Longipteryx chaoyangensis Zhang et al., 2001

Wang, Xuri, Zhao, Bo, Shen, Caizhi, Liu, Sizhao, Gao, Chunling, Cheng, Xiaodong & Zhang, Fengjiao, 2015, New material of Longipteryx (Aves: Enantiornithes) from the Lower Cretaceous Yixian Formation of China with the first recognized avian tooth crenulations, Zootaxa 3941 (4), pp. 565-578 : 566-576

Longipteryx chaoyangensis Zhang et al., 2001

Emended diagnosis. rostrum approximately 60% of the skull length; dentition restricted to premaxilla and the rostral-most portion of dentary; large, recurved and labiolingually compressed teeth with crenulations developed along the caudal margins; middle cervical vertebrate heterocoelous; distal region of sternum with developed carina and lateral processes; coracoids with nearly straight lateral margin; second phalanx of minor digit reduced to a small triangle; pubis curved and with perpendicular pubic-foot; tarsometatarsus fused proximally, metatarsal IV surpasses the distal end of metatarsal III; ratio of tibiotarsus length to tarsometatarsus length approximate 1.6; trochleae of metatarsals I-IV almost on the same level; tibiotarsus shorter than humerus and ulna (modified from Zhang et al. 2001 & O’Connor et al. 2011).

Holotype. Longipteryx chaoyangensis Zhang et al., 2001 (IVPP-V12325, Fig. 1 ).

Referred specimen. DNHM-D2889, a nearly complete and articulated adult individual preserved in tuff with feather impressions around the neck, forelimbs and hindlimbs ( Fig. 2 , 3 ; Table 1). The specimen is deposited at the Dalian Natural History Museum, Dalian City, Liaoning Province, China.

Locality and Horizon of the referred specimen. Yuanjiawa fossil locality, Dapingfang town, Chaoyang City, Liaoning Province, China; Yixian Formation, Lower Cretaceous ( Swisher et al. 2002; Liu et al. 2011).

Description. The skull is preserved in right lateral view ( Fig. 4 ). The cranial portion is crushed and preserved disarticulated, so it is hard to describe the precise anatomical characteristics. The premaxilla is relatively straight, and the dorsal and ventral margins are parallel along the whole length. The tip is sharp and smooth, not hook shaped as that of Boluochia zhengi Zhou, 1995. The premaxilla bears 4 teeth ( Fig. 5 ). The teeth are exposed mostly in labial view. The first tooth is very small. The second is larger than the first but smaller than the third and the fourth teeth. The first two teeth are similar in outline. Both basal parts of them are not as expanded as those of the third and the fourth teeth. All teeth are labiolingually compressed and slightly recurved caudally from a distinct concavity close to the apex. Their anterior margins are smooth and clean, but their caudal margins are relatively expanded labiolingually and very special structures can be observed on the caudal margins. The structures are different from serrations developed on the teeth of small theropods. At least two lines of serrations can be observed on the caudal margins of the second and fourth teeth, whereas, serrations on theropod teeth are regularly arranged in one line on the caudal margin. The serrations on premaxillary teeth 2 and 4 of DNHM-D2889 have no uniform outlines. Some are semicircular and some are like oval or obtusangular in lateral profile. These structures have not been recognized previously within Mesozoic birds and are totally different from the serrations or any other reported tooth ornamentations in non-avian dinosaurs, so, we term them crenulations. The articulations to the premaxilla and the nasal are obscure due to the poor preservation.

The mandibular bones remain unfused. The dentary expands caudoventrally so the ventral margin is relatively concave. The dentary is about 60% of the skull in length. Mandibular fenestrae are absent, but a lateral groove is present along the middle shaft of the right dentary.There are at least 3 teeth preserved at the rostral-most portion of the dentary. The first tooth is mostly overlapped by the third premaxillary tooth. Very faint crenulations are present on the exposed caudal margin. The second and third teeth are exposed in lingual view. Both of them are smaller than those of the premaxilla. Their exposures of these teeth prohibit examining their caudal margins so the presence or absence of crenulations on their caudal margins cannot be confirmed.

There are at least seven cervical vertebrae preserved, including the atlas and the axis. It is hard to determine the exact count and morphology of the cervical vertebrae due to poor preservation, however the third cervical is the longest of these. All preserved cervical vertebrae are concave laterally. The thoracic vertebrae are crushed and preserved dis-articulated, therefore their number and morphology cannot be determined with certainty. There are at least ten thoracic vertebrae preserved, that is those bearing ribs anterior to the synsacrum. The synsacrum is composed of at least six vertebrae as indicated by the preserved transverse processes. The distal part of the synsacrum appears to be dorsoventraly compressed and the transverse processes of the fused sacral vertebrae enlarge caudally. There are at least five free caudal vertebrae preserved indicated by their preserved transverse processes. The last two are smaller than the anterior caudals. The pygostyle, preserved in ventral view, is robust and completely synostosed. The ventrolateral processes are prominent. Considering the distal end of the pygostyle is worn off and the preserved length is approximately the same as that of the tarsometatarsus, it is consistent with other longipterygids, which typically possess a proportionately large pygostyle ( O’Connor et al. 2011).

