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. 2021 Jun 16;239(5):1066–1074. doi: 10.1111/joa.13487

The evolutionary and functional implications of the unusual quadrate of Longipteryx chaoyangensis (Avialae: Enantiornithes) from the Cretaceous Jehol Biota of China

Thomas A Stidham 1,2,3,✉, Jingmai K O'Connor 4
PMCID: PMC8546525  PMID: 34137030

Abstract

While the morphology and evolution of the quadrate among early birds and through the evolutionary origin of birds is not well known, we add to knowledge about that past diversity through description of the morphology of the quadrate in the unusually elongate skull of the Cretaceous enantiornithine bird Longipteryx chaoyangensis. The lateral and caudal surfaces of the quadrate are well exposed in two specimens revealing morphologies typical of early birds and their dinosaurian close relatives like a small otic head and two mandibular condyles. However, both skeletons exhibit quadrates with a unique, enlarged lateral crest that has not been previously described among Mesozoic birds. It is possible that the rostral surface of this lateral expansion served as the origination site for enlarged jaw musculature in a manner similar to the enlarged subcapitular tubercle in extant galloanserine birds. The caudally concave surface of the quadrate likely reflects some aspect of cranial pneumaticity, with its shape and position reminiscent of quadrates found in close non‐avialan maniraptoran relatives. It is possible that this lateral crest has a wider distribution among enantiornithines and other early birds and that the crest has been misidentified as the orbital process in some more damaged specimens. In addition, the enlarged lateral mandibular condyle (relative to the medial condyle) differs from the condition typically reported among enantiornithines and could indicate a difference in jaw function or mechanics in this bird with an elongated rostrum, or simply misinterpretations of morphology. Further examination of the quadrate in temporally early and phylogenetically stemward birds, along with their close outgroups, could greatly impact the study of several different aspects of bird biology including assessment of phylogenetic relationships, interpretation of the function and kinematics of the skull, reconstruction of foraging paleoecology, and evolution of skull morphological diversity among Mesozoic birds.

Keywords: bird, Cretaceous, enantiornithine, kinematics, lateral crest, Longipterygidae, quadrate

Study of the quadrate of the extinct enantiornithine bird Longipteryx documents new morphologies among birds including an extensive lateral crest and caudolateral fossa that may have been related to evolutionary changes in their bite, and may provide new material for phylogenetic assessment across stemward birds. Our work also highlights an increase in morphological character variability among enantiornithine quadrates, and indicates some potential areas of misinterpretation in previous studies.

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1. INTRODUCTION

Over the last few decades, the Early Cretaceous fossiliferous sediments of northeastern China have produced a wealth of derived feathered dinosaurs that have revolutionized our understanding of the diversity, evolution, interrelationships, and paleobiology of early birds and their close relatives. In the span of less than 30 years, thousands of specimens have been uncovered and the number of recognized species of Mesozoic birds has more than doubled (O'Connor et al., 2011b; Wang et al., 2019). With such a large number of fossils being discovered, most of the research focus has been on new material, and larger in‐depth studies of taxa and individual specimens remain to be completed for most taxa. As a result, many aspects of the morphological evolution and structure of these early birds remain unclear. Morphological details are further obscured by the primarily two‐dimensional, crushed preservation that characterizes the majority of specimens.

The quadrate is a particularly important bone in the skull of living birds. Uniquely, the quadrate integrates different functional areas of the skull, bridging the braincase with the lower jaw, and connecting with the palate and jugal bar that ventrally encloses the orbit. This combination of articulations and unfused contacts with the squamosal, prootic, quadratojugal, pterygoid, and articular results in a highly mobile, streptostylic quadrate. This mobility has facilitated the pivotal role of the quadrate in the evolution and functionality of cranial kinesis in birds (Bock, 1964; Dawson et al., 2011; Zelenkov & Stidham, 2018). The crown bird quadrate can move in a wide variety of directions, including rotating around its long dorsoventral axis (Claes et al., 2017; Dawson et al., 2011). The quadrates of crown birds also are highly varied in their morphologies and that diversity likely relates to the equally diverse functional or biomechanical uses of the jaw, variation in pneumaticity, and their unique evolutionary histories. Given the great diversity of Cretaceous stem birds with their inferred and documented dietary breadth (O'Connor, 2019; O'Connor & Chiappe, 2011), we naturally would hypothesize that the quadrate of early birds should similarly reflect that diversity in its morphology and function. However, detailed studies of Mesozoic bird quadrate morphology are relatively few and largely restricted to crownward ornithuran birds (Bell & Chiappe, 2020; Elzanowski et al., 2000; Elzanowski & Stidham, 2011). Despite the preservation of quadrates in many bird fossils from the Jehol Biota of China (O'Connor & Chiappe, 2011; Wang & Zhou, 2017; Wang & Zhou, 2020), their descriptive treatment has been understandably relatively brief in initial publications on otherwise complete skeletons. As a step towards understanding the diversity of quadrate morphology among stem birds, we examine in detail the quadrates of the enantiornithine Longipteryx chaoyangensis which are preserved and exposed on the holotype and referred skeletons.

