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. 2022 Dec 16:10:e13919.
doi: 10.7717/peerj.13919. eCollection 2022.

Forty new specimens of Ichthyornis provide unprecedented insight into the postcranial morphology of crownward stem group birds

Juan Benito  1   2 , Albert Chen  1   2 , Laura E Wilson  3 , Bhart-Anjan S Bhullar  4   5 , David Burnham  6 , Daniel J Field  2   7
Affiliations

Forty new specimens of Ichthyornis provide unprecedented insight into the postcranial morphology of crownward stem group birds

Juan Benito et al. PeerJ. .

Abstract

Ichthyornis has long been recognized as a pivotally important fossil taxon for understanding the latest stages of the dinosaur-bird transition, but little significant new postcranial material has been brought to light since initial descriptions of partial skeletons in the 19th Century. Here, we present new information on the postcranial morphology of Ichthyornis from 40 previously undescribed specimens, providing the most complete morphological assessment of the postcranial skeleton of Ichthyornis to date. The new material includes four partially complete skeletons and numerous well-preserved isolated elements, enabling new anatomical observations such as muscle attachments previously undescribed for Mesozoic euornitheans. Among the elements that were previously unknown or poorly represented for Ichthyornis, the new specimens include an almost-complete axial series, a hypocleideum-bearing furcula, radial carpal bones, fibulae, a complete tarsometatarsus bearing a rudimentary hypotarsus, and one of the first-known nearly complete three-dimensional sterna from a Mesozoic avialan. Several pedal phalanges are preserved, revealing a remarkably enlarged pes presumably related to foot-propelled swimming. Although diagnosable as Ichthyornis, the new specimens exhibit a substantial degree of morphological variation, some of which may relate to ontogenetic changes. Phylogenetic analyses incorporating our new data and employing alternative morphological datasets recover Ichthyornis stemward of Hesperornithes and Iaceornis, in line with some recent hypotheses regarding the topology of the crownward-most portion of the avian stem group, and we establish phylogenetically-defined clade names for relevant avialan subclades to help facilitate consistent discourse in future work. The new information provided by these specimens improves our understanding of morphological evolution among the crownward-most non-neornithine avialans immediately preceding the origin of crown group birds.