The furcula is Y-shaped. Its rami are flattened and robust, and diverge at an angle of 60°, which is wider than that of L. chaoyangensis (50°) (Zhang et al. 2001). The hypocleidum is relatively slim and long, and is nearly equal to the rami in length. The right scapula is preserved nearly completely, and only is missing the distal end. The scapular blade is straight and tapers towards the caudal end. The left scapula is covered caudally by the furcula and some thoracic ribs. The left coracoid is preserved completely and strut-like. Its lateral margin is straight and its length approximately 2.4 times its width. The sternum is broken and partly covered by the left humerus and thoracic ribs. It is hard to determine the detailed morphology, but the lateral trabecula is present on the left side, and is the same shape as that of L. chaoyangensis , but very different from that of Longirostravis hani Hou et al., 2004 , which lateral sternal processes end in a unique three-branched, “moose-horn”- like expansion ( Hou et al. 2004).

Elements length Skull length 70 Dentary length 42 Coracoid length 24 Coracoid width 11 Scapular length 28* Humerus length 40 Ulna length 42 Radius length 40 Alular metacarpal length 5 Alular phalanx I length 9 Alular claw length 8 Major metacarpal length 17 Major digit phalanx I length 12 Major digit phalanx II length 11 Major digit claw length 7 Minor metacarpal length 23 Femur length 31 Tibiotarsus length 38 Fibula length 15# Tarsometatarsus length 24 Metatarsal I

Phalanx 1 7 Phalanx 2 6 Metatarsal II

Phalanx 1 4 Phalanx 2 6 Phalanx 3 7 Metatarsal III

Phalanx 1 5 Phalanx 2 4 Phalanx 3 7 Phalanx 4 7 Metatarsal IV

Phalanx 1 5 Phalanx 2 4 Phalanx 3 4 Phalanx 4 6 Phalanx 5 9

Notes: * represents incomplete element; # represents estimated length.

The humerus is sigmoid, and its length approximately equal to that of the ulna and the radius. The deltopectoral crest is prominent and ends at the one fourth of the humerus length. The proximal two thirds of the ulna is relatively straight and the distal one third is slightly bowed. The radius is straight and slim, and is about 70% of the ulnar width in diameter. The left ulnare is preserved in dorsal view, and is trapezoid-shaped. The alular metacarpal is very short, and is about 30% of the length of the major metacarpal. The major metacarpal is straight and robust. The minor metacarpal is tightly attached to the major metacarpal but is longer than it and projects distally of it. The alular digit is composed of two phalanges. The first phalanx is straight and slim, about the same length of the first phalanx of the major digit. The second phalanx of the alular digit is relatively short and has indications of a horny sheath preserved. The major digit is composed of three phalanges. The first phalanx is longer than the second, and the former is about 1.3 times of the latter in diameter. The third phalanx is smaller than the first two phalanges, and also has indications of a horny sheath preserved. Only the first phalanx of the minor digit is preserved, and is the smallest of all the manual digit phalanges ( Fig. 6 , 7 ).

The pelvic girdle is poorly preserved, only the left ischium and the left pubis are partly preserved in lateral view. The ischium is relatively complete and strap-like. The iliac peduncle is approximately the same width as the pubic peduncle, not like the condition in Rapaxavis pani Morschhauser et al., 2009, which iliac peduncle is narrow and longer than the broad pubic peduncle ( Morschhauser et al. 2009; O’Connor et al. 2011). A dorsal process is prominent near the proximal end, which is wider than both the iliac peduncle and the pubic peduncle. Only the proximal portion of the left pubis is preserved; it is relatively straight and expanded at the proximal end.

The femur is longer than the tarsometatarsus but much shorter than the tibiotarsus. However, the femur length is almost equal to that of the tibiotarsus in the holotype of L. chaoyangensis . The femoral shaft is relatively straight. The lateral condyle is not prominent and only slightly expanded at the distal end. The tibiotarsus is long and relatively straight. The proximal part of right fibula is preserved, and is short and slim. The distal tarsals seem fused with metatarsals II–IV. The trochleae for the pedal digits are almost on the same plane. All digits possess sharp and strongly curved claws. The claws are almost the same both in shape and in size. The hallux is reversed. The first phalanx of the hallux, the third and the fourth phalanx of the third digit and the third phalanx of the fourth digit are sub-equal in length and longer than the rest ( Fig. 8 ).

