First Middle Devonian galeaspid from the Haikou Formation in Yunnan Province

MENG Xin-Yuan Zhu Min,3 WANG Jun-Qing PAN Zhao-Hui,3 GAI Zhi-Kun,3*

(1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences Beijing 100044)

(2 University of Chinese Academy of Sciences Beijing 100049 * Corresponding author: gaizhikun@ivpp.ac.cn)

(3 CAS Center for Excellence in Life and Paleoenvironment Beijing 100044)

Abstract The Early Emsian Event (E’Em Event), the most significant bio-event for Chinese Devonian vertebrates, has significantly impacted on the diversity of galeaspids. The endemic Galeaspida almost became extinct after the Mid-Emsian Event (M’Em Event). Only few galeaspid taxa survived from these events, such as Clarorbis apponomedianus from the Eifelian of Guangxi,South China, and an indeterminate galeaspid from the Frasnian of Ningxia, Northwest China.Here, we report the first Middle Devonian galeaspid, Dongfangaspis sp., from the Haikou Formation in Wuding, Yunnan Province. The new material is more suggestive of the type species of Dongfangaspis, D. major, than Laxaspis and Polybranchiaspis in its suborbicular headshield with small inner cornual process, broad and nearly aequilate ventral rim, and about 45 pairs of branchial fossae. Dongfangaspis bears the largest number of branchial fossae ever recorded in galeaspids, which probably play an important role in Dongfangaspis surviving from the E’Em and M’Em events. The new finding represents the second Middle Devonian fossil record of galeaspids,and extends the chronological range of Dongfangaspis from the Pragian (Early Devonian) to the Eifelian (Middle Devonian).

Key words Wuding, Yunnan; Middle Devonian; Haikou Formation; galeaspid; E’Em Event

1 Introduction

The Galeaspida is a group of ‘ostracoderms’ (jawless stem-gnathostomes) that thrived during the Siluro-Devonian period (Tarlo, 1967; Zhu, 1992; Janvier, 1996; Zhu and Gai, 2006;Janvier et al., 2009; Gai et al., 2018). The endemic galeaspids underwent quick radiation in South China soon after the Silurian-Devonian Boundary (S/D) Event, but were replaced by the cosmopolitan forms after the Early Emsian Event (E’Em Event), and almost disappeared after the Mid-Emsian Event (M’Em Event) (Zhu, 2000). To our knowledge, only two galeaspid species survived to Middle-Late Devonian. One isClarorbis apponomedianusfrom the Eifelian of Guangxi, South China, which represents the first convincing record of the Middle Devonian galeaspids in China (Pan and Ji, 1993). The other is an indeterminate galeaspid from the Zhongning Formation in the Hongshiwan Section of Zhongwei, Ningxia, Northwest China (Pan et al., 1987), which is referred to as the Frasnian age (Jia et al., 2010). In Ningxia,the age of the Zhongning Formation ranges from late Frasnian to Famennian. The Late Devonian tetrapodSinostega(Zhu et al., 2002), tetrapod-like fishHongyu(Zhu et al., 2017),and the antiarchs includingRemigolepisandNingxialepis(Pan et al., 1987; Jia et al., 2010)were found from the uppermost part of the Zhongning Formation in the Shixiagou Section,Famennian in age. The Zhongning Formation in the Hongshiwan Section (about 100 km southwestern of the Shixiagou Section) is very thin and yields the youngest known galeaspid together withLepidophloeum rhombicum,Remigolepis zhongweiensis, andR. xiangshanensis.The fish-bearing strata roughly correspond to the lower part of the Zhongning Formation in the Shixiagou and Dadaigou Sections (Jia et al., 2010). Here we report a new specimen ofDongfangaspisfrom the Haikou Formation (Eifelian, Middle Devonian) in Wuding, Yunnan Province. The Early-Middle Devonian strata are well developed in Wuding (Liu, 1994; Wang and Zhu, 1995) and rich in fossil fishes including galeaspids (Liu, 1973), placoderms (Liu and Wang, 1981; Wang and Wang, 1983; Wang, 1992; Wang and Zhu, 1995; Zhu et al., 2016; Pan et al., 2017), and sarcopterygians (Fan, 1992). However, galeaspid fossils have not been found in the Middle Devonian strata in the region. The youngest galeaspid record in Yunnan Province isWumengshanaspis cuntianensisfrom the Soutoushan Formation (Emsian, Early Devonian)near the Cuntian village, Yiliang County, northeastern Yunnan (Wang and Lan, 1984). The new material ofDongfangaspisis not only the first Middle Devonian galeaspid record in Yunnan,but also the second one worldwide.

