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Pulmonary Function and Metabolic Physiology of Theropod Dinosaurs

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Science  22 Jan 1999:
Vol. 283, Issue 5401, pp. 514-516
DOI: 10.1126/science.283.5401.514

Abstract

Ultraviolet light analysis of a fossil of the theropod dinosaurScipionyx samniticus revealed that the liver subdivided the visceral cavity into distinct anterior pleuropericardial and posterior abdominal regions. In addition, Scipionyx apparently had diaphragmatic musculature and a dorsally attached posterior colon. These features provide evidence that diaphragm-assisted lung ventilation was present in theropods and that these dinosaurs may have used a pattern of exercise physiology unlike that in any group of living tetrapods.

Lung structure and ventilation in theropod dinosaurs is assumed to have resembled the specialized flow-through, air sac pulmonary system of extant birds, the closest living relatives of the theropods (1). However, some fossil soft tissue evidence, as well as osteological similarities between crocodilians and theropods, suggests that these dinosaurs may have had relatively unmodified septate lungs that were ventilated with the assistance of an active, hepatic piston–diaphragm mechanism (2). Those conclusions are based, in part, on the distinct, vertically oriented, thoracic-abdominal separation of the visceral cavity in the theropod Sinosauropteryx (Coelurosauria: Compsognathidae) (Fig. 1, bottom). Additionally, the leading edge of the abdominal cavity in this dinosaur appears to have been defined by a remarkably crocodilian-like, anterior surface of the liver. These attributes, as well as the ubiquitous occurrence among theropods of a triradiate pelvis similar to that of crocodilians, well-developed gastralia, and specialized rib morphology (3), suggest that these dinosaurs had a crocodilian-like septate lung that was ventilated, in part, with a hepatic piston diaphragm. Such a diaphragm was likely to have been powered by diaphragmatic muscles that extended between the pubes, gastralia, and liver (2).

Figure 1

Similar body cavity partitioning in two theropods, Scipionyx (top) andSinosauropteryx (bottom; image digitally reversed for purposes of comparison). Anterior is to the right. Arrows indicate the probable anterior border of the liver, which formed a distinct, vertical subdivision of the pleuropericardial and abdominal cavities. Note also the dorsal position of the posterior colon inScipionyx. The image of Scipionyx was recorded under ultraviolet illumination. Abbreviations: c, colon; pc, posterior colon; ∗, diaphragmatic muscles; ∗∗, pectoral girdle musculature.Scipionyx specimen courtesy of Soprintendenza Archeologica, Salerno, Italy.

A recently described new theropod from Italy, Scipionyx samniticus (Coelurosauria: Maniraptoriformes), contains nearly complete preservation of the articulated skeleton (4). The specimen also has remnants of a variety of soft tissues, including portions of the intestines, liver, trachea, and skeletal muscles (Fig. 1, top). Here we describe these soft tissues and discuss their implications for pulmonary structure and function inScipionyx. We also discuss their significance for earlier conclusions about theropod lung morphology and function.

Portions of the large intestine and trachea of Scipionyx are visible and appear to have been preserved in situ (Fig. 1) (4,5). Notably, the posterior colon, or colorectal intestine, is situated far dorsally, at about the same level as the vertebrae in the lumbar-sacral region. This condition is comparable to the position of the colon in living taxa such as crocodilians and mammals (Fig. 2A) (6). In contrast, the colon (or rectum) of birds is invariably suspended by the dorsal mesentery (mesocolon) so that it is situated in the mid-abdominal cavity, some distance from the roof of the cavity (Fig. 2B) (7). This mid-abdominal suspension of avian large (and small) intestines provides a distinct segregation of the colon from the dorsally and medially attached abdominal air sacs (which extend caudally from the dorsally attached parabronchi). Therefore, it is unlikely that avian-style, abdominal air sacs were present inScipionyx. Abdominal air sacs are of fundamental importance to the function of both neo- and paleopulmo portions of the lung in extant birds (8). Their likely absence inScipionyx is an indication that an avian style, flow-through, air sac lung was not present in this theropod.

Figure 2

Schematic representation of the relation of the posterior colon (pc) to the roof of the abdominal cavity in (A) crocodilians and (B) birds. Areas in gray represent the coelomic cavity. Unlike crocodilians and the theropodScipionyx, the posterior colon of birds is situated some distance from the roof of the visceral cavity. In birds, abdominal air sacs occupy the dorsal abdominal cavity [(B) modified from (7)].

A section of the trachea is preserved in the posterior cervical region, immediately anterior to the scapulocoracoid complex (4). Like the trachea of crocodilians, Scipionyx's trachea in this region is situated well ventral to the vertebral column. In contrast, except in specialized, long-necked birds, the avian posterior cervical trachea is usually positioned dorsally and adjacent to the vertebral column, thereby facilitating entry of the trachea into the dorsally attached parabronchi (9).

