A new ornithuromorph (Aves) with an elongate rostrum from the Jehol Biota, and the early evolution of rostralization in birds

Abstract

A new species of Early Cretaceous ornithuromorph with an elongate rostrum is described from the Sihedang locality of the Lower Cretaceous Yixian Formation in north-eastern China. Like the longipterygid enantiornithines, rostral elongation in Dingavis longimaxilla gen. et sp. nov. is achieved primarily through the maxilla, whereas neornithines elongate the premaxilla and rostralization is far more extreme than observed in early birds. Notably, in the rostrum of Xinghaiornis, the most ‘longirostrine’ Early Cretaceous ornithuromorph, the premaxilla and maxilla contribute to the rostrum equally. These lineages together highlight the diversity of configurations in which early birds experimented with rostralization of the skull. The 65% upper limit in rostral proportions of Early Cretaceous taxa with elongate maxillae and the fact that this morphology was abandoned in more derived taxa suggests that in Aves this skull configuration provided less structural stability.

Full text

Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=tjsp20
Download by: [Jingmai K. O’Connor] Date: 15 January 2016, At: 06:38
Journal of Systematic Palaeontology
ISSN: 1477-2019 (Print) 1478-0941 (Online) Journal homepage: http://www.tandfonline.com/loi/tjsp20
A new ornithuromorph (Aves) with an elongate
rostrum from the Jehol Biota, and the early
evolution of rostralization in birds
Jingmai K. O'Connor, Min Wang & Han Hu
To cite this article: Jingmai K. O'Connor, Min Wang & Han Hu (2016): A new ornithuromorph
(Aves) with an elongate rostrum from the Jehol Biota, and the early evolution of rostralization
in birds, Journal of Systematic Palaeontology, DOI: 10.1080/14772019.2015.1129518
To link to this article: http://dx.doi.org/10.1080/14772019.2015.1129518
View supplementary material
Published online: 11 Jan 2016.
Submit your article to this journal
Article views: 74
View related articles
View Crossmark data

A new ornithuromorph (Aves) with an elongate rostrum from the Jehol Biota, and
the early evolution of rostralization in birds
Jingmai K. O’Connor *, Min Wang and Han Hu
Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China
(Received 16 June 2015; accepted 24 November 2015)
A new species of Early Cretaceous ornithuromorph with an elongate rostrum is described from the Sihedang locality of the
Lower Cretaceous Yixian Formation in north-eastern China. Like the longipterygid enantiornithines, rostral elongation in
Dingavis longimaxilla gen. et sp. nov. is achieved primarily through the maxilla, whereas neornithines elongate the
premaxilla and rostralization is far more extreme than observed in early birds. Notably, in the rostrum of Xinghaiornis,
the most ‘longirostrine’ Early Cretaceous ornithuromorph, the premaxilla and maxilla contribute to the rostrum equally.
These lineages together highlight the diversity of configurations in which early birds experimented with rostralization
of the skull. The 65% upper limit in rostral proportions of Early Cretaceous taxa with elongate maxillae and the fact that
this morphology was abandoned in more derived taxa suggests that in Aves this skull configuration provided less structural
stability.
http://zoobank.org/urn:lsid:zoobank.org:pub:9D8A429F-BBA7-47EF-BFD0-ADFB7118833A
Keywords: Ornithothoraces; Cretaceous; Jehol; Mesozoic birds; skull
Introduction
The rostrum (facial skeleton) is the most variable portion
of the archosaur skull and extant birds cover nearly the
entire spectrum of viable skull morphospace (Marug
an-
Lob
on & Buscalioni 2003). In neornithines, the rostrum is
defined by the premaxilla (Baumel & Witmer 1993) and
the maxilla is heavily reduced and fused to the premaxilla,
not significantly contributing to the facial skeleton, but in
non-avian theropods and basal birds the rostrum is formed
by both the premaxilla and maxilla. Here we use the term
‘rostrum’ to refer to the facial skeleton following
Marug
an-Lob
on & Buscalioni (2003). In extant avian
theropods, the neornithines, the contribution of the ros-
trum to the skull varies from 30 to <85%, and the beak
encompasses a huge variety of morphologies (Marug
an-
Lob
on & Buscalioni 2003; Gill 2007). The rostrum and its
horny beak, together with the jaw musculature, form the
avian feeding mechanism. While tooth morphology can
be used to infer diet in mammals, neornithines lack teeth
and have adapted the shape of their rostra to suit a diver-
sity of feeding habits (e.g. carnivorous, filter-feeding,
mud-probing, seed-eating), allowing them to access a
wide variety of trophic resources (Gill 2007). However,
thus far this diversity appears to be largely a characteristic
of Neornithes despite the fact that Cretaceous pterosaurs
achieved extreme rostral proportions (Marug
an-Lob
on &
Buscalioni 2003). Rostral proportions in early birds as far
as we know are much more conservative (O’Connor &
Chiappe 2011). The earliest bird, the Late Jurassic
Archaeopteryx, has a mesorostrine skull (rostral contribu-
tion 5070%) in which the rostrum accounts for roughly
half the total length (rostral length is very difficult to pre-
cisely measure from most fossil specimens). Mesorostral
proportions also represent the plesiomorphic condition
within both Archosauria and Theropoda (Marug
an-Lob
on
& Buscalioni 2003). Similar proportions were retained in
other basalmost birds Jeholornis (52%), Confuciusornis
(55%) and Sapeornis (53%), lineages all found only in the
Early Cretaceous Jehol Biota (130.7120 Ma) (Z. Zhou
2006; Z.-H. Zhou & Zhang 2006). Only in the most
diverse clade, the Enantiornithes, were significant excur-
sions in rostral proportions observed (Zhang et al. 2000;
Hou et al. 2004; Morschhauser et al. 2009; O’Connor
et al. 2009). However, even these departures remained
within the mesorostrine morphospace with the rostrum of
Longipteryx representing the upper known limit, contrib-
uting to 65% of the skull length (O’Connor & Chiappe
2011). All Jehol enantiornithines with rostral elongation
are inferred to form a clade, the Longipterygidae
(O’Connor et al. 2009). Although once considered the
most diverse recognized Early Cretaceous enantiornithine
*Corresponding author. Email: jingmai@ivpp.ac.cn
ÓThe Trustees of the Natural History Museum, London 2016. All rights reserved.
