October 21, 2008

Matt Wedel offers a misleading, longwinded, ad hominen critique of a paper I wrote with colleagues on the new theropod dinosaur, Aerosteon riocoloradensis, and the significance of its pneumatic features. Some personalized aspects of the commentary and erroneous claims push the limits of the “good practice” guidelines posted for commentary in this journal.

In this paper, we did our best to:

1. Present the pneumatic evidence as clearly as possible (Figs. 4-16).
2. Cite the literature thoroughly and fairly (95 citations).
3. Critique available hypotheses for the evolution of avian intrathoracic air sacs and respiratory mechanics.
4. Outline more clearly in tabular format our osteological correlates (Table 4).
5. Diagram more specifically particular stages as supported by current fossil evidence (Fig. 17).

In the short first trackback, Wedel outlines and agrees with all of the main points of the paper.  He then digresses to critique earlier papers and ends by explaining what “we’ve been up to”, referring to papers by himself, Pat O’Connor and Leon Claessens—research we cited many times in the paper, both positively for evidence and in critique.  Much of the personalized negativity of the second trackback is clearly generated by Wedel’s sense that the press unfairly aggrandized our work compared to theirs, which we somehow slighted and miscited.

Neither we nor Pat O’Connor (pers. comm.) feel that personalized, ad hominem blogs like Wedel’s advance scientific understanding or enhance collegiality.

I. Wedel’s Points

Specifically, Wedel claimed the following main points:

We specifically did not make this general claim.  We claimed it was the first solid evidence (actually hollow evidence!) of pneumatic appendicular elements similar to those invaded by intrathoracic air sacs in birds.  We said:

“With the exception of evidence presented below, however, pneumatic invasion of appendicular skeletal bone within the thorax has not been reported on conclusive evidence outside crown birds (Neornithes).” 

We specifically did not make this claim anywhere in the paper.  Besides anastomosing relations along the axial column that render inexact the boundaries of air sac supply in some mature birds, we cited the work of many authors over the course of the last century that have clarified the limited distribution of cervical air sacs within the axial column of extant avians including ratites.  We reported accurately that the cervical air sacs in Sruthio (ostrich) extend posteriorly as far as the abdominal air sacs; despite Wedel’s repeated claims, we did not state that this posterior diverticulum invaded the axial column.  We opined that for some researchers, including us (and Wedel in a previous paper), pneumatic evidence from the axial column alone will remain ambiguous regarding its pneumatic source(s), because of the lack of closely matching osteological correlates (continuous pleurocoels) in extant birds or apneumatic division along the axial column in fossils.  Our use of “pleurocoel” for an invaginated fossa on the side of the centrum—one that is considerably larger than a typical neurovascular foramen—is unlikely to engender confusion in the context of our discussion and is a condition that is rare among extant avians:

“Ventilatory air sacs, unfortunately, are the least likely to leave evidence of their presence in skeletal bone. Paleontologists and comparative anatomists, as a result, have focused on axial pneumaticity, and opinion has split as to the meaning of observed patterns. In extant birds, pneumatic invasion by cervical air sacs is usually restricted to the cervical and anterior thoracic vertebrae and their respective ribs [1], [16]–[22]. The posterior thoracic, synsacral, and caudal vertebrae, in contrast, are pneumatized by diverticulae extending directly from the lung or from abdominal air sacs [1], [16], [19], [21], [22]. Some authors have concluded, therefore, that the lung and abdominal air sacs must also be responsible for pneumaticity in the posterior half of the axial column in nonavian dinosaurs and, on this basis, have packed the thoracic cavity of theropods with a full complement of avian ventilatory air sacs [33]. An opposing view is that the continuous series of pleurocoels observed in many nonavian dinosaurs suggests that the nonventilatory, paraxial cervical air sacs extended posteriorly along the column [26], [34].