In visible light, Scipionyx's liver appears as a small hematic halo restricted to the ventral margin of the visceral cavity (4, 5). However, the liver is more accurately visualized under ultraviolet illumination, where it fluoresces as a suboval, indigo-colored mass that extends from the vertebral column to the ventral body wall (Fig. 1) (10). As in crocodilians,Scipionyx's liver is situated ahead of the large intestine and fills the anteriormost portion of the abdominal cavity (2). Furthermore, as in crocodilians and the theropodSinosauropteryx (Fig. 1), the anterior border of the liver in Scipionyx is vertically oriented and completely subdivides the visceral cavity into anterior pleuropericardial and posterior abdominal regions (2). In bothScipionyx and Sinosauropteryx, the pleuropericardial cavity appears largely empty because delicate lung tissues were not fossilized.

Hepatic piston, diaphragm-assisted breathing in crocodilians is powered by the diaphragmatic muscles that originate on the gastralia and distinctly shaped pubes and insert on the lateral surfaces of the liver (2). As in other theropods, the triradiate pelvis ofScipionyx is remarkably like that of modern and, especially, basal crocodilians (such as protosuchids): in particular, the rodlike rami of the pubes are elongate with a marked distal expansion, or “boot” (Fig. 3) (11). In living crocodilians, these osteological features are particularly well suited to accommodate diaphragmatic muscle function (2). Specifically, the stout, rodlike pubic rami most likely provide enhanced stability required to withstand contractile force of the extensive diaphragmatic muscles; the expanded pelvic boot in crocodilians is necessary to allow sufficient area for attachment of the ventral portion of the diaphragmatic muscles.

Figure 3

Probable remnants of the diaphragmatic muscles inScipionyx. Portions of pectoralis and caudofemoralis muscles are also preserved in the specimen. Abbreviations: dm, diaphragmatic muscle; p, pubis. Specimen courtesy of Soprintendenza Archeologica, Salerno, Italy.

Significantly, a small group of longitudinally oriented muscle fibers that extend anteriorly from the right pubis in Scipionyxappear to be remnants of the diaphragmatic musculature (Figs. 1 and 3) (12). The position and orientation of these fibers resemble some of the posteriormost lateral diaphragmatic muscle fibers in crocodilians (2). The longitudinally oriented, deep external oblique muscle is also found in this region in extant reptiles (13). However, it is unlikely that these fibers inScipionyx were components of this muscle. Tetrapods with parasagittal limb posture, such as theropods, would be unlikely to have had longitudinally oriented flank musculature; such musculature is associated with the production of lateral bending of the trunk during locomotion in animals, such as lizards, that have a sprawling posture (13).

Together, these features are consistent with Scipionyxhaving used hepatic piston, diaphragm-assisted breathing (similar to that which occurs in extant crocodilians) and with hypothesized breathing mechanisms for Sinosauropteryx (2). These attributes are inconsistent with Scipionyx having had an avian-style, lung air sac system. Moreover, data indicative of diaphragm breathing in such disparate forms asSinosauropteryx and Scipionyx reinforce the hypothesis that diaphragm-assisted lung ventilation was widespread in theropod dinosaurs.

The absence of respiratory turbinates in theropod dinosaurs indicates that they were likely to have maintained ectotherm-like resting, or routine, lung ventilation and metabolic rates (14). As in extant reptiles (for example,Varanus), costal breathing seems adequate to have supported active rates of oxygen consumption in such animals. Consequently, on the basis of the physiology of extant, fully terrestrial ectotherms, the necessity for a specialized diaphragm to supplement costal lung ventilation in theropods would seem anomalous. However, recent analysis suggests that expansion of lung ventilatory capacity might have allowed the relatively unmodified septate lungs of dinosaurs to have achieved active rates of O2-CO2exchange that might have approached, or even overlapped, those of a few extant mammals (15). Perhaps the presence of diaphragm-assisted lung ventilation in theropods indicates that, although these dinosaurs maintained ectotherm-like routine metabolic rates, they were, nevertheless, capable of sustaining active oxygen consumption rates and activity levels well beyond those of even the most active living reptiles. Such a pattern of metabolic physiology is unknown in extant tetrapods.

This pattern of metabolic physiology in theropods might seem inconsistent with the presence of a hepatic-piston diaphragm in extant crocodilians, none of which appears to have particularly enhanced capacity for oxygen consumption during exercise (16). However, relatively low aerobic capacity in recent crocodilians, all of which are aquatic, might not represent the ancestral condition. Early (Triassic) crocodylomorphs (for example,Protosuchus and Terrestrisuchus) might have had enhanced aerobic capacities because they appear to have been fully terrestrial and cursorial with habitually upright limb posture (17).

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