Longipteryx chaoyangensis (junior synonyms “Camptodontornis yangi” and “Shengjingornis yangi”) is known from the Yixian and Jiufotang formations near Chaoyang and Jinzhou in Liaoning Province, China (Li et al., 2010; Li et al., 2012; Wang et al., 2015; Zhang et al., 2000; Zhang et al., 2001). Commonly, Longipteryx is placed together with Boluochia, Rapaxavis, Shanweiniao, and Longirostravis, forming the clade Longipterygidae (O'Connor et al., 2016; Wang et al., 2018; Wang et al., 2016). This clade is characterized by rostra that account for 60% or more of the total skull length (Figure 1), a dentition that is restricted to the premaxilla and rostral tip of the dentary, and a proportionately large pygostyle (O'Connor et al., 2009; O'Connor et al., 2011a). Among these taxa, Boluochia and Longipteryx form a clade (Longipteryginae), united by the presence of a unique tarsometatarsus morphology in which metatarsal IV projects distally farther than metatarsal III (O'Connor, 2019; O'Connor et al., 2011a). Of the longipterygids, only Longipteryx is known from multiple specimens, and these are among the best preserved of the entire clade (Li et al., 2010; Wang et al., 2015; Zhang et al., 2001). Longipteryx is the most robust of the longiptergyids, and characterized by proportionally longer wings, for which the taxon gets its name (Zhang et al., 2001).

FIGURE 1.

FIGURE 1

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Right lateral view of the skull of the Longipteryx chaoyangensis holotype IVPP V12325. Osteological abbreviations: q, quadrate; rp, possible retroarticular process. Scale bar equals 1 cm

The Longipterygidae is a fairly basal enantiornithine clade, which—in light of their diversity and unusual morphology—suggests that the enantiornithines evolved much earlier than indicated by their first appearance in the fossil record (Hou et al., 2004; Zhang et al., 2001). This hypothesis has been supported subsequently by inferences of evolutionary rates (Wang & Lloyd, 2016). Although not truly longirostrine by crown group standards (O'Connor & Chiappe, 2011), the elongate rostrum and unique dentition of longipterygids relative to other enantiornithines, along with their other unique skeletal features, suggests some significant functional and/or ecological differences in longipterygids as compared with other enantiornithines. In particular, these morphologies would seem to suggest differences and variation in feeding and or diet as compared with other known Mesozoic birds (O'Connor, 2019; O'Connor & Chiappe, 2011). Originally, Longipteryx was compared with extant kingfishers (Zhang et al., 2001) and was regarded as a piscivore based on its robust, recurved, and labiolingually compressed teeth (O'Connor & Chiappe, 2011). However, piscivory has not been supported by direct evidence in the form of ingested fish remains that are commonly preserved in specimens of the piscivorous Jehol ornithuromorph Yanornis (O'Connor, 2019). The identification of small crenulations on the distal margin of the large and recurved teeth in Longipteryx seemingly support a hypercarnivorous diet relative to other enantiornithines (Wang et al., 2015), but the general absence of gastroliths and preserved ingested remains in enantiornithines could indicate a diet of soft invertebrates for the clade (O'Connor, 2019). A recent study indicates that the tooth enamel in Longipteryx is more than eight times thicker than that of another indeterminant enantiornithine and that, in general, enantiornithine enamel is thicker than that of other known Mesozoic birds (Li et al., 2020). This difference was proposed to support the hypothesis of a piscivorous diet in Longipteryx (Li et al., 2020). However, the absence of similarly thick enamel in the teeth of other purported Mesozoic piscivores Ichthyornis and Hesperornis (Dumont et al., 2016) potentially conflicts with that dietary hypothesis.

