Thursday 15 January 2015

Preserved stomach contents in Early Cretaceous Ornithuromorph Birds.

The Early Cretaceous Jehol Group of China has produced a remarkable number of well-preserved fossils of Mesozoic Birds, adding greatly to our understanding of the early history of this group, including many specimens with preserved stomach contents, providing useful insights into the diet and biology of these animals. One of the earliest described instances with such contents was a specimen of the Ornithuromorph Bird (all modern Birds are Ornihuromorphs, belonging to a single subgroup of these Birds, the Neornithes), Yanornis martini, which was found with preserved Fish in its abdomen. Subsequent to this a second specimen of the same species was found with a large collection of gastroliths (swallowed stones used to grind up hard food, usually plant matter), leading to this species being considered to be only seasonally piscavorous (Fish-eating), or even primarily herbivorous.

In a paper published in the journal PLoS One on 14 April 2014, Xiaoting Zheng of the Institute of Geology and Paleontology at Linyi University and the Tianyu Natural History Museum of Shandong, Jingmai O’Connor of the Key Laboratory of Vertebrate Evolution and Human Origin at the Institute of VertebratePaleontology and Paleoanthropology, Fritz Huchzermeyer of the Department ofParaclinical Sciences at the University of Pretoria, Xiaoli Wang and Yan Wang of the Institute of Geology and Paleontology at Linyi University, Xiaomei Zhang of the Tianyu Natural History Museum of Shandong and Zhonghe Zhou of the Key Laboratory of Vertebrate Evolution and Human Origin at the Institute of Vertebrate Paleontology and Paleoanthropology, describe ten new specimens of Yanornis martini with preserved stomach contents.

All ten of the new specimens contain Fish in their stomach contents, strongly supporting the idea that this species was primarily piscavorous. In all specimens Fish remains are present in the crop, most have Fish remains within the abdominal cavity and one contains Fish remains along with gastroliths. All specimens are almost complete and well-articulated. Fish within the abdomen are preserved as masses of macerated bones clumped together in the body and overlapped by ribs in lateral view. Fish within the crops are preserved either as bony masses or as body outlines containing bones. Some of the bony masses within the crops resemble the regurgitation pellets produced by some modern piscavorous Birds.

Yanornis martini preserving whole fish in the crop and macerated fish bones in the ventriculus: (A) full slab, scale bar equals five cm; (B) detail of the crop, scale bar equals one cm; (C) detail of the ventriculus, scale bar equals one mm. Zheng et al. (2014).

Several Birds appear to contain identifiable Fish remains. One contains a large assemblage of distinctive scales thought to have come from Protopspherus sp., an early Paddlefish, while three specimens contain complete Fish skeletons attributed to the early Osteoglossomorph ( the group that inlcudes the modern Bone Tonguesa and Mooneyes) Jinanichthys, which is very common in the Jehol beds.

The presence of gastroliths in the body cavity of two specimens of Yanornis martini is problematic. Many modern Birds swallow small stones to help them grind up tough plant matter in their gizzards, which they cannot process orally due to their lack of teeth. Some herbivorous Dinosaurs are also known to have used gastroliths to aid digestion. However no modern Bird uses gastroliths to aid the digestion of Fish, which are a particularly soft form of food, and there seems to be no good reason why Yanornis should have done so either. In addition Yanornis, unlike any modern Bird, had a well-developed set of teeth, although these appear to have been used in prey capture rather than food processing.

The gastroliths of Yanornis martini are highly variable in size, ranging from 0.2 – 2.7 mm. This is unusual, as most modern Birds tend to choose stones of roughly the same size, and other Mesozoic Birds appear to have behaved in a similar way, for example in Archaeorhynchus all the gizzard stones found have been about 2 mm in diameter, and in Hongshanornis they have been about 1 mm in diameter. The majority of the Yanornis gastroliths have been towards the smaller end of the size range, which is also puzzling, as it was a far larger Bird than Hongshanornis, and therefore unlikely to favour much smaller gizzard stones.

One of the preserved Yanornis martini specimens with gastroliths is in lateral view, and shows these stones to be distributed throughout the entire length of the body cavity. This is different to the situation found in preserved gizzard stones, which tend to be found in a tight clump, representing the position of the gizzard. This leads Zheng et al. to conclude that this Bird had inadvertently ingested the stones, probably while feeding on stranded Fish on a shoreline, and subsequently died of sand impaction in the intestinal tract. This is relatively common in modern seabirds, accounting for about 1% of natural deaths (the artificial threat of plastic impaction has proved even more deadly to some species), and has also been recorded in other Birds including domestic poultry. Birds ingest sand particles with their food, which is able to pass freely through the small intestine, where the food is carried in a liquid medium, but is deposited in the large intestine where liquid is reabsorbed. This deposited sand can build up in the ventral-most loop causing the intestine to become blocked. Once this happens nothing else is able to pass through the intestine, and the entire digestive tract will also become blocked, which is eventually fatal.

