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Possible courtship behaviour of Devonian fish: Evidence from large radial trace fossils in northwestern China
Accepted Manuscript Possible courtship behaviour of Devonian fish: Evidence from large radial trace fossils in northwestern China
Ruiwen Zong, Yiming Gong PII: DOI: Reference:
S0031-0182(18)30301-8 doi:10.1016/j.palaeo.2018.05.042 PALAEO 8798
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
31 March 2018 30 May 2018 30 May 2018
Please cite this article as: Ruiwen Zong, Yiming Gong , Possible courtship behaviour of Devonian fish: Evidence from large radial trace fossils in northwestern China. Palaeo (2018), doi:10.1016/j.palaeo.2018.05.042
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ACCEPTED MANUSCRIPT Possible courtship behaviour of Devonian fish: evidence from large radial trace fossils in northwestern China Ruiwen Zong1, 2，Yiming Gong1* 1. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan
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430074, China
2. Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences, Nanjing Institute of Geology and Palaeontology, Nanjing, 210008, China
Corresponding author: [email protected]
ABSTRACT One kind of mysterious underwater circle observed on the seafloor near southern Amami-Oshima
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Island in subtropical Japan has attracted widespread attention, but its origin has long been unknown. In recent years, based on successive underwater photography, they were shown to represent the patterned structures
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constructed by male pufferfishes. Here we present a large radial trace fossil from the Upper Devonian Hongguleleng Formation in western Junggar, Xinjiang, Northwest China. They are circular or near-circular patterned structures consisting of numerous radial grooves and ridges. Based on morphological analysis of these
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trace fossils and comparison with the modern patterned structures made by pufferfish for courtship, we suggest that this trace fossil may be patterned structures made by male fish in the Devonian to attract females. If true, these
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structures would be the first reported example of courtship behaviour in the trace fossils of fish, and suggest that animal courtship behaviour has existed for at least 360 million years. These trace fossils provide new material for
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research on the breeding strategies and sexual selection of Devonian animals, and new insight on the origin and evolution of courtship behaviour.
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Keywords: Ethology; Mating; Breeding strategy; Late Devonian; Hongguleleng Formation
1. Introduction
Courtship behaviour is very common in living animals. Typically, to attract a mate, the male will show the female its more developed or colourful body organs or structures, or will perform some complex actions (West, 2009). Among these behaviours, the former type is easier to identify, and evidence of it has even found for ancient animals (cf. Wang et al., 2013; Zheng et al., 2017). However, although complex actions for courtship, as animal behavioural processes, may be
ACCEPTED MANUSCRIPT identified through continuous observation of living animals, it is very difficult to identify such behaviours in the fossil record. Because animal behaviour cannot be directly observed from fossil specimens like their body structures can be, most such behaviours are speculative based on “frozen behaviours” in the body fossil record, morphological analysis of animals, or trace fossils preserved in the strata (Boucot, 1990).
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Trace fossils, as records of the life activities of ancient animals, are chronicles of behavioural processes (Seilacher, 2007). Unfortunately, trace makers are seldom preserved with their trace fossils, and the identities of the trace makers for many trace fossils are therefore unclear. Moreover, many trace fossils lack comparable cases among living animals; thus, we have a very limited understanding of the behaviours of extinct animals. Here, we reported some large radial
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circular patterned structures from the Upper Devonian marine strata of Xinjiang, Northwest China, analysed their morphology, and compared them with similar patterned structures exhibited
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by an extant animal, which has specific behavioural purpose. We propose that these patterned structures were made by Devonian male fish to attract the mates, and thus represent an example of
2. Materials and methods
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courtship behaviour in the fossil record.
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The specimens in this paper were obtained from the Upper Devonian Hongguleleng
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Formation in the Yangzhuang section, 5 km northwest of Baiyang town, western Junggar, Xinjiang (Fig. 1A, B). The Hongguleleng Formation is widely distributed in the northern part of
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western Junggar, and is well exposed in the Wulankeshun and Bulongguoer sections (Fan and Gong, 2016; Wang et al., 2016). It can be divided into three members, as follows from the bottom to top: the lower member is composed of thin layers of bioclastic limestones, shelly limestones, argillaceous limestones, calcareous siltstones, and shales; the middle member consists of greygreen and grey-purple pyroclastic rocks and several beds of sandy limestones; the upper member comprises grey-yellow calcareous clastic rocks with several bioclastic limestone interlayers (Hou et al., 1993). The age of this formation is primarily Famennian (Ma et al., 2017). The lower member yields large amount shelly and reefoid coral fossils, whereas the middle member yields abundant trace fossils, including Teichichnus, Rosselia, Rhizocorallium, and Zoophycos (Fan and
ACCEPTED MANUSCRIPT Gong, 2016), as well as ammonites and buried in situ exuviae of phacopids (Zong et al., 2015; Zong and Gong, 2017), which together indicate that this member was deposited in a relatively calm neritic environment. Large radial, circular patterned structure are preserved on the surfaces of tuffites from the middle–upper part of the middle member of the Hongguleleng Formation (Fig. 1C), which is overlain by fine argillaceous shales. The underlying strata yield a few ammonites, exuviae of trilobites, and dwelling traces of sea anemones. The middle member of the
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Hongguleleng Formation of the Yangzhuang section has similar lithological and biological features to those of the nearby Wulankeshun section, and these two sections can be compared with each other. The level of the radial circular patterned structure is equivalent to the 11th bed of the middle member of the Hongguleleng Formation in the Wulankeshun section, which formed in an
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offshore transition environment (Fan and Gong, 2016).