2 Geological setting

The specimen IVPP V 15926 was collected in the 1980s from the middle part of the Haikou Formation at a site between Longtan and Zhaojiazhuang villages near the county of Wuding, Yunnan Province (Fig. 1A). The Devonian strata, well developed and rich in fish fossils in Wuding County, comprise the Posongchong, Pojiao, Jiucheng, and Haikou formations in ascending chronological order (Fig. 1B). The first galeaspid fossil record in the region isHuananaspis(Liu, 1973) from the Lower Devonian Posongchong Formation, which overlies unconformitably the Lower Ordovician Hongshiya Formation (Fig. 1B). The new galeaspid material was collected from the yellow medium-thick bedded quartz sandstone of the middle part of the Haikou Formation, in which antiarchs and sarcopterygians are diverse and abundant, represented byDianolepis liuiandThursius wudingensis(Chang, 1965; Fan,1992; Ritchie et al., 1992). The vertebrate assemblage was also known from the lower part of the Qujing Formation in Qujing and Zhaotong (Chang, 1965; Pan and Wang, 1978; Fan, 1992;Ritchie et al., 1992). Therefore, it was named the Qujing Assemblage and aged as the late Eifelian (Zhao and Zhu, 2010).

Fig. 1 Maps of the fossil locality of Dongfangaspis sp. (A) and the fish-bearing lithological column (B)in Wuding, Yunnan Province, China

3 Material and methods

The new material ofDongfangaspissp. is an incomplete headshield (IVPP V 15926),which is permanently housed and accessible for examination in the collections of the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Chinese Academy of Sciences.The holotype ofDongfangaspis major(IVPP V 4421) housed in IVPP, and the holotype of‘Dongfangaspis qujingensis’ (GMC V1753) and the referred specimen ofLaxaspiscf.L.qujingensis(GMC V2072) housed in the Geological Museum of China (GMC) are reexamined and photographed for comparative study. The fossils were prepared mechanically using a vibro tool with a tungsten-carbide bit or a needle. All measurement data were obtained via a digital vernier caliper. In addition, the specimens were examined under the Olympus SZ61 zoom stereo microscope and photographed with a Canon EOS 5D Mark III camera. The pictures for the general morphology were conducted by the Canon macro photo lens EF 100 mm 1:2.8L,while the close-up of the ornamentation was acquired with the Canon macro photo lens MP-E 65 mm 1:2.8 1-5×.

4 Systematic paleontology

Type speciesDongfangaspis majorLiu, 1975 (Fig. 2A, B).

Diagnosis (emended) Large-sized polybranchiaspid fish; headshield sub-circular, about 230 mm in length, 250 mm in width, slightly wider than long; rostral margin round, blunt;inner cornual process leaf-shaped; ventral rim broad, nearly aequilate with a width of 20 mm;the inner margin of the ventral rim nearly parallel with the lateral margin of the headshield;median dorsal opening transversely elongated oval in shape, with a convex posterior margin;orbital opening round, dorsally positioned; pineal opening almost level with the posterior margin of the orbital openings; about 45 pairs of branchial fossae; eight pairs of lateral transverse canals with branched distal ends; ornamentation of the headshield composed of tinygranular tubercles.

