From Kunlun Pass Basin, Northeastern Tibetan Plateau and Their Bearings on Development of Water System and Uplift of the Area

SCIENCE CHINA Earth Sciences

• RESEARCH PAPER • April 2010 Vol.53 No.4: 485–500 doi: 10.1007/s11430-010-0048-5

Pliocene cyprinids (Cypriniformes, Teleostei) from Kunlun Pass Basin, northeastern Tibetan Plateau and their bearings on development of water system and uplift of the area

WANG Ning & CHANG Mee-mann*

Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China

Received November 23, 2009; accepted February 25, 2010

Here described are the cyprinid fossils from the Pliocene Lower Member of Qiangtang Formation of the Kunlun Pass Basin, northeastern Tibetan Plateau, collected at a locality 4769 m above the sea level (asl). The materials consist of numerous disarticulated and incomplete bones as well as thousands of pharyngeal teeth, fin rays, and vertebrae. The fossils were referred to the genus Gymnocypris, lineage Schizothoracini, family Cyprinidae; the lineage Schizothoracini; and the family Cyprinidae respectively. The Schizothoracini is a freshwater fish group endemic to the Tibetan Plateau and its surrounding area. Previous workers on living schizothoracins regarded that Gymnocypris belongs to the highly specialized grade of the group, colonizing higher altitudes than other members of the group. Two species are so far unequivocally assigned to the genus, i.e., G. przewalskii and G. eckloni, and they are inhabiting Qinghai Lake and the waters on both north (the Golmud River) and south (upper reach of the Yellow River) sides of the East Kunlun Mountain, respectively. The abundant fossil schizothoracins occur in the Kunlun Pass Basin on the southern slope of the East Kunlun Mountain (at 4769 m asl), close to the present Golmud River, indicating comparatively rich waters in the area and possible connections between the water systems on north and south sides of the East Kunlun Mountain during the Pliocene. This also suggests a more humid climate in the area during the Plio- cene than it is today. The presence of the highly specialized schizothoracin Gymnocypris may also imply less amplitude of uplift (approximately 1000 m) in the area since the Pliocene than previously proposed.

Gymnocypris, Schizothoracini, Pliocene, Kunlun Pass Basin of northeastern Tibetan Plateau, development of water system, uplift of the area

Citation: Wang N, Chang M M. Pliocene cyprinids (Cypriniformes, Teleostei) from Kunlun Pass Basin, northeastern Tibetan Plateau and their bearings on development of water system and uplift of the area. Sci China Earth Sci, 2010, 53: 485–500, doi: 10.1007/s11430-010-0048-5

The Kunlun Mountain stretches along the southern border the area that is closely linked to the uplift of the Tibetan of Qaidam Basin, northeastern Tibetan Plateau, whereas Plateau and the global climate and environmental changes Kunlun Pass Basin is situated on the south slope of the mid- [5, 6]. The geology of this area has long attracted the atten- dle section of the East Kunlun Mountain (Figure 1). It is a tion of geologists and paleontologists worldwide. Paleon- fault basin, formed at the beginning of the late Cenozoic [2, tological studies conducted in this area, however, have fo- 3]. It contains comparatively thick late Cenozoic sediments cused mainly on palynology, ostracods, and mollusks, indi- (~700 m [4]), which documented the geological history of cating significant environmental changes since the Pliocene [7-10]. Vertebrate fossils from the Basin have not yet been specifically reported. *Corresponding author (email: [email protected]) There was only one fossil fish locality known in Tibetan

Figure 1 Geological map of East Kunlun Mountain and surrounding area, northeastern Tibetan Plateau (Based on Geological Map of Qinghai Province [1]).

Plateau (Lunbola Basin [11]) before the team from the are extremely rare (Figure 2). Described so far from this Natural History Museum of Los Angeles County (LAM) area were Plesioschizothorax macrocephalus [11], a fossil and Institute of Vertebrate Paleontology and Paleoanthro- genus and species originally referred to the family Cyprini- pology (IVPP), led by Wang Xiaoming, started to work in dae; Hsianwenia wui [14], another fossil genus and species Qaidam Basin, northeastern Tibetan Plateau, at the end of referred to the subfamily Schizothoracinae (=Oreininae, last Century. Several vertebrate fossil localities, including Cyprinidae); and several disarticulated pharyngeal bones fish remains, were found in Qaidam Basin [12–14] (Figure with teeth referred to the Barbinae [13] of the Cyprinidae. 2). During the field seasons of 2006 and 2007, the team Both Plesioschizothorax macrocephalus and Hsianwenia worked in the Kunlun Pass Basin and discovered numerous wui were considered as belonging to the subfamily disarticulated fish bones and teeth as well as some mam- Schizothoracinae by Chang et al. [14]. mals [17]. The fish fossils were collected from the locality The Cyprinidae is the largest family of freshwater fishes. KL0607 (35°38′09.0″N, 94°05′05.6″E), about two kilome- Although works abound as to the phylogeny of the group ters east of the Qingzang Railway and 116 km southwest to during the last two decades, both from morphological and Golmud City, Qinghai Province (Figure 1). The altitude of molecular aspects [18-27], views are equally abundant the locality is 4769 m above the sea level (asl). This is one among ichthyologists on recognition of the subgroups of the of the few localities uncovered recently from the Plateau family, their scope, and their interrelationships. For pos- with a large quantity of fossil fish, and it is one of the high- sessing the unique “anal scales”, schizothoracins are re- est vertebrate fossil localities in the world. The fish remains garded as a monophyletic subfamily (Schizothoracinae) [16, from the Kunlun Pass Basin were collected from the Lower 28-32] or a subgroup (Schizothoracini) within the subfam- Member of the Qiangtang Formation [6]. The age of the ily Cyprininae [19, 33]. For their restricted distribution, Lower Member of the Qiangtang Formation is 2.58-1.77 schizothoracins usually were not included or only one spe- Ma based on a magnetostratigraphic study, ranges from the cies was included in a number of phylogenetic analyses of late Pliocene to early Pleistocene according to Song et al. the Cyprinidae or Cypriniformes [20-22, 24-27]. Because [6], or late Pliocene according to Wang et al.’s work on of lack of specimens, the group was rarely discussed in fossil mammals [17]. In this paper we adopt the view in the these works. Wherever more specimens of this group were latter work. The fish-bearing deposits are fluvial-lacustrine involved, the group was frequently treated as monophyletic dark gray mudstones intercalated with yellow brown muddy [18, 19, 31, 32, 33-37], regardless of which taxonomic rank sandstones or siltstones. (subfamily, lineage or tribe) the group is placed at. In a few The Cenozoic fossil fishes found from Tibetan Plateau recent works dealing with the phylogeny of the Cyprinidae, WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 487