Based on the specific morphological structure of the specimens (i.e. pairs of radial grooves
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and ridges, transverse grooves connecting adjacent pairs of radial grooves, and the middle parts of grooves deeper and wider than both ends), they may represent a new type of trace fossil. However, because these fossils are preserved on the surfaces of hard tuffites with dense joints and fissures, it
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is difficult to obtain intact specimens to store type specimens, or to conduct more detailed indoor
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research; therefore, these trace fossils are not named in this paper. Measurement and photography
3. Results
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of all specimens were completed in the field.
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All of the described specimens are preserved in fine, hard tuffites of the middle member of the Hongguleleng Formation (Fig. 2A). There are four individual specimens, including two nearly complete specimens, and two that are only about three-fifths preserved; their specimen numbers are Y-H-1 (Fig. 2B), Y-H-2 (Fig. 2C), Y-H-3 (Fig. 2D), and Y-H-4 (Fig. 2E), respectively. The shape of the specimens is circular or near-circular, and they show a radial patterned structure in the interior of the circle. Apart from the diameters and the numbers of radial grooves of the four specimens, the other characteristics are fairly similar. The diameter of specimen Y-H-1 is about 1.2 m, and there are 33 radial grooves at the periphery of the specimen (Figs. 2B, 3A–B). Specimen Y-H-2 is well preserved, but there are only 25 radial grooves at the periphery, and the
ACCEPTED MANUSCRIPT diameter is 1.1 m. Specimen Y-H-3 has the largest diameter, up to 1.3 m, and there are only 23 radial grooves preserved at the periphery. The diameter of specimen Y-H-4 is 1.15 m, and only 24 radial grooves are preserved at the periphery. To summarise the above four specimens, these patterned structures preserved on the surfaces of beds have the following characteristics: circular or near-circular shape composed of a core and dozens of radial grooves and ridges, with a diameter from 1.1 to 1.3 m. The internal part of the core is sunken, with a slightly prominent ring
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around it. The radial grooves and ridges diverge in pairs outwards from the core, with 10 to 15 radial grooves near the core and two or more bifurcations outwards (Fig. 3B–C), reaching up to 25 to 40 radial grooves at the periphery. The radial grooves are narrower and shallower near the core compared with the outer part, but at the outermost edge, the ridges have similar narrowness and shallowness to the core, and some of the grooves are bent (Fig. 3D). The width of the radial
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grooves is less than those of the radial ridges; the deepest groove is 2.5 cm deep, whereas the shallowest is only 0.5 cm deep. There are no concentric ring in these patterned structures, but
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there are transverse grooves between some adjacent radial grooves (Fig. 3B–C). The middle parts of the radial ridges are 0.5 to 1 cm above the bedding surface of the tuffites, and gradually decline
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on both sides; the edges of ridges are evenly extend into the radial grooves, and the transverse section of the radial grooves and ridges shows asymmetric sinusoidal shapes (Fig. 3B, E). There is
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residual fine mud fillings still preserved in some grooves (Fig. 3D), and the composition of these
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fillings is identical to that of the overlying strata. Although all of these patterned structures are preserved on the exposed surfaces of tuffites,
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they were not caused by later weathering, based on their consistent morphology, smooth radial grooves, and the fillings found in some grooves. They differ from common inorganic sedimentary structure because of the regularity of the radial grooves and ridges, transverse grooves connecting adjacent pairs of radial grooves, and bending at the ends of some grooves. Moreover, the strata that contain these patterned structures formed in a relatively calm neritic environment where water energy was very weak; therefore, inorganic causes can also be excluded. The only reasonable explanation for these patterned structures is that they are related to biological processes, and are large trace fossils.