We are inclined to support the latter, more conservative interpretation that pleurocoels in nonavian dinosaurs are a product of paraxial cervical air sacs and provide, at best, ambiguous evidence for intrathoracic ventilatory air sacs. First, pleurocoels are rare in birds, and no living bird has an unbroken cervical-to-caudal series of pleurocoels as occurs in some nonavian dinosaurs, including the one we describe below [31]. As Wedel [26] has underscored, pleurocoels extend posteriorly in the axial column of saurischian dinosaurs to a variable extent, but neither adults nor juveniles of any species show an apneumatic gap. Allotting an unbroken series of pleurocoels of graded form, as in the case we describe below, to three different pneumatic sources (cervical air sacs, lung diverticulae, abdominal air sacs) is difficult to defend. Drawing a direct analogy based on birds for the source(s) of pneumaticity in the posterior axial column in nonavian dinosaurs [22], [31], [33], thus, is problematic.

Second, cervical air sacs have been observed extending to the posterior end of the vertebral column in birds. Several authors have described cervical air sacs extending posteriorly beyond the abdominal air sacs in the ostrich (Struthio camelus) [21], [36]. Ratites have relatively smaller abdominal sacs than in other birds and, as nonvolant basal avians, serve as better analogs for nonavian saurischians than volant neognaths [37].

Finally, the posterior portion of the avian axial skeleton is completely transformed by extensive coossification of vertebrae and girdle bone and by posterolateral rotation of the pubes away from the midline, which allows unobstructed distal extension of the viscera and abdominal air sac under the synsacrum and caudal vertebrae. The pelvic space in nonavian saurischians, in contrast, is not nearly as open and continuous with the thoracic cavity, offering comparably less space for these air sacs [37].

More conclusive evidence of intrathoracic ventilatory air sacs in fossils, in sum, will require an osteological signature of pneumatic structures in nonaxial (appendicular) bones, which that cannot be dismissed as an elaboration of the paraxial cervical air sacs. We now turn attention to previous reports of such pneumaticity in the appendicular skeleton of nonavian dinosaurs.”

Whether ratites are secondarily flightless or not is irrelevant, when our point concerned anatomical analogy; they are superior functional analogs than a hummingbird.  Second, ratites are basal within Neornithes and therefore are stronger than a hummingbird for phylogenetic comparisons.

The point we made concerning the abdominal air sac in nonavian theropods is that it could not possibly have occupied the volume it does in extant avians under the posterior axial column; the articulated preservation of pubes in Aerosteon and posterior dorsal and sacral centra nearly close the pelvic outlet.   Again, the correlation would be stronger to extant avians regarding posterior axial pneumaticity, if the configuration of the pelvic girdle and form and sequence of pneumatic openings closely resembled each other:

“the posterior portion of the avian axial skeleton is completely transformed by extensive coossification of vertebrae and girdle bone and by posterolateral rotation of the pubes away from the midline, which allows unobstructed distal extension of the viscera and abdominal air sac under the synsacrum and caudal vertebrae. The pelvic space in nonavian saurischians, in contrast, is not nearly as open and continuous with the thoracic cavity, offering comparably less space for these air sacs [37].”

This is absurd.  In their 2005 paper and elsewhere, O’Connor and Claessens make the claim that there is a marked division of pneumaticity between posterior dorsal and sacral portions of the vertebral column.  They claimed this is also true in other theropods.  We did not see this in Aerosteon; we have not seen this in any other theropod; and we did not see any pneumatic gaps or divisions in excellent juvenile ornithomimid material, as we reported.

This important observation on Majungasaurus in the 2005 paper, however, could not be verified because the relevant posterior dorsal vertebrae were not described or figured until 2007.  That was our point—that when these critical vertebrae were described and figured, there is considerable question in our minds that they support the notion of a diminution of pneumaticity or division between dorsal (i.e., lung diverticulae) and sacral (abdominal diverticulae) pneumaticity.  We don’t see this in Aerosteon nor in other abelisauroid vertebral material at hand.  We quoted the relevant papers over this issue, so as to make their description and interpretations as clear as possible:

“Wedel [26] pointed out that such a pneumatic hiatus has never been reported in saurischian dinosaurs that exhibit axial pneumaticity in presacral and sacral regions of the vertebral column. A hiatus might be expected to occur in young individuals, if axial pneumatization is derived from multiple sources as in living birds. Immature individuals of the ornithomimid Sinornithomimus as young as one year in age [56], however, show the same continuous and gradational pattern of presacral pleurocoels as occurs in subadults of the same species or adults of other ornithomimid genera [57].
Recently O'Connor proposed that axial pneumaticity in the abelisaurid theropod Majungasaurus can be used “to refine inferences related to pulmonary structure” [35: 159], because “it shows a reduction in the pneumaticity in the last two dorsal neural arches, with enhanced pneumaticity in sacral aches [31: 22]. Specifically, the “size and number of neural arch foramina” are reduced in dorsal vertebrae 12 and 13, whereas the same are “enhanced” in sacral vertebrae, indicating “two different sources of pneumatization” [33: 253]. The actual differences, however, were not described, and dorsal vertebrae 12 and 13 were not figured until recently [35: figs. 3, 12, 13].