Journal of Systematic Palaeontology, 2016
http://dx.doi.org/10.1080/14772019.2015.1129518
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

clade, in some recent analyses the group has collapsed
into two clades, the Longipterygidae Boluochia CLongip-
teryx and the Longirostravidae Rapaxavis CShanweiniao
CLongirostravis (O’Connor et al. 2009; S. Zhou et al.
2014).
The Early Cretaceous record of the Ornithuromorpha,
the derived avian lineage that includes living birds, has
steadily grown over the last decade due nearly entirely to
discoveries of largely complete specimens from the Jehol
Group in north-eastern China (S. Zhou et al. 2013b;S.
Zhou et al. 2014; M. Wang et al. 2015). At the last time
rostral proportions were investigated in the Enantior-
nithes, the sister group to the Ornithuromorpha and the
first major avian radiation, no ornithuromorph preserved
rostral proportions similar to those observed in the longip-
terygids; Yanornis had the most elongate rostrum, contrib-
uting approximately 57% of the skull length. However,
new discoveries have expanded the range of known rostral
proportions in the Ornithuromorpha, and the recently
described taxon Xinghaiornis lini has the longest recog-
nized Early Cretaceous avian rostrum, forming approxi-
mately 67% of the total skull length (X.-R. Wang et al.
2013). Here we describe another specimen with relatively
elongate rostral proportions representing a new species,
Dingavis longimaxilla gen. et sp. nov. We compare the
structure of the rostrum in the new specimen to that of
Xinghaiornis and longipterygid enantiornithines, and dis-
cuss the bearing of this discovery on our current under-
standing of rostral evolution in early birds.
Systematic palaeontology
Class Aves Linnaeus, 1758
Pygostylia Chiappe, 2002
Ornithothoraces Chiappe, 1995
Ornithuromorpha Chiappe 2001
Definition. The first ancestor of Neornithes that is not
also an ancestor of the Enantiornithes, and all of its
descendants.
Remarks. We use the formerly node-based taxon Orni-
thuromorpha (Chiappe 2001,2002) to refer to Neornithes
and all taxa that are more closely related to it than to the
Enantiornithes (O’Connor et al. 2015). We are thus pro-
viding this taxon with a stem-based definition. Although
the proposed definition does not strictly equate with the
published node-based definition, it does provide a formal
definition for the current widespread usage of this term in
most recent literature (Bell et al. 2010; O’Connor et al.
2010; S. Zhou et al. 2013a; M. Wang et al. 2015). We feel
that node-based definitions are premature at this time
given the fluctuating morphology of basal bird phyloge-
nies and the rapid rate of discovery of new material. For
example, the avian status of Archaeopteryx is now
debated, with growing evidence this taxon may be more
closely related to troodontids (Xu et al. 2011). Further-
more, it is recognized that the next youngest avifauna, the
Jehol, represents a relatively derived fauna with the earli-
est known ornithuromorphs being already derived mem-
bers of a specialized clade of Early Cretaceous waders,
the Hongshanornithidae (M. Wang et al. 2015). Therefore,
any node-based definition at this time would be expected
to change, especially if any fossils are found that fill the
temporal gap between Archaeopteryx and the Jehol avi-
fauna. We support the use of stem-based definitions until
we achieve greater phylogenetic clarity.
Genus Dingavis gen. nov.
Type species. Dingavis longimaxilla sp. nov.
Etymology. The genus name is in honour of the late dis-
tinguished Chinese geologist Wenjiang Ding, often con-
sidered the ‘father of Chinese geology’, who brought
Amadeus William Grabau to Beijing University in 1920.
Professor Ding was the first person to teach palaeontology
in China and he also served as the chief editor
of Palaeontologia Sinica, one of the earliest Chinese jour-
nals to receive international recognition.
Diagnosis. See diagnosis of type and only species below.
Dingavis longimaxilla sp. nov.
(Figs 13)
Diagnosis. A large basal ornithuromorph with the follow-
ing unique combination of characters: rostrum forms
6365% of total skull length; jugal process of lacrimal
caudolaterally excavated; both upper and lower jaws
edentulous; length of carpometacarpus Cmajor digit
exceeds humeral length by 25%; short alular metacarpal
(13.7% of major metacarpal); tarsometatarsus with small
but sharp medial and lateral plantar crests, plantar surface
not excavated; metatarsal II much shorter than metatarsal
IV; metatarsal II and IV trochlea plantarly displaced; and
metatarsal II trochlea strongly angled craniomedially.
Holotype. Institute of Vertebrate Paleontology and
Paleoanthropology (IVPP) V20284, a nearly complete
adult individual preserved in dorsal view with gastroliths
and trace impressions of integument around the neck.
Etymology. The species name refers to the elongate
maxilla that distinguishes this taxon from all other Jehol
ornithuromorphs.
Occurrence. Sihedang, Liaoning Province, north-eastern
China; Lower Cretaceous, Yixian Formation, Jehol
Group.
Description. We conducted X-ray analysis of the slab to
extract additional morphological information
2 J. K. O’Connor et al.
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

(Supplemental Figs 1, 2). Although the specimen is articu-
lated and appears fairly complete (Figs 1,2), the bone is
poorly preserved in most places, obscuring morphological
details.
Skull. The skull is exposed primarily in left lateral view.