ACCEPTED MANUSCRIPT 4. Discussion Radial trace fossils have been found in Cambrian to Quaternary strata (Hӓntzschel, 1970). Some, like the specimens from Xinjiang described above, consist of a core and numerous radial ridges (grooves), but previously described specimens, such as Asterichnus, Gyrophyllites, Capodistria, Skolichnus, and Micatuba, are much smaller in size, and their ridges (or grooves,
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rays) generally are narrower and not bifurcated (Bandel, 1967; Chamberlain, 1971; Uchman, 1995, 1998, 2010). Glockerichnus has bifurcated ridges (Uchman, 1998), but lacks transverse grooves or ridges between radial grooves or ridges. Estrellichnus is larger than other radial trace fossils (Uchman and Wetzel, 2001); its diameter typically reaches half that of the specimens from Xinjiang, and even approaches the diameter of the latter, but it has narrower and straighter radial
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ridges without bifurcations, and thus differs from the latter. Moreover, most described radial trace fossils were preserved in flysch deposits, and are mainly regard as the feeding structures of
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animals (Uchman, 1998; Uchman and Wetzel, 2001). Phoebichnus, typified by Phoebichnus trochoides Bromley and Asgaard, 1972, occurred in the same shallow marine siliciclastic deposits
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with the specimens from Xinjiang, its diameter typically reaches even exceeds that of the latter (Bromley and Asgaard, 1972; Evans and Mcilroy, 2016). However, Phoebichnus displays less
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numerous radial grooves, and its grooves are not bifurcated; moreover it presents obvious backfill structures in the radial grooves, which are interpreted as the burrows of axiids crustaceans (Evans
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and Mcilroy, 2016). There are no apparent backfill structures in the transections of the Xinjiang trace fossils (Fig. 3E), transections of the radial grooves or ridges are parabolic in shape, and
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fillings in the grooves have the same composition as the overlying strata. In addition, these trace fossils formed in an infertile environment with very few organisms, and are dispersed and similar in size. The above evidence shows that these trace fossils were left on the surface sediments by organisms, but are unlikely to have been feeding or burrowing structures within the sediments. Based on the larger sizes, bifurcated radial ridges and grooves, developed transverse grooves, and bending at the ends of radial grooves, these specimens from Xinjiang represent a new kind of radial trace fossil. There were no body fossils near the radial trace fossils in western Junggar, which makes it
ACCEPTED MANUSCRIPT difficult to determine the identity of the trace maker. The middle member of the Hongguleleng Formation yields some invertebrate fossils, such as trilobites, ammonoids, and brachiopods (Zong et al., 2015, 2016; Zong and Gong, 2017); moreover, sea anemones and polychaetes may also coexist with above invertebrates based on trace fossils (Fan and Gong, 2016). Among these animals, brachiopods, sea anemones, and ammonoids are unlikely to make such radial trace fossils, because the first two are marine benthos and the latter is nektonic organism. There are sculptures or
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scratches on the surface of trace fossils which produced by trilobites (i.e. Cruziana, Rusophycus), therefore, trilobites can also be eliminated from the trace maker based on the smooth grooves and ridges of the radial trace fossils. Polychaetes will produce radial trace fossils during feeding or burrowing, such as mentioned above Skolichnus and Asterichnus, however, these feeding or burrowing structures are obviously different from the radial trace fossils from Xinjiang, so the
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polychaetes are not trace maker.
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On the seafloor near Amami-Oshima Island, Japan, a similar patterned structure has been reported, composed of a radial central zone and two concentric outer and inner zones (Fig. 4A, B). The central zone is composed of numerous radial grooves and ridges (Fig. 4C; Kawase et al.,
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2013). The large radial trace fossils from the middle member of the Hongguleleng Formation are
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very similar to the central zone of the patterned structures found offshore of Japan in size and shape; the diameter of the central zone of modern patterned structure is between 62 and 100 cm,
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and the number of pairs of grooves and ridges is from 24 to 32, whereas the diameters of the trace fossils from Xinjiang are between 110 and 130 cm, and the number of pairs of grooves and ridges
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is from 25 to 40. Both have a raised ring around the core of the patterned structure, and the radial grooves and ridges show two or more bifurcations outward from the core. Both kinds of grooves are smooth, although the width of radial grooves is larger in the modern patterned structures, with narrower radial ridges, whereas the opposite is observed for the specimens from Xinjiang (that is, the width of the radial grooves is less than the ridges), and obvious transverse grooves connect adjacent pairs of radial grooves. In addition, the two patterned structures formed in similar environments; the modern patterned structures were discovered on the seafloor at water depths from 10 to 30 m (Kawase et al., 2013), and the Devonian specimens were preserved in an offshore
ACCEPTED MANUSCRIPT transition environment at water depths from about 10 to 30 m (Fan and Gong, 2016). The modern seafloor patterned structures were made by the small male pufferfish Torquigener albomaculosus Matsuura 2015 (Fig. 4B-D, Matsuura, 2015; Kawase et al., 2013). The radial grooves are furrows made by fish’s pectoral fins, anal fins and caudal fins during swimming; the sediments in the grooves are pushed out and deposited on both sides to form the
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radial ridges. Based on the similarity of the radial trace fossils from Xinjiang with these patterned structures, we speculate that the trace maker of this trace fossil may also have been a fish. There are deeper and wider part in the middle of the radial grooves, which become shallower and narrower toward both ends in the trace fossils; this patterned structure is also consistent with the modern carved traces of the fins of some fish (Wang et al., 2003). Fish was prosperous in the
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Devonian, and the finned fish including cartilaginous, acanthochetes, sarcopterygians, and now the most common actinopterus, all already existed in that era (Zhu, 2007). Some fossil tooth of
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small sharks have been found in the Upper Devonian (Famennian) strata in the western Junggar (Xia, 1996; Wang et al., 2015). They show that fish existed in western Junggar in the Late Devonian, and thus may have been the trace makers. However, in contrast with the specimens
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from Japan, the radial grooves of the Xinjiang specimens are narrower and longer; therefore,
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compared with the living pufferfish Torquigener albomaculosus, the trace makers for these large radial trace fossils were also longer.