Review of the posterior dorsal-to-sacral vertebral series in Majungasaurus suggests an equally plausible alternative explanation. The two posteriormost dorsal vertebrae have narrower, shorter transverse processes with single-headed ribs [35]. In preceding dorsal vertebrae, a pair of pneumatic fossae open on either side of the parapophysis (infraprezygapophyseal and infradiapophyseal fossae) as well as one farther posteriorly (infrapostzygapophyseal fossa). The loss of a distinct parapophyseal process eliminates the ridge of bone that divided the two anterior fossae, leaving a more broadly open area. Although not mentioned in the description, a distinct small funnel-shaped fossa is maintained in this area in dorsal 12 [[35: fig. 12C]], and a more broadly open fossa still remains in dorsal 13 [35: fig. 13A], representing the fusion of infraprezygapophyseal and infradiapophyseal fossae in both vertebrae. Counting the infrapostzygapophyseal fossa, two of the three fossae present in more anterior dorsal vertebrae appear in reduced form in these posteriormost dorsal vertebrae.

The mid sacral vertebrae are preserved, and each has two fossae visible on the ventral aspect of the diapophysis [35: fig. 13A]. Unlike any of the infradiapophyseal fossae in the presacral column, these are invaginated with a sharp-rimmed opening. The likely explanation for this is the increase surrounding bone from massive sacral attachments and fusion of adjacent neural arches. The pneumatic diverticulae thus are better surrounded by bone, compared to the posteriormost dorsal vertebrae with their reduced transverse processes.

It appears, in sum, that the “reduction” and “enhancement” of pneumatic fossae between posterior dorsal and sacral vertebrae in Majungasaurus is directly related to “reduction” and “enhancement” of vertebral structure. Regarding the reduced fossae in dorsal 12, O'Connor remarked, “Concomitant with the reduction in neural arch laminae, pneumatic foramina are only present immediately adjacent to the postzygapophyses” [35: 144]. This reduction of the size of the pneumatic fossae, nonetheless, was presented as prima facie evidence for separation of cervical and abdominal “focal centers” of pneumatic diverticulae [31: 22].

The situation in Aerosteon is instructive for the contrast that it provides across the same vertebral transition. In this case, pneumaticity appears to peak in the last dorsal, with a large pneumatic canal in the transverse process that is not present in sacral vertebrae (Figure 4C). The pleurocoels, in addition, develop a posterodorsally inclined partition in the posteriormost dorsal vertebrae that passes into the sacral series unchanged. The axial column of Aerosteon does not suggest a clean partitioning based on the number or size of pneumatic spaces, but rather a gradation in pleurocoel form that extends from the anterior cervical vertebrae through the distal caudal vertebrae. As in other saurischians, there is no pneumatic gap separating distinct zones.

O'Connor and Claessens [33: 253] have argued that the “general pattern of pneumaticity in Majungasaurus is expressed throughout Theropoda … indicating a consistent and widespread pattern of pneumatic invasion by caudally located air sacs in non-avian theropods.” Their cited tabulation of theropod vertebral pneumaticity, however, does not include any examples of axial pneumaticity partitioned by an apneumatic gap. The data from Majungasaurus, although well preserved and described [35], is not qualitatively different from information on saurischian vertebral pneumaticity that has been available for more than a century [58]–[60]. On this evidence alone, the source of posterior axial pneumaticity in nonavian saurischians is likely to remain controversial, even if posterior axial pneumaticity in most extant avians is derived from diverticulae of the lung and abdominal air sacs [26].”