The rostrum forms 6365% of the skull length. This is
greater than the proportion observed in any other Jehol
ornithuromorph with the exception of Xinghaiornis
(Tables 1,2). The premaxillary corpus is preserved in lat-
eral view. As far as can be discerned, the premaxilla is
edentulous. As in enantiornithines with the most elongate
rostra, the premaxillary corpus is low (length is roughly
three to four times the height) and the dorsal and ventral
margins are nearly parallel. The left maxillary process is
not preserved. A crack separates the frontal processes,
which are preserved in dorsal view. Rostrally, a suture is
present between the left and right processes. They become
unfused along their distal halves. Although the processes
do not reach the frontals, the distalmost extremity of both
processes is not preserved. The right premaxillary corpus
is visible in ventral view in articulation with the elongate
right maxilla. The rostral ends of the premaxillae appear
to be unfused (Fig. 3). The maxilla also appears to be
toothless, although small teeth cannot be ruled out due to
the poor preservation. The premaxilla-maxilla contact is
level with the rostral preserved ends of the frontal pro-
cesses. Consistent with the interpretation that this is not a
crack, the premaxilla articulates laterally with the maxilla.
Caudally, the right maxilla is poorly preserved; the blunt
caudal end is approximately level with the lacrimal. Distal
and ventral to the caudal end of the maxilla is a slightly
curved rod-like bone that is probably one of the jugal
bones. The left lacrimal is preserved in articulation with
the frontal. The craniodorsal process is weakly angled ros-
troventrally and the caudodorsal process is angled caudo-
dorsally, as in other basal birds (e.g. Jeholornis,
Sapeornis,Pengornis). The ventral process is laterally
excavated so that the cross section of this process is
L-shaped. This morphology is also observed in some
Figure 1. Dingavis longimaxilla gen. et sp. nov., holotype, IVPP V20284, full slab photograph. Scale bar D20 mm.
New Chinese Cretaceous ornithuromorph bird 3
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

enantiornithines (e.g. Parabohaiornis,Pengornis). The
frontals are petal-shaped and strongly domed as in other
Early Cretaceous birds. Preserved in the orbit, two bones
form an expanded articulation (Fig. 3); we suggest this is
the right pterygoid-quadrate articulation.
The mandible is slightly displaced rostral to the cra-
nium so that the mandibular symphysis is located proxi-
mal to the rostral end of the premaxillae (Fig. 3). The left
dentary appears to be preserved primarily in lateral view.
The mandibular symphysis appears to be fully fused and
U-shaped, probably incorporating a predentary bone
(Z.-H. Zhou & Martin 2011). The width of the mandibular
symphysis suggests a very wide lower bill, similar to
some living birds such as ducks, but also observed in Epi-
dendrosaurus. The bone forming the rostral margin is
heavily recrystallized, and we cannot rule out the possibil-
ity that the preserved morphology is exaggerated by taph-
onomic processes. Breaks in the bone separate the
remaining left dentary from the mandibular symphysis.
The dentary is long and straight, contributing to more
Figure 2. Dingavis longimaxilla gen. et sp. nov., holotype, IVPP V20284, interpretative drawing. Anatomical abbreviations: 15, pha-
langes one through five; ca, caudal vertebrae; cc, cnemial crest; cmc, carpometacarpus; co, coracoid; cv, cervical vertebrae; de, dentary;
ep, extensor process; es, extensor sulcus; f, furcula; fe, femur; fi, fibula; fr, frontal; g, gastralia; ga, gastroliths; ha, hallux; hs, horny
sheath; hu, humerus; il, ilium; is, ischium; ma, major digit; mi, minor metacarpal; mtIIV, metatarsals IIV; p, phalanx; pb, pubes; pc,
proximal carpal; pm, premaxilla; py, pygostyle; ra, radius; s, synsacrum; sc, scapula; st, sternal fragments; tc, attachment of the m. tibia-
lis cranialis; tb, tibiotarsus; th, thoracic vertebrae; tm, tarsometatarsus; ul, ulna; l and r represent left and right side, respectively. Scale
bar D20 mm.
4 J. K. O’Connor et al.
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

than two-thirds the length of the mandible. Caudally the
dentary is unforked, forming a caudoventrally sloping
articulation with the surangular. The poorly preserved left
angular is visible unfused to the surangular. The mandibu-
lar bones are usually preserved completely unfused in
other basal ornithuromorphs. Two condylar structures pre-
served near the left mandibular joint are interpreted as the
mandibular and otic processes of the left quadrate. A frag-
ment of the left splenial is visible between the two denta-
ries in dorsal view; its preserved portion ends well caudal
to the mandibular symphysis. Both the upper and lower
jaws appear to be edentulous. Although patchy dark min-
eralization between the left dentary and splenial superfi-
cially resembles teeth, this mineralization is observed
throughout the specimen.
Axial skeleton. At least eight cervical vertebrae are pre-
served in near articulation (Figs 1,2). Some poorly pre-
served fragments underlying the proximal vertebra may
represent the axis; the atlas is either not preserved or is
overlain by the skull but could not be identified in the
X-rays due to low resolution (Supplemental Figs 1, 2). The
vertebrae are elongate, with their length more than twice
exceeding their dorsoventral height in lateral view. The
articular surfaces appear to be heterocoelic. A low neural
spine can be observed in a vertebra caudal in the series.
The thoracic vertebrae are mostly obscured by other ele-
ments. The synsacrum is fully fused with the neural spines,
forming a spinal crest along the dorsal surface. Unfortu-
nately, it is so well consolidated that in the absence of
Figure 3. Maxillary elongation in Early Cretaceous ornithothor-
acines. A, B, Dingavis longimaxilla gen. et sp. nov., holotype,
IVPP V20284; A, photograph; B, interpretative drawing. C,
interpretative drawing of the skull of Rapaxavis (Enantiornithes)
for comparison (modified from O’Connor et al. 2011). Anatomi-
cal abbreviations: an, angular; cv, cervical vertebrae; de, den-
tary; fp, frontal process; fr, frontal; jg, jugal; la, lacrimal; ms,
mandibular symphysis; mx, maxilla; na, nasal; pa, parietal; pm,
premaxilla; ptq, pterygoid quadrate articulation?; qd, quad-
rate; sp, splenial; su, surangular; th, teeth; l and r represent left
and right side, respectively. Scale bars D10 mm.