RemarksDongfangaspisis a monospecific genus, which was erected by Liu (1975)based on the holotype ofDongfangaspis majorfrom the Guanshanpo Formation of the Pingyipu Group in Jiangyou, Sichuan (Fig. 2A). The holotype is the only specimen and incomplete, which results in the diagnosis ofDongfangaspisbeing not distinctive enough to separate it fromLaxaspisandPolybranchiaspis. For example, three species,D. paradoxus,D.yunnanensis(Fang et al., 1985), and ‘D. qujingensis’ (Pan and Wang, 1981; Pan, 1992) were once referred toDongfangaspis. However,D. paradoxusandD. yunnanensis(Fang et al.,1985) from the Xishancun Formation in Qujing, Yunnan, were later recognized as the junior synonyms ofPolybranchiaspisliaojiaoshanensis, whereas ‘D. qujingensis’ is more suggestive ofLaxaspisqujingensisthanD. major(Zhu and Gai, 2006). Another specimen GMC V2072,which was initially classified as ‘D. qujingensis’, differs from the holotype of ‘D. qujingensis’on the broader headshield and round, blunt rostral margin. Therefore, it probably represents a new species ofLaxaspisand was temporarily denominated asLaxaspiscf.L. qujingensis(Zhu et al., 2015).

Material An incomplete headshield, IVPP V 15926.

Locality and horizon A site between Longtan and Zhaojiazhuang villages in Wuding County, Yunnan; Haikou Formation, Eifelian, Middle Devonian.

Diagnosis Large-sized polybranchiaspid fish; broad and nearly aequilate ventral rim with a width of 35-37 mm; more than 37, and estimated 45 pairs of branchial fossae; at least three lateral transverse canals; ornamentation of the headshield composed of tiny-granular tubercles.

Remarks The new material from the Haikou Formation in Wuding County is more suggestive ofD. majorthanLaxaspisandPolybranchiaspisin its small inner cornual process,broad and nearly aequilate ventral rim, and about 45 pairs of branchial fossae. However, the lack of data on the median dorsal opening precludes erecting a new species for the new specimen.Fig. 3 Photographs, interpretive drawing and restoration ofDongfangaspissp. from Wuding, Yunnan

Fig. 2 Photographs and restoration of Dongfangaspis and Laxaspis A. the holotype IVPP V 4421 of the type species of Dongfangaspis, D. major Liu, 1975 from the Guanshanpo Formation, Pingyipu Group, Yanmenba, Jiangyou, Sichuan, in dorsal view; B. restoration of D. major;C. ‘Dongfangaspis qujingensis’ from the Xishancun Formation, Qujing, Yunnan Province, Early Devonian(early Lochkovian), GMC V1753, in ventral view; D. GMC V2072 from the upper part of the Xishancun Formation, Qujing, Yunnan Province was referred to ‘Dongfangaspis qujingensis’,but was recognized as Laxaspis cf. L. qujingensis

A. an incomplete headshield, holotype, IVPP V 15926, in ventral view;B. interpretive drawing (right half) and restoration (left half), in dorsal view;C. close-up of granular tubercles on the headshield (box region 1 of Fig. 3A);D. close-up of granular tubercles on the ventral ring (box region 2 of Fig. 3A);

E. close-up of the branchial fossae (box region 3 of Fig. 3A)Abbreviations: br.f, branchial fossa; ebrd, impression of extrabranchial division of the branchial fossa;ib.r, interbranchial ridge; ltc, lateral transverse canal; mar.v, marginal vein; md.o, median dorsal opening;obr.f, oralo-branchial fenestra; orb, orbital opening; va.p, plexus of subcutaneous vascular canals;

vr, ventral rim; vr.v, ventral rim vein

Description The new specimen V 15926 is an incomplete headshield, representing a large-sized polybranchiaspid fish. The preserved length of the headshield is 155 mm, and the maximum length is estimated to be 200 mm. The length of headshield in the holotype ofDongfangaspis majoris about 200 mm, while about 60 mm inPolybranchiaspis, and about 130 mm inLaxaspis(Zhu et al., 2015). Obviously, the length of the new headshield is close to that ofD. major. The dorsal part of the headshield can only be observed ventrally, showing a dorsally convex ‘dome’. A round impression with a diameter of 10 mm, preserved in the anterior part of the headshield, probably represents the orbital opening (orb, Fig. 3A, B),which is closer to the midline than the lateral margin of the headshield. Three sensory canals probably for the lateral transverse canal (ltc, Fig. 3A, B) are observed on the internal surface of the headshield. The ornamentation of the headshield exhibits numerous tiny, dense granular tubercles (Fig. 3C). There are about 8-10 tubercles per square millimetre.