Figure 2 Map of Cenozoic fossil fish localities and distribution of Recent Gymnocypris species in Tibetan Plateau, based on Wu and Wu [15] and Chen and Cao [16]. however, schizothoracins were considered non-monophy- tion and environment. We were able to identify some of the letic [38-41]. bones as belonging to Gymnocypris sp. indet., and a few In most morphological and molecular studies of the Cy- others to the lineage Schizothoracini gen. and sp. indet. priniformes and Cyprinidae, the subfamily Cyprininae [19, (subfamily Cyprininae). For the rest of bones, we could 20, 26, 27] or Series Barbini [18] is well supported, and the only refer them to the family Cyprinidae gen. and sp. indet. Schizothoracini, where included, is treated as one of its without any specifications. subgroups [19, 33]. In this paper, we follow Howes [19] and The zoogeography of the living schizothoracins has been Kullander et al. [33] to refer the materials, which we are studied and the evolutionary process of the group deduced able to identify as belonging to Gymnocypris, to the [30, 42]. The living schizothoracins were considered to have Schizothoracini lineage (=Tribe Oreinini [33], Schizotho- developed in correlation with the uplift of the Tibetan Pla- racinae [28]), subfamily Cyprininae. As for the lineage teau and were divided into three grades: primitive, special- (Tribe) name, we prefer Schizothoracini to Oreinini at pre- ized, and highly specialized. The division of the three sent, pending further works to clarify the priority of the ge- grades was based on the extent of modifications of their nus name, Schizothorax or Oreinus [33]. The lineage scales, barbells, and rows of pharyngeal teeth, and their dis- Schizothoracini is a comparatively large group with nu- tribution at three successive altitudes at which water tem- merous morphologically similar genera and species. The perature and precipitation decrease, and solar radiation and phylogenetic relationship of the group is in need of further evaporation increase [30]. The genus Gymnocypris from our work. materials falls in the highly specialized grade. From the numerous fish bones collected from the locality KL0607, Kunlun Pass Basin, we could recognize fishes belonging to two cypriniform families, the Cyprinidae and 1 Materials and methods Nemacheilidae. In this paper, we describe the cyprinid bones and discuss some problems concerning their distribu- All fish remains from Kunlun Pass Basin consist of disar- 488 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 ticulated, incomplete bones. They do not seem buried in situ 2 Systematic paleontology but sorted and transported by water, then re-deposited, for only relatively thick bones or thick parts of bones are pre- Superorder Ostariophysi Sagemehl, 1885 served. Usually the bigger and thicker bones are black to Order Cypriniformes Bleeker, 1859/60 dark brown and smaller and thinner bones light, and they Family Cyprinidae Bonaparte, 1840 stand out against the lighter-colored matrix. The specimens Subfamily Cyprininae sensu Howes, 1991 of Gymnocypris, schizothoracins, and cyprinids are num- Lineage Schizothoracini sensu Howes, 1991 bered as IVPP V 16925-16932, IVPP V 16908-16910, and (=Tribe Oreinini, Kullander et al., 1999) IVPP V 16933-16940 respectively. Genus Gymnocypris Günther, 1868 Materials used for comparison include dry skeletons and Gymnocypris sp. indet. disarticulated bones of 15 species of the Schizothoracini and 5 species of other cyprinines. They are: Referred specimens: IVPP V 16925.1-32, anterior parts Gymnocypris przewalskii IVPP OP 343, complete skele- of dentaries; IVPP V 16926.1-55, posterior parts of angu- ton; and IVPP OP 344, disarticulated bones; loarticulars; IVPP V 16927.1-14, ventral parts of quadrates; G. eckloni IVPP OP 345, disarticulated bones; IVPP V 16928.1-40, posterior parts of maxillae; IVPP V Oxygymnocypris stewartii IVPP OP 346, disarticulated 16929.1-42, kinethmoids; IVPP V 16930.1, a large part of a bones; left pharyngeal bone with teeth and bases of broken teeth, Schizopygopsis pylzovi IVPP OP 347, IVPP OP 348, dis- lacking the end part of the posterior edentulous process; articulated bones; IVPP V 16931.1, os suspensorium; IVPP V 16932.1-7, S. stoliczkai IVPP OP 349, IVPP OP 350, disarticulated supracleithrums. bones; Dentary: Seventeen left and 15 right dentaries were rec- S. younghusbandi IVPP OP 351, disarticulated bones; ognized, but none of them is intact. On specimen IVPP V Platypharodon extremus IVPP OP 352, disarticulated 16925.1, a large part of the left dentary is preserved, only bones; with its posterior part along with the posterodorsal part of Gymnodiptychus pachycheilus IVPP OP 353, disarticu- the coronoid process lacking. Its anterior branch bends lated bones; medially with a deep and narrow joint facet to meet its Ptychobarbus dipogon IVPP OP 354, disarticulated counterpart. The anterior branch shows a broad and horizontal dorsal surface, with a foramen located at the middle bones; point between the joint facet and the origin of the coronoid Schizothorax macropogon IVPP OP 355, disarticulated process, for the passage of the mandibular branch of the bones; trigeminal (V) nerve. The foramen opens on the lateral sur- S. o’connori IVPP OP 356, disarticulated bones; face of the dentary closer to the upper rim of the first sen- S. waltoni IVPP OP 357, disarticulated bones; sory canal opening than to the dorsal margin of the lateral S. oligolepis IVPP OP 358, disarticulated bones; surface (Figure 3A). The groove accomodating the insertion S. prenanti IVPP OP 359, disarticulated bones; of the anguloarticular and Meckel’s cartilage is clearly S. chongi IVPP OP 360, disarticulated bones; shown in the medial face of the dentary (Figure 3B). The Barbodes schwanenfel IVPP OP 361, disarticulated most characteristic feature of the dentary is that the man- bones; dibular sensory canal is very broad and the openings leading Spinibarbus sinensis IVPP OP 362, disarticulated bones; from it to the surface are very large. Two and an upper half Balantiocheilus melanopterus IVPP OP 363, disarticu- of the oval shaped openings can be seen in the specimen, lated bones; leading from the mandibular canal onto the ventrolateral Cyprinus carpio IVPP OP 364, disarticulated bones; surface of the dentary. The vertical diameter of the openings Carassius auratus IVPP OP 365, disarticulated bones. is roughly comparable to the depth of the part of the lateral All specimens are stored in the collections of IVPP. surface of the dentary above the sensory canal openings (Figure 3A). The origin of the coronoid process is opposite The fossil bones were easily picked out or screen-washed to the posterior edge of the second sensory canal opening. from the comparatively soft matrix and then cleaned me- Among Recent schizothoracins, such large-sized, cavity- chanically using a thin needle under binocular WILD- M7A like mandibular canal openings have only been observed in stereomicroscope. Photographs were taken by CANON 1Ds the species of the genera Gymnocypris (Figure 3C, D) and digital camera connected to OLYMPUS SZX12 stereomi- Oxygymnocypris (Figure 3E, F) [31]. The fossil dentary is croscope. The way of measurements of the pharyngeal bone more similar to that of Gymnocypris than to Oxygymno- follows Chu [43] and the terms of teeth are according to cypris. In Oxygymnocypris, the dentary is slenderer, the Vasnetsov [44]. General osteological terminology follows dorsal side of its anterior branch is narrower, and its coron- that of Conway et al. [45]. oid process is situated more backward (posterior to the third WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 489

