balaur implies that a superficially dromaeosaurid-like taxon represents the enlarged, terrestrialised descendant of smaller and probably volant ancestors.”
In other words,
Cau et al. nested Balaur after Archaeopteryx, which makes Balaur a flightless (= nonvolent) bird. Unfortunately Balaur was unlike the birds Cau et al. nested Balaur with, Sapeornis and Zhongjiaornis (Fig. 2). These two big-wing birds both have a pygostyle (reduced tail). Balaur does not. Details and other red flags follow.
Figure 2. Balaur compared to Zhongjiaornis and Sapeornis, sisters recovered by Cau et al. 2015. Unfortunagely both these taxa had a pygostyle and the former lacked teeth. Both also were likely volant based on the large size of their forelimbs.
Cau et al. 2015
used the Brusatte et al. (2014) tree (860 characters vs. 152 taxa) to nest Balaur as a sister to Sapeornis (Fig. 1), a taxon with a pygostyle and very large forelimb/wings that was a more derived sister to Archaeopteryx. Cau et al. recovered more than a million MPTs in this test.
In addition, Cau et al. used the Lee et al. (2014) tree (1549 characters vs. 120 taxa) to nest Balaur close to Zhongjianopterus (Fig. 1) several nodes more derived than Archaeopteryx and slightly more derived than Sapeornis. Cau et al. recovered 1152 MPTs in this test.
Figure 3. Balaur nested in the large reptile tree nests with Velociraptor, but that nesting is based on a relatively few limb traits.
that Balaur is different than most other theropods. The goal here is to find out which theropods (birds included!) it is most like.
Added figure 4. Balaur sacral vertebrae colorized. Click to enlarge.
Unfortunately, or perhaps fortunately,
the matrix of the large reptile tree was not designed specifically for theropods. And worse yet, only about two dozen forelimb and hindlimb traits are preserved in Balaur that are listed in the large reptile tree character list. That’s a magnitude fewer than the competing tests (not sure how many of those characters are pectoral, pelvic and limb characters, though). Nevertheless the large reptile matrix recovered a fully resolved tree nesting Balaur with a theropod of similar size, Velociraptor, as in the original nestings (Cziski et al. 2010; Brusatte et al. 2013).
In the evolution and origin of birds
Aurornis represents a clade that was getting smaller and more gracile that ultimately led to all birds — and all tested birds have a reduced scythe claw. Opposite this trend, Balaur was built like a tank. Balaur fuses a long list of bones that otherwise do not fuse in sister taxa, but do occasionally fuse by convergence in more distantly related theropods.
Figure 4. How Baluar fits within the current taxon list, within the Theropoda. Here it nests between Aurornis and Archaeopteryx, flights and pre-bird, nevertheless it did flap its wings based on coracoid length.
Cau et al. considered
the sole phalanx of vestigial manual digit 3 to be the fusion of phalanges 1-3. That may be so… OR the distal phalanges might not have been preserved. Either way it makes no difference to the large reptile tree (Fig. 4).
Figure 5. Balaur (in vertical and horizontal configurations) compared to Haplocheirus and Velociraptor, Aurornis, Archaeopteryx and Gallus. Balaur nests with Velociraptor in the large reptile tree.
Convergent with living birds,
the Balaur anterior sacrum is wide and the pubis of Balaur bows laterally, producing a wide area for the guts between them. This could also be the result of a switch to herbivory (as Cau et al. speculates) and, if so, the twin scythe claws may have been used only for climbing trees. A second scythe-like ungual was not necessary to open the guts of a dinosaur with more efficiency, but a second large claw might have helped a heavier, perhaps less mobile herbivorous Balaur hang more easily on a tree trunk with both medial and lateral digits opposing one another.
Despite the fact
that the manus is subequal to the pes in Balaur, Cau et al. considered those forelimbs ‘reduced’ by comparison to the flying birds, Sapeornis and Zhongjiaornis (Fig.1), perhaps due to insularism (living on an island). They suggested that Balaur may have had a proportionally shorter-tail and a less raptorial-looking foot than previously depicted. The tail was not pygostylic and the pes was trenchant. We’ve seen co-author D. Naish make such hopeful suggestions before, based on a lack of attention to such red flags as that long tail on Balaur. Naish also prefers to shoehorn taxa into existing clades (like pterosaurs into the Ornithodira), rather than allow the tree to recover new clades (like the Tritosauria and Fenestrasauria).
Balaur was feathered and, with those long, but small, coracoids, it flapped feebly. No doubt it was too large and bulky to fly.
Cau et al. (2015) report, “The sister taxon relationship recovered between Balaur and the short-tailed Sapeornis is quite unexpected. According to that topology, the short pygostyle-bearing tail of Sapeornis evolved independently of the same condition in more crownward birds.”