The other clade of longipterygids, formed by Longirostravis, Shanweiniao, and Rapaxavis (Longirostravinae), is very different from Longipteryx. Their overall smaller size with more delicate crania and proportionately shorter wings demonstrates that longipterygids as a whole likely were ecologically diverse (Hou et al., 2004). Longirostravis has been interpreted as a mud‐prober (Hou et al., 2004; O'Connor & Chiappe, 2011). However, the presence of teeth is thought to make distal rhynchokinesis (a form of cranial kinesis utilized by many extant sediment probers) unlikely (O'Connor, 2019). Furthermore, the thin nasal and schizorhinal morphology of the external nares has been hypothesized as a central bending zone, and the Longirostravinae also have been interpreted as wood‐probers (Morschhauser et al., 2009; O'Connor, 2019). In contrast, the robust internarial bar in Longipteryx is hypothesized to prevent bending and cranial kinesis (O'Connor, 2019). Given the large uncertainty concerning the diet of longipterygids and most enantiornithines, a better understanding of the morphology of the quadrate may potentially shed light on the biomechanics of the jaw and clarify the function of the unique rostrum in Longipteryx.

2. MATERIALS

The two specimens (that have the best preserved quadrates) described below in detail are housed in the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences (IVPP) in Beijing, and an additional less well‐preserved quadrate is discussed from a referred specimen at the Dalian Natural History Museum (DNHM) in Liaoning, China (Wang et al., 2015). The specimen IVPP V21702 whose quadrate is described below is from a recently referred fossil (Li et al., 2020) that is the current focus of multidisciplinary studies underway. The current location of the originally referred specimen with a skull IVPP V12552 (Zhang et al., 2001) is unknown. IVPP V21702 and the holotype are both inferred to be adult individuals based on the presence of bony fusions in the hand and foot.

3. RESULTS

3.1. Longipteryx chaoyangensis holotype IVPP V12325

The right quadrate is exposed in caudal view (Figure 2). The otic head appears to have been quite narrow mediolaterally (~1.5 mm), while the mandibular end is quite wide (4.3 mm), at about one half of the dorsoventral height of the quadrate (9.0 mm). Part of the articular surface of the otic head may be preserved where there is a flattened though still convex facet that is directed dorsally and rounded in outline, and it is positioned on the dorsal end of the quadrate body (corpus quadrati) or “shaft.” The informal term “shaft” here reflects the thin caudal edge of the body of the quadrate on the medial margin of the bone. The otic facet is not offset or distinct from the shaft. The lateral (squamosal) side of the dorsal end is damaged and partially missing such that the morphology of the entire otic head is not clear. However, it would appear that the otic head probably was not much larger than what is preserved. A portion of the dorsal part of the shaft is broken away, and there is a fracture through the shaft in the approximately ventral one‐third of the shaft. It appears that the otic head and more ventral portions of the shaft might have been slightly twisted around their dorsoventral axis. As preserved, it would appear that the quadrate did not have the deeply bowed morphology that makes the caudal margin concave in lateral view present in some other enantiornithines (e.g., Rapaxavis and Pengornis) (O'Connor & Chiappe, 2011), but alternatively the missing part and other break in the bone could point to a somewhat concave caudal margin (with the bone being overly flattened in the currently caudally exposed preserved portion of its morphology, see comparisons below).

FIGURE 2.

FIGURE 2

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The quadrates of Longipteryx chaoyangensis. (a) Right quadrate of holotype IVPP V12325 in caudal view. (b) Outline drawing of holotype right quadrate highlighting major features; dashed line indicates possible extent of lateral crest. (c) Right quadrate of referred specimen DNHM D2889 in caudolateral view (ventral end broken). (d) Left quadrate of referred specimen IVPP V21702 in caudal view. (e) Right quadrate of referred specimen IVPP V21702 in oblique caudolateral view (specimen is crushed). Osteological abbreviations: cf, caudolateral fossa; d, depression; lc, lateral crest; mc, medial mandibular condyle; oh, otic head; op, possible orbital process; qj, quadratojugal facet; and s, shaft. Scale bar equals 5 mm

The caudal surface of the shaft is mediolaterally very narrow through its entire length. It widens in its ventral end, expanding in width just dorsal to the mandibular condyles. Interestingly, there is a thin but extensive lateral crest that projects off the shaft. This crest (termed here crista lateralis) extends from the craniodorsal edge of the quadratojugal articulation on the lateral margin dorsally at least to the level adjacent to the preserved dorsolateral edge of the otic head. This crest clearly is a separate feature from the orbital process (which is typically directed rostrally, not laterally), and this thin lateral crest extends from the shaft to form much of the lateral margin of the quadrate ending on the lateral mandibular process. There are no cracks or fractures in the ventral base of the crest that could indicate that the position of this thin sheet of bone is displaced, but its lateral margin clearly is damaged along its length obscuring its lateral extent. The crest appears to narrow in mediolateral width dorsally, but even at its dorsal preserved end, the mediolateral width of the crest nearly equals that of the mediolateral width of the shaft. This lateral crest is deeply concave on its caudal face near its ventral base, forming a ventral caudolateral fossa (termed here fossa caudolateralis ventralis) that is deepest at its base, bounded medially by the shaft, and with a ventral end dorsal to the lateral mandibular condyle. No foramen or other pneumatic feature appears to be associated with the lateral crest or this ventral caudolateral fossa.

