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A Reply to Ruben on Theropod Physiology
Castles Made of Sand: John Ruben, Airways, Conchae, Downy Dinos, and Physiological Perambulations
Put a group of paleontologists in a room. Show them the movie adaptation of Michael Crichton’s “Jurassic Park” and carefully observe their individual reactions to the scene in which we see a Velociraptor fog up a window with its breath. We have in this hypothetical scenario, a litmus test for one of the most acrimoniously disputed subjects within dinosaur paleontology: the physiology of these marvelous animals.
There is something of a false dichotomy in this field: dinosaurs were either ectotherms, or endotherms. Unfortunately, reality doesn’t cooperate with our simplistic view of things, and the matter is far more complicated. For now, though, this convenient if unrealistic dichotomy will suffice. Since 1969, it has been increasingly argued that at least some dinosaurs were endothermic, to some degree. As always in science, there remains the opposition. The leading light of the body of paleontologists, who suggest that dinosaurs were ectothermic to some degree, is arguably John Ruben, of Oregon State University. Ruben has also become the unofficial physiological laureate of the “thecodont” ancestry camp, and thus is work is particularly important to the general field of avian phylogenetics.
While Ruben’s research is incisive, and his conclusions intriguing, in several regards their veracity must be called into question, for a variety of reasons. Ruben has consistently failed to falsify the hypothesis that some dinosaurs were endotherms of an indeterminate degree.
The view that Dinosauria are endothermic is in fact an old idea, resurrected from the history of the discipline. Sir Richard Owen first proposed in 1841 that his “fearfully great lizards” were most like mammals in their physiology—a conclusion he inferred largely from the osteology of the pelvic girdle and the parasagittal gait shared with Mammalia. Other researchers concurred with this view, and it was not until the late 19th Century that the consensus on dinosaur physiology underwent a drastic change, whereby these animals were rendered slothful, stereotypical ectotherms barely capable of sustained activity (Bakker 1986).
The modernist era of dinosaur paleontology largely agreed with this drastic revision in dinosaur physiology (e.g., Colbert et al 1946), and it was arguably not until the 1969 description of Deinonychus antirrhopus, that the case for dinosaur endothermy was reborn (Ostrom 1969, Bakker 1986). Perhaps the single most influential researcher in this renaissance was Ostrom’s former Yale student, the enigmatic Robert Bakker, who in a series of papers argued forcefully for endothermy in Dinosauria, and in particular, Theropoda (Bakker 1971, 1972, 1974, 1975, 1980, 1986).
The French histologist Armand J. de Ricqles presented data to support Bakker’s conclusions (1974, 1980, 1983) and argued that histological data gleaned from long bones in Dinosauria indicated rapid growth rates and high resting metabolic rate. The debate triggered by this work ultimately culminated in a symposium in 1980 to examine the matter (and of which Bakker was highly critical in his 1986 work). Since this time, further work has increasingly substantiated the argument that at least some dinosaurs were endothermic (see summaries in Farlow in Dodson et al 1990, Padian et al in Tanke & Carpenter 2001, and Paul 2002).
Recently, John Ruben and his colleagues have raised the most serious objections to the view that Dinosauria were largely or wholly endothermic in their physiology yet offered. This work is primarily based on one fundamental assumption: that soft-anatomy, and not osteology, will be the primary determinant of physiological capabilities (Ruben 1995). Based on review of Theropoda, extant archosaur lineages, and lepidosaurs, Ruben et al have presented three key assertions which they argue conclusively falsify endothermy in Dinosauria: a) the pathway followed by air upon inhalation through the external nares in Dinosauria is like that seen in lepidosaurs, b) dinosaurs lacked respiratory conchae, and c) theropods possessed a pelvovisceral pump and were thus incapable of avian grade aerobics (Ruben 1995, 1996, Ruben et al 1996, 1997, 1998, 1999, Ruben & Jones 2000).
The validity of these conclusions, however, must be called into question by the evidence available, and at this time, Ruben and his associates have failed to demonstrate that dinosaurs were uniformly ectothermic, by these three criteria.