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Based on the continuous under-water observations, the male pufferfish Torquigener albomaculosus makes these patterned structures to attract a mate, and in the middle part—the so-
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called “nest”—to mate and lay eggs (Kawase et al., 2013). These trace fossils may represent analogous patterned structures made by the Devonian male fish on seafloor sediments to attract females (Fig. 5), and may similarly have been used as nests for spawning and mating; thus, they may be an early manifestation of courtship behaviour. Underwater video of modern pufferfish shows that after mating successfully, the male and female pufferfish will spawn and mate at the “nest” in the middle of the patterned structure; the central zone becomes cluttered and is gradually destroyed. The specimens in Xinjiang are well preserved, which suggests that these patterned structures may have been left after male courtship failure; that is to say, females were not attracted
ACCEPTED MANUSCRIPT to mate by the patterned structures drawn by the males, and these patterned structures were thus preserved to form trace fossils. Courtship behaviour is common in living animals, and males use their more developed organs, more attractive body colouration, or complex actions to attract the attention of females. However, evidence of such behaviour is much rarer for ancient animals, and has only been
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reported for a few Mesozoic and Cenozoic insects and tetrapods (cf. Wang et al., 2013; Wappler et al., 2015; Lockley et al., 2016; Zheng et al., 2017). Aside from the pufferfish from offshore of Japan, other living fish also create patterned structures in the sediments to attract mates and produce offspring (Gladstone, 1994). Among the living birds, some build “fake nests” to attract females (Powesland et al., 1992); a similar phenomenon even existed among Cretaceous theropod
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dinosaurs (Lockley et al., 2016). Although sexual organs of Devonian fish have been identified, as well as evidence of mating behaviour (Long et al., 2015), courtship behaviour has not previously
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been reported. We report these Late Devonian trace fossils from Xinjiang as the first case of fish courtship behaviour in the fossil record. They also record a mating process of ancient animals, and show that in the Devonian, some male animals used their wisdom and bodies to make complex
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5. Conclusions
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movements rather than relying on the advantages of body organs to attract females.
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Some circular or near-circular patterned structures from the Upper Devonian Hongguleleng Formation in Xinjiang, Northwest China, are presented. Based on morphological analysis of these
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patterned structures and comparison with the modern patterned structures made by pufferfish for courtship, these patterned structures are considered as large radial trace fossils and may be made by male fish in the Devonian to attract females. These structures would be the first reported example of courtship behaviour in the trace fossils of fish. They suggest that animal courtship behaviour has existed at least since the Late Devonian, and provide new insight on the origin and evolution of courtship behaviour, as well as new material for research on the breeding strategies and sexual selection of Devonian animals.
ACCEPTED MANUSCRIPT Acknowledgments We thank Alfred Uchman, one anonymous reviewer and Editor-in-Chief Thomas J. Algeo for the constructive comments on the manuscript. We would like to thank Zhen Shen,Chao Guo and Junyan Dong, all from China University of Geosciences (Wuhan) for their help in the field work. We are also very grateful to Ruoying Fan, who give helpful advices on the early version of the manuscript. This work was supported by the Natural Science Foundation of China (Nos. 41702006, 41290260, 41472001), the Open Foundation of Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences (Nanjing Institute of Geology and Palaeontology) (No. 2017KF05) and China Postdoctoral Science Foundation (No. 2017M620342).
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ACCEPTED MANUSCRIPT Figure 1 A–B. Location map of the large radial trace fossils in western Junggar; C. Stratigraphical column of the Upper Devonian Hongguleleng Formation in the Yangzhuang section
Figure 2 Large radial trace fossil of the courtship behaviour of fish from the Upper Devonian Hongguleleng Formation in western Junggar
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A. Outcrop of trace fossils where they are preserved on the surfaces of fine and hard tuffites of the Hongguleleng Formation; B–E. Field photographs of four examples of the large trace fossil, their specimen numbers are Y-H-1, Y-H-2, Y-H-3 and Y-H-4, respectively.