Citations in the paper are extensive and appropriate to the content of the references.  It is to date the most complete published summary of  literature on the question of the fossils, air sacs, and respiratory mechanics.  If we were challenging an idea or observation, we tried to quote the source to avoid misrepresentation.

Wedel is free to be completely convinced (in contrast to at least one of his previous publications) of the close match between pneumaticity in neognaths and the osteological correlates we can observe in saurischians.  Others, however, must be allowed to hold a different opinion without unfair caricature.   We did not claim, as Wedel repeatedly asserted, that all axial pneumaticity in saurischians must originate from cervical air sacs.  We said we favor that interpretation from the fossil evidence, but that the multi-source condition in extant birds creates serious ambiguity.  Here is the strongest support we gave it in the text:

“We are inclined to support the latter, more conservative interpretation that pleurocoels in nonavian dinosaurs are a product of paraxial cervical air sacs and provide, at best, ambiguous evidence for intrathoracic ventilatory air sacs.”

“Inferences about postcranial pneumaticity in Aerosteon are very dependent on the condition in extant birds (Neornithes), the only extant outgroup with comparable skeletal structures related to pneumatization. Because only a single outgroup is available, soft-tissue inferences are weaker [55: level–two inference]. Osteological correlates must establish a convincing link for soft-tissue inference.

Anterior axial pneumaticity (cervical to anterior dorsal vertebrae plus their associated ribs) has long been attributed to cervical air sacs in saurischian dinosaurs like Aerosteon. Pleurocoels, pneumatic neural arches, and costal pneumatocoels closely match those in extant birds derived from diverticulae of the cervical air sacs. Posterior axial pneumaticity (posterior dorsal, sacral, and caudal vertebrae) occurs sporadically in nonavian saurischians and has been attributed either to cervical air sacs or to diverticulae extending directly from the lung and abdominal air sacs [23], [26], [27], [22], [31], [33], [35], [37]. In Aerosteon posterior axial pneumaticity has a similar form to that elsewhere among nonavian saurischians—a posterior extension without hiatus of the pneumatic pattern established in the anterior axial column.

In living birds, anterior and posterior axial pneumaticity develops during growth as diverticulae invade the axial skeleton from cervical air sacs, lung diverticulae, and caudal (abdominal) air sacs. These separate sources for axial pneumaticity can leave a pneumatic hiatus in the thoracic vertebrae, where the approaching diverticulae fail to fully anastomose. In Gallus, for example, there is an apneumatic hiatus in the thoracic vertebrae that may persist in the adult [20].

Wedel [26] pointed out that such a pneumatic hiatus has never been reported in saurischian dinosaurs that exhibit axial pneumaticity in presacral and sacral regions of the vertebral column. A hiatus might be expected to occur in young individuals, if axial pneumatization is derived from multiple sources as in living birds. Immature individuals of the ornithomimid Sinornithomimus as young as one year in age [56], however, show the same continuous and gradational pattern of presacral pleurocoels as occurs in subadults of the same species or adults of other ornithomimid genera [57].”

II. Historical Note

We are of the opinion that personalized, ad hominem blogs like the pair from Wedel do little to advance scientific understanding or enhance collegiality but have the opposite effect.  We will not add to that effort by recounting personal information regarding our perceptions of the intentions or actions of others.

We state only the following for the record:

1. The exceptional pneumaticity in girdle elements in Aerosteon was initially reported in an abstract in the Journal of Vertebrate Paleontology  (Alcober et al., 1998) with details presented in 2005.   The material has been available for study since that abstract was published and has been examined by several researchers.
2. We prepared a manuscript on Aerosteon for Science early in 2005 that was rejected largely on the basis of one reviewer’s opinion that air sacs could not possibly initially have evolved in non-avian dinosaurs for heat loss (one of the possibilities we regard as plausible and in need of testing as outlined in the paper).
3. Later that year, O’Connor and Claessens (2005) published a Nature paper with a similar focus.  We eventually decided to publish a longer paper with more extensive documentation of pneumatic features and proposed evolutionary stages—the present paper.
4. A press release was held in Mendoza Province, Argentina, at the time of publication of the paper in PLoS ONE to highlight the work, support of the sponsor of the expedition (National Geographic) that led to the discovery of the fossils, and, most importantly, to bolster efforts to build a local museum in Malargue near the area of discovery.