Table 1. Select measurements of the holotype of Dingavis long-
imaxilla gen. et sp. nov. (IVPP V20284) in mm. Parentheses
indicate incomplete measurements.
Right Left
Skull length 58.64
Synsacrum 28.2
Pygostyle 7.8
Humerus 48.9 (51)
Ulna (44.9) (52)
Carpometacarpus 30.4 29.9
Alular metacarpal 4.1 (3.6)
Alular digit phalanx 1 12.4 12.5
Alular digit phalanx 2 4.9 5
Major digit phalanx 1 14 13.2
Major digit phalanx 2 13.2 13.2
Major digit phalanx 3 3.9 4
Minor digit phalanx 1 6.6 7.9
Scapula 38.4 (36.4)
Pubis 42.7 
Femur (16) 36.1
Tibiotarsus 55.6 55.4
Tarsometatarsus 37.9 40.6
Table 2. Comparative rostral lengths of Early Cretaceous Jehol
ornithothoracines (referable to Ornithuromorpha unless other-
wise specified). Measurements were taken from the holotype
specimens with the exception of Yanornis martini, and all speci-
mens were studied first hand with the exception of Xinghaiornis
lini and Gansus zheni. Parentheses indicate estimated
measurements.
Skull
length
Rostral
length
Rostral %
of skull
Dingavis 58.64 37 63
Yanornis martini STM9-51 57 32.7 57
Iteravis (4346) 26 57
Gansus zheni 46.3 26.5 57
Xinghaiornis lini 69.6 46.9 68
Longipteryx (Enantiornithes) 55 (35.6) 65
Longirostravis (Enantiornithes) (33) (25) 
Rapaxavis (Enantiornithes) 31 18 59
New Chinese Cretaceous ornithuromorph bird 5
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

preserved transverse processes it is impossible to estimate
the number of fused vertebrae. However, the synsacrum is
proportionately long, as in other ornithuromorphs. The cau-
dal series is incompletely preserved; the pygostyle is pre-
served in lateral view revealing a slightly upturned,
triangular profile, characteristic of early ornithuromorphs.
Thoracic girdle. Both scapulae are preserved; the left is
in dorsolateral view and the right is dorsomedially exposed
(Figs 1,2). A well-developed acromion was clearly pres-
ent, but its morphology cannot be clearly determined (acro-
mion small in Xinghaiornis). It appears to be straight. The
scapular blade is strongly curved and tapered as in other
ornithuromorphs. The omal end of the right coracoid is vis-
ible near the proximal end of the right scapula. A fragment
identified as the omal end of the right clavicular ramus is
visible between the right scapula and humerus. It is delicate
and tapered. Partially underlying the left ilium is a frag-
ment we identify as the caudal part of the sternum includ-
ing the left intermediate trabecula (Fig. 2). A more robust
fragment preserved lateral to this piece may be part of the
left lateral trabecula. Fragments ventral to the left scapula
are probably also part of the sternum. Many rib fragments
and several isolated gastralia are preserved ventral to these
fragments, proximal to the left ilium.
Thoracic limb. Both humeri are in caudal view. The
humeral shaft is twisted, clearly visible in the right ele-
ment, which is well preserved compared to most other ele-
ments. The proximal articular surface is strongly convex
proximocaudally. The capital incision is wide and very
shallow. The region of the ventral tubercle lacks any signs
of pneumaticity (excavated in some enantiornithines,
pneumatopore in some Late Cretaceous enantiornithines
and living birds). The deltopectoral crest is slightly less
than shaft width (slightly greater than shaft width in Xing-
haiornis) and extends for more than one-third the length
of the humerus. Proximally, it is not continuous with the
humeral head but separated by a slight concavity. This
crest steadily decreases in width distally but ends rather
abruptly. Distally, the olecranon fossa is well developed
but whether muscle grooves were developed cannot be
determined due to abrasion. The left ulna and radius are
poorly preserved and the two elements overlap on the
right. The ulna is proximally bowed as in other Early Cre-
taceous birds; it has a blunt olecranon process. The
straight radius is fairly robust, being more than half the
thickness of the ulna.
A single free carpal is preserved on the left, and two on
the right; these preserve no anatomical information. The
hand (carpometacarpus Cmajor digit) is 25% longer than
the humerus; in other Early Cretaceous ornithuromorphs
the hand is typically subequal to the humerus (e.g. Hon-
gshanornis,Schizooura,Xinghaiornis,Yanornis)or
shorter (e.g. Iteravis,Gansus,Piscivoravis,Zhongjianor-
nis). The humerus is approximately 10% shorter than the
hand in Yixianornis. Proximally the major and minor
metacarpals are fully fused to the distal carpals. The major
metacarpal is straight with an even thickness; the cranial
margin is weakly concave. The minor metacarpal is
slightly less than half (44%) the thickness of the major
metacarpal. The minor metacarpal is completely straight
(as in Yixianornis,Gansus and others), whereas it is dis-
tinctly bowed in some taxa (e.g. Piscivoravis). Distally,
the minor metacarpal ends short of the major metacarpal.
The distal ends of these two metacarpals are unfused. The
alular metacarpal does not appear to be fully fused to the
major metacarpal (fused on the left, slightly separated on
the right). This element is also proportionately short, being
only 13.7% of the total length of the carpometacarpus,
whereas it is typically 20% or greater in other early orni-
thuromorphs (O’Connor & Sullivan 2014). Clearest on the
left, the alular metacarpal has a moderate extensor process,
also present in some Early Cretaceous ornithuromorphs
(e.g. Gansus,Hongshanornis) but absent in others (e.g.