The articulation with the quadratojugal is not a fully formed cotyle, but is a flattened caudolaterally directed facet on the caudolateral apex of lateral mandibular process. The lateral crest just dorsal to the quadratojugal facet actually extends as far lateral as the quadratojugal facet, and perhaps extended slightly further (Figure 2). The lateral tip of the lateral mandibular condyle just ventral to the quadratojugal contact is broken away. The area on the caudal surface of the quadrate immediately dorsal to the mandibular condyles is relatively flat except for an area just dorsal to the medial end of the lateral mandibular condyle where there is a small, circular depression on the caudal face of the bone. The lateral mandibular condyle is wider than the medial condyle, whereas the opposite condition previously was reported in other enantiornithines (O'Connor & Chiappe, 2011). The ventral edge of the lateral mandibular condyle is nearly flat, and there does not appear to be a caudal labrum on the condyle. The caudal edge of the lateral mandibular condyle is nearly straight as well. The medial mandibular condyle has a slightly concave ventral margin such that the lateral part is concave and the medial part is convex. The medial mandibular condyle is positioned slightly dorsal relative to the lateral mandibular condyle. The caudal margin of the medial mandibular condyle is convex with the rounded and somewhat inflated medial part of the medial condyle projecting a bit caudally relative to the remaining surface of the mandibular condyles. Therefore, the caudal margin of the medial mandibular condyle is caudal relative to that of the lateral condyle. The medial mandibular condyle is more bulbous medially, and it has a concave articular surface in caudal view. There does not appear to be a caudal labrum on the medial condyle, but there is a faint line where the articular surface meets the bone of the caudal surface. There also does not appear to have been a distinct mandibular vallecula between the mandibular condyles. Instead, there is a sloping contact (dorsomedial to ventrolateral) connecting the medial and lateral mandibular condyles with no distinct concavity or valley.

A bone to the left of the quadrate could be part or all of the pterygoid (or ectopterygoid). It has a long process that seems to contact the unexposed medial margin of the quadrate. There also is a more rostral facet that might articulate with an orbital process if present. It is unclear, but it looks like there also is a small retroarticular process on the lower jaw (Figure 1).

3.2. Longipteryx chaoyangensis IVPP V21702 referred specimen

The skull is preserved with the ventral surface of the palate exposed. The left and right quadrates are caudally exposed. The right quadrate preserves the otic head, which is missing on the left side (Figure 2d,e). The dorsoventral height of the quadrate is 9.0 mm, and the mediolateral width of the mandibular condyles is 4.6 mm. The caudal margin of the quadrate shaft is a thin and straight edge. The otic head has a flattened articular surface and is expanded slightly in the direction of the lateral crest. Just ventral to the otic head, the lateral crest is narrow with a nearly uniform mediolateral width and a dorsoventrally straight edge (for 1.3 mm), but the crest widens ventrally defining what appears to be a convex lateral margin (Figure 2e). The lateral crest extends ventrally approaching the mandibular condyles, but much of its surface is covered. However, it is clear that the ventral preserved width (near 2 mm) is greater than its dorsal width. A very deep ventral caudolateral fossa (deeper than the state in the holotype) excavates the ventral portion of the lateral crest bounded medially by the straight thin caudal margin of the quadrate shaft as in IVPP V12325 (better preserved on the left side). Again, there does not appear to be a foramen in the fossa. The lateral mandibular process is broken near its tip, and the medial mandibular condyle is covered or broken. The area that is immediately dorsal to the medial mandibular condyle is relatively flat, in contrast to the deep adjacent ventral caudolateral fossa. Medial relative to the right quadrate's orientation, there is a flattened piece of bone that appears to be rostral to the lateral crest. It is possible that this bone fragment represents part of the orbital process.