Most of the left ventral rim of the headshield is preserved in the holotype. The headshield curves ventrally to form a flat ventral rim. The ventral rim is wide and elongate, with a preserved length of 155 mm. The ventral rim is nearly aequilate, with the maximum width of 37 mm in the middle part, and the minimum width of 35 mm in the posterior part. The lateral edge of the ventral rim is strengthened by a thickening dermal ring with a width of 5 mm,where the dorsal part of the headshield curves ventrally. The ornaments on the thickened ring are much larger than those on the dorsal part of the headshield, with about 4 tubercles per square millimetre (Fig. 3D).

The ventral rims embrace a large oralo-branchial fenestra (obr.f, Fig. 3A), under which a large oralo-branchial chamber exists. The oralo-branchial fenestra is probably covered by one or two dermal ventral plates, but not preserved in our specimen. Numerous branchial fossae can be observed along the lateral margin of the oralo-branchial fenestra. The branchial fossae, separated by thin interbranchial ridges (ib.r, Fig. 3E), are reduced to slender and parallel grooves. The width of branchial fossa is about 3.0 mm. There are about 37 branchial fossae observed along the lateral margin of the oralo-branchial fenestra in a length of 11.0 cm. The total length of the lateral margin of the oralo-branchial fenestra is about 13.5 cm with an average of one external branchial opening per 3.0 mm. As such, the total number of the branchial fossae may have been about 45 pairs as that ofDongfangaspis majorestimated by Janvier (2004). There exists a round, small pit at the distal extremity of each branchial fossa,which is interpreted as the extra-branchial division of the branchial fossa (ebrd, Fig. 3E) lying dorsally to each external branchial opening (Janvier, 2004).

An elongate canal probably for the marginal vein (mar.v, Fig. 3E) flanks the oralo-branchial fenestra. Along its course, the canal of the marginal vein projects a small canal extending laterally to the ventral rim, probably for the ventral rim vein (vr.v, Fig. 3E) (Gai et al., 2019). Each canal of the ventral rim vein ramifies into 3-5 branches at its distal extremity. Numerous rami from adjacent ventral rim veins intersect each other to form a rich network or plexus of subcutaneous vascular canals (va.p, Fig. 3E) at the boundary between the exo- and endo-skeletons.