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Figure 3 Morphological characteristics of a Late Devonian large radial trace fossil (Y-H-1)
A. Morphology of specimen Y-H-1; B. Schematic diagram of specimen Y-H-1 and transverse section of the radial
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grooves; C. Left enlarged view of figure A, showing the branching pattern of the radial grooves; D. Morphology of
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the end of a radial groove and its interior argillaceous fillings; E. Cross section of a radial groove and ridge.
Figure 4 Underwater patterned structure created by Torquigener albomaculosus on the seafloor near Amami-
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Oshima Island, Japan
A. The complete structure of the underwater patterned structure; B. Plan view of underwater patterned structure
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and the trace-making pufferfish (white arrow); C. Local enlargement of the “nest” in the central part of the patterned structure and the pufferfish (white arrow); D. Pufferfish building the patterned structure (modified after
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Kawase et al., 2013).
Figure 5 Reconstruction of the trace fossils of courtship behaviour of Late Devonian fish in western Junggar A. The fish uses its body to make the “convex concave” core on the surface of the sediments; B. The fish digs radial grooves by constantly swinging its fins over the surface of the sediments; C. Transverse grooves are excavated between adjacent pairs of radial grooves during swimming; D. After courtship failure, the patterned structures on the surface of the sediment is preserved, covered by sediment and becomes a trace fossil.
ACCEPTED MANUSCRIPT Highlights:
Some large radial trace fossils were presented from the Upper Devonian in NW China. These trace fossils may be patterned structures made by male fish to attract females. First reported example of courtship behaviour in the trace fossils of fish.
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Animal courtship behaviour has been existed at least since the Late Devonian.
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Ruiwen Zong, Yiming Gong PII: DOI: Reference:
S0031-0182(18)30301-8 doi:10.1016/j.palaeo.2018.05.042 PALAEO 8798
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
31 March 2018 30 May 2018 30 May 2018
Please cite this article as: Ruiwen Zong, Yiming Gong , Possible courtship behaviour of Devonian fish: Evidence from large radial trace fossils in northwestern China. Palaeo (2018), doi:10.1016/j.palaeo.2018.05.042
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ACCEPTED MANUSCRIPT Possible courtship behaviour of Devonian fish: evidence from large radial trace fossils in northwestern China Ruiwen Zong1, 2，Yiming Gong1* 1. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan
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430074, China
2. Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences, Nanjing Institute of Geology and Palaeontology, Nanjing, 210008, China
Corresponding author: [email protected]
ABSTRACT One kind of mysterious underwater circle observed on the seafloor near southern Amami-Oshima
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Island in subtropical Japan has attracted widespread attention, but its origin has long been unknown. In recent years, based on successive underwater photography, they were shown to represent the patterned structures
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constructed by male pufferfishes. Here we present a large radial trace fossil from the Upper Devonian Hongguleleng Formation in western Junggar, Xinjiang, Northwest China. They are circular or near-circular patterned structures consisting of numerous radial grooves and ridges. Based on morphological analysis of these
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trace fossils and comparison with the modern patterned structures made by pufferfish for courtship, we suggest that this trace fossil may be patterned structures made by male fish in the Devonian to attract females. If true, these
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structures would be the first reported example of courtship behaviour in the trace fossils of fish, and suggest that animal courtship behaviour has existed for at least 360 million years. These trace fossils provide new material for
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research on the breeding strategies and sexual selection of Devonian animals, and new insight on the origin and evolution of courtship behaviour.
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Keywords: Ethology; Mating; Breeding strategy; Late Devonian; Hongguleleng Formation
1. Introduction
Courtship behaviour is very common in living animals. Typically, to attract a mate, the male will show the female its more developed or colourful body organs or structures, or will perform some complex actions (West, 2009). Among these behaviours, the former type is easier to identify, and evidence of it has even found for ancient animals (cf. Wang et al., 2013; Zheng et al., 2017). However, although complex actions for courtship, as animal behavioural processes, may be
ACCEPTED MANUSCRIPT identified through continuous observation of living animals, it is very difficult to identify such behaviours in the fossil record. Because animal behaviour cannot be directly observed from fossil specimens like their body structures can be, most such behaviours are speculative based on “frozen behaviours” in the body fossil record, morphological analysis of animals, or trace fossils preserved in the strata (Boucot, 1990).