Figure 3 Dentary of fossil Gymnocypris IVPP V 16925.1 (A, B) and Recent Gymnocypris IVPP OP 345 (C, D) and Oxygymnocypris IVPP OP 346 (E, F). A, C, E ventrolateral view. B, D, F dorsomedial view. cp, coronoid process; fd, foramen for passage of mandibular branch of trigeminal nerve (V) in dorsal side; fl, foramen for passage of mandibular branch of V in lateral side; gac, groove accomodating anguloarticular and Meckel’s cartilage; j, joint facet for counterpart; mo, mandibular sensory canal openings. Scale bars: 2 mm. sensory opening) than that in Gymnocypris. And the fora- Since the narrow bone bands dividing the openings outside men of the passage of the mandibular branch of V in the the sensory canal are broken, only wide groove instead of lateral surface of the dentary is closer to the dorsal margin canal can be seen in our specimen (Figure 4A, B, and D). than to the upper rim of the sensory canal openings in Oxy- Such broad sensory canal in anguloarticular, in continuation gymnocypris. with that in dentary, has only been observed in Gymno- Anguloarticular: Twenty-six left and 29 right anguloar- cypris among Recent schizothoracins (Figure 4E). The ticulars were identified from our materials. Specimen IVPP anguloarticular of Oxygymnocypris bears similarly V 16926.1 shows a well preserved right anguloarticular, developed sensory canal as that of Gymnocypris, but the only with a small anterior part missing. It is an elongated caliber of the canal is visibly narrower (Figure 4F). bone plate with its anterior part narrowing and stretching Quadrate: The ventral parts of eight left and six right forward to insert into the groove on the medial side of the quadrates were found. All of the fossil quadrates lost their dentary (Figure 4A–D). Its posterodorsal part is thickened. dorsal plates, and only the specimen IVPP V 16927.1 has On the dorsal side of this part lies the well-developed socket comparatively intact ventral part (Figure 5A, B). The ven- for receiving the articular head of the quadrate (Figure 4A), tral part of the quadrate is shaft-like, broad and thick in the whereas on its ventromedial side is a small articular facet front whereas narrow and thin in the rear, and tapers into a for the retroarticular (Figure 4B). The medial face of the tip in the posterior end. The anterior articular facet for the anguloarticular is somewhat uneven, covered with pits, anguloarticular joint socket is rather broad. The groove ac- short grooves and ridges. The area where the Meckel’s car- commodating the symplectic is clearly shown on the medial tilage originates is clearly shown (Figure 4C). Anterior to side of the bone, and the groove stretches anteriorly close to the base of the socket for the articular head of the quadrate, the articular facet in the front. The lateral margin of the the bone bends slightly inwards, forming a smooth lateral bone is blade-like. The anterior portion of the dorsolateral surface (Figure 4A, B, and D). The broad mandibular sen- surface of the bone is covered with pits and short grooves sory canal seems traversing the bone just beneath the socket. leading backward from the pits, whereas the ventromedial 490 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4

Figure 4 Anguloarticular of IVPP V 16926.1 (A–D) and Recent Gymnocypris IVPP OP 345 (E) and Oxygymnocypris IVPP OP 346 (F). A, dorsal view. B, ventral view. C, medial view. D–F, lateral view. ar, articular facet for retroarticular; co, Meckel’s cartilage origin; mc, mandibular sensory canal; sq, socket for articular head of quadrate. Scale bars: 2 mm.