The Nasal Airway
Reviewing the cranial osteology of Dromaeosaurus albertensis following Currie (1995), tyrannosaurids, and ornithomimids, Ruben (1996) and Ruben et al (1996, 1997) asserted that the nasal airway of Theropoda was a simple, constricted tube, and that air being inhaled through the external nares followed a straight path through the airway to the internal nares. Concomitant to this assertion, was the restoration of the internal nares as immediately caudoventral to the external nares in said taxa.
Ruben and his colleagues are demonstrably incorrect in all of these arguments. The restoration of the dromaeosaurid nasal airway presented in Ruben (1996) and Ruben et al (1996, 1997) is based not on the figured material in Currie’s 1995 review of the taxon, but rather on an artistic representation of the skull of Dromaeosaurus albertensis. Moreover, Ruben’s work failed to position the internal nares of the theropod taxa sampled correctly, and further failed to appreciate the extent and development of mediorostral maxillary sinuses in these fossils.
Mediorostral maxillary sinuses appear to be present in all Tetanurae, and are certainly present in Neotetanurae (Witmer 1990, 1995, 1997, Holtz in Tanke & Carpenter 2001, Paul 2002). In Coelurosauria, these structures were sufficiently enlarged in the medial aspect, so as to physically seal the rostral portion of the internal nares, and restrict the internal narial opening to a caudal orientation (Witmer 1997, Norell & Makovicky 1999, Paul 2002). This pattern is readily apparent in tyrannosaurids (Holtz in Tanke & Carpenter 2001, Paul 2002).
These data render Ruben’s placement of the internal narial opening as far forward as figured in Ruben (1996) entirely incorrect. Moreover, the presence and substantial development of the mediorostral maxillary sinuses would have diverted incident air in the nasal airway dorsally over the sinus complex, to the point where it would have reached the caudal border of the rostral nasal airway, roughly situated at the rostrodorsal margin of the antorbital fenestra. Here postantral struts meet medially to divert the nasal airway caudoventrally to the internal nares (Witmer 1997, Paul 2002).
Correctly restored, the passage taken by the nasal airway in Tetanurae, or at least Coelurosauria, can be rendered as such: straight, with a caudoventral diversion at the junction of the rostral nasal airway and the rostrodorsal margin of the antorbital fenestra.
Respiratory Conchae: The Elusive “Rosetta Stone” of Theropod Physiology
Ruben and his colleagues have repeatedly advanced the presence of respiratory conchae or lack thereof, as prima facie evidence to either uphold or refute the endothermic physiology of an extinct form. In a series of papers (Ruben 1996, Ruben et al 1996, 1997, 1999, Ruben & Jones 2000), Ruben et al have asserted that theropod nasal airways lack respiratory conchae, and are thus unsuitable for supporting an elevated resting metabolic rate and endothermy. This conclusion stems from the assumption that the presence of respiratory conchae in mammals and birds is linked to prevention of dehydration by reabsorbing water in the nasal airway, and thus helping to support the strenuous aerobic exertions of endotherms. The absence of respiratory conchae in bradyaerobes has been advanced as a verification of the correlate between respiratory conchae presence, and elevated metabolism (and the reverse).
Ruben’s conclusions are troubling for several reasons. First and foremost, the presence or absence of respiratory conchae is not a reliable correlate of metabolic level and general physiology. This observation alone falsifies Ruben’s presentation of this argument as definitive. Respiratory conchae are absent or reduced in a stunning array of tachyaerobic, alpha endothermic animals ranging from ratites to Procellariiformes and Falconiformes amongst Aves, to all manner of mammals including whales, anteaters, bats, elephants, and nearly all of the primates (Bang 1966, 1971, Scott 1954, Negus 1958, Coulombe et al 1965, Dorst 1973, Olson 1985, Paul 1988, Feduccia 1996, Paul 2002).
By Ruben’s criteria these taxa should be bradyaerobes, a conclusion, which is clearly indefensible. The data, which weakens the correlate between presence/absence of respiratory conchae and elevated metabolic rate, is by no means limited to this material, however. There is compelling evidence to suggest that respiratory conchae are non-essential exaptations for moisture retention amongst tachyaerobes. A variety of original adaptive roles for respiratory conchae have been produced, and the author refers the reader to Paul (2002) for a succinct bibliography of such work.