Keywords: Avialae; Birds; Euornithes; Ichthyornis; Mesozoic; Ornithology; Ornithurae; Palaeontology; Postcranial; Skeleton.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Simplified cladogram showing the most commonly recovered phylogenetic positions of Ichthyornis and relevant Mesozoic avialans.
White branches highlight phylogenetic uncertainty within the major clade Ornithurae, which includes Ichthyornis, Hesperornithes, and the bird crown group (Neornithes). Taxa in bold are figured, superscript numbers indicate the corresponding illustration. For Confuciusornithidae, the illustration corresponds to Eoconfuciusornis zhengi; for Enantiornithes, the illustration corresponds to Cathayornis yandica; for Hongshanornithidae the illustration corresponds to Hongshanornis longicresta; for “Yanornithidae” the illustration corresponds to Abitusavis lii; for Hesperornithes the illustration corresponds to Brodavis varneri; for Neornithes the illustration corresponds to Asteriornis maastrichtensis. Quotation marks associated with “Yanornithidae” reflect the fact that this clade has not been consistently recovered in several recent phylogenetic analyses, including the present study. Illustrations courtesy of R. Olivé, used with permission.
Figure 2
Figure 2. Reconstruction of the skeleton of Ichthyornis dispar, showing elements described in the present study that exhibit novel morphological information for Ichthyornis.
Elements in yellow correspond to those skeletal elements not previously known or described for Ichthyornis, while elements in blue indicate those skeletal elements that were known for Ichthyornis but for which novel morphological information is provided by the specimens described in this study. Elements in grey correspond to those for which little novel information is provided by the specimens described here. The reconstructed skeleton is a composite incorporating multiple specimens described in this study (see Table 1). All specimens are scaled to the dimensions of the FHSM VP-18702 specimen.
Figure 3
Figure 3. Reconstruction of the skeleton of Ichthyornis dispar, showing elements that are described here for the first time.
The reconstructed skeleton is a composite incorporating numerous new specimens described in this study (see colour-coded legend and Table 1). All specimens are scaled to the dimensions of FHSM VP-18702.
Figure 4
Figure 4. Anterior cervical vertebrae of Ichthyornis.
(A) ALMNH:Paleo:3316 axis, (B) KUVP 119673 3rd cervical, (C) KUVP 119673 4th cervical, (D) FHSM VP-18702 possible 4th or 5th cervical, and (E) KUVP 119673 6th cervical, in cranial, dorsal, lateral, ventral, and caudal views. (F) KUVP 119673, cervical and anterior thoracic vertebrae in anatomical connection as preserved in the specimen, with probable vertebral numbers indicated. Scale bar equals 5 mm.
Figure 5
Figure 5. Mid and posterior cervical vertebrae of Ichthyornis specimen KUVP 25472.
(A) 6th or 7th cervical vertebra, (B) 7th or 8th cervical vertebra, (C) 10th cervical vertebra and (D) 11th cervical vertebra; in cranial, dorsal, lateral, ventral, and caudal views. Scale bar equals 5 mm.
Figure 6
Figure 6. Anterior thoracic vertebrae of Ichthyornis.
(A) KUVP 25472 12th vertebra, (B) KUVP 119673 12th vertebra, (C) KUVP 119673 13th vertebra, (D) KUVP 119673 14th vertebra, (E) ALMNH:Paleo:3316 13th vertebra, and (F) KUVP 25472 15th vertebra, in cranial, dorsal, lateral, ventral, and caudal views. Scale bar equals 5 mm.
Figure 7
Figure 7. Mid-to-posterior thoracic vertebrae of Ichthyornis specimen KUVP 25472.
(A) Indeterminate mid thoracic vertebra 1, (B) indeterminate mid thoracic vertebra 2, (C) indeterminate mid thoracic vertebra 3, (D) indeterminate posterior thoracic vertebra 1, (E) 2 mid-thoracic vertebrae in anatomical connection; in cranial, dorsal, lateral, ventral, and caudal views. Scale bar equals 5 mm.
Figure 8
Figure 8. Synsacra of Ichthyornis.
(A) FHSM VP-18702, (B) KUVP 119673 (C) KUVP 157821 and (D) ALMNH:Paleo:3316 in dorsal, right lateral, ventral, left lateral and cranial views. Numbers indicate sacral vertebral order. The 1st sacral vertebra in FHSM VP-18702 is incompletely fused, and the 1st and 11th sacral vertebrae in KUVP 119673 are unfused and not pictured here. Scale bar equals 1 cm.
Figure 9
Figure 9. Caudal vertebrae and ribs of Ichthyornis.