Figure 5 Quadrate of IVPP V 16927.1 (A, B) and Recent Gymnocypris IVPP OP 345 (C, D). A and C, dorsal view. B and D, ventral view. a, articular facet for anguloarticular joint socket; dpl, dorsal plate; gs, groove containing symplectic. Scale bars: 2 mm. surface of the bone is rather smooth. Although only the preserved basal part, the dorsal process is fairly broad and ventral part was preserved, the fossil is very similar to the forms a nearly right angle with the posterior part of the bone equivalent part of the quadrate in Gymnocypris (Figure 5C, (Figure 6A, B). The sigmoid lower margin and the D). knob-like posterior end of the maxilla occur mostly in cy- Maxilla: Posterior parts of 21 left and 19 right maxillae prinines [20]. Combination of downward bent posterior end were found. As far as we can see from the preserved parts, it and broad dorsal process seems most similar to that in is a long bone, with its lower margin sigmoidally curved Gymnocypris among schizothoracins (Figure 6C, D). and posterior end bent down and widened into a round knob. Kinethmoid: The kinethmoid is a rod-like, bisymmetrical The anterior part of the maxilla is broken. Judged from its small bone, with its upper and lower parts expanded and WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 491

Figure 6 Maxilla in IVPP V 16928.1 (A, B) and Recent Gymnocypris IVPP OP 345 (C, D). A and C, lateral view. B and D, medial view. dpr, dorsal process; pk, posterior knob. Scale bars: 2 mm.

flattened in anterior-posterior direction and its middle part deep and narrow (Figure 7A–C). There is a shallow depression in the anterior surface of its upper part for the attachment of the ligament connecting the bone with the dorsal processes of the premaxillae, whereas the rugged posterior surface of its lower part with two tiny processes on its ventrolateral margin probably serves for the attachment of the connective tissue linking it with the mesethmoid [46] and the vomer [47]. The lateral side of the middle part is concave, accommodating the cartilage linking the nasal and preethmoid [46, 48]. From the lateral view, the dorsal margin of the bone is arc-like. The width of the upper part is comparable to that of the lower part, and is much broader than that of the middle part. It is impossible to look through the kinethmoid in all species of cyprinids. From all what we could examine, the bone at our hand is most similar to the kinethmoid of Gymnocypris (Figure 7D–F). Pharyngeal bone: From our material we found only one small pharyngeal bone. The bone is crescent-shaped and relatively slender. Its anterior edentulous process, tapering anteroventrally to a pointed tip, is comparable in length with the dentigerous surface. If Chu’s [43] method of measurements is followed, the estimated length of the bone (~0.55 mm) should not be much influenced by the lack of the end part of the posterior edentulous process. Then the length/ width (~0.19 mm) ratio of the pharyngeal bone is approximately 2.9. The dorsal edge of the bone is narrow, whereas the ventromedial surface is broad (Figure 8A). The pitted

surface is expanded in its middle part, extending forward to Figure 7 Kinethmoid in IVPP V 16929.1 (A–C) and Recent Gymno- the point opposite to A1 (Figure 8B). The anterior angle is cypris IVPP OP 345 (D–F). A and D, front view. B and E, posterior view. broken, and the posterior angle is not preserved. Judged C and F, lateral view. d, depression for ligament connecting dorsal processes of premaxillae. p, process for connective tissue linking mesethmoid from the three preserved teeth and four bases of broken and vomer. Scale bars: 1 mm. teeth observed in the bone, it can be confirmed that there 492 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4

Figure 8 Pharyngeal bone in IVPP V 16930.1 (A, B) and Recent Gymnocypris IVPP OP 345 (C, D), Schizopygopsis IVPP OP 351 (E, F), Oxygymnocypris IVPP OP 346 (G, H), Ptychobarbus IVPP OP 354 (I, J), and Gymnodiptychus IVPP OP 353 (K, L). A, C, E, G, I, and K, dentigerous sides; B, D, F, H, J, and L, pitted sides. aa, anterior angle; ae, anterior edentulous process; de, dorsal edge; pa, posterior angle; pe, posterior edentulous process; vs, ventromedial surface. Scale bars: 0.5 mm for A and B, 3 mm for C–L. are two rows of pharyngeal teeth. The four teeth in the inner (sensu Cao et al. [30]). row (row A) are stronger than the three teeth in the outer Os suspensorium: In specimen IVPP V 16931.1, only row (row B). The tooth formula is 3, 4 /. The preserved the outer arm of a left os suspensorium (parapophysis of the teeth A1, B1, and B2 are elliptically cylindrical, with 4th vertebra) is preserved. The inner arm is broken, leaving slightly recurved tips. Their spoon-like grinding surfaces are its base sticking out from the outer arm close under the longer than wide, and flanked with lateral ridge-like edges. pyramid-like top. The outer arm is, on the whole, an elon- B1 is slightly stronger than B2. The grinding surfaces of B1 gated arched strip with smooth surfaces, except its thick and B2 are more oblique than that of A1 (Figure 8A). This upper head with the pyramid-like process, fitting into the fossil pharyngeal bone is similar to that of several special- fossa on the lateral side of the 4th centrum (Figure 9A). On ized and highly specialized Recent schizothoracin genera the posterodorsal side of the bone the area under the top is (sensu Cao et al. [30]), e.g., Diptychus, Ptychobarbus, fenestrated (Figure 9B). The outer arm is widest at the bi- Gymnodiptychus, Schizopygopsis, Chuanchia, Gymnocypris, furcating point of the inner arm that should have formed the and Oxygymnocypris, based on the tooth formula (3, 4 /) suspensorium, but is missing in our specimen. From the and spoon-like grinding surface [15, 16]. The pharyngeal bifurcating point downwards, the outer arm (or parapophy- bone of Oxygymnocypris (Figure 8G, H) is much slenderer sis) becomes thinner and bending moderately inwards. The than that of Gymnocypris (Figure 8C, D) and the fossil bone distal end is slightly expanded and blunt. According to Wu (Figure 8A, B), with the length/width ratio more than 3.6 and Chen [11], the distal end of the 4th parapophysis (outer [15, 16]. Our observation shows that the pitted surfaces in arm of the os suspensorium) in Recent schizothoracins is Ptychobarbus and Gymnodiptychus (Figure 8I–L) are much expanded (Figure 9C–J), whereas those of other cyprinines narrower than that of Gymnocypris (Figure 8C, D) and the are always narrow (Figure 9K–N). Among Recent fossil (Figure 8A, B). Furthermore, according to Chu [43], schizothoracins we have checked, the shape of the outer arm the anterior edentulous process is rather short, only about of the os suspensorium is quite different between different two thirds of the length of the dentigerous surface in Dip- genera (Figure 9C–J), and the fossil os suspensorium is tychus. The fossil pharyngeal bone is more similar to that of most similar to that of Gymnocypris (Figure 9C, D). Gymnocypris (Figure 8C, D) than to that of Schizopygopsis Supracleithrum: Four left and three right supracleithrums (Figure 8E, F), particularly in the contour of the anterior were found from our materials. The supracleithrum is a ver- edentulous process. There are three rows of pharyngeal tical, elongated, and flattened bone, with its upper part teeth in “primitive schizothoracins” and all “barbines” slightly bent inwards. Its uppermost part is nearly triangular WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 493