Perhaps most damaging to the case Ruben et al. have built around respiratory conchae, is the infidelity with which such structures are preserved in the fossil record. The respiratory conchae of animals are consistently situated on sheets of cartilage or bone in the mediorostral or rostral portion of the cranium, and as such, are rarely preserved (Bang 1966, Dorst 1973, Paul 2002). Indeed, no such structures have ever been observed in fossil Aves (Olson 1985, Feduccia 1996, Paul 2002). As Paul (2002) points out, under Ruben’s strict correlate hypothesis, this would force one to argue for bradyaerobiosis in all fossil birds. Such a scenario further demonstrates the serious flaws in Ruben’s reliance on respiratory conchae as indicators of physiology.
Contra Ruben (1996) there is no pattern of consistent preservation of respiratory conchae in fossil taxa, and thus it is not possible to conclusively use such structures in these fossils to determine the metabolic rate and physiology of said forms. The features which Ruben (1996) isolated as indicative of the presence of respiratory conchae, are similarly inconsistently observed and cannot be considered as definitive markers whereby the presence of respiratory conchae can be determined (Buhler 1981, Witmer 1995, 1997, Paul 2002).
In the final analysis, the respiratory conchae argument advanced by Ruben and his colleagues must be considered one of the weakest ever advanced in defense of dinosaur ectothermy. There is no reliable correlate between respiratory conchae presence/absence and metabolic rate, nor is there any reliable preservation of respiratory conchae whereby their presence or absence could be determined without equivocation in the first place.
Downy Dinos and Theropod Aerobic Capacity
Ruben and his colleagues assert that Theropoda possessed a pelvovisceral piston in which diaphragmatic musculature anchored to the procumbent pubes operates upon the hepatic capsule, ventilating the lungs (Ruben et al, 1996, 1997, 1998, 1999).
Pelvovisceral systems are further characterized by an airtight post-pulmonary septum inferior to the liver, which preserves a pressure differential between the cranial and caudal aspects of the thorax (Gans & Clark 1976, Perry 1988, 1990). Osteological characters associated with such a system include (following Mook 1921, Gans & Clark 1976, Duncker 1978, Perry 1988, 1990, Ruben et al 1997, Paul 2002):
a) Thoracic ribs articulate with the dorsal vertebrae via hyper-elongated transverse processes and single proximal heads
b) Gastralia do not meet medially, and are instead set in a cartilaginous sheet
c) Pubes mobile, procumbent
d) Lumbar region formed by reduction of the caudal thoracic ribs
e) Sternal ribs doubled
f) Diverticula largely absent, pneumatic excavation of bones inconsistent or absent, most especially caudal to the post-pulmonary septum
Characters a, b, c, and d, are biomechanical necessities of a pelvovisceral pump. The modified rib articulation with the dorsal vertebrae and failure of the gastralia to meet medially permits the cranial aspect of the thorax (superior to the post-pulmonary septum) to present a smooth surface both dorsally and ventrally in which the viscera can readily move in concert with the action of the diaphragmatic musculature. Similarly, such musculature requires mobility and a procumbent orientation of the pubes (and most likely a high breadth ratio). The presence of a lumbar region is consistently observed in all taxa in which a pelvovisceral pump is found, and is therefore most logically considered to be an essential aspect of the system as a whole. The doubling of the sternal ribs assists in regulation of the pelvovisceral mechanism. The absence or inconsistent presence of pneumatic excavation of the bones caudal to the post-pulmonary septum is particularly indicative of such an aerobic system, as the septum maintains a pressure differential between the fore and aft thoracic compartments.
Ruben et al presented their conclusions on the aerobic system present in Theropoda following the 1996 description of the holotype Sinosauropteryx prima (NGMC 2124) (Ji & Ji 1996) from the Lower Cretaceous Yixian lagerstatten of China, in which a concentration of carbonized material is preserved in the caudal region of the thorax. Ruben and his colleagues identified the material as the liver, and argued that the cranial aspect of this region was convex, demonstrating the presence of a post-pulmonary septum, and thus by inference, a pelvovisceral pump. Ruben et al further asserted that muscle fibers preserved in the type Sinosauropteryx were indicative of the requisite diaphragmatic musculature, inserting on the distal pubes (Ruben et al 1997, Feduccia 1999). Ruben and his colleagues have further maintained that the type Scipionyx samniticus (Sasso & Signore 1998) recovered from Cretaceous strata of Italy validates said claims (Ruben et al 1999).