I’ll print this addition in red: Cau et al. also report, “The topology that results from our use of the dataset modified from Lee et al. (2014) agrees with most analyses of avialan relationships (e.g., Cau & Arduini, 2008; O’Connor, Chiappe & Bell, 2011; O’Connor et al., 2013;Wang et al., 2014) in depicting a single origin of the pygostylian tail among birds. Here we should note that topological discrepancies and alternative placements of problematic taxa may be influenced by artefacts in coding practice, or by the logical basis of character statement definition followed by different authors (Brazeau, 2011).We therefore consider it likely that some discrepancies between the updated analyses of Brusatte et al. (2014) and Lee et al. (2014)—including the alternative placements of Balaur and Sapeornis among basal avialans—reflect artefacts of coding rather than actual conflict in the data. In conclusion, we consider the consensus among the results of these alternative tests (i.e., Balaur as a non-pygostylian basal avian) as the phylogenetic framework for the discussion on its evolution and palaeoecology.”
Naish’s note is correct.
I glazed over their conclusion, and now I see why. But that’s not the end of this nesting problem.
Added Figure 1. The Cau et al tree based on the Brusatte et al. tree. Note the nesting of Balaur among long-tailed (pink) post-Archaeopteryx birds, but a sister to Sapeornis, which has a pygostyle (yellow). This tree is distinct from added figure 2. Click to enlarge.
Added figure 2. The Cau et al. tree based on the Lee et al. tree. Note the nesting of Balaur exactly between the long-tailed (pink) theropods and pygostylic, perching (retroverted hallux, yellow) birds, distinct from added figure 1. An odd nesting, especially considering that Jeholornis and Jixiangornis had an proto-retroverted hallux.
That brings up a whole new topic I also glazed over earlier, the retroverted hallux, which originates with Zhongianornis and Sapeornis in the Cau/Lee cladogram. Shenzhourapator (= Jeholornis) and Jixiangornis demonstrate the expected intermediate morphology for perching. Balaur, on the other hand, shows no sign of an intermediate or reversed hallux. More basal taxa (Rahonavis, Archaeopteryx, etc.) likewise do not have a reversed hallux, the perching toe.
Cau et al. listed the following traits supporting the placement of Balaur among Avialae. With relatively few traits (none listed below), the large reptile tree nested Balaur just outside of the Avialae (Archaeopteryx). Perhaps the solution to the Balaur problem lies somewhere around this node. Traits that could have arisen as a result of a tree-clinging behavior and the strain on the joints that that produces as size increases are marked with a bullet (•). But a size increase may not have occurred until after the bird split.
- the hypertrophied and proximally placed coracoid tubercle •
- the anterior placement of the condyles of the humerus •
- the proximally fused carpometacarpus with a laterally shifted semilunate carpal •
- the closed intermetacarpal space •
- the reduced condyles on metacarpals I–II •
- the slender metacarpal III – (vestige)
- the reduced phalangeal formula of the third digit – (vestige)
- the extensively fused tibiotarsus •
- the extensively fused tarsometatarsus •
- the distal placement of the articular end of first metatarsal •
- the large size of the hallux • (but it is oriented anteriorly, not reversed)
- and the elongation of the penultimate phalanges of the pes •
Added figure 3. From Brusatte et al. 2013, the nesting of Balaur far from the birds, within the dromaeosaurs.Aurornis is missing here. A later paper by Brusatte et al. 2014, (Fig. 1) changed much of this topology and included Aurornis.
Balaur was derived from dromaeosaurids in the large reptile tree (based on a limited number of theropods and birds). Balaur had a long tail, not a pygostyle. It had forelimbs similar in size relative to the torso, as those of pre-birds, not post-Archaeopteryx birds. The laterally expanded gut indicates a likely switch to herbivory. The second scythe-like claw likely aided tree-clinging. Balaur did not have a perching toe.
Brusatte, et al. 2013. The osteology of Balaur bondoc, an island-dwelling dromaeosaurid (Dinosauria: Theropod) from the Late Cretaceous of Romania. Bulletin of the American Museum of Natural History, 374:1-100.
Brusatte S, Lloyd G,Wang S, Norell M. 2014. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Current Biology 24:2386–2392 DOI 10.1016/j.cub.2014.08.034.
Csiki Z, Vremir M, Brusatte SL, Norell MA 2010. An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania. Proceedings of the National Academy of Sciences of the United States of America 107 (35): 15357–15361.
Cau A, Brougham T and Naish D. 2015. The Phylogenetic Affinities of the Bizarre Late Cretaceous Romanian Theropod Balaur bondoc (Dinosauria, Maniraptora): Dromaeosaurid or Flightless Bird? PeerJ. 3: E1032. DOI: dx.doi.org/10.7717/peerj.1032
Lee MSY, Cau A, Naish D, Dyke GJ. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345(6196):562–566 DOI 10.1126/science.1252243.
EME = (TransylvanianMuseum Society, Dept. of Natural Sciences, Cluj-Napoca, Romania)