Archaeorhynchus,Piscivoravis,Schizooura). As a conse-
quence of the extensor process, the proximal margin of the
carpal is concave, as in some basal ornithuromorphs and
most living birds. The alular digit is composed of two pha-
langes; the first is slightly bowed, less than half the length
of the carpometacarpus and roughly the same thickness as
the minor metacarpal. The second phalanx is a weakly
recurved ungual. The proximal two phalanges of the major
digit are nearly equal in length, but the caudal margin of
the first phalanx forms a dorsoventrally compressed keel-
like expansion as in other ornithuromorphs. The caudal
expansion is absent at the proximal end of the phalanx but
rapidly expands, reaching maximum thickness by the proxi-
mal third and maintaining this thickness distally (expanded
proximally in Xinghaiornis). The absence of this expansion
proximally accommodates the phalanx of the minor digit,
preserved in articulation on the right. A similar morphology
is observed in Iteravis. The distal ungual phalanx is small
and nearly straight. The minor digit preserves a single
wedge-shaped phalanx that appears to include the second
phalanx fused to it distally (preserved free in Piscivoravis)
so that the distal end tapers sharply (e.g. Iteravis,
Hongshanornis).
Pelvic girdle. The pelvic girdle is fairly complete but
preserved largely in dorsal view with the elements dorso-
ventrally stacked over one and other obscuring some fea-
tures (Figs 1,2). In dorsal view the cranioventral margin
of the ilium forms nearly a 90angle that separates the
convex rostral margin from the deeply concave lateral
margin, as in many other Jehol ornithuromorphs (e.g.
Archaeorhynchus,Piscivoravis,Schizooura,Xinghaior-
nis). Rostrally the preacetabular wing of the ilium is con-
cave and appears to have been very wide, although this is
exaggerated by compression. The postacetabular wing of
the ilium is medially curved and tapered caudally. The
6 J. K. O’Connor et al.
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

left ischium is preserved ventral and medial to the left
ilium. A fragment of the distal end of the right is also pre-
served. The left ischium is medially curved so that it is lat-
erally convex and medially concave. Medial curvature is
observed in other ornithuromorphs preserved in partial
dorsal view (e.g. Piscivoravis,Schizooura). It appears to
have a low dorsal process located mid-corpus, as in most
other ornithuromorphs (a distinct, pointed process appears
to be unique to Xinghaiornis). The ventral surface is con-
cave and the distal half is tapered. The pubes are pre-
served only slightly disarticulated, visible in the X-ray
(Supplemental Fig. 1). The medially and dorsally curved
pubes are distally unfused but would have contacted in
vivo, as evidenced from the change in texture visible on
the medial surface of the distal left pubis. The distal ends
are expanded relative to the shaft, as in Iteravis, although
they do not form a distinct boot like that present in some
enantiornithines (e.g. Pengornis,Longipteryx).
Pelvic limb. The femur is short and straight, slightly
shorter than the tarsometatarsus (femur much longer
than tarsometatarsus in Xinghaiornis) and approximately
65% the length of the tibiotarsus (Table 1). The lateral sur-
face of the left femur is smooth proximally, indicating
the absence of a posterior trochanter, present in enantiorni-
thine birds (Chiappe & Walker 2002). A weak fibular con-
dyle appears to be present distally. The tibiotarsus bears a
proximocranially projecting cnemial crest and a short fibu-
lar crest. Distally, in cranial view, a well-developed exten-
sor sulcus is visible on the left. On the right in caudal view
the tibial cartilaginous trochlea is well developed but is dis-
tally limited in its extension up the cranial surface, similar
to other basal ornithuromorphs (e.g. Piscivoravis). The fib-
ula is short, fat and rapidly tapered distally.
The left tarsometatarsus is preserved in dorsal view,
whereas the right is in plantar view. The tarsometatarsus
is fully fused, although the presence of shallow grooves
allows identification of the individual metatarsals; these
grooves may represent a rudimentary flexor sulcus. Meta-
tarsal III is the longest, followed by metatarsal IV; meta-
tarsal II ends short of the metatarsal IV trochlea. A fairly
robust tubercle for the m. tibialis cranialis is present on
the dorsomedial surface of metatarsal III, just below the
proximal articular surface where this metatarsal is plan-
tarly displaced, as in other ornithuromorphs. This tubercle
is well developed in enantiornithines whereas it is typi-
cally more delicate in ornithuromorphs (e.g. Apsaravis,
Hongshanornis) or not developed at all (e.g. Piscivora-
vis); the tubercle in Dingavis is well developed compared
to other ornithuromorphs. As in other basal ornithuro-
morphs, no hypotarsus is present. Very low but distinct
medial and lateral plantar crests are present, as in Gansus
(Y.-M. Wang et al. 2015), but the plantar surface is not
deeply excavated as in Xinghaiornis. The metatarsal III
trochlea is the widest. The trochlea of metatarsals II and
IV are preserved plantarly displaced relative to metatarsal
III. A vascular foramen is present between metatarsals III
and IV, visible on the left. The trochlea of metatarsal II
appears to be strongly angled, similar to Piscivoravis. The
lateral condyle of the metatarsal IV trochlea, excavated
by a deep collateral pit, projects farther plantarly than the
medial condyle, also observed in Apsaravis. The right
metatarsal I is preserved nearly in articulation (Figs 1,2).
It is short (12% of metatarsal II) and articulates with the
plantar surface of metatarsal II so that the hallux was fully
reversed. It is also slightly twisted so that the surface
between the two articulations is concave. The shaft is
sharply tapered proximally; the trochlea is mediolaterally
wide. The pedal phalangeal formula is 2-3-4-5-x. The two
phalanges of the first digit are subequal in length. The
pedal phalanges in the other digits decrease in length dis-
tally. The proximal phalanx of the third digit is the longest
and most robust in the foot. The total length of the third
digit is less than that of the tarsometatarsus, as in Chang-
maornis (longer in Gansus) (Y.-M. Wang et al. 2013).
The pedal unguals are all small, subequal, with very little
curvature. This foot morphology strongly resembles that
of Changmaornis from the Xiagou Formation (Y.-M.
Wang et al. 2013,2015).