Ruben et al have relied exclusively on the data available from preserved soft-anatomy, minimizing osteological factors in their analyses (Ruben 1995, Ruben & Jones 2000). The soft anatomy of the type Sinosauropteryx displays an overall poor state of preservation, and thus data derived from this material is largely ambiguous until such time as soft-tissues are found preserved with greater fidelity in similar theropods (Martill et al 2000, Paul 2002).
Due to haphazard and unsupervised preparation of NGMC 2124 by amateurs, the slab was shattered symmetrically into at least twelve pieces (Ji & Ji 1996, Paul 2002), and subsequent restorative measures have largely obscured the original extent and form of the carbonized region (Paul 2002). Breakage and infilling have destroyed the original cranial aspect of the carbonized region, such that its form and the degree to which it extended cranially cannot be ascertained with certainty (Paul 2002). The dorsal, central, and ventral margins identified by Ruben et al (1997) as displaying a convex arc, in fact delineate a pseudo-margin resulting from the inadequate preparation of the specimen. Thus, the initial conclusion that the carbonized material displays a convex arc in cranial aspect is not unequivocally substantiated at this time.
Moreover, the liver of both birds and crocodiles, the two extant nodes of Archosauria, display convex cranial arcs, and the presence of such an arc in and of itself is not indicative of a pelvovisceral system (Duncker 1979, Brackenbury 1987, Paul 1988, Paul 2002). Ruben et al infer a post-pulmonary septum, in concordance with their argument that the carbonized material displays a convex arc in cranial aspect, however, the reason why such a septum must be present given a convex cranial arc, is not clear. Furthermore, the height of the liver (assuming the material represents as much) is not a reliable correlate of a pelvovisceral system. Liver anatomy is highly variable throughout the ontogeny of any given taxon and individual animal, and more germane, there is no consistent difference in the size and position of the liver in crocodiles, and birds (Siwe 1937, Brackenbury 1987, Secor & Diamond 1995, Paul 2002). Curiously, a post-pulmonary septum is observed in none of the remaining Sinosauropteryx material (Ackerman 1998, Chen et al 1998, Paul 2002).
Ruben et al (1997) attempted to mitigate these ambiguities with the soft-anatomy of Sinosauropteryx by arguing that preserved muscle fibers in the type Scipionyx were oriented in a position to be expected of diaphragmatic musculature. However, these fibers—if they are indeed muscle fibers—have subsequently been identified as components of M. obliquus and M rectus, muscles of the abdomini, by virtue of their configuration (Paul 2002).
Further doubt is cast on the conclusions pertaining to the aerobic capacity in Sinosauropteryx made by Ruben and his colleagues, by the soft anatomy of Scipionyx samniticus. In the type Scipionyx, the intestinal tract is preferentially preserved at the expense of other viscera, and a structure immediately caudal to the sternum, distal ends of the humeri and proximal blade of the scapula, is most logically associated with the liver (Sasso & Signore 1998, Ruben et al 1999, Paul 2002). Ironically, the cranial orientation of the liver in Scipionyx is entirely incongruent with the position of the alleged liver in Sinosauropteryx. The position of the intestines in Scipionyx and the carbonized matter in Sinosauropteryx are identical, and given these data, the most logical conclusion is that the latter represents the fossilized post-mortem decay of the intestinal tract (Paul 2002).
Thus, even offering Ruben’s research the benefit of the doubt (i.e., assuming they have identified the carbonized material in Sinosauropteryx correctly), the data presented in Ruben et al (1997, 1999), is not sine qua non verification of a pelvovisceral pump in Theropoda, in that the soft-anatomy is sufficiently ambiguous to render definitive conclusions based on such, wholly speculative at this time.
Given these limitations, the osteological data is currently the most reliable in determining the aerobic faculties of Theropoda. While Ruben (1995) and Ruben & Jones (2000) have argued that osteological factors are largely inconsequential to the operation of aerobic systems, there is no apparent reason why this should be so, and indeed the suite of characters which are biomechanical necessities for the respective systems of aerobic regulation, seem to directly refute this assertion.