Figure 9 Fossil os suspensorium in IVPP V 16931.1 (A, B) and Recent Gymnocypris IVPP OP 345 (C, D), Schizopygopsis IVPP OP 351 (E), Oxygymno- cypris IVPP OP 346 (F), Platypharodon IVPP OP 352 (G), Ptychobarbus IVPP OP 354 (H), Gymnodiptychus IVPP OP 353 (I), Schizothorax IVPP OP 357 (J), Barbodes IVPP OP 361 (K), Spinibarbus IVPP OP 362 (L), Cyprinus IVPP OP 364 (M), and Carassius IVPP OP 365 (N). A, C, and E–M, front view. B and D, back view. do, distal end of outer arm; ia, inner arm; uh, upper head. Scale bars: 0.5 mm for A and B, 2 mm for C–N. and pointed at the top. Two tiny but prominent processes must have been covered by the posttemporal bone. A are shown at the two lower angles of the triangle. The lat- groove with an opening at its bottom can be noticed close to eral surface of the upper part of the bone is smooth and the posterior edge of this part, transmitting the sensory canal 494 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4

Opercle: Seven left and 11 right anterodorsal fragments of the opercles were identified by its prominent opercular arm and typical articular fossa for the process at the rear margin of the hyomandibular. The opercular arm protrudes anterodorsally, forming an obtuse angle with the dorsal margin of the bone. The articular fossa is situated very close to the base of the opercular arm (Figure 11D). The lateral surface of the opercle is generally smooth, but covered by a few scattered openings with shallow grooves leading from them and arranged in a radiating way from the base of the arm (Figure 11E). Thick spine-like fin ray: More than one thousand well-preserved unbranched, spine-like fin rays have been collected, and most of them are with their distal ends broken and in left or right halves. They are strong, serrated at their posterior edge. The serrations emerge a short distance up the base of the fin ray, and the proximal few ones are weaker than the distal ones. Twenty serrations are preserved on the most completely preserved ray IVPP V 16910.1, and the serrations stand either perpendicular to the ray or Figure 10 Supracleithrum in IVPP V 16932.1 (A, B) and Recent Gym- somewhat with the tip pointing distally (Figure 11F, G). nocypris IVPP OP 345 (C, D). A and C, lateral view; B and D, medial view. sc, sensory canal. Scale bars: 2 mm. These rays look like the posteriormost unbranched fin rays in the dorsal fin of Recent schizothoracins. The spine-like fin rays of similar structure were previously found in fossils to the lateral line on the body. The broadest part of the bone, of Hsianwenia wui (Schizothoracinae) from Yahu [14] and covered with tiny pits, is close to its upper-middle part, in Cyprinidae gen. et sp. indet. from Lulehe area, Qaidam where the bone is bending. The lower part of the bone is Basin [13]. In some other cyprinines, such as Cyprinus, narrow and shaft-like, covered with longitudinal thin Carassius and many other cyprinines, the spine-like fin rays grooves (Figure 10A). The medial surface of the bone is are usually with tips of the serrations pointing proximally. smooth (Figure 10B). Judged from the shape of the bone, the ornamentation on the lateral surface, and the two tiny Cyprinidae gen. et sp. indet. processes on the medial side of the dorsalmost part, the fos- Referred specimens: IVPP V 16933.1–29, anterior parts sil bone is most similar to the supracleithrum of Gymno- of urohyals; IVPP V 16934.1–11, ventral hypohyals; IVPP cypris (Figure 10C, D). V 16935.1–30, anterior ceratohyals; IVPP V 16936.1–23, Schizothoracini gen. et sp. indet. posterior ceratohyals; IVPP V 16937.1–4, interhyals; IVPP V 16938.1–26, posterodorsal parts of hyomandibulars; Referred specimens: IVPP V 16908.1–1392, detached IVPP V 16939.1–4, first pectoral radials; IVPP V 16940. pharyngeal teeth; IVPP V 16909.1–18, anterodorsal parts of 1–11, medialmost pelvic radials. opercles; IVPP V 16910.1–1568, unbranched fin rays with Urohyal: The anterior part of the urohyal is narrow, with serrations on the posterior edge. two long and nearly parallel anterior processes for connec- Pharyngeal teeth: More than one thousand scattered tion of the ventral hypohyals (Figure 12A). The horizontal pharyngeal teeth were picked out from the deposits in ventral plate is almost lost except the very anterior portion. Kunlun Pass Basin. These teeth are of similar shape as those Only a small part of the vertical dorsal plate is preserved on the pharyngeal bone described above, with their crowns (Figure 12B). standing straight on the neck or slightly bent anteriorly. Tips Ventral hypohyal: Three left and eight right ventral hy- of the teeth are curved posteriorly in different extent. The pohyals were discovered. The bone is somewhat triradiate, spoon-like grinding surface of various widths is covered with an anteroventrally protruding process (Figure 12C, D). with fine, longitudinal stripes (Figure 11A–C). Pharyngeal Posteriorly, the bone is composed of two joint facets, the teeth of this type are common in Recent schizothoracins [15, ventral broader one for the connection to the anterior cera- 16, 43]. Although pharyngeal teeth with spoon-like grinding tohyal and the dorsal narrower one for the dorsal hypohyal surfaces also exist in several other cyprinin genera such as to attach. The lateral and dorsal surfaces of the bone have Barbodes and Spinibarbus, which are closely related with scattered fossae and pits, whereas the medial surface is schizothoracins, the pharyngeal teeth of Barbodes and comparatively smooth. Spinibarbus are more laterally depressed and the grinding Anterior ceratohyal: Fifteen left and 15 right anterior surfaces are narrower than that of schizothoracins. ceratohyals were unearthed. The bone is relatively thick and WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 495