Gastroliths. Approximately 40 gastroliths are visible in
the region of the pelvic girdle. Additional stones are scat-
tered about the slab. These stones are fairly large (24
mm), smooth and moderately polished. We interpret these
as gizzard stones underlying the pelvic region. The deli-
cate overlying bone is crushed and broken, revealing the
underlying stones. These gastroliths are similar in size,
morphology and mineralogy to those preserved in speci-
mens of Iteravis and Gansus (S. Zhou et al. 2014; Y.-M.
Wang et al. 2015) but are more numerous in IVPP
V20284, potentially indicating slight dietary differences.
Alternatively, the gastroliths in specimens of Iteravis and
Gansus may represent incomplete aggregates.
Phylogenetic analysis
In order to confirm our morphological inferences, we
placed IVPP V2084 in an expanded version of the
O’Connor & Zhou (2013) Mesozoic bird matrix (see Sup-
plemental material). The data set has been modified to
include only Jeholornis (other taxa considered junior syno-
nyms of this taxon) and exclude the probable scansoriopter-
ygid Zhongornis. Recently described ornithuromorphs were
also included (Archaeornithura,Iteravis,Schizooura).
Although very little information is available we also added
Xinghaiornis, the first analysis to include this important
taxon (X.-R. Wang et al. 2013). The modified matrix con-
sists of 61 taxa, 30 of which are considered ornithuro-
morphs. We analysed the data using the TNT software
New Chinese Cretaceous ornithuromorph bird 7
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

(Goloboff et al. 2008). We conducted a heuristic search
using tree bisection reconnection (TBR), retaining the sin-
gle shortest tree out of every 1000 replications. This pro-
duced three most parsimonious trees with a length of 889
steps. A second round of TBR produced a total of 860
most parsimonious trees of the same length. In the strict
consensus tree (Fig. 4), Dingavis is part of a basal poly-
tomy of taxa more derived than Archaeorhynchus,which
includes Patagopteryx,Jianchangornis,Zhongjianornis,
Schizooura,Xinghaiornis,Vorona and Chaoyangia. This
tree is only weakly supported, with a consistency index of
0.374 and a retention index of 0.651. Bremer support val-
ues are also very low indicating that the current topology
would largely collapse in trees a single step longer.
Discussion
The new specimen IVPP V20284 can be assigned to the
Ornithuromorpha on the basis of the curved scapula,
plough-shaped pygostyle, globose humeral head, caudally
expanded first phalanx of the major digit, proximally pro-
jecting cnemial crest on the tibiotarsus and well-fused tar-
sometatarsus. IVPP V20284 can be distinguished from
other known taxa by its elongate rostrum and maxilla,
hand that is 25% longer than the humerus and proportion-
ately short alular metacarpal; thus, we erect the new taxon
Dingavis longimaxilla gen. et sp. nov. Previously, all bird
specimens from the newly discovered Sihedang locality
appeared to be referable to a single taxon, Iteravis huch-
zermeyeri (S. Zhou et al. 2014). However, as discoveries
continued, additional ornithuromorph diversity has sur-
faced (Liu et al. 2014). These authors described three new
specimens they assigned to a new species of Gansus,G.
zheni. Although we do not consider these specimens to be
referable to Gansus, previously only known from the Xia-
gou Formation (You et al. 2006), we also recognize minor
differences that suggest they are not referable to Iteravis
huchzermeyeri. The discovery of the edentulous Dingavis
provides evidence of greater trophic diversity in the Sihe-
dang avifauna. Furthermore, similarities in preservation
(bones somewhat three dimensional, colour of the fossil-
ized bone and similar lithology of the slab) suggest that
the holotype of Xinghaiornis lini may also be from Sihe-
dang rather than the Sihetun locality, as reported (Z.-H.
Zhou pers. comm.). A study of the histology in the holo-
type of Iteravis huchzermeyeri has suggested the three-
dimensional preservation of Sihedang specimens is tapho-
nomic, not due to the presence of medullary bone
(O’Connor et al.2015). This increased taxonomic diver-
sity (potentially as many as four ornithuromorph species)
further weakens hypotheses that the Sihedang locality
may represent a breeding site of Iteravis (S. Zhou et al.
2014).
Rostralization in Early Cretaceous birds
In Aves, the plesiomorphic skull is characterized by small
premaxillae and mesorostrine proportions. In neorni-
thines, the premaxilla is expanded and forms a majority of
the rostrum in all taxa, whereas the maxilla is greatly
reduced. Expansion of the premaxilla is a derived feature
within Aves that evolved outside Neornithes, present in
Late Cretaceous ornithurine Hesperornis (Marsh 1880).
Varying degrees of premaxillary expansion also evolved
in parallel in the Early Cretaceous Confuciusornithi-
formes and in at least one lineage of enantiornithines,
present in the Late Cretaceous Gobipteryx (Elzanowski
1977; Chiappe et al. 2001).
In contrast, rostral elongation in Dingavis and the Early
Cretaceous longipterygid enantiornithines was achieved
primarily by lengthening the maxilla (e.g. Rapaxavis,
Longipteryx,Longirostravis)(Fig. 3C) an extinct mor-
photype within Aves. Notably, the premaxillary corpus is
also somewhat elongated in these taxa relative to the
Figure 4. Hypothetical phylogenetic relationships of Mesozoic
birds (trees D860, length D889 steps). Nodes: 1, Aves; 2,
Pygostylia; 3, Confuciusornithiformes; 4, Sapeornithiformes; 5,
Enantiornithes; 6, Longipterygidae; 7, Ornithuromorpha; 8,
Ornithurae; 9, Hesperornithiformes; 10, Neornithes.
