Intra-gastric phytoliths provide evidence for folivory in basal avialans of the Early Cretaceous Jehol Biota

Abstract

Angiosperms became the dominant plant group in early to middle Cretaceous terrestrial ecosystems, coincident with the timing of the earliest pulse of bird diversification. While living birds and angiosperms exhibit strong interactions across pollination/nectivory, seed dispersal/frugivory, and folivory, documentation of the evolutionary origins and construction of that ecological complexity remains scarce in the Mesozoic. Through the first study of preserved in situ dietary derived phytoliths in a nearly complete skeleton of the early diverging avialan clade Jeholornithidae, we provide direct dietary evidence that Jeholornis consumed leaves likely from the magnoliid angiosperm clade, and these results lend further support for early ecological connections among the earliest birds and angiosperms. The broad diet of the early diverging avialan Jeholornis including at least fruits and leaves marks a clear transition in the early evolution of birds in the establishment of an arboreal (angiosperm) herbivore niche in the Early Cretaceous occupied largely by birds today. Morphometric reanalysis of the lower jaw of Jeholornis further supports a generalized morphology shared with other herbivorous birds, including an extant avian folivore, the hoatzin.

Fig. 1. Line-drawing, photography, and CL scans of the specimen of Jeholornis prima (IVPP V14978).

The stomach area from which the phytoliths were extracted is shaded gray in (a) and shown in the CL scan in (d). c, d are focused views of the skull and thoracic region from the CL scans. Black arrows in (d) indicate the gastroliths preserved associated with the residue (black arrows in b) sampled from the digestive tract, and the parallel white arrows indicate thoracic and sternal ribs. c coracoid, cav caudal vertebrate, cb ceratobranchial, che chevron, cv cervical vertebrate, de dentary, ep epibranchial, fe femur, fr frontal, gst gastroliths, hu humerus, II-2 manual digit phalanx II-2, III-3 manual digit phalanx III-3, isc ischium, jp jugal process, ju jugal, lc lacrimal, na nasal, pa parietal, pd postdentary, pl palatine, pm premaxilla, pob postorbital, pu pedal ungual, pub pubis, pzg pre- and post-zygapophyses, qu quadrate, rec rectrix, res residue, sc scapula, sk skull, stc stomach content, sq squamosal, syn synsacrum, tib tibiotarsus, tmt tarsometatarsus, to tooth, ul ulnae, w wing feathers.

Fig. 2. Comparison between fossil phytoliths extracted from the digestive tract of Jeholornis prima (IVPP V14978) and modern phytoliths.

a, b Fossil blocky phytoliths with wavy ridgelines from the stomach content of Jeholornis prima (IVPP V14978), consistent with the blocky phytoliths in modern magnoliid leaves; c blocky phytoliths with wavy ridgelines, extracted from Lirianthe coco leaves (an extant species of Magnoliales) collected from Guangxi Province, China; d, e fossil phytoliths with radiate lines and a conical projection in the center, which is similar to the hair base phytoliths in modern plants; f hair base phytoliths extracted from extant Ficus tikoua leaves collected from Gongga Mountain, Sichuan, China. Scale bar is equal across all panels.

Fig. 3. PCA plot of 3D lower jaw shape including Jeholornis and extant birds, with a focus on comparison with extant herbivorous birds.

The 3D model of the mandible of Jeholornis prima is based on Jeholornis prima STM 3–8 (see ref. ).

Fig. 4. Artist’s reconstruction of Jeholornis prima with potential angiosperm arboreal herbivorous feeding ecology proposed here.

The leaf of Cretaceous angiosperm was reconstructed as the diet of Jeholornis.