Fossil Evidence of Avian Crops from the Early Cretaceous of China

Fossil evidence of avian crops from the Early Cretaceous of China Xiaoting Zhenga,b, Larry D. Martinc, Zhonghe Zhoud,1, David A. Burnhamc, Fucheng Zhangd, and Desui Miaoc aInstitute of Geology and Paleontology, Linyi University, Linyi, Shandong 276000, China; bShandong Tianyu Museum of Nature, Pingyi, Shandong 273300, China; cDivision of Vertebrate Paleontology, Biodiversity Institute, University of Kansas, Lawrence, KS 66045; and dKey Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China Contributed by Zhonghe Zhou, August 3, 2011 (sent for review July 13, 2011) The crop is characteristic of seed-eating birds today, yet little is A number of other Mesozoic birds and their theropod relatives known about its early history despite remarkable discoveries of have recently been reported with gizzard stones (gastroliths), in- many Mesozoic seed-eating birds in the past decade. Here we re- cluding the basal ornithurines Yanornis (8) and Archaeorhynchus port the discovery of some early fossil evidence for the presence of (9), the oviraptosaur Caudipteryx, and the ornithomimosaur a crop in birds. Two Early Cretaceous birds, the basal ornithurine Shenzhousaurus (10), confirming that the presence of a muscular Hongshanornis and a basal avian Sapeornis, demonstrate that an grinding stomach is primitive for birds. It may well have occurred essentially modern avian digestive system formed early in avian in most species but is only documented in forms that foraged evolution. The discovery of a crop in two phylogenetically remote on the ground and thereby came into contact with small stones. lineages of Early Cretaceous birds and its absence in most inter- The discovery of crops in combination with stomach stones vening forms indicates that it was independently acquired as a spe- demonstrates the presence at an early date of an essentially cialized seed-eating adaptation. Finally, the reduction or loss of modern avian digestive system. teeth in the forms showing seed-filled crops suggests that grani- vory was possibly one of the factors that resulted in the reduction Description and Comparison of teeth in early birds. Among the avian specimens we examined at the Tianyu Museum of Nature, at least three preserve clear evidence of a crop. Of paleornithology | feeding these, Sapeornis chaoyangensis (2, 3) is the most basal bird that preserves this structure, and we discovered two examples (STM espite the discoveries of more than 30 genera of fossil birds 15-15 and STM 15-29). STM 15-29 (Fig. 2 A and B) is a semi- from the Early Cretaceous lacustrine deposits in north- articulated skeleton with the neck and head pulled away from the D z eastern China and many examples of dietary adaptations (1), it body for 5 cm. The skeleton is exposed dorsolaterally, with the remains unknown whether a crop was present in these birds. wings folded. The right manus has moved away from the body. Recently we examined hundreds of Early Cretaceous birds The sacrum is viewed dorsally, but the legs are laterally exposed. The crop is represented by a roughly circular mass (z3cmin housed at the Tianyu Museum of Nature in Shandong Province, diameter) of seeds. The outside was rimmed by a layer of larger China, and found several specimens belonging to two taxa with seeds ranging from 4 to 6 mm in diameter, and the anterior unequivocal evidence of crops. One of them is Sapeornis, one of portion of this layer had floated out, spreading over an area of the basal birds presumed to have an herbivorous diet (2, 3), and some 9 × 2.5 cm (Fig. 2B). The center of the mass is densely the second taxon is the basal ornithurine Hongshanornis (4). packed with more than 70 smaller seeds showing an individual Both have preserved seeds in the anatomical location of the crop diameter of z2 mm. The seed mass was inset against the front of in extant birds. In some cases, even the soft tissue outline of the the furcula as in modern birds. The second specimen, STM 15-15 crop can be observed and resembles closely the structure in (Fig. 2 C and D) shows a cylindrical discoloration (darkening) of modern birds. the sediments just below the ventral surface of the cervical ver- In extant birds a crop is a ventral pouch of the esophagus tebrae, extending a few centimeters anteriorly. This seems to be and is situated anterior to the shoulder girdle just in front of a trace of the esophagus, and it is faintly visible around the seed the furcula (5) (Fig. 1). In fossils its position is indicated by mass. The seeds were closely packed one against the other, in- a roughly spherical mass of seeds that is easily discriminated dicating that there was little or no fleshy surface around them. from stomach contents