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Trace fossils, as records of the life activities of ancient animals, are chronicles of behavioural processes (Seilacher, 2007). Unfortunately, trace makers are seldom preserved with their trace fossils, and the identities of the trace makers for many trace fossils are therefore unclear. Moreover, many trace fossils lack comparable cases among living animals; thus, we have a very limited understanding of the behaviours of extinct animals. Here, we reported some large radial
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circular patterned structures from the Upper Devonian marine strata of Xinjiang, Northwest China, analysed their morphology, and compared them with similar patterned structures exhibited
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by an extant animal, which has specific behavioural purpose. We propose that these patterned structures were made by Devonian male fish to attract the mates, and thus represent an example of
2. Materials and methods
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courtship behaviour in the fossil record.
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The specimens in this paper were obtained from the Upper Devonian Hongguleleng
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Formation in the Yangzhuang section, 5 km northwest of Baiyang town, western Junggar, Xinjiang (Fig. 1A, B). The Hongguleleng Formation is widely distributed in the northern part of
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western Junggar, and is well exposed in the Wulankeshun and Bulongguoer sections (Fan and Gong, 2016; Wang et al., 2016). It can be divided into three members, as follows from the bottom to top: the lower member is composed of thin layers of bioclastic limestones, shelly limestones, argillaceous limestones, calcareous siltstones, and shales; the middle member consists of greygreen and grey-purple pyroclastic rocks and several beds of sandy limestones; the upper member comprises grey-yellow calcareous clastic rocks with several bioclastic limestone interlayers (Hou et al., 1993). The age of this formation is primarily Famennian (Ma et al., 2017). The lower member yields large amount shelly and reefoid coral fossils, whereas the middle member yields abundant trace fossils, including Teichichnus, Rosselia, Rhizocorallium, and Zoophycos (Fan and
ACCEPTED MANUSCRIPT Gong, 2016), as well as ammonites and buried in situ exuviae of phacopids (Zong et al., 2015; Zong and Gong, 2017), which together indicate that this member was deposited in a relatively calm neritic environment. Large radial, circular patterned structure are preserved on the surfaces of tuffites from the middle–upper part of the middle member of the Hongguleleng Formation (Fig. 1C), which is overlain by fine argillaceous shales. The underlying strata yield a few ammonites, exuviae of trilobites, and dwelling traces of sea anemones. The middle member of the
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Hongguleleng Formation of the Yangzhuang section has similar lithological and biological features to those of the nearby Wulankeshun section, and these two sections can be compared with each other. The level of the radial circular patterned structure is equivalent to the 11th bed of the middle member of the Hongguleleng Formation in the Wulankeshun section, which formed in an
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offshore transition environment (Fan and Gong, 2016).
Based on the specific morphological structure of the specimens (i.e. pairs of radial grooves
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and ridges, transverse grooves connecting adjacent pairs of radial grooves, and the middle parts of grooves deeper and wider than both ends), they may represent a new type of trace fossil. However, because these fossils are preserved on the surfaces of hard tuffites with dense joints and fissures, it
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is difficult to obtain intact specimens to store type specimens, or to conduct more detailed indoor
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research; therefore, these trace fossils are not named in this paper. Measurement and photography
3. Results
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of all specimens were completed in the field.
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All of the described specimens are preserved in fine, hard tuffites of the middle member of the Hongguleleng Formation (Fig. 2A). There are four individual specimens, including two nearly complete specimens, and two that are only about three-fifths preserved; their specimen numbers are Y-H-1 (Fig. 2B), Y-H-2 (Fig. 2C), Y-H-3 (Fig. 2D), and Y-H-4 (Fig. 2E), respectively. The shape of the specimens is circular or near-circular, and they show a radial patterned structure in the interior of the circle. Apart from the diameters and the numbers of radial grooves of the four specimens, the other characteristics are fairly similar. The diameter of specimen Y-H-1 is about 1.2 m, and there are 33 radial grooves at the periphery of the specimen (Figs. 2B, 3A–B). Specimen Y-H-2 is well preserved, but there are only 25 radial grooves at the periphery, and the
ACCEPTED MANUSCRIPT diameter is 1.1 m. Specimen Y-H-3 has the largest diameter, up to 1.3 m, and there are only 23 radial grooves preserved at the periphery. The diameter of specimen Y-H-4 is 1.15 m, and only 24 radial grooves are preserved at the periphery. To summarise the above four specimens, these patterned structures preserved on the surfaces of beds have the following characteristics: circular or near-circular shape composed of a core and dozens of radial grooves and ridges, with a diameter from 1.1 to 1.3 m. The internal part of the core is sunken, with a slightly prominent ring
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around it. The radial grooves and ridges diverge in pairs outwards from the core, with 10 to 15 radial grooves near the core and two or more bifurcations outwards (Fig. 3B–C), reaching up to 25 to 40 radial grooves at the periphery. The radial grooves are narrower and shallower near the core compared with the outer part, but at the outermost edge, the ridges have similar narrowness and shallowness to the core, and some of the grooves are bent (Fig. 3D). The width of the radial
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grooves is less than those of the radial ridges; the deepest groove is 2.5 cm deep, whereas the shallowest is only 0.5 cm deep. There are no concentric ring in these patterned structures, but
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there are transverse grooves between some adjacent radial grooves (Fig. 3B–C). The middle parts of the radial ridges are 0.5 to 1 cm above the bedding surface of the tuffites, and gradually decline
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on both sides; the edges of ridges are evenly extend into the radial grooves, and the transverse section of the radial grooves and ridges shows asymmetric sinusoidal shapes (Fig. 3B, E). There is
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residual fine mud fillings still preserved in some grooves (Fig. 3D), and the composition of these
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fillings is identical to that of the overlying strata. Although all of these patterned structures are preserved on the exposed surfaces of tuffites,
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they were not caused by later weathering, based on their consistent morphology, smooth radial grooves, and the fillings found in some grooves. They differ from common inorganic sedimentary structure because of the regularity of the radial grooves and ridges, transverse grooves connecting adjacent pairs of radial grooves, and bending at the ends of some grooves. Moreover, the strata that contain these patterned structures formed in a relatively calm neritic environment where water energy was very weak; therefore, inorganic causes can also be excluded. The only reasonable explanation for these patterned structures is that they are related to biological processes, and are large trace fossils.