The left quadrate appears to be a bit crushed and distorted. The lateral portion of the lateral crest is partially broken, but part of the lateral margin appears intact near the level of the dorsal end of the ventral caudolateral fossa (demonstrating the great width of the crest). The ventral caudolateral fossa is rather deep and also lacks a foramen. The straight, thin caudal edge of the quadrate shaft is exposed. The lateral part of the lateral mandibular condyle is broken away, and the caudal projection of the medial mandibular condyle is distorted with the condyle twisted dorsally and facing caudally. The medial mandibular condyle extends far medially ending in a rounded projection. There is no vallecula present, and the mandibular condyles appear relatively flat.

4. COMPARISONS

There is some morphological variation present among the quadrates examined and those preserved in another referred specimen (DNHM D2889) (Wang et al., 2015). The straight (unbowed) morphology of the quadrate shaft in the holotype specimen IVPP V12325 may be the true morphology, or possibly result from the caudal exposure of this thin element, or derive from fractures in the bone. Caudal bowing also is not clearly present in the referred specimen IVPP V21702, which also is caudally exposed. At first glance, the quadrate shaft appears somewhat bowed such that the caudal margin is concave (in lateral view) in a referred specimen of Longipteryx, DNHM D2889 (Wang et al., 2015). However, close examination of the preserved quadrate in DNHM D2889 (Figure 2c) shows a nearly straight margin (with a hint of concavity) in its dorsal half that is unbroken, with the bowed portion primarily restricted to the ventral half where the specimen is broken and fractured. The restriction of the caudal bowing to the broken area suggests that the concavity may not be natural. Overall, the evidence for a caudally concave margin (lateral view) of the quadrate in Longipteryx is poor, and in all examined specimens the caudal margin appears to be nearly straight or only slightly concave at most. This difference either indicates the occurrence of variation in this feature among the Longipterygidae, or that the bowed quadrate morphology observed in Rapaxavis also could be the result of similar taphonomic or preservational distortion (O'Connor et al., 2011c). The taxa with reported caudal bowing should be reexamined.

The lateral crest was not described or illustrated explicitly in the original treatment of Longipteryx (Zhang et al., 2000; Zhang et al., 2001). However, Zhang and coauthors (2001) state in their description of the quadrate that the orbital process was not well developed. It is likely that they misinterpreted this lateral crest as a reduced orbital process in the holotype. In the holotype and IVPP V21702, the rostral surface is not exposed and faces into the slab, and thus the orbital process is not clearly visible in either specimen. In IVPP V21702, the right quadrate is still more or less in articulation with the squamosal and jaw, and the thin quadrate shaft is exposed projecting away from the slab. Furthermore, there is no evidence of breakage to suggest an orbital process would have extended from the shaft consistent with our interpretation that the quadrate is exposed in caudal view.

In the holotype specimen, the right side of the skull is exposed revealing the right quadrate. It can be clearly observed (Figure 2) that the maximum width of the lateral crest is subparallel to the long axis through the mandibular condyles and its maximum height is subparallel with the shaft. In addition, there are no fractures in the specimens that could indicate that the orientation of the lateral crest has been altered. The long axis of the orbital process of birds and non‐avialan theropods is roughly rostrocaudally oriented, and the axis of the process forms a near right angle to the long axis through the mandibular condyles (Elzanowski et al., 2000; Elzanowski & Stidham, 2011; Hendrickx et al., 2015). The orientation of this lateral crest as expanded mediolaterally with its ventral lateral edge joining and being continuous with the dorsal part of the lateral mandibular process just dorsal to the contact with the quadratojugal helps to demonstrate that it is not the orbital process which would join the body of the quadrate ventrally near its mediolateral center. An expanded and somewhat similar crest on the lateral side of the quadrate also occurs in some non‐avialan theropod groups, though frequently perforated by a notch or foramen, and frequently dorsally restricted (Hendrickx et al., 2015).

Furthermore, the orbital process is quite large in theropods including birds (Elzanowski et al., 2000; Elzanowski & Stidham, 2010; Elzanowski & Stidham, 2011; Hendrickx et al., 2015), and extends far beyond the limits of the mandibular condyles unlike this newly described lateral crest in a basal bird. It is possible that this lateral crest has a wider distribution among early birds, particularly among enantiornithines, and has either been overlooked or potentially misinterpreted as the orbital process as we suspect is the case here.

The depth of the ventral caudolateral fossa varies between the holotype and IVPP V21702 in a manner similar to fossa variation in at least some crown group birds (Elzanowski & Stidham, 2010). However, the presence and extent of the lateral crest is similar in specimens where it is visible. The crushed and broken quadrate in DNHM D2889 (Wang, et al., 2015; Figure 2c) also preserves fragments deriving from the lateral crest and appears to have an otic head similar in morphology to the other specimens. The proportionately wider lateral mandibular condyle also appears consistent across known specimens of Longipteryx.