5 Discussion and conclusion

Dongfangaspiscan be assigned to the Polybranchiaspidae (Zhu and Gai, 2006; Gai et al., 2018; Shan et al., 2020; Jiang et al., 2021; Meng and Gai, 2021), which was established by Liu (1965) and includesBannhuanaspis,Dongfangaspis,Polybranchiaspis,Laxaspis,andDamaspis. However, the diagnostic features ofDongfangaspisare not clear enough to distinguish it fromLaxaspisandPolybranchiaspisbecause of the poorly preserved specimen.The new specimen ofDongfangaspisis more suggestive ofD. majorthanLaxaspisandPolybranchiaspisin its subcircular headshild with small inner cornual process, broad and nearly aequilate ventral rim, and about 45 pairs of branchial fossae (Fig. 4A). By contrast,Laxaspis(Fig. 4B) andPolybranchiaspis(Fig. 4C) are oval with developed inner cornual process and median dorsal spine. The ventral rim ofLaxaspisis broad, but nonuniform in the width showing a pointed front end and a much wider rear end (Fig. 4B). The ventral rim ofPolybranchiaspis(Fig. 4C) is aequilate as that ofDongfangaspis, but much narrower than that ofDongfangaspis(Fig. 4A). Last but the most important,Dongfangaspisexhibits the largest number of branchial fossae, possibly up to 45 pairs, ever recorded in galeaspids. The branchial fossae inLaxaspis(Fig. 4B) andPolybrabchiaspis(Fig. 4C) are 18 and 12 pairs respectively.The Silurian galeaspids Dayongaspidae, Xiushuiaspidae, Hanyangaspidae, Eugaleaspiformes and the oldest polybranchiaspiformPlatylomaspishave the least branchial fossae (6-7 pairs),probably representing the most general condition (Janvier, 2004). The “polybranchic” (more than ten pairs of branchial fossae) condition began with the radiation of Polybranchiaspiformes in the lower Lochkovian Xishancun Formation in Qujing, Yunnan Province. However, the branchial fossae of the galeaspids during this stage are less than 20 pairs, e.g., 12 pairs inPolybranchiaspis, and 18 pairs inLaxaspis. In the Pragian of Early Devonian, the branchial fossae burst into more than 30 pairs in some taxa, such as 32 pairs inLopadaspis(Wang et al., 2001), 35 pairs inZhaotongaspis(Wang and Zhu, 1994), and 45 pairs inDongfangaspis(Janvier, 2004). This indicates that the number increase of branchial fossae in galeaspids is an evolutionary trend throughout the geological time and has occurred independently in different lineages. Janiver (2004) considered that galeaspids probably adopted a strategy to compensate for the flattening of their headsheild and branchial fossae by increasing the number of branchial fossae.

Fig. 4 The diagnostic differences of Dongfangaspis (A), Laxaspis (B), and Polybranchiaspis (C)A-C, left half part of the headshield, in dorsal view, not to scale

The Devonian global events were characterized by sea-level rise and fall, ocean anoxic/hypoxic events, and biological extinctions/turnovers (Walliser, 1996; Becker et al., 2012;Qie et al., 2018). The Early Emsian Event (E’Em Event) is characterized by a changeover from strong endemic fauna to cosmopolitan fauna in South China (Fig. 5) (Zhu, 2000). The Mid-Emsian Event (M’Em Event) refers to the Daleje Event connected with a transgression,which is named after the changes in lithology (from carbonates to shales) and fauna (most species of Mimosphinctidae vanished) near the base of the Daleje Formation in Bohemia(Walliser, 1996). Except for the faunal changes mentioned above, galeaspids can also be used to signify the Devonian events (Fig. 5). As one of the three major groups of Galeaspida, the oldest fossil record of Polybranchiaspiformes can be traced back to the early Telychian of Llandovery, Silurian (Gai et al., 2018). However, they did not undergo their radiation until the beginning of the Early Devonian, known as thePolybranchiaspis-Laxaspisassemblage(Assemblage I) (Zhu and Wang, 2000) or the Xishancun Assemblage (Zhao and Zhu, 2010)from the lower Lochkovian Xishancun Formation in Qujing, Yunnan Province. The galeaspids in the Xishancun Formation are characterised by the radiation of Polybranchiaspiformes,which consists of 11 polybranchiaspid species (Liu et al., 2018). However, the diversity of Polybranchiaspiformes suddenly declined by the Pragian of Early Devonian (Gai et al., 2018)(Fig. 5). Compared to the high diversity of Huananaspiformes, only two unusually largesized polybranchiaspiforms survived in Pragian in China. One isNanningaspiszengifrom the Nakhaoling Formation of Guangxi (Gai et al., 2018), the other isDongfangaspis majorfrom the Guanshanpo Formation of Sichuan (Liu, 1975) (Fig. 5). After the middle Emsian of Early Devonian, the near-shore, shallow-water environment with muddy substratum and rich terrigenous clastics disappeared in South China (Qie et al., 2019). The endemic galeaspids almost became extinct after the Mid-Emsian event, i.e., Huananaspiformes and Eugaleaspiformes had gradually declined and onlyWumengshanaspis cuntianensissurvived into the late Emsian (Zhu, 2000) (Fig. 5). By the Eifelian of Middle Devonian, only few taxa of Polybranchiaspiformes can be found in China, such asClarorbis apponomedianusfrom the Eifelian of Guangxi, South China (Pan and Ji, 1993) and an indeterminate galeaspid from the Frasnian of Ningxia, Northwest China (Pan et al., 1987) (Fig. 5). The discovery of the first Middle Devonian galeaspid from the Haikou Formation in Wuding, Yunnan Province reveals thatDongfangaspisalso survived from the E’Em and M’Em events, which extends its chronological range from the Pragian of Early Devonian to the Eifelian of Middle Devonian.These latest occurrences of Polybranchiaspiformes are distributed from the Middle Devonian of Yunnan and Guangxi in South China to the Upper Devonian of Ningxia in Northwest China.However, when and how did they start to migrate from the South China Block to the North China Block remains unknown and should be further explored in the future.