ACCEPTED MANUSCRIPT 4. Discussion Radial trace fossils have been found in Cambrian to Quaternary strata (Hӓntzschel, 1970). Some, like the specimens from Xinjiang described above, consist of a core and numerous radial ridges (grooves), but previously described specimens, such as Asterichnus, Gyrophyllites, Capodistria, Skolichnus, and Micatuba, are much smaller in size, and their ridges (or grooves,
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rays) generally are narrower and not bifurcated (Bandel, 1967; Chamberlain, 1971; Uchman, 1995, 1998, 2010). Glockerichnus has bifurcated ridges (Uchman, 1998), but lacks transverse grooves or ridges between radial grooves or ridges. Estrellichnus is larger than other radial trace fossils (Uchman and Wetzel, 2001); its diameter typically reaches half that of the specimens from Xinjiang, and even approaches the diameter of the latter, but it has narrower and straighter radial
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ridges without bifurcations, and thus differs from the latter. Moreover, most described radial trace fossils were preserved in flysch deposits, and are mainly regard as the feeding structures of
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animals (Uchman, 1998; Uchman and Wetzel, 2001). Phoebichnus, typified by Phoebichnus trochoides Bromley and Asgaard, 1972, occurred in the same shallow marine siliciclastic deposits
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with the specimens from Xinjiang, its diameter typically reaches even exceeds that of the latter (Bromley and Asgaard, 1972; Evans and Mcilroy, 2016). However, Phoebichnus displays less
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numerous radial grooves, and its grooves are not bifurcated; moreover it presents obvious backfill structures in the radial grooves, which are interpreted as the burrows of axiids crustaceans (Evans
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and Mcilroy, 2016). There are no apparent backfill structures in the transections of the Xinjiang trace fossils (Fig. 3E), transections of the radial grooves or ridges are parabolic in shape, and
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fillings in the grooves have the same composition as the overlying strata. In addition, these trace fossils formed in an infertile environment with very few organisms, and are dispersed and similar in size. The above evidence shows that these trace fossils were left on the surface sediments by organisms, but are unlikely to have been feeding or burrowing structures within the sediments. Based on the larger sizes, bifurcated radial ridges and grooves, developed transverse grooves, and bending at the ends of radial grooves, these specimens from Xinjiang represent a new kind of radial trace fossil. There were no body fossils near the radial trace fossils in western Junggar, which makes it
ACCEPTED MANUSCRIPT difficult to determine the identity of the trace maker. The middle member of the Hongguleleng Formation yields some invertebrate fossils, such as trilobites, ammonoids, and brachiopods (Zong et al., 2015, 2016; Zong and Gong, 2017); moreover, sea anemones and polychaetes may also coexist with above invertebrates based on trace fossils (Fan and Gong, 2016). Among these animals, brachiopods, sea anemones, and ammonoids are unlikely to make such radial trace fossils, because the first two are marine benthos and the latter is nektonic organism. There are sculptures or
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scratches on the surface of trace fossils which produced by trilobites (i.e. Cruziana, Rusophycus), therefore, trilobites can also be eliminated from the trace maker based on the smooth grooves and ridges of the radial trace fossils. Polychaetes will produce radial trace fossils during feeding or burrowing, such as mentioned above Skolichnus and Asterichnus, however, these feeding or burrowing structures are obviously different from the radial trace fossils from Xinjiang, so the
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polychaetes are not trace maker.