seems in continuation with that in the anterior ceratohyal, possibly for the hyoidean artery to traverse [45]. Its ventral margin is blade-like. The lateral side is relatively rough, with shallow fossae close to the posterior angle. The medial side of the bone is almost smooth, except several tiny pits near its posterior angle. Interhyal: Three left and one right interhyals were ob- tained. The bone is rod-like. Its lower end bends slightly anteriorly with a concave facet for articulation with the posterior ceratohyal, whereas its upper end is comparatively flat, for articulation with the hyomandibular and symplectic (Figure 12I, J). Close to its lower end, the posterior side of the bone carries a ridge (Figure 12K). The lateral side of the bone for adherence to the medial side of the preopercle is uneven, whereas the medial side of the interhyal is comparatively smooth. Hyomandibular: Seven left and 19 right posterodorsal fragments of the hyomandibular were recognized by the characteristic articular area with the neurocranium on top of the bone and the rounded articular process for the opercle at the rear margin. On the lateral side, a rather sharp ridge stretches backward starting from a point under the opercle process (Figure 12L). Many small pits are shown on the medial side of the bone, and especially on a raised area an- teroventral to the opercular process (Figure 12M). Antero-

dorsal to this area, part of a large opening can be seen, Figure 11 Pharyngeal teeth IVPP V 16908.1–3 (A–C), opercle IVPP V which usually accommodates the hyomandibular ramus of 16909.1 (D, E) and unbranched fin ray with serrations IVPP V 16910.1 (F, the facial nerve (VII) and the efferent hyoidean artery. G). D and F, lateral view; E and G, medial view. ah, articular fossa for hyomandibular; di, distal end; dm, dorsal margin; g, grinding surface; oa, Pectoral radials: One left and three right first (outer- opercular arm; pr, proximal end. Scale bars: 1 mm for A–E, 2 mm for F most) pectoral radials were found. The radial is somewhat and G. elongated with broad front margin, which should have at- tached to the posteroventral side of the scapula. The poste- of rectangular shape, with its posterior end deeper than the rior part of the bone is narrow with a rod-like end. The dor- anterior, and middle part slightly constricted (Figure 12E, F). sal side of the bone is rugged and the ventral surface is Its thick anterior end bears two joint facets for the two hy- comparatively smooth (Figure 12N, O). The medial surface pohyals to attach, one facet facing front for the ventral hy- of the bone must have clung to the second pectoral radial pohyal and the other facing medially for the dorsal hypo- and the lateral surface connected to the proximal end of hyal. The posterior end of the anterior ceratohyal is com- pectoral fin rays. paratively thin, and is in connection with the posterior cera- Pelvic radials: Six left and five right medialmost pelvic tohyal. The dorsal margin is slightly concave. Along the radials were found. The radial is roughly “boomer- margin is a groove with several pits sitting in the bottom. ang”-shaped with the medial margin arc-like and the lateral The ventral margin is deeply concave and thin, with its margin concave (Figure 12P, Q). The bone slightly bends middle part nearly blade-like. Both lateral and medial sur- dorsal-ventrally. The anterior terminal of the bone is com- faces of the anterior ceratohyal are entirely covered with paratively broad, whereas the bone becomes narrower pos- pits and shallow grooves leading from the pits towards the teriorly, with a sharp rear tip. There is a tiny notch on the back. anterior terminal, presumably accommodating the small Posterior ceratohyal: Twelve left and 11 right posterior process in the middle of the posterior margin of the basip- ceratohyal were found. The bone is triangular, with a deep terygium. anterior margin in connection with the anterior ceratohyal and a posterior angle (Figure 12G, H). At the very posterior end of the bone is a small process pointing posterodorsally. 3 Discussion The joint facet for the interhyal is situated at the postero- 3.1 Identification of fossil fish materials dorsal edge of the bone, just in front of the process. Along the anterior two thirds of its dorsal margin is also a narrow Part of the fossil bones unearthed form the Kunlun Pass groove with foramina sitting in the bottom. The groove Basin is assigned to the genus Gymnocypris, based on the 496 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4