Discussion. DNHM-D2889 possesses several enantiornithine synapomorphies, such as the Y-shaped furcular, the distal tarsals fused with metatarsals II-IV, but metatarsals II-IV unfused along their lengths, and the minor metacarpal longer than the major metacarpal. Furthermore, the elongate rostrum, about 60% of the total skull length, the dentition restricted to the premaxilla and the rostral-most portion of the dentary, the coracoid with a nearly straight lateral margin, and the pygostyle longer than the tarsometatarsus, place it firmly within Longipterygidae (O’Connor et al. 2009; 2011).

Longipterygidae includes six genera and six species to date. They are distinguishable both in morphology and in size ( Tab. 2 ). Boluochia zhengi Zhou, 1995 originally was named by Zhou Zhonghe in 1995 and then was promoted to be a higher level taxon (Boluochiaformes, Boluochidae ) (Zhou & Zhang 2006). Recent studies show that Boluochia zhengi belongs to Longipterygidae and it is closely related to L. chaoyangensis ( O’Connor et al. 2010) . Both the original and the revised diagnosis of B. zhengi has features that show that it is a small enantiornithine: tip of premaxilla hook shaped; metatarsal IV longer than II and III and laterally deflected along the distal one-fifth of the tarsometatarsus; pygostyle 20% longer than tarsometatarsus; metatarsals II-III subequal in length (Zhou & Zhang 2006; O’Connor et al. 2010). The premaxilla of DNHM-D2889 is preserved completely and with teeth arranged along its ventral margin, but differs from B. zhengi with its tip is relatively tapered and smooth, and its metatarsal II is much shorter than metatarsal III in length. Longirostravis hani is also much smaller than DNHM-D2889 and its teeth are much more closely spaced and smaller than those of DNHM-D2889 (see Hou et al. 2004). Shanweiniao cooperorum O’Connor et al., 2009 is much smaller than DNHM-D2889 and its second phalanx of manual major digit reduced and wedge-shaped, very different from that of DNHM-D2889. Especially, S. cooperorum has an elongate tail composed of at least four closely aligned rectrices (O’Connor et al. 2009). Rapaxavis pani is much smaller than DNHM-D2889 and its manual digits are much more reduced than those of

DNHM-D2889 (see Morschhauser et al. 2009; O’Connor et al. 2011). Shengjingornis yangi Li et al., 2012 is similar to DNHM-D 2889 in size, but its manual digits are also much more reduced than those of DNHM-D2889 and the ratio of the intermembral index (humerus+ulna/femur+tibiotarsus) (1.0) is lower than that of DNHM- D2889 (1.2) (see Li et al. 2012). Li et al. (2010) reported a Longipterygidae bird, named Camptodontus yangi , which preserved a longitudinal groove in the anterolateral facet of each premaxillary tooth crown. However, the specimen is incomplete and preserved disarticulated, the diagnosis was obscure and no detailed dentation photographs were provided. Based on the descriptions and comparisons (see Li et al. 2010), it is probably a synonym of Longipteryx chaoyangensis , so, the validity and anatomical characteristics of Camptodontus yangi will need to be re-examined. Longipteryx chaoyangensis is the type species of Longipterygidae . It shows close similarities with DNHM-D2889, such as the heterocoelous middle cervical vertebrate, the metatarsal IV longer than the other metatarsals, and the tibiotarsus shorter than the humerus and the ulna (see Zhang et al. 2001). There are also some minor differences between them, such as the ratio of the intermembral index, ratio of femur to tibiotarsus, ratio of femur to humerus and the interclavicular angle ( Tab. 3 ). These differences can be attributed to ontogenetic variation since the holotype of L. chaoyangensis is not an adult individual. Moreover, we observed that the tooth crenulations we found in DNH-D2889 are present in the holotype of L. chaoyangensis (IVPP-V12325) when we re-examined it ( Fig. 9 ). They are not as prominent and developed as those of DNHM-D2889. Perhaps they were damaged during the preservation of that fossil or during its preparation, or, perhaps the tooth crenulations are not as developed as those of DNHM-D2889 because IVPP-V12325 is not an adult individual. Determining the intraspecific variation in development and morphology of tooth crenulations among different individuals awaits recovery of further specimens. The use of theropod tooth morphology for taxonomic purposes has been examined by a number of workers ( Currie et al. 1990; Rauhut & Werner 1995; Sankey et al. 2002). Currie et al. (1990) have shown that theropod tooth morphology (including tooth serrations) is reliable for diagnosing taxa to familial, and in some cases to higher taxonomic levels. Up to date, the crenulations only have been recognized in DNHM-D2889 and IVPP-V12325 among enantiornithines or even within Aves. Based on the anatomical characteristics and comparisons with other longipterygids, we consider DNHM-D2889 as new material of L. chaoyangensis .