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On the seafloor near Amami-Oshima Island, Japan, a similar patterned structure has been reported, composed of a radial central zone and two concentric outer and inner zones (Fig. 4A, B). The central zone is composed of numerous radial grooves and ridges (Fig. 4C; Kawase et al.,
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2013). The large radial trace fossils from the middle member of the Hongguleleng Formation are
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very similar to the central zone of the patterned structures found offshore of Japan in size and shape; the diameter of the central zone of modern patterned structure is between 62 and 100 cm,
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and the number of pairs of grooves and ridges is from 24 to 32, whereas the diameters of the trace fossils from Xinjiang are between 110 and 130 cm, and the number of pairs of grooves and ridges
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is from 25 to 40. Both have a raised ring around the core of the patterned structure, and the radial grooves and ridges show two or more bifurcations outward from the core. Both kinds of grooves are smooth, although the width of radial grooves is larger in the modern patterned structures, with narrower radial ridges, whereas the opposite is observed for the specimens from Xinjiang (that is, the width of the radial grooves is less than the ridges), and obvious transverse grooves connect adjacent pairs of radial grooves. In addition, the two patterned structures formed in similar environments; the modern patterned structures were discovered on the seafloor at water depths from 10 to 30 m (Kawase et al., 2013), and the Devonian specimens were preserved in an offshore
ACCEPTED MANUSCRIPT transition environment at water depths from about 10 to 30 m (Fan and Gong, 2016). The modern seafloor patterned structures were made by the small male pufferfish Torquigener albomaculosus Matsuura 2015 (Fig. 4B-D, Matsuura, 2015; Kawase et al., 2013). The radial grooves are furrows made by fish’s pectoral fins, anal fins and caudal fins during swimming; the sediments in the grooves are pushed out and deposited on both sides to form the
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radial ridges. Based on the similarity of the radial trace fossils from Xinjiang with these patterned structures, we speculate that the trace maker of this trace fossil may also have been a fish. There are deeper and wider part in the middle of the radial grooves, which become shallower and narrower toward both ends in the trace fossils; this patterned structure is also consistent with the modern carved traces of the fins of some fish (Wang et al., 2003). Fish was prosperous in the
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Devonian, and the finned fish including cartilaginous, acanthochetes, sarcopterygians, and now the most common actinopterus, all already existed in that era (Zhu, 2007). Some fossil tooth of
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small sharks have been found in the Upper Devonian (Famennian) strata in the western Junggar (Xia, 1996; Wang et al., 2015). They show that fish existed in western Junggar in the Late Devonian, and thus may have been the trace makers. However, in contrast with the specimens
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from Japan, the radial grooves of the Xinjiang specimens are narrower and longer; therefore,
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compared with the living pufferfish Torquigener albomaculosus, the trace makers for these large radial trace fossils were also longer.
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Based on the continuous under-water observations, the male pufferfish Torquigener albomaculosus makes these patterned structures to attract a mate, and in the middle part—the so-
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called “nest”—to mate and lay eggs (Kawase et al., 2013). These trace fossils may represent analogous patterned structures made by the Devonian male fish on seafloor sediments to attract females (Fig. 5), and may similarly have been used as nests for spawning and mating; thus, they may be an early manifestation of courtship behaviour. Underwater video of modern pufferfish shows that after mating successfully, the male and female pufferfish will spawn and mate at the “nest” in the middle of the patterned structure; the central zone becomes cluttered and is gradually destroyed. The specimens in Xinjiang are well preserved, which suggests that these patterned structures may have been left after male courtship failure; that is to say, females were not attracted
ACCEPTED MANUSCRIPT to mate by the patterned structures drawn by the males, and these patterned structures were thus preserved to form trace fossils. Courtship behaviour is common in living animals, and males use their more developed organs, more attractive body colouration, or complex actions to attract the attention of females. However, evidence of such behaviour is much rarer for ancient animals, and has only been
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reported for a few Mesozoic and Cenozoic insects and tetrapods (cf. Wang et al., 2013; Wappler et al., 2015; Lockley et al., 2016; Zheng et al., 2017). Aside from the pufferfish from offshore of Japan, other living fish also create patterned structures in the sediments to attract mates and produce offspring (Gladstone, 1994). Among the living birds, some build “fake nests” to attract females (Powesland et al., 1992); a similar phenomenon even existed among Cretaceous theropod
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dinosaurs (Lockley et al., 2016). Although sexual organs of Devonian fish have been identified, as well as evidence of mating behaviour (Long et al., 2015), courtship behaviour has not previously
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been reported. We report these Late Devonian trace fossils from Xinjiang as the first case of fish courtship behaviour in the fossil record. They also record a mating process of ancient animals, and show that in the Devonian, some male animals used their wisdom and bodies to make complex
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5. Conclusions
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movements rather than relying on the advantages of body organs to attract females