Figure 12 Fossils identified as cyprinids. A and B, IVPP V 16933.1 urohyal; C and D, IVPP V 16934.1 ventral hypohyal; E and F, IVPP V 16935.1 anterior ceratohyal; G and H, IVPP V 16936.1 posterior ceratohyal; I–K, IVPP V 16937.1 interhyal; L and M, IVPP V 16938.1 hyomandibular; N and O, 16939.1 first pectoral radial; P and Q, 16940.1 medialmost pelvic radial. A, C, N, and P, dorsal view; D, O, and Q, ventral view; B, E, G, I, and L, lateral view; F, H, J, and M, medial view; K, posterior view. ahs, articular facet to hyomandibular and symplectic; an, articular area with neurocranium; apc, articular facet to posterior ceratohyal; ao, articular process for opercle; du, dorsal plate of urohyal; gha, groove accommodating hyoidean artery; jac, joint facet to anterior ceratohyal; jdh, joint facet to dorsal hypohyal; ji, joint facet to interhyal; jvh, joint facet to ventral hypohyal; ona, opening accommodating hyomandibular ramus of facial nerve and efferent hyoidean artery; pvh, processes connecting ventral hypohyals. Scale bars: 1mm for A–D, I–K, and N–Q; 2mm for E-H, L, and M. following observations. The mandibular sensory canal in the the pharyngeal bone of Ptychobarbus, Gymnodiptychus, and dentary and anguloarticular is very broad and its cavity-like Oxygymnocypris is much slenderer than in our fossils and sensory canal pores are very large. This is typical only for Gymnocypris. The elongated kinethmoid is almost identical Gymnocypris and Oxygymnocypris among schizothoracins. to that of Gymnocypris; the shaft-like ventral part of quad- The dentary and anguloarticular are much deeper in Gym- rate, and the outer arm of the os suspensorium (parapophy- nocypris and our fossils than in Oxygymnocypris. As in sis of the 4th vertebra) with its slightly expanded, blunt dis- Gymnocypris, the supracleithrum is slender, with a small tal end are all most similar to that of Gymnocypris in many triangular top part, carrying two small processes at the of their detailed structures (see above). lower angles of the triangle, and a long shaft-like lower part. The numerous detached spoon-like pharyngeal teeth have The pharyngeal bone is comparatively broad, having a tooth its grinding surface longer than wide, showing many fine formula as 3, 4 /. Though having the same tooth formula, longitudinal stripes; the opercle has smooth outer surface WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 497 and scattered openings and grooves leading from them; and schizothoracin genera already existed in the Kunlun Pass the thick spine-like fin ray bears distally pointing serrations Basin area during the Pliocene. at its posterior edge. Those are the features that could all be assigned to schizothoracins. Had we had better knowledge 3.2 Implications on development of water system and about morphology of more schizothoracin species, we could environment have referred these bones to specific genera, likely including Gymnocypris. The rest of the bones referred to the Cy- Recent schizothoracins are endemic to aquatic systems of prinidae also bear general similarities to those of the Tibetan Plateau and its surrounding areas, comprising Schizothoracini or even the Gymnocypris. We were not able 11–12 genera and nearly one hundred species and subspe- to assign them to a subgroup of the family partly because of cies. The Schizothoracini is a unique group of the Cyprini- their incomplete preservation and partly because of our in- dae that is adapted to high altitudinal environment in Cen- sufficient knowledge of the osteology of the living cyprinids tral Asia [15, 16, 28, 50]. The three grades of living (2420 species) in general and schizothoracins (around 100 schizothoracins are distributed at successive altitudes: the species and subspecies) in particular. The assignment of primitive grade inhabiting water systems at an altitude from these bones to the Schizothoracini gen. et sp. indet. and Cy- 1250 m to 2500 m asl, the specialized grade from 2750 m to prinidae gen. et sp. indet. does not exclude the possibility of 3750 m asl, and the highly specialized grade from 3750 m them being schizothoracins or even Gymnocypris. to 4750 m asl [30]. The genus Gymnocypris is regarded as The three grades of schizothoracins, the primitive, spe- one of the highly specialized schizothoracin genera. Al- cialized, and highly specialized (see above), were later though the phylogeny of the lineage Schizothoracini is not studied phylogenetically based on morphological characters. well resolved thus far and remains a challenge for those The results show that the three grades are monophyletic [31, who are interested in the problem, there is little doubt that G. 32]. Recently, however, several phylogenetic works on eckloni and G. przewalskii are closely related or form a sis- schizothoracins based on molecular data came to the con- ter pair [35, 49]. The two species are distributed in north- clusions that not all of the three grades are monophyletic. eastern Tibetan Plateau, spreading over the water systems He et al.’s analysis [35] suggested that the primitive and the both to the northern and southern sides of the East Kunlun highly specialized grades are monophyletic, but the special- Mountain. G. przewalskii inhabits the Qinghai Lake and its ized grade is not. Oxygymnocypris stewartii of the highly surrounding area, north of the East Kunlun Mountain, specialized grade was not included in this analysis. In the whereas G. eckloni is dwelling in the Golmud River north analysis by He and Chen [49] of the highly specialized of the Kunlun Mountain Pass, and the upper reach of the group with Oxygymnocypris stewartii included, however, all Yellow River east to the Pass and south of the East Kunlun species of the grade but Oxygymnocypris stewartii form a Mountain [49, 51–53] (Figure 2). monophyletic group. Our fossils were found from the Kunlun Pass Basin, just There has long been debate on the composition and mo- south of the Kunlun fault system, on the southern slope of nophyly of many genera of the lineage Schizothoracini. The the East Kunlun Mountain and southwest of the main peak genus Gymnocypris is regarded as one of the highly spe- of the range, Yuzhu Mountain (6179 m asl, Figure 1). To- cialized schizothoracin genera, comprising about 10 living day, the fish locality (KL0607) is situated somewhere in species and subspecies colonizing most of the main aquatic between the Qaidam Basin and the drainage of the upper systems on Tibetan Plateau [15, 16]. The monophyly of the reach of the Yellow River, at an altitude of 4769 m asl, and genus Gymnocypris was not supported by He et al. [35] the Kunlun Pass Basin has a desert environment. The fish based on complete mitochondrial cytochrome b sequences, remains collected from this locality were all disarticulated, but the total number of species of the genus they included in and no complete or even partially articulated skeletons were their analysis was only four. Inferred from the same kind of found. They were all collected from the surface of the out- molecular data, with eight species and subspecies included, crop belonging to the Lower Qiangtang Formation. As the He and Chen [49] also came to the conclusion that the spe- remains were all thick bones and thick parts of