To date, the only way to infer the trophic habit of enantiornithines from the Jehol Group is through their cranial or dental morphology ( O’Connor et al. 2013). Longipterygids constitute a distinct clade within enantiornithines because they have a unique long rostrum, dentition restricted to the premaxilla and rostral-most portion of the dentary, and relatively long forelimbs. They are interpreted as having fed on fish, worms or bivalves (Zhang et al. 2001; Hou et al. 2004; Morschhauser et al. 2009; O’Connor et al. 2009; Li et al. 2013). DNHM-D2889 preserves crenulations on the caudal margins of its premaxillary teeth and probably on the dentary teeth. This form of tooth ornamentation has neither been observed among birds, nor among non-avian dinosaurs. We consider the crenulations as true structures because they are only present on the caudal margins of these teeth. If they were formed by glue or sediments, they would probably also present on the anterior margins of premaxillary teeth. They are not an artefact of preparation because they are prominently arranged in two lines along the caudal margin, and their surfaces are smooth, which may be interpreted as worn facets. Moreover, very faint crenulations also can be observed in the holotype of L. chaoyangensis , on the caudal margins of premaxillary teeth (IVPP-V12325). These tooth crenulations are not the first ornament found on teeth within Aves, since longitudinal grooves on the lingual surface of premaxillary teeth have been observed in Sulcavis geeorum O’Connor et al., 2013 ( O’Connor et al. 2013). The diversity of dental shapes may reflect differences in food items between taxa ( O’Connor et al. 2013). The large, recurved, and labiolingually compressed teeth with crenulations and recurved sharp manual and pedal claws suggest that Longipteryx chaoyangensis probably occupied more extensive trophic niches than previously thought. They could probably prey on not only fish but also some small terrestrial vertebrates. This feeding habit further expanded their food chain and their living space. This unique dental specialization not only expands the diversity of dental morphologies among Mesozoic birds, but also explained why longipterygids were the most diversified enantiornithines.

Figures

FIGURE 1. Photograph of the holotype of Longipteryx chaoyangensis (IVPP-V 12325).

FIGURE 2. Photograph of DNHM-D 2889, a nearly complete and articulated adult individual from the Lower Cretaceous Yixian Formation and referred to Longipteryx chaoyangensis Zhang et al., 2001.

FIGURE 3. Line drawing of DNHM-D 2889, a nearly complete and articulated adult individual from the Lower Cretaceous Yixian Formation and referred to Longipteryx chaoyangensis Zhang et al., 2001.

FIGURE 4. Detailed photograph of the skull of DNHM-D 2889, a nearly complete and articulated adult individual from the Lower Cretaceous Yixian Formation and referred to Longipteryx chaoyangensis Zhang et al., 2001.

FIGURE 5. Detailed photograph of the dentition of DNHM-D 2889 in labial view. A, photograph of the dentition; B, close up of the first right premaxillary tooth; C, close up of the second right premaxillary tooth; D, close up of the third right premaxillary tooth; E, close up of the fourth right premaxillary tooth.

FIGURE 6. Detail of the left carpometacarpus of DNHM-D 2889.

FIGURE 7. Detail of the right wing of DNHM-D 2889.

FIGURE 8. Detail of the right foot of DNHM-D 2889.

FIGURE 9. Detailed photograph of the dentation of Longipteryx chaoyangensis (IVPP-V 12325) in labial view. A, photograph of the dentition; B, close up of the first right premaxillary tooth.

Tables

TABLE 2. Comparison of select measurements (mm) of the named longipterygids.

Specimen	Femur	Humerus	Ulna	Radius	Tibiotarsus
DNHM-D2889	31	40	42	40	38
IVPP-V12325	29	42	47	43	30
Shengjingornis	38	41	42	43	44
Rapanxavis	19	23	23	23	23
Shanweiniao	18	22	23	18	23
Longirostravis	20	24	25	--	25
Boluochia	--	--	--	--	24

TABLE 3. Comparisons of important bone lengths between DNHM-D 2889 and Longipteryx chaoyangensis (IVPP- V 12325).

Specimen	intermembral index	femur/tibiotarsus	femur/ humerus	clavicle/hypocleideum
DNHM-D2889	1.2	0.8	0.8	1.1
L. chaoyangensis	1.5	1.0	0.6	1.8