by its location outside of the ribcage. The postcranial skeleton is nearly intact, with the ribcage still in The discovery of a crop in two phylogenetically separate avian its original position. Counting five vertebrae posterior to the end lineages opens a window for our understanding of dietary ad- of the neck and within the ribcage there is a small mass of pol- aptation in the early avian radiation and may also help us better ished stones. A few of the stones are scattered away from the understand the great diversity in the Early Cretaceous, which main concentration. The main mass indicates the position of the occurred approximately 20 million years after the earliest bird, gizzard. Just posteroventral to this mass is a pocket of coprolitic Archaeopteryx (6, 7). material in the position of the intestines. The outline of the In modern seed-eating birds the crop provides storage, so that skeleton and positioning of the crop and gizzard is remarkably similar to that found in modern birds (Fig. 2). a number of seeds can be gathered quickly and then processed fi later in a more secure location without interference from com- The skeleton of Sapeornis,asinArchaeopteryx, lacks an ossi ed petitors and/or predators. The mucus in the crop softens hard sternum, but the maxilla was edentulous, whereas the premaxilla has a small number of teeth that are elongated anteroposteriorly. seeds so that they are more easily ground by the gizzard. The The mandible was toothless and covered by a horny bill, as was gizzard may be a more basal feature for birds, because it is widely distributed in sister groups, such as modern crocodilians. In re- cent birds the gizzard is posterior to the proventriculus or glan- Author contributions: X.Z., L.D.M., and Z.Z. designed research; X.Z., L.D.M., Z.Z., and D.M. dular part of the stomach. The practice of collecting large performed research; X.Z., D.A.B., and F.Z. contributed new reagents/analytic tools; D.A.B. numbers of small stones in the gizzard is characteristic of seed and F.Z. analyzed data; and L.D.M., Z.Z., and D.M. wrote the paper. eaters among modern birds and is often correlated with a well- The authors declare no conflict of interest. developed crop. 1To whom correspondence should be addressed. E-mail: [email protected]. 15904e15907 | PNAS | September 20, 2011 | vol. 108 | no. 38 www.pnas.org/cgi/doi/10.1073/pnas.1112694108 Downloaded by guest on October 3, 2021 Fig. 1. Relative position of the crop (c) and gizzard (g) in a modern bird (some skeletal elements removed for clarity). e, esophagus. probably also the case with the maxilla. It seems that the pre- maxillary teeth in Sapeornis were suitable for cutting fibrous material, such as stems attached to seeds, and this was likely the use of the horny bill as well. One specimen of the basal ornithurine bird Hongshanornis longicresta (4) (STM 35-3; Fig. 3) shows a seed mass in front of the furcula that extends under the anterior sternum, a position Fig. 2. Photographs of two specimens of Sapeornis chaoyangensis housed similar to that for the crop in the modern hoatzin. Hongshanornis at the Tianyu Museum of Nature with preservation of a crop. (A) STM 15-29, is a small ornithurine characterized by a short wing and the total a partially articulated skeleton. (B) Close-up view of the crop region anterior to the furcula on the counterslab of STM 15-29. (C) STM 15-15, a nearly loss of teeth. It was thought in some ways to be more basal than complete articulated skeleton. (D) Close-up view of the crop region anterior Yanornis (9). There are more than 20 seeds in STM 35-3, and to the furcula in STM 15-15. Arrows point to seeds in the crop. c, crop; cv, they are all of one type, being oval and approximately 4 mm long cervical vertebrae; f, furcula; gs, gizzard stone; se, seed. and 2 mm wide (Fig. 3B). Posteriorly, below the position of the fifth dorsal vertebra, there is a mass of more than 50 small independently several times in various lineages of early avian (1-mm) gastroliths, indicating a muscular gizzard at approxi- EVOLUTION mately the usual position in birds. evolution [e.g., Sapeornis, Zhongjianornis (14), Confuciusornithidae (15), Enantiornithes (16) and Ornithurae (4, 9)]. All birds from Discussion the beginning of the Cenozoic are toothless. Although reduction Most modern birds with crops are seed eaters and use crops to of body weight has often been cited as an important factor for store and soften foods and regulate their flow through the di- reduction or loss of teeth in birds, we believe the dietary adap- gestive tract before they pass to a powerfully muscled portion of tation was probably an equally if not more important factor in the stomach, the gizzard (5).

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