Bleedin’ Enormous Eyeballs

A while ago, I stopped making that many living restorations of what I thought oviraptorids, among my favorite groups of animals that ever lived, looked like. This was because some serious questions of their potential organismal biology remained unknown. One of these was the shape and extent of the horny covering of the beak, the rhamphotheca; but another feature included the size of the eyeballs. A few studies, one old (Kundrát and Janáček, 2007) and two new (Schmitz and Motani, 2011; Zelenitzky et al., 2011 [and free here], tell us that dinosaurs like oviraptorids may well have been nocturnal or crepuscular, suited for a low-light lifestyle.

I bring this up not because I disagree with anything one of these studies says, but because a particular question seems left out of the discussion. But first, let me summarize a few things, also mentioned by Ed Yong over at Not Exactly Rocket Science (if you do not read this blog, you really should).

update: Mickey Mortimer points out I missed scleral ossicles in an oviraptorid, and have amended the text to reflect this.

Advanced Hearing in a Small Oviraptorid Skull

First up, Martin Kundrát and Jiří Janáček tackled one of the earliest described oviraptorid skulls, ZPAL MgD-I/95, originally reported by Osmólska (1976) as a juvenile of Oviraptor (as Oviraptor sp.). This specimen has a storied history taxonomically, including having been treated (multiple times) as a juvenile of various other taxa (first by Paul, 1988 as Oviraptor yanshini then later [Paul, 2010] to his abominable Citipati gracilis [as “Ingenia” yanshini to which Paul continued to allot the skull was referred], which was also argued by Barsbold, 1986, whom Kundrát and Janáček (2007) follow). That this skull is treated as a juvenile is important, because Kundrát and Janáček argue, based on obliteration of some cranial sutures, the skull is that of an adult; the authors do not elaborate on this point, and GI 100/978 (holotype of Citipati osmolskae Clark et al., 2001, see also 2002) possesses the same open sutures as does ZPAL MgD-I/95, although the frontals interdigitate in a distinctive pattern, while that of ZPAL MgD-I/95 does not (which may suggest a more juvenile condition).

Kundrát and Janáček (K&J) used CT scanning on ZPAL MgD-I/95 in order to develop a picture of the internal spaces in the bones of the skull, especially the pneumatization of the bones surrounding the braincase. Clark et al. (2002) did this for Citipati osmolskae, but did not elaborate on this work as they were specializing their study on cranial osteology. One of K&J’s findings was that the bones surrounding the internal ear were heavily pneumatized, and would have assisted in the transmission of sound, improving the oviraptorid’s hearing. This would have been of extensive aid for the animal in helping it catch sound sin a low-light (nocturnal or crepuscular) environment, as a second advanced sense would only improve the primary sense (vision).

Other Advances Senses?

A study in press by Zelenitzky et al. purports the relative sizes of the olfactory bulbs of most major avian groups and some outlying nonavian theropods, including Citipati (they used GI 100/978, so they mean Citipati osmolskae) where the relative olfaction capability is low, below the regression line when body mass is compared to the size of the olfactory bulbs. This implies that for its size, the smelling ability was not particularly advanced, which was true for ornithomimosaurs assessed by the authors as well. I will not go further in discussing this paper until it’s published, but the authors through the Witmer Lab have made all of their data available and this improves the ability to discuss what has been in the news. On top of this, Larry Witmer blogs the similarities of this study with that of the other unpublished study, Schmitz and Motani, here. This work implies that oviraptorids probably did not have very good olfaction, and thus a poorer sense of smell than, say, a dromaeosaurid (Bambiraptor feinbergi Burnham et al., 2000).

Eyeball Size

Oviraptorid skulls are particularly notable for the very large diameters of the fenestrae, including the external bony nares, orbit, infratemporal and supratemporal fenestrae. But the enormous sizes of these fenestrae are only moderately known due to incomplete or obscure description of the skulls of these fascinating animals.

Skull of a PIN oviraptorid skull (provisionally, "Big Beak") illustrating the cranial fenestrae. Each square of the grid represents 1cm.

Particular emphasis is shown here on the relative size of the orbit (as the title of this post alludes to), while additional features should be noted.

1) The orbital rim of the frontal, lachrymal (probably including a fused prefrontal element) are nearly perpendicular to the sagittal plane, causing the orbit itself to be almost exclusively facing laterally.

2) The orbit is by far the largest fenestra in the skull, with exception of the subtemporal fenestra, which is only apparent in ventral view of the skull, but houses passage of various mandibular muscles (more on that later).

3) Diameter of the orbit is nearly the size if not greater than the width of the paired frontals. This has extra implications I will get to in a bit.

4) Almost regardless of the orientation of the skull, the lachrymal bar forming the anterior rim of the orbit is bowed laterally rather than medially, expanding into the anterior aspect of the eyeball.

To put some of this into perspective, we can refer to yet another paper assessing the senses of theropods: Stevens (2006) used ophthalmic field  perimetry (OPV, “ophthalmic visual perimetry”) measurements and cranial reconstructions to determine the relative overlapping fields of vision for various theropods. While Stevens did not assess an oviraptorid, he used methods that are adaptable to oviraptorids. Generally, the plane of the bony orbit can help determine how much overlap the vision fields of each eye could overlap if the eyeball were situated 50% of the way out of the socket (the plane of the orbit transects the equator of the eyeball); Stevens attempted to view the center of an hypothetical pupil for each eye from across the snout, and the points at which the pupil could not be seen across the snout (from various head orientations) restricts the overlapping view of vision.