bones and cies formerly referred to the genus Gymnocypris do not the fossil-bearing deposits consist of coarser muddy sand- form a monophyletic group. Among them, only two species, stones or siltstones as well as fine mudstones, we suggest i.e., G. przewalskii and G. eckloni, form a sister pair, that the water in the Pass Basin Lake was not entirely static, whereas most of other species and subspecies of the genus and it is possible that some kind of transporting and sorting group with various species of the genus Schizopygopsis and of the fish bones happened during the process of burying. In one species with Chuanchia. Part of our materials, e.g., addition, as suggested by Wu et al. [3] and Song et al. [6], dentary with broad mandibular sensory canal and large the Kunlun Pass Basin at present is in the permafrost zone openings, pharyngeal bone with two rows of pharyngeal and the exposed surface of strata were disturbed by strong teeth, etc., was identified as belonging to the genus Gymno- frozen-thaw action, which might also have aided in the con- cypris, and was referred to the “highly specialized grade”. centration of the heavy bones and heavy parts of bones. In other words, at least one of the highly specialized As the majority of modern Gymnocypris live in lakes and 498 WANG Ning, et al. Sci China Earth Sci April (2010) Vol.53 No.4 rivers with broad valleys [15, 54], the abundant Gymno- ous than the recent suggestion proposed by Wang et al. [55], cypris remains collected from the Kunlun Pass Basin may i.e., 2700±1600 m. It is also different from Wu et al.’s esti- indicate a relatively extensive water system in the area of mation [3], i.e., the elevation (altitude) of the Kunlun Pass the Kunlun Pass basin during the Pliocene. This is in accor- was 1000–1500 m during the period of 7.0–1.1 Ma, based dance with the result suggested both by Wu et al. [3] on the on studies on fossil ostracods [8, 9] and pollens [7], imply- basis of the geomorphological evidences from the pass area ing a rigorous uplift after 1.1 Ma. and by Wang et al. [55] based on their study of the stable The localities of the recently discovered fossil isotopes in fossil vertebrates and invertebrates from the schizothoracins from the Qaidam Basin, i.e., that from the same deposits (Lower Member of the Qiangtang Formation) Oligocene of Wulan Husentu, Lulehe area with an altitude where our fish remains were collected. Consequently, the of 3022 m asl [13] and that from the Pliocene of Yahu [14] climate must be relatively humid in the area of Kunlun Pass at an altitude of 2772–2863 m asl, are outside of the distri- Basin during the Pliocene, compared with the desert-like bution area of modern schizothoracins. The locality from climate today, a point also made by Wu et al. [3] and Wang the central area of Tibetan Plateau, the Neogene of Lunbola et al. [55]. And there might be closer connections between Basin, Baingoin County [11], falls in the distribution area of the water systems of the Qaidam Basin north of the East the Recent “highly specialized” schizothoracins but with a Kunlun Mountain (the area around the Golmud River and present altitude of 4540–4550 m asl. All these fossil forms Qinghai Lake) and the upper reach of the Yellow River have three rows of pharyngeal teeth, and should be referred south of the mountain during the Pliocene than there are to the “primitive grade” of the lineage. That grade has a today. In other words, the water systems of the three areas recent distribution at the altitude from 1250 m to 2500 m asl might have been, in some way, continuous during that time. [30]. All the fossil localities yielding “primitive grade” This is especially meaningful given the fact that the living schizothoracins are situated well above the altitudes at schizothoracins from the Golmud River and that from the which the living schizothoracins of the “primitive grade” upper reach of the Yellow River on both sides of the East inhabit. Thus, we suggest that the height of the Qaidam Ba- Kunlun Mountain belong to the same species, G. eckloni, sin and other parts of the Tibetan Plateau must have been and that the species is most closely related to G. przewalskii considerably lower during the period from the Oligocene to from the Qinghai Lake. The relationship and distribution of Pliocene than it is today. these fishes indicate that the separation of G. eckloni and G. przewalskii must have occurred before the separation of the We thank Wang Xiaoming for his outstanding leadership in our fieldwork population of G. eckloni from the Golmud drainage and the on the Tibetan Plateau, which led to the discovery and collection of the populations from the upper reach of the Yellow River fossil fishes described here and elsewhere, and for his helpful discussion, drainage. In other words, when Qinghai Lake became iso- Miao Desui for stylistic improvement, Liu Huanzhang, Chen Yifeng and He lated, still connected were Golmud drainage and the water Shunping for providing Recent specimens and useful discussion, Wu Yunfei for useful discussion, Zhang Lixun, Zhao Changming, Li Qin, Dong Lu, system that were to become the recent upper reach of the and Bai Xiaoguang for providing Recent specimens, Liu Juan, Tseng Jack, Yellow River. The differentiation of the populations of G. Li Qiang, and Wang Zhao for collecting and preparation of fossils, and eckloni caused by the separation of their habitats must have Gao Wei for taking photographs. This study was supported by the National been influenced by the further uplift of the East Kunlun Natural Science Foundation of China (Grant Nos. 40432003, 40802010), Knowledge Innovation Program of the Chinese Academy of Sciences Mountain Range since the Pliocene. (Grant No. KZCX2-YW-Q09), CToL Project under the U.S. National Sci- ence Foundation to R. Mayden (Grant No. EF0431326), and the Ecocarp Project (European Commission, INCO-DEV Programme, Grant No. 3.3 Implications on uplift of East Kunlun Mountain ICA4-CT-2001-10024). According to Cao et al. [30], more than 80% of species of the genus Gymnocypris inhabit the water systems at the 1 Wu X N, Wen X B, Li D F, et al. Geological map of Qinghai Prov- altitude between 3750 m to 4750 m. Whereas the habitat of ince. In: Ma L F, ed. Geological Atlas of China (in Chinese). Beijing: G. eckloni can reach the altitude of 4200 m asl, the habitat Geological Publishing House, 2002. 334–335 of G. przewalskii, the Qinghai Lake, is at a relatively low 2 Kidd S F M, Molnar P. Quaternary and active faulting observed on the 1985 academia Sinica-Royal Society geotraverse of Tibet. Phil altitude of 3200 m asl [15]. Since representatives of the ge- Trans R Soc Lond A, 1988, 327: 337–363 nus appeared abundantly in the area of the Kunlun Pass Ba- 3 Wu Y Q, Cui Z J, Liu G N, et al. Quaternary geomorphological evo- sin during the Pliocene, it is natural to assume that the alti- lution of the Kunlun Pass area and uplift of the Qinghai-Xizang (Ti- tude of the water system then in the Pass area was probably bet) Plateau. Geomorphology, 2001, 36: 203–216 4 Cui Z J, Wu Y Q, Liu G N. Discovery and character of the somewhere within the interval between 3200–4200 m asl. It Kunlun-Yellow River Movement. 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