8 J. K. O’Connor et al.
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

plesiomorphic condition (O’Connor & Chiappe 2011). The
upper limit in rostral elongation in both lineages is approxi-
mately equal (Longipteryx 65%; Dingavis 6365%). This
could be merely coincidence or it may suggest that there
are structural limitations to elongating the rostrum through
the maxilla that do not permit truly longirostrine propor-
tions (>70% skull length). This may ultimately have led
this structural organization to be abandoned during avian
evolution. Notably, if limitations existed in the construction
of the avian skull, no such structural limitations are present
in the Pterosauria. This clade includes taxa with rostral
elongation achieved through both the premaxilla (e.g. Pter-
anodon,Tropeognathus) and maxilla (e.g. Gnathosaurus,
Zhenyuanopterus) (Witton 2013) and also reached
extremes of rostralization even greater than observed in
Aves (Marug
an-Lob
on & Buscalioni 2003). We suggest
this may be due to differences in the articulation between
the premaxilla and the maxilla in pterosaurs (extensive
contact between the bones) and birds (short articulation
between fairly delicate processes), the former affording
greater structural stability.
The longest rostrum in an Early Cretaceous bird is
observed in Xinghaiornis (X.-R. Wang et al. 2013). This
taxon shows yet another skull configuration in which the
premaxilla and maxilla contribute equally to the facial
margin. In Xinghaiornis both the premaxilla and the max-
illa are elongated but the premaxilla significantly more so
than the maxilla, which plesiomorphically is much more
elongate than the premaxilla. Although Xinghaiornis is
not truly longirostrine in proportions, the presence of pre-
maxillary elongation probably allowed this lineage to
achieve a greater degree of rostralization than any other in
the Early Cretaceous. Xinghaiornis and Dingavis are both
from the Yixian Formation, probably both from the Sihe-
dang locality, and both fall in the polytomy of basal orni-
thuromorphs only more derived than Archaeorhynchus
(Fig. 4). Differences in the rostral configuration of these
two sympatric taxa highlight the diversity of skull config-
urations present in early birds as they diversified into new
niches and evolved rostral modifications to suit a variety
of trophic habitats. Although parallel diversity evolved in
the Neornithes, this was achieved primarily through modi-
fications to the premaxilla, whereas basal birds show a
greater diversity of configurations but within a more lim-
ited morphospace. Dingavis,Xinghaiornis and the longip-
terygids thus represent early avian experiments in skull
rostralization.
Acknowledgements
We thank Dahan Li for preparing the specimen, and Jie
Zhang for photography. JO’C was supported by the Insti-
tute of Vertebrate Paleontology and Paleontology
[KN215509], and MW by the National Science
Foundation for Fostering Talents in Basic Research of the
National Natural Science Foundation of China
[J1210008]. We also thank two anonymous reviewers for
their comments on an earlier version of this manuscript.
Supplemental data
Supplemental material for this article can be accessed
here: http://dx.doi.org/10.1080/14772019.2015.1129518
ORCID
Jingmai K. O’Connor http://orcid.org/0000-0002-3898-8283
Min Wang http://orcid.org/0000-0001-8506-1213
Han Hu http://orcid.org/0000-0001-5926-7306
References
Baumel, J. J.&Witmer, L. M. 1993. Osteologia. Pp. 45132
in J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans & J.
C. Vanden Berge (eds) Handbook of avian anatomy:
Nomina anatomica avium.2
nd
edition. Nuttall Ornithologi-
cal Club, Cambridge.
Bell, A.,Chiappe, L. M.,Erickson, G. M.,Suzuki, S.,Watabe,
M.,Barsbold, R.&Tsogtbaatar, K. 2010. Description and
ecologic analysis of a new Late Cretaceous bird from the
Gobi Desert (Mongolia). Cretaceous Research,31,1626.
Chiappe, L. M. 2001. Phylogenetic relationships among basal
birds. Pp. 125139 in J. Gauthier & L. F. Gall (eds) New
perspectives on the origin and early evolution of birds. Pea-
body Museum of Natural History, New Haven.
Chiappe, L. M. 2002. Basal bird phylogeny: problems and solu-
tions. Pp. 448472 in L. M. Chiappe & L. M. Witmer (eds)
Mesozoic birds: above the heads of dinosaurs. University of
California Press, Berkeley.
Chiappe, L. M.,Norell, M. &Clark, J. 2001. A new skull of
Gobipteryx minuta (Aves: Enantiornithes) from the Creta-
ceous of the Gobi Desert. American Museum Novitates,
3346,115.
Chiappe, L. M.&Walker, C. A. 2002. Skeletal morphology
and systematics of the Cretaceous Euenantiornithes (Orni-
thothoraces: Enantiornithes). Pp. 240267 in L. M. Chiappe
& L. M. Witmer (eds) Mesozoic birds: above the heads of
dinosaurs. University of California Press, Berkeley.
Elzanowski, A. 1977. Skulls of Gobipteryx (Aves) from the
Upper Cretaceous of Mongolia. Palaeontologica Polonica,
37, 153165.
Gill, F. B. 2007. Ornithology. 3rd edition. W. H. Freeman and
Company, New York, 758 pp.
Goloboff, P. A.,Farris, J. S.&Nixon, K. C. 2008. TNT, a free
program for phylogenetic analysis. Cladistics,24, 774786.
Hou, L.,Chiappe, L. M.,Zhang, F. &Chuong, C.-M. 2004.
New Early Cretaceous fossil from China documents a novel
trophic specialization for Mesozoic birds. Naturwissenschaften,
91,2225.
Liu, D.,Chiappe, L. M.,Zhang, Y.-G.,Bell, A.,Meng, Q.-J.,
Ji, Q. &Wang, X.-R. 2014. An advanced, new long-legged
bird from the Early Cretaceous of the Jehol Group (north-
New Chinese Cretaceous ornithuromorph bird 9
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016

eastern China): insights into the temporal divergence of
modern birds. Zootaxa,3884, 253266.
Marsh, O. C. 1880. Odontornithes: a monograph on the extinct
toothed birds of North America. Professional Papers of the
Engineer Department, US Army,18(7), 1201.
Marug
an-Lob
on, J.&Buscalioni, A. D. 2003. Disparity and
geometry of the skull in Archosauria (Reptilia: Diapsida).