5. DISCUSSION

The quadrates of Longipteryx display a combination of widely occurring and apparently plesiomorphic traits, in addition to some derived conditions. The Longipteryx quadrate has two (medial and lateral) mandibular condyles that occur among basal crown group birds like galloanserines (Elzanowski & Stidham, 2010; Elzanowski & Stidham, 2011), hesperornithiforms (Bell & Chiappe, 2020; Elzanowski et al., 2000), other enantiornithines (O'Connor & Chiappe, 2011), the basal pygostylian Sapeornis (Hu et al., 2020a), and derived non‐avialan maniraptorans such as Linheraptor (IVPP V16923; Dromaeosauridae) (Xu et al., 2010; Xu et al., 2015) and Mei (IVPP V12733; Troodontidae) (Xu & Norell, 2004). That morphology paired with the short retroarticular processes present in several of those clades could indicate some underlying plesiomorphic functional or jaw/quadrate kinematic related aspects of those morphologies. The reported occurrence of three mandibular condyles in the enantiornithine Piscivorenantiornis (Wang & Zhou, 2017; Wang & Zhou, 2020) should be reexamined because that character state is otherwise unknown outside of neoavian birds. The presence of a larger lateral mandibular condyle as compared with the medial mandibular condyle in Longipteryx also is reported in Piscivorenantiornis (Wang & Zhou, 2017), but contrasts with the condition previously described for most enantiornithine birds (Hu & O'Connor, 2017; O'Connor & Chiappe, 2011; O'Connor et al., 2011b). That key difference in quadrate morphology (likely with a corresponding alteration to the articular bone) coupled with the elongate rostrum and proportionately thick tooth enamel (Li et al., 2020) in Longipteryx could indicate an evolutionary change in jaw or feeding function, or perhaps biomechanics, reflecting ecological diversity within enantiornithines. However, it is also possible that the anatomical orientation of the quadrate has been misinterpreted in at least some specimens of other enantiornithine taxa such that the lateral condyle was identified as the medial condyle as we demonstrate was the case in Shenqiornis (see below).

The small otic head in Longipteryx is unlike that of ornithuran birds where the head becomes widened along a roughly mediolateral axis (Bell & Chiappe, 2020; Elzanowski et al., 2000), and even bifurcated as in neognaths (Elzanowski & Stidham, 2010; Elzanowski & Stidham, 2011). It should be noted that reversion of the otic head to a state similar to the primitive condition (small and undivided) occurs among some crown birds (e.g., lovebirds) (Stidham, 2010). The nature of the articulation between the otic head and the squamosal (and prootic, if present) and the exact shape of the otic head in the close outgroups to Avialae is unclear at present. In some taxa like Confuciusornis and Linheraptor, the otic head is not laterally exposed, being covered frequently by the squamosal. In oviraptorosaurs, the quadrate contacts both the squamosal and braincase in a fashion somewhat similar to crown birds although this morphology is considered to be derived independently (Balanoff & Norell, 2012; Balanoff et al., 2009). Certainly, the otic head of the most basal avialans is not enlarged as in crownward ornithurans, but the exact nature of the contact with the squamosal (and even the prootic) is not known. However, in many basal stem birds it appears the main body of the quadrate (shaft) is mediolaterally slender with a small, flattened, and unbifurcated otic head (Chiappe et al., 1999; Hu et al., 2020a).

The unique lateral crest with its concave ventral caudolateral fossa is present in three well‐preserved quadrates of Longipteryx, and thus does not appear to reflect intraspecific variation or distortion of an individual fossil. The crest is a relatively large albeit thin structure and seems to extend for much of the quadrate's dorsoventral height, extending from just below the otic head ventrally on to the dorsal margin of the lateral mandibular process. The excavated caudal surface of the lateral crest of the quadrate is reminiscent of the concavities present in troodontids and some dromaeosaurids. For example, troodontids like Mei long have a pneumatic foramen on the caudal surface near its dorsoventral midpoint (Gao et al., 2012), and the dromaeosaurid Linheraptor (Xu et al., 2010; Xu et al., 2015) exhibits a slight caudal concavity near its dorsoventral midpoint, not as extreme or in the same position as that in Longipteryx. The quadrate of the enantiornithine Pengornis is reportedly caudally bowed and perforated by a pneumatic foramen (O'Connor & Chiappe, 2011). A pneumatic foramen also is reported on the medial surface of the quadrate in the bohaiornithid enantiornithines Zhouornis and Shenqiornis (Wang et al., 2010; Zhang et al., 2014), and on the medial surface dorsal to the mandibular condyles in Archaeopteryx (Alonso et al., 2004). The general occurrence of a caudal or caudolateral concavity or foramen in these groups and other distantly related theropods (Hendrickx et al., 2015) supports our interpretation of this excavated caudolateral surface in Longipteryx as a pneumatic feature and apparently separate from the medial pneumaticity reported among early birds. The position of these paravian pneumatic features along the rostral margin of the external acoustic meatus suggests that they are related to auditory pneumaticity. The wide‐spread occurrence of these features supports inferences that quadrate pneumaticity may be broadly plesiomorphic for Avialae and its close relatives (Alonso et al., 2004; Hendrickx et al., 2015; Witmer, 1990).