(A) KUVP 25472, caudal vertebra indeterminate, (B) KUVP 119673, caudal vertebrae indeterminate; in cranial, dorsal, lateral, ventral and caudal views; (C) FHSM-VP 18702, thoracic and sternal ribs and (D) KUVP 119673 anterior, thoracic, and sternal ribs, in lateral and medial views. Scale bar equals 1 cm.
Figure 10
Figure 10. Sterna of Ichthyornis.
(A) FHSM VP-18702 in left lateral, dorsal, cranial, ventral and right lateral views; (B) KUVP 119673 in dorsal, left lateral and ventral views and (C) NHMUK A 905 in medial, cranial and right lateral views. Scale bar equals 1 cm.
Figure 11
Figure 11. Sterna of Ichthyornis.
(A) YPM 1450 in dorsal, cranial and ventral views and (B) YPM 1461 in left lateral, dorsal, cranial, ventral and right lateral views. Scale bar equals 1 cm.
Figure 12
Figure 12. Furculae of Ichthyornis.
(A) NHMUK A 905 medial furcula fragment in dorsal, ventral, cranial, caudal, lateral and medial views; (B) BHI 6420 left omal furcula fragment, (C) ALMNH:Paleo:3316 right omal furcula fragment and (D) KUVP 157821 right omal furcula fragment, in lateral, dorsal, medial, and ventral views. Scale bar equals 5 mm.
Figure 13
Figure 13. Coracoids of Ichthyornis.
(A) FHSM VP-18702 right coracoid, (B) BHI 6420 right coracoid omal and sternal fragments, (C) KUVP 119673 right coracoid, (D) KUVP 2281 left coracoid, (E) KUVP 2284 right coracoid and (F) MSC 7841 right coracoid, in dorsal, lateral, ventral and medial views. Scale bar equals 1 cm.
Figure 14
Figure 14. Scapulae of Ichthyornis.
Views for each in clockwise order: medial, lateral, ventral, dorsal. (A) FHSM VP-18702 left scapula, (B) KUVP 2281 left scapula, and (C) NHMUK A 905 right scapula. Scale bar equals 1 cm.
Figure 15
Figure 15. Size distribution of Ichthyornis humeri.
Largely complete humeri included in this study in cranial and caudal views. Scale bar equals 1 cm.
Figure 16
Figure 16. Three-dimensional morphology of Ichthyornis humeri.
Showing the three-dimensionally preserved humerus of KUVP 119673 (A) and KUVP 2300 (C) in comparison with the flattened left humerus of KUVP 119673 (B), in cranial, dorsal, caudal, ventral and proximal views. Scale bar equals 1 cm.
Figure 17
Figure 17. Detailed proximal and distal morphology of Ichthyornis humeri.
(A) ALMNH:Paleo:1786 right proximal humerus in cranial, caudal and proximal views; and (B) MSC 7841 right distal humerus in cranial, caudal and lateral views. Scale bar equals 5 mm.
Figure 18
Figure 18. Ulnae of Ichthyornis.
(A) FHSM VP-18702 in dorsal and ventral views, (B) KUVP 119673 in cranial, dorsal, caudal and ventral views, (C) KUVP 2284 in cranial and caudal views, (D) YPM 1450 and (E) YPM 1740 in cranial, dorsal, caudal and ventral views. Scale bar equals 1 cm.
Figure 19
Figure 19. Detailed proximal and distal morphology of Ichthyornis ulnae.
(A) MSC 5916 left proximal ulna and (B) MSC 7841 left distal ulna in cranial, dorsal, caudal, ventral and proximal views. Scale bar equals 5 mm.
Figure 20
Figure 20. Radii of Ichthyornis.
(A) KUVP 25472, (B) KUVP 119673 and (C) YPM 1471 in cranial, dorsal, caudal and ventral views, (D) proximal radius of MSC 6200 and (E) distal radius of KUVP 157821 in cranial, dorsal, caudal and ventral views. Scale bars equals 1 cm.
Figure 21
Figure 21. Free carpal bones of Ichthyornis.
(A) ALMNH:Paleo:3316 right ulnar carpal and (B) KUVP 2284 left ulnar carpal in cranial, dorsal, caudal, ventral and proximal views; (C) FHSM VP-18702 left radial carpal, in cranial, dorsal, caudal, ventral, proximal and distal views. Scale bar equals 5 mm.
Figure 22
Figure 22. Carpometacarpi of Ichthyornis.
(A) YPM 1724, (B) FHSM VP-18702, (C) BHI 6420, (D) KUVP 123459 and (E) KUVP 157821, in cranial, dorsal, caudal, ventral, proximal and distal views. Scale bar equals 5 mm.
Figure 23
Figure 23. Manual phalanx II-1 of Ichthyornis.
(A) FHSM VP-18702 left phalanx, (B) KUVP 2284 right phalanx, (C) ALMNH:Paleo:3316 right phalanx, (D) BHI 6420 right phalanx and (E) BHI 6421 right phalanx, in dorsal (left) and ventral (right) views. Scale bar equals 5 mm.
Figure 24
Figure 24. Manual phalanges II-2 and III-1 of Ichthyornis.
(A) KUVP 25469 right II-2 phalanx, (B) ALMNH:Paleo:3316 right II-2 phalanx and (C) BHI 6420 right II-2 phalanx in caudal, ventral, dorsal and cranial views; and (D) III-1 phalanx in dorsal and ventral views. Scale bar equals 5 mm.