Biological Journal of the Linnean Society,80,6788.
Morschhauser, E.,Varricchio, D. J.,Gao, C.-H.,Liu, J.-Y.,
Wang, X.-R.,Cheng, X.-D. &Meng, Q.-J. 2009. Anatomy
of the Early Cretaceous bird Rapaxavis pani, a new species
from Liaoning Province, China. Journal of Vertebrate Pale-
ontology,29, 545554.
O’Connor, J.&Chiappe, L. M. 2011. A revision of enantiorni-
thine (Aves: Ornithothoraces) skull morphology. Journal of
Systematic Palaeontology,9, 135157.
O’Connor, J. K. &Zhou, Z.-H. 2013. A redescription of
Chaoyangia beishanensis (Aves) and a comprehensive phy-
logeny of Mesozoic birds. Journal of Systematic Palaeontol-
ogy,11, 889906.
O’Connor, J. K.,Gao, K.-Q. &Chiappe, L. M. 2010. A new
ornithuromorph (Aves: Ornithothoraces) bird from the Jehol
Group indicative of higher-level diversity. Journal of Verte-
brate Paleontology,30, 311321.
O’Connor, J. K. &Sullivan, C. 2014. Reinterpretation of the
Early Cretaceous maniraptoran (Dinosauria: Theropoda)
Zhongornis haoae as a scansoriopterygid-like non-avian, and
morphological resemblances between scansoriopterygids and
basal oviraptorosaurs. Vertebrata Palasiatica,52,330.
O’Connor, J. K.,Wang, X.-R.,Chiappe, L. M.,Gao, C.-H.,
Meng, Q.-J.,Cheng, X.-D. &Liu, J.-Y. 2009. Phylogenetic
support for a specialized clade of Cretaceous enantiornithine
birds with information from a new species. Journal of Verte-
brate Paleontology,29, 188204.
O’Connor, J. K.,Wang, M.,Zhou, S. &Zhou, Z.-H. 2015.
Osteohistology of the Lower Cretaceous Yixian Formation
ornithuromorph (Aves) Iteravis huchzermeyeri. Palaeonto-
logica Electronica,18,111.
O’Connor, J. K.,Zheng, X.-T.,Sullivan, C.,Chuong, C.-M.,
Wang, X.-L.,Li, A.,Wang, Y.,Zhang, X.-M. &Zhou, Z.-
H. 2015. Evolution and functional significance of derived
sternal ossification patterns in ornithothoracine birds. Jour-
nal of Evolutionary Biology,28, 15501567.
Wang, M.,Zheng, X.-T.,O’Connor, J. K.,Lloyd, G. T.,
Wang, X.-L.,Wang, Y.,Zhang, X.-M. &Zhou, Z.-H.
2015. The oldest record of Ornithuromorpha reveals
heterogeneous rates of morphological evolution among
Early Cretaceous birds. Nature Communications,6, 6987.
Wang, X.-R.,Chiappe, L. M.,Teng, F.-F. &Ji, Q. 2013. Xing-
haiornis lini (Aves: Ornithothoraces) from the Early Creta-
ceous of Liaoning: an example of evolutionary mosaic in
early birds. Acta Geologica Sinica, English Edition,87,
686689.
Wang, Y.-M.,O’Connor, J. K.,Li, D.-Q. &You, H.-L. 2013.
Previously unrecognized ornithuromorph bird diversity in
the Early Cretaceous Changma Basin, Gansu Province,
northwestern China. PLoS ONE,8(10), e77693.
Wang, Y.-M.,O’Connor, J. K.,Li, D.-Q. &You, H.-L. 2015.
New information on postcranial skeleton of the Early Creta-
ceous Gansus yumenensis (Aves: Ornithuromorpha). Histor-
ical Biology, doi: 10.1080/08912963.2015.1006217.
Witton, M. P. 2013. Pterosaurs: natural history, evolution,
anatomy. Princeton University Press, Princeton, 204 pp.
Xu, X.,You, H.-L.,Kai, D. &Han, F.-L. 2011. An Archaeop-
teryx-like theropod from China and the origin of Avialae.
Nature,475, 465475.
You, H.-L.,Lamanna, M. C.,Harris, J. D.,Chiappe, L. M.,
O’Connor, J.,Ji, S.-A.,L€
u, J.-C.,Yuan, C.-X.,Li, D.-Q.,
Zhang, X.,Lacovara, K. J.,Dodson, P. &Ji, Q. 2006. A
nearly modern amphibious bird from the Early Cretaceous
of northwestern China. Science,312, 16401643.
Zhang, F.,Zhou, Z.,Hou, L. &Gu, G. 2000. Early diversifica-
tion of birds: evidence from a new opposite bird. Kexue
Tongbao,45(24), 26502657.
Zhou, S.,O’Connor, J. K. & Wang, M. 2014. A new species
from an ornithuromorph dominated locality of the Jehol
Group. Chinese Science Bulletin,59(36), 53665378.
Zhou, S.,Zhou, Z.-H. &O’Connor, J. K. 2013a. Anatomy of
the Early Cretaceous Archaeorhynchus spathula.Journal of
Vertebrate Paleontology,33, 141152.
Zhou, S.,Zhou, Z.-H. &O’Connor, J. K. 2013b. A new pisciv-
orous ornithuromorph from the Jehol Biota. Historical Biol-
ogy,26, 608618.
Zhou, Z. 2006. Evolutionary radiation of the Jehol Biota: chro-
nological and ecological perspectives. Geological Journal,
41(34), 377393.
Zhou, Z.-H. &Martin, L. D. 2011. Distribution of the preden-
tary bone in Mesozoic ornithurine birds. Journal of System-
atic Palaeontology,9,2531.
Zhou, Z.-H. &Zhang, F.-C. 2006. Mesozoic birds of China a
synoptic review. Vertebrata Palasiatica,44,7498.
10 J. K. O’Connor et al.
Downloaded by [Jingmai K. O’Connor] at 06:38 15 January 2016