Theropoda lack all the osteological modifications permitting the operation of a pelvovisceral pump, and in particular, lack the modification of the proximal heads of the ribs and the communication of the gastralia seen in crocodiles. In Theropoda, the thoracic ribs articulate with moderate or reduced transverse processes of the dorsal vertebrae via bifurcated proximal heads, and thus the dorsal surface of the rib cage in theropods is sharply corrugated (Ostrom 1969, Paul 1988, Britt 1997, Paul 2002). The gastralia meet medially in Theropoda, and were not imbedded within a cartilaginous sheet (Ostrom 1969, Paul 1988, Dodson et al 1990, Paul 2002). These characters would have precluded the formation of a sub-cylindrical, smooth-walled tube in which the viscera could be acted upon by diaphragmatic muscles (Paul 2002), and these data alone, demonstrate that the presence of a pelvovisceral system in Theropoda, was a biomechanical impossibility.
The absence of a lumbar region, inadequacy of the distal pubes to support diaphragmatic musculature and immobility of the pubes (especially in opisthopubic taxa, e.g. Eumaniraptora) further argue against the presence of such a hepatic piston, as is seen in crocodiles (contra Ruben et al). To preclude the assertion of negative evidence, review of the osteological characters associated with avian or paravian aerobic capacities, which are, or are not present in Theropoda, is germane. Characters associated with the avian aerobic system include (after Zimmer 1935, Bellairs & Jenkin 1960, King 1966, Schmidt-Nielsen 1972, Olson 1973, Perry 1983, Beale 1985, Paul 1988, Perry 1989, McLelland 1989, Bramble & Jenkins 1998, Paul 2002):
a) Postcrania consistently pneumatic, infiltrated by pulmonary diverticula
b) Proximal thoracic rib heads bifurcated, forming a corrugated dorsal rib cage
c) Caudal ribs not reduced
d) Sternocostal hinge present
e) Sternal ribs are singular, not double, and usually ossified
f) Ossified uncinate processes
g) Gastralia meet medially
In Theropoda the postcrania are consistently pneumatized, displaying invasion of pulmonary diverticula. Pneumaticity of postcranial elements extends to the sacrum and caudal vertebrae in some Theropoda (Russell & Dong 1993, Britt 1997, Paul 2002), in contrast to the pattern expected had an airtight post-pulmonary septum existed in life. The proximal heads of the thoracic ribs, in even the most basal Theropoda, are bifurcated and articulate with the dorsal vertebrae via moderate transverse processes, as detailed above. The caudal ribs in Theropoda are not reduced, and consequently, a lumbar region is absent, as detailed above. The sterna and coracoids of avepectoran theropods (i.e., Maniraptoriformes), articulate via a hinge joint permitting sternal kinesis (Paul 1987, 1988, Norell & Makovicky 1999, Burnham et al 2000, Paul 2002). Contrary to Ostrom (1969), the sternal ribs of Maniraptoriformes are singular, and ossified (Barsbold 1983, Paul 1988, Ji et al 1998, Norell & Makovicky 1999, Xu, Wang & Wu 1999, Paul 2002). Ossified uncinate processes are present in derived maniraptoran taxa (Paul 1988, Xu, Wang & Wu, 1999, Norell & Makovicky 1999, Xu et al 2000, Burnham et al 2000, Paul 2002). Lastly, the gastralia of Theropoda meet medially, and were not set in a cartilaginous sheet, as in crocodiles, as detailed elsewhere.
It is thus concluded, that the osteology of Theropoda is inconsistent with the presence of a pelvovisceral pump, and at least in two regards, the operation of such a pump would have been a biomechanical impossibility. On the contrary, all the modifications of the thoracic and pectoral skeleton, as well as the vertebrae seen in Theropoda, are congruent with those observed in Avialae, arguing the presence of a similar aerobic system in at least some theropods. Considering the ambiguity of the soft-anatomy at hand, current analyses must rely on the osteological data until such time as better-preserved soft-tissues become available.
Considering the dubious nature of Ruben’s central conclusions regarding the physiology of Theropoda, detailed herein, the argument that endothermy in theropods has been falsified must be seen as speculative at this time. Until further data comes to light, the matter will remain open to contention.
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