Early evolution of diurnal habits in owls (Aves, Strigiformes) documented by a new and exquisitely preserved Miocene owl fossil from China

Abstract

SignificanceOwls, with their largely nocturnal habits, contrast strikingly with the vast majority of diurnal birds. A new spectacular late Miocene owl skeleton from China unexpectedly preserves the oldest evidence for daytime behavior in owls. The extinct owl is a member of the clade Surniini, which contains most living diurnal owl species. Analysis of the preserved eye bones documents them as consistent with diurnal birds, and phylogenetically constrained character mapping coincides with a reconstruction of an early evolutionary reversal away from nocturnal habits in this owl group. These results support a potential Miocene origin of nonnocturnal habits in a globally distributed owl group, which may be linked to steppe habitat expansion and climatic cooling in the late Miocene.

Keywords: Linxia; Strigidae; Surniini; diurnal; fossil.

Fig. 1.

Photograph and line drawing of the complete holotype specimen of M. diurna (STM 20-1). Anatomical abbreviations: al, alular digit; b, bony residue; c, ceratobranchial; cr, cranial process of sternum; dc, deltopectoral crest; ep, extensor process; er, ossified extensor rectinaculum; ex, extensor sulcus; fe, femur; fi, fibula; fm, foramen magnum; hu, humerus; hy, hypotarsal crest; im, intermetacarpal space; is, ischium; lc, lateral condyle; lt, left tibiotarsus; mc, medial condyle; mm, major metacarpal; mp, manual phalanx; ms, mandibular symphysis; mtII, trochlea of metatarsal II; p, patella; pd, pedal digits; pg, paraglossum; qu, quadrate; ra, radius; rad, radiale; ri, rib; rs, rostrum; rt, right tibiotarsus; sc, scapula; sk, skull; so, scleral ossicle; st, sternum; sy, synsacrum; tm, tarsometatarsus; tr, tracheal ring; ul, ulna; and uln, ulnare.

Fig. 2.

(A) Details of the skull of the holotype of M. diurna STM 20-1 and (B) half set of the scleral ring of S. ulula (USNM 610389) superimposed on a flattened reconstruction of the ring in Miosurnia. Abbreviations: af, antorbital fenestra; at, atlas; ax, axis; ba, basihyal; c, ceratobranchial; ci, cricoid; cv, cervical vertebra; dp, dorsal process of jugal bar; EXT, external scleral ring diameter; INT, internal scleral ring diameter; j, jugal; la, lacrimal; lac, lateral mandibular condyle of the quadrate; mec, medial mandibular condyle of the quadrate; na, naris; nf, nutrient foramen; oc, occipital condyle; opq, otic process of the quadrate; pa, palatine; po, postorbital process; ps, parasphenoid; pt, pterygoid; qu, quadrate; so, scleral ossicle; sw, squamosal wing; sy, symphysis; tf, temporal fossa; tn, transverse nuchal crest; tr, tracheal ring; vf, ventral medial foramen; and zy, zygomatic process. The mandibular foramen is indicated with an asterisk.

Fig. 3.

Scatterplot of the pFDA results illustrating the different areas of diurnal and nocturnal species in the discriminant space. The returned pFDA 1 and pFDA 2 are derived from analyses using the average reconstruction of the orbit and scleral ring diameter (SI Appendix, Table S2). The fossil owl is closest to the living diurnal/crepuscular ferruginous pygmy owl (G. brasilianum).

Fig. 4.

Plot of the summary of simmap results. Posterior probabilities are presented for each internode, represented by the individual pie charts with expanded detail of the owl clade (Left). Note the broad diurnal activity across the entire phylogeny, the shift to nocturnal habits among the ancestral owl, and the reconstructed reversal to diurnality in the clade Surniini marked by one of the arrows labeled as (0,1,0). Results of an additional test with extant taxa only are in SI Appendix, Fig. S7.

Fig. 5.

Photographic detail of the thoracic region of M. diurna (STM 20-1) with X-ray computed tomography rendering of the unregurgitated dietary pellet materials preserved in situ. The bone residues are characterized by a honeycomb-like structure, visualized in red, with blue indicating infilling sediments. The different materials were selected and rendered in Avizo (9.2 Thermo Fisher Scientific) based on density related to the gray-scale values of the CT scan.