Archaeorhynchus preserving significant soft tissue including probable fossilized lungs

Abstract

We describe a specimen of the basal ornithuromorph Archaeorhynchus spathula from the Lower Cretaceous Jiufotang Formation with extensive soft tissue preservation. Although it is the fifth specimen to be described, unlike the others it preserves significant traces of the plumage, revealing a pintail morphology previously unrecognized among Mesozoic birds, but common in extant neornithines. In addition, this specimen preserves the probable remnants of the paired lungs, an identification supported by topographical and macro- and microscopic anatomical observations. The preserved morphology reveals a lung very similar to that of living birds. It indicates that pulmonary specializations such as exceedingly subdivided parenchyma that allow birds to achieve the oxygen acquisition capacity necessary to support powered flight were present in ornithuromorph birds 120 Mya. Among extant air breathing vertebrates, birds have structurally the most complex and functionally the most efficient respiratory system, which facilitates their highly energetically demanding form of locomotion, even in extremely oxygen-poor environments. Archaeorhynchus is commonly resolved as the most basal known ornithuromorph bird, capturing a stage of avian evolution in which skeletal indicators of respiration remain primitive yet the lung microstructure appears modern. This adds to growing evidence that many physiological modifications of soft tissue systems (e.g., digestive system and respiratory system) that characterize living birds and are key to their current success may have preceded the evolution of obvious skeletal adaptations traditionally tracked through the fossil record.

Keywords: Aves; Jehol; Ornithuromorpha; lungs; respiration.

Fig. 1.

Archaeorhynchus STM7-11 (main slab, dorsal view) preserving integument (millimeter scale visible in Lower lefthand corner). Small rectangles indicate autapomorphies of Archaeorhynchus, enlarged for detail [spatulate edentulous dentary (10× magnification); coracoid with wide omal margin and blunt procoracoid (3× magnification); metatarsal I and digit I reduced (3× magnification)]. ac, acrocoracoid process; mtI, metatarsal I; pr, procoracoid process. Numbers refer to the six rectrices on the Right side of the body. Image courtesy of J. Zhang (Institute of Vertebrate Paleontology and Paleoanthropology, Beijing).

Fig. 2.

Comparison of the macroscopic and microscopic lung morphology in Archaeorhynchus STM7-11 and living birds: (A) counterslab of STM7-11 showing the ventral aspect (medial surface of ribs exposed): plausible lung tissue is located in the boxed area (enlarged in B). (Scale bar, 1 cm.) (B) Close-up of lungs with arrows indicating impressions made by the ribs. (Scale bar, 1 cm.) Boxed area is enlarged on C. (C) Close-up of the boxed area in B showing the costal impressions (red arrows) on the presumptive right lung. (Scale bar, 5 mm.) (D) Dorsal view of the embryonic lungs of the ostrich (Struthio camelus) showing deep costal sulci (rib impressions). (Scale bar, 3 cm.) (E) A longitudinal slice of the embryonic lung of the domestic fowl (Gallus gallus domesticus) showing deep costal sulci (rib impressions), (Scale bar, 1 mm.) (F) SEM image of sample ‘2’ from the lung preserved in the counterslab showing presumptive parabronchus of the fossilized lung. The parabronchial lumen is surrounded by parenchyma (gas exchange tissue)-like tissue. (Scale bar, 10 μm.) (G) Latex cast preparation of the lung of the domestic fowl showing a parabronchus that consists of a parabronchial lumen (PL) surrounded by exchange tissue (ET). (Scale bar, 250 μm.) (H) Close up of boxed area in F showing presumptive gas exchange tissue with minuscular air space-like cells (some of which are indicated by asterisks) that resemble the air capillaries of the lung of the modern avian lung. (Scale bar, 5 μm.) (I) Exchange tissue of the lung of the ostrich showing air capillaries (asterisks), the terminal gas exchange units. (Scale bar, 20 μm.) cs, costal sulci; ET, parenchyma-like tissue for gas exchange; LL, left lung; PL, probable parabronchial lumen; RL, right lung; tr, trachea; vc, location of the vertebral column.

Fig. 3.

Details of the feathers preserved in Archaeorhynchus STM7-11. (A) details of rectrices forming the tail fan showing the medially striped rachis (white arrows indicate edge of rachis and medial stripe). (Scale bar, 5 mm.) (B) Apparently rachis-less body feathers covering the neck. (Scale bar, 1 mm.) (C) Pennaceous secondary covert of the right wing preserved as an impression in the carbon (white arrow indicates narrow rachis). (Scale bar, 1 mm.) (D) Pennaceous secondary coverts of the left wing (counterslab; arrow indicates rachis). (Scale bar, 5 mm.) (E) Pennaceous secondary coverts of the left wing (main slab). (Scale bar, 5 mm.) (Scale bars in A, D, and E equal 5 mm, and in B and C they equal 1 mm.) Image courtesy of J. Zhang (Institute of Vertebrate Paleontology and Paleoanthropology, Beijing).