The ventral caudolateral fossa on the ventral and lateral edge of the quadrate in Longipteryx most likely was outside of the tympanic cavity (as is that area in living birds), and the fossa helped to form or was adjacent to the external auditory meatus. Its concavity (as a likely pneumatic structure) therefore likely derives from an external ear rather than middle ear feature. In birds, the tympanic membrane connects to the quadrate only on the caudal face of the otic process via Platner's ligament (Claes et al., 2017; Saunders et al., 2000). As such, most of the tympanic membrane (and middle ear) is caudal and medial to the body of the quadrate, and its surface is oblique to the dorsoventral axis of the quadrate (visible in Coturnix coturnix IVPP OV1886 and Nycticorax nycticorax IVPP OV1861) (Claes et al., 2017; Saunders et al., 2000). While the pneumaticity observed on the caudal surface of the quadrate in non‐avialans could derive from a position of the tympanic membrane further ventral relative to its crown avian position on the otic process alone (Claes et al., 2017; Saunders et al., 2000), this is highly unlikely given that any more lateral (and ventral) placement or extension of the tympanic membrane (such as attachment of this membrane along the lateral crest of this quadrate) would not only greatly enlarge the volume of the tympanic cavity (impacting audition), but would also require a significant lengthening of the columella (stapes) to reach the mediolateral level of the lateral ventral edge of the quadrate.

This ventral caudolateral fossa on the quadrate with a lateral crest has not been reported previously in enantiornithines and could suggest homoplasy in the evolution of this potential pneumaticity related feature. However, this thin quadrate crest may have a wider taxonomic distribution and is potentially phylogenetically informative. Perhaps it has been lost in some fossils because of taphonomy or during mechanical preparation. It also may have been overlooked in fossil specimens (as the case here), or even interpreted in other crushed specimens as a different structure such as the orbital process itself. Re‐examination of published images of the bohaiornithid Shenqiornis DNHM D2950/1 (O'Connor & Chiappe, 2011; Wang et al., 2010) suggest the preserved quadrate was misidentified as the right, when in fact it is the left element. If this reinterpretation is correct, then a lateral crest and caudal fossa also is present in this taxon, and the presence of a lateral mandibular condyle that is wider than the medial likely is a more widespread condition among the Enantiornithes, including that illustrated in Gobipteryx (Elzanowski, 1976). This reinterpretation is supported by the presence of a lateral mandibular condyle that is wider than the medial condyle in another bohaiornithid Longusunguis (Hu et al., 2020b). In the description of that holotype, the quadrate was similarly correctly identified as the left in caudal view but incorrectly described as having a wider medial condyle (Wang et al., 2014). Furthermore, lateral expanded crests (frequently perforated or notched) occur in some theropod groups beyond the immediate outgroups to Avialae (Hendrickx et al., 2015), and their distribution could suggest a phylogenetically wider and more primitive occurrence of the crest among theropods, or perhaps similar functional aspects to quadrate morphology across these disparate groups.

The rostral surface of the lateral crest may have functioned to increase the surface area available for attachment of the mandibular adductor musculature. Its large size (and possibly correlated larger musculature) also might have created torque around the dorsoventral long axis of the quadrate (and its small otic head), rotating it somewhat counterclockwise in dorsal view (during a bite), in addition to aiding in overall bite force production or increasing the speed of mouth closure. This hypothesized scenario parallels the condition in galloanserine birds where there is an enlarged subcapitular tubercle for origination of the m. adductor mandibulae externis on the lateral side of the otic process ventral to the squamosal condyle, and where rotational kinematics around the dorsoventral axis are known during feeding (Claes et al., 2017; Dawson et al., 2011).