Interpretative drawing of the alimentary canal of Yanornis superimposed over laterally preserved specimen. Enlarged red box shows preservation of sand compacted in the intestines. The grit is clearly too caudally located to represent gizzard stones. The oesophagus is drawn in a way to demonstrate its flexibility; it leads to the small proventriculus (pyloric sphincter indicated by dashed circle), followed by the larger ventriculus, and then the intestines and cloaca. Scale bar equals 1 cm. Zheng et al. (2014).

The crop of Birds is a modified muscular oesophagus used to store food which cannot be immediately processed or digested. This is thought to be a key evolutionary adaptation for the group, which need a constant supply of food to support the energetic costs of flying, but which cannot afford the extra weight of fatty food reserves used by groups such as Mammals. The crop is a variable organ, with some Birds having evolved highly specialized crops, while others have lost it altogether. In piscavorous Birds it is typically a simple swelling on the oesophagus, though this can be highly expandable (most notably in Pelicans). The crops of Yanornis martini appear to have been essentially similar to those of modern piscavorous Birds, with more than one fish present in the crop of at least one specimen, and others containing disarticulated bones, which may have been going to have been regurgitated, in the manor of modern Cormorants, Raptors and Owls.

A crop has also been found in Hongshanornis, a smaller early Ornithuromorph Bird interpreted to have been herbivorous, and like in modern herbivorous Birds this crop forms a well-developed pouch. This suggests that the crop may have been present in the earliest Ornithuromorphs, though it has never been found in the closely related Enantiornithes. A crop has also been found in the basal Pygostylian Sapeornis, which would suggest that if it was absent in Enantiornithes then it may have been secondarily lost, and possible crops have been suggested in long boney-tailed Bird Jeholornis and the Ornithischian Dinosaur Brachylophosaurus, although since no trace of a crop has ever been found in Theropod Dinosaurs this is probably a case of convergent evolution.

The crop has generally been accepted as an adaptation for storing food without processing, as Birds have lost their teeth, which in turn is explained by a need to reduce weight in order to facilitate flying. However this explanation does not fit with the observed state in Yanornis martini, which has both a well-developed crop and a large number of teeth. Moreover, by the time of the Jehol Biota Birds had been flying for around 30 million years, and toothed Birds are still present in deposits from the Late Cretaceous, 50 million years later, suggesting strongly that the presence of teeth was not a major impediment to flying (Pterosaurs were also for a long time thought to have lost their teeth as an adaptation to flying, but numerous toothed members of this group have also been found from a variety of locations in the last 20 years). Under this explanation the crop evolved to act as a holding area for the muscular gizzard, which took over food processing from the teeth. However while some Jehol Birds (Hongshanornis and Sapeornis) have a gizzard, a crop and a reduced number of teeth, there is no clear pattern in these Birds, and many show very well developed sets of highly specialized teeth. Zheng et al.therefore conclude that teeth were lost in Birds long after the appearance of the crop and gizzard, though the flexible food processing offered by these organs may have facilitated this.

Yanornis martini preserving macerated fish bones in the crop and ventriculus: (A) full slab, scale bar equals four cm; (B) detail of the crop, scale bar equals one cm; (C) detail of the ventriculus, scale bar equals one mm. Zheng et al. (2014).

See also…

The deposits of the Jehol Group in northeastern China have yielded a spectacular number of fossil Birds and closely related non-Avian Theropod Dinosaurs over the past three decades. The most numerous and diverse group of Birds in this assemblage are the Enantiornithines, toothed Birds related but not ancestral to the modern Neornithine Birds, with about 27... 
The dominant group of Birds during much of the Cretaceous Period were the Enatiornithine, toothed Birds related, but not ancestral, to modern Birds. The largest known species of Enatiornithine from the Early Cretaceous is Pengornis houi, described from a...
The two surviving groups of Archosaurs, Crocodilians and Birds, show very different reproductive strategies.  Crocodilians have paired ovaries and produce large clutches of small eggs, which mature slowly prior to being laid, and make a relatively small investment in parental care. Birds have only a single ovary, a...
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