Now look at the above image again, and compare:

Skull of a PIN oviraptorid skull (provisionally, "Big Beak"), as above, but with a green "eyeball" inserted into the orbits. Because of the point of section where the rostral view of the skull is shown, the "eyeball" appears to overlap limiting bones -- this is an illusion.

Two green circles are illustrated in this image. The first is the maximum-sized eyeball possible, from just outside the median interobital septum (as in birds) and within the margin proscribed by the orbital rim. The eyeball matches the curvature of the rostral and dorsal orbital rims. This isn’t a perfect analogy, as not all eyeballs are perfectly spherical as described above, but this illustrates diameter without making assumption of ellipsoids distorted along the rostral-caudal or ventral-dorsal axes. An additional constraint includes the scleral ring, but this ring typically does not constrain the size of the ball, but merely its inner (open) diameter constrains the size of the visible eye and maximum size or aperture of the pupil.

The second green circle represents a more “conservative” eyeball size, and roughly corresponds to the inner diameter of the scleral ring that might be expected for an oviraptorid theropod.

Skull of a PIN oviraptorid skull (provisionally, "Big Beak"), as above but with a hypothetical scleral ring shown in grey.

However, problematically, a scleral ring is unknown in most any oviraptorids, which can be because of a variety of factors including the material is extremely thin and thus does not preserve well, or that it almost never ossifies, or that it is easily lost (which does not explain preservation of scleral rings in dromaeosaurids and protoceratopsids from the same sediments as most oviraptorids are recovered from). Scleral ossicles are known in GI 100/978 (Citipati osmolskae), but they are disarticulated, none are in contact with one another, and despite excellent preservation of the skull and skeleton, there are only five of them.

Citipati osmolskae (GI 100/978), with green arrows pointing to scleral ossicles ("SO").

Five scleral ossicles, from a partial scleral ring, preserved in the right orbit and below it were removed during preparation (fig. 1). They are roughly square in shape with irregular margins and a gently concave medial surface. They are similar to those of other basal coelurosaurs such as troodontids and dromaeosaurids. [Clark et al., 2002:pg.12]

It is thus very difficult impossible to determine Schmitz and Motani’s method for assessing acuteness of vision or diel (preference to time of day for activity) in an oviraptorid, because the objective criteria for pupil diameter are missing. It might be possible, using a method whereby the relative thinness of the scleral ring, rather than its diameter, might aid in inferring diel, but I doubt the limited amount of data in this regards helps. Similarly, CT work on oviraptorid endocranial anatomy is limited: Clark et al. (2002) briefly described the endocranial vault and associated pneumatic recesses overlying the endocranium in GI 100/978 (Citipati osmolskae) while Osmólska (2004) described the dorsal endocranial surface in GI 100/31 (referred to “Ingenia” yanshini), illustrating what may be very large optic lobes.

It should be clear at this point that oviraptorids probably had bleedin’ enormous eyeballs. Application of Stevens’ work implies there may have been a very limited amount of binocular overlap, enough so that this might inhibit typical predatory behavior far lower than that inferred for dromaeosaurs, which would have been quintessential in this regard. Instead, oviraptorids would have had extremely acute hearing, extremely acute vision, limited overlap of visual fields, and may very well have been nocturnal or crepuscular (I’m drawing a very broad prediction here).

I’m not even close to practically assessing the skull shown above to the literature described herein, and will not be for some time, but I felt not comparing my favorite theropods to recent work was a shame, but have done so largely through previously published assessments of these issues. What is there have been incredibly limited, and the amount of information we don’t have about oviraptorid skulls is amazingly limited compared to, say, Velociraptor mongoliensis, and I find this to be something of a shame.

Burnham, D. A., Derstler, K. L., Currie, P. J., Bakker, R. T., Zhou Z.-h. & Ostrom, J. H. 2000. Remarkable new birdlike dinosaur (Theropoda: Maniraptora) from the Upper Cretaceous of Montana. University of Kansas Paleontological Contributions 13:1-14.
Clark, J. M., Norell, M. A. & Barsbold R. 2001. Two new oviraptorids (Theropoda: Oviraptorosauria) Late Cretaceous Djadoktha Formation, Ukhaa Tolgod, Mongolia. Journal of Vertebrate Paleontology 21(1):209–213.
Clark, J. M., Norell, M. A. & Rowe, T. 2002. Cranial anatomy of Citipati osmolskae (Theropoda, Oviraptorosauria), and a reinterpretation of the holotype of Oviraptor philoceratops. American Museum Novitates 3364:1-24.
Kundrát, M. & Janáček, J. 2007. Cranial pneumatization and auditory perceptions of the oviraptorid dinosaur Conchoraptor gracilis (Theropoda, Maniraptora) from the Late Cretaceous of Mongolia. Naturwissenschaften 94(9):769-778.
Osmólska, H. 1976. New light on skull anatomy and systematic position of Oviraptor. Nature 262:683–684.
Osmólska, H. 2004. Evidence on relation of brain to endocranial cavity in oviraptorid dinosaurs. Acta Palaeontologica Polonica 49(2):321-324.
Paul, G. S. 1988. Predatory Dinosaurs of the World: A Complete Illustrated Guide. Simon & Shuster (New York City).
Paul, G. S. 2010. The Princeton Field Guide to Dinosaurs. Princeton University Press (Princeton).
Schmitz, L. & Motani R. 2011. Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science 332:705-708.
Stevens, K. A. 2006. Binocular vision in theropod dinosaurs. Journal of Vertebrate Paleontology 26(2):321-330.
Zelenitzky, D. K., Therrein, F., Ridgely, R. C., McGee, A. R. & Witmer, L. M. 2011. Evolution of olfaction in non-avian theropod dinosaurs and birds. Proceedings of the Royal Society of London, B 278:3625-3634.

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