In addition, that potential enhancement to the surface area for muscle origination, along with the presence of a small retroarticular process on the jaw and relatively flat mandibular condyles on the quadrate (with only a slight offset dividing them), might mean that Longipteryx (and perhaps enantiornithines more widely) were adept at shifting their jaws rostrocaudally (in a manner somewhat similar to extant waterfowl), or even required extra leverage to open their mouths. While the retroarticular process appears relatively small, it should have provided a point of insertion for the m. depressor mandibulae and aided in the opening of the mouth. Its relatively small size as compared with crown group species with an enlarged retroarticular process means that the morphology in Longipteryx likely was not strongly linked to gaping (i.e. opening the mouth within a hard substrate) (Beecher, 1951; Mayr, 2005; Zusi, 1967). With the diet of Longipteryx and other enantiornithines largely being unknown at present, the relationship between these morphological and functional features, and dietary diversity and foraging ecology is not known. However, it is notable that both Longipteryx and bohaiornithids, the clade that includes Shenqiornis, have a fairly robust skull morphology consistent with the interpretations that this lateral crest could have facilitated increased adductor musculature and bite forces. The thickened tooth enamel identified in Longipteryx (Li et al., 2020) might reinforce that interpretation.

The lateral crest is not present in known Mesozoic ornithurans (Bell & Chiappe, 2020; Elzanowski et al., 2000; Elzanowski & Stidham, 2011), and it appears to be absent in known specimens of Archaeopteryx (Alonso et al., 2004; Elzanowski & Wellnhofer, 1996; Mayr et al., 2007) suggesting that it is a derived enantiornithine feature within birds. However, the extent of this feature within enantiornithines is at this time uncertain. Interestingly, some dromaeosaurids like Linheraptor have a rostrally to rostrolaterally projecting crest (lateral to the orbital process and termed “lateral flange” by some authors) (Xu et al., 2010; Xu et al., 2015) that is positioned near and restricted to the dorsal end of the bone (rather than extending ventrally and contacting the mandibular process as in Longipteryx). Some more basal theropod dinosaurs have other lateral expansions that could suggest a potentially common basis in homology or function at a more general level for this lateral structure within theropods. While it is highly unlikely that these structures in non‐avialans and Longipteryx are strictly homologous across those taxa, these lateral crests may reflect an underlying similarity in function as serving for increased surface area for muscle origination and subsequently an increase or change in bite force or kinematics.

While the orbital process is not clearly visible in the skeletons of Longipteryx (fragments may be present in one specimen, see above), it is a plesiomorphic structure for Avialae present in close outgroups, more distantly related theropods, Archaeopteryx, basal birds, and ornithurans (Alonso et al., 2004; Bell & Chiappe, 2020; Chiappe et al., 1999; Elzanowski et al., 2000; Elzanowski & Wellnhofer, 1996; Hendrickx et al., 2015; Mayr et al., 2007; Xu et al., 2015). Given the morphology and structure of that large process in those avialan taxa, it is likely the orbital process in Longipteryx is rather large and also extended quite far dorsally, but future specimens are required to confirm its exact size and shape.

The morphology of the quadrate needs to be documented in greater detail across more specimens of temporally early and phylogenetically basal birds, in addition to close relatives of Avialae. Those data potentially will impact greatly the study of several different aspects of bird evolution including phylogenetic reconstruction (as a source of new or revised character data), functional and kinematic interpretations of the skull, foraging paleoecology, and added knowledge of the evolution of skull diversity among birds in ancient ecosystems.

AUTHOR CONTRIBUTIONS

TAS and JKO designed the study, collected and analyzed the data, created the figures, and wrote and edited the manuscript.

ACKNOWLEDGMENTS

The authors thank Xing Xu for access to comparative specimens and for discussion. TAS is funded by the National Natural Science Foundation of China (NSFC 41772013). Additional support was provided to JKO by the National Natural Science Foundation of China (NSFC 41688103) and the Strategic Priority Research Program of Chinese Academy of Sciences (XDB26000000). We thank Philip Cox and anonymous reviewers for comments on an earlier draft of the manuscript.

Stidham, T.A. & O'Connor, J.K. (2021) The evolutionary and functional implications of the unusual quadrate of Longipteryx chaoyangensis (Avialae: Enantiornithes) from the Cretaceous Jehol Biota of China. Journal of Anatomy, 239, 1066–1074. 10.1111/joa.13487

DATA AVAILABILITY STATEMENT

All data related to this study are included within the paper.

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Data Availability Statement

All data related to this study are included within the paper.

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