Figure 25
Figure 25. Pelves of Ichthyornis specimen KUVP 119673.
(A) Right pelvis and (B) left pelvis, in lateral and medial views. Scale bar equals 1 cm.
Figure 26
Figure 26. Femora of Ichthyornis.
(A) ALMNH:Paleo:3316 left femur in cranial, lateral, caudal and medial views; (B) proximal right femur of ALMNH:Paleo:1319 in (clockwise order from upper left) cranial, caudal, lateral, dorsal and medial views and (C) right femur of FHSM VP-18702 in medial (left) and caudal (right) views. Scale bar equals 5 mm.
Figure 27
Figure 27. Tibiotarsi and fibula of Ichthyornis.
(A) ALMNH:Paleo:3316 left tibiotarsus proximal and distal fragments, (B) FHSM VP-18702 right tibiotarsus, (C) ALMNH:Paleo:3412 left distal tibiotarsus and (D) FHSM VP-18702 right fibula. Scale bars equal 5 mm.
Figure 28
Figure 28. Tarsometatarsi of Ichthyornis.
(A) ALMNH:Paleo:3316 left tarsometatarsus proximal and distal fragments, (B) FHSM VP-18702 right tarsometatarsus, (C) ALMNH:Paleo:1310 left distal tarsometatarsus and (D) MSC 13214 right tarsometatarsus proximal and distal fragments. Scale bar equals 5 mm.
Figure 29
Figure 29. Pedal phalanges of Ichthyornis.
FHSM VP-18702 (A) phalanx III:1?, (B) phalanx III:2?, (C) phalanx IV:1? (D) phalanx IV:2?; ALMNH:Paleo:3316 (E) phalanx IV:1? Scale bar equals 5 mm.
Figure 30
Figure 30. Phylogenetic results of analyses using a modified version of the morphological matrix from Torres, Norell & Clarke (2021), excluding Apsaravis ukhaana.
(A) Results from Bayesian inference; node values indicate Bayesian posterior probabilities. (B) Results of parsimony analyses: single most parsimonious tree, branch values indicate bootstrap support values (left of bar) and Bremer decay indices (right of bar). Taxonomic names in white indicate taxa illustrated in the figure, the corresponding illustration is indicated by the superscript numbers. Branches in white indicate the position of Ichthyornis dispar, the focal taxon of this study. Illustrations courtesy of R. Olivé, used with permission.
Figure 31
Figure 31. Phylogenetic results of analyses using a modified version of the morphological matrix from Wang et al. (2020c), excluding Apsaravis ukhaana.
(A) Results from Bayesian inference; node values indicate Bayesian posterior probabilities. (B) Results from parsimony analyses; strict consensus of ten most parsimonious trees, branch values indicate bootstrap support values (left of bar) and Bremer decay indices (right of bar). Taxonomic names in white indicate taxa illustrated in the figure. Branches in red indicate the position of Falkatakely forsterae, highlighting remarkable lability in its phylogenetic position recovered from analyses employing different phylogenetic optimality criteria. Branches in white indicate the position of Ichthyornis dispar, the focal taxon of this study. Illustrations courtesy of R. Olivé, used with permission.
Figure 32
Figure 32. Body mass estimates for selected Ichthyornis specimens.
Body mass correlates represented, in order of increasing Percent Prediction Error (after Field et al., 2013) are: maximum diameter of the coracoid’s humeral articulation facet (HAF), maximum coracoid lateral length (CLL), least coracoid shaft width (CSW), maximum humerus length (HL), least humerus shaft circumference (HC), least humerus shaft diameter in cranial view (HD), maximum femur length (FL), least femur shaft circumference (FC), least femur shaft diameter in cranial view (FD) and maximum tarsometatarsus length (TaL). The vertical box and bold text indicate the probable immature nature of specimen KUVP 2284.
Figure 33
Figure 33. Skeletal reconstructions of Ichthyornis dispar.
(A) Three-dimensional skeletal reconstruction using a composite of the specimens described in this study; (B), complete skeletal reconstruction of Ichthyornis dispar, including reconstructed fragmentary and missing elements. The reconstruction shown here includes unfused uncinate processes on the thoracic ribs, which we consider to be the most conservative explanation for their absence in known specimens of Ichthyornis; see the morphological description for discussion on the presence of uncinate processes in Ichthyornis. Skeletal reconstruction courtesy of K. van Grouw, used with permission.
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