Fig. 5 Diversity at genus level and phylogenetic tree of galeaspids projected against stratigraphy in the Silurian-Devonian of China Abbreviations: Go. Gorstian; Ho. Homerian; Sh. Sheinwoodian; Lu. Ludfordian

AcknowledgementsWe are grateful to Zhao Ridong, Yi Chunjuan, Lin Xianghong, and Li Qiang for their fieldwork, Guo Xiaocong, Yang Dinghua for the illustrations, Zhao Wenjin and Zhu Youan for the reviewing. This work was supported by Strategic Priority Research Program of CAS (XDB26000000), National Natural Science Foundation of China (41972006,42072026, 42130209), Key Research Program of Frontier Sciences, CAS (QYZDB-SSWDQC040), National Program for Support of Topnotch Young Professionals (W02070206).

云南中泥盆統(tǒng)海口組盔甲魚類的首次發(fā)現(xiàn)

孟馨媛1,2朱 敏1,2,3王俊卿1潘照暉1,3蓋志琨1,2,3

(1 中國(guó)科學(xué)院古脊椎動(dòng)物與古人類研究所，中國(guó)科學(xué)院脊椎動(dòng)物演化與人類起源重點(diǎn)實(shí)驗(yàn)室 北京 100044)
(2 中國(guó)科學(xué)院大學(xué) 北京 100049)
(3 中國(guó)科學(xué)院生物演化與環(huán)境卓越創(chuàng)新中心 北京 100044)

摘要：早埃姆斯期生物事件是中國(guó)泥盆紀(jì)脊椎動(dòng)物演化過(guò)程中最重要的生物事件，對(duì)盔甲魚類的生物多樣性產(chǎn)生了重大影響。在埃姆斯期之后，具有濃厚區(qū)域性色彩的盔甲魚類幾乎滅絕，只有少數(shù)屬種遺存，如發(fā)現(xiàn)于華南廣西中泥盆統(tǒng)艾菲爾階的近中顯眶魚(Clarorbis apponomedianus)以及西北寧夏上泥盆統(tǒng)弗拉階的一個(gè)多鰓魚類未定種。首次報(bào)道了產(chǎn)自云南省武定縣?？诮M的第一個(gè)中泥盆世盔甲魚——東方魚未定種(Dongfangaspissp.)。與寬甲魚(Laxaspis)和多鰓魚(Polybranchiaspis)相比，這件新標(biāo)本呈現(xiàn)出明顯的東方魚屬的特征：近圓形的頭甲，內(nèi)角小，腹環(huán)寬且近乎等寬，約有45對(duì)鰓囊。東方魚具有有史以來(lái)數(shù)目最多的鰓囊，這可能幫助它們?cè)谠?、中埃姆斯期生物事件中幸存下?lái)。這一新發(fā)現(xiàn)也是第二個(gè)中泥盆世盔甲魚類化石記錄，并將東方魚屬的生存時(shí)代從早泥盆世布拉格期擴(kuò)展到了中泥盆世艾菲爾期。

關(guān)鍵詞：云南武定，中泥盆世，海口組，盔甲魚類，早埃姆斯期生物事件

中圖法分類號(hào)：Q915.861文獻(xiàn)標(biāo)識(shí)碼：A文章編號(hào)：2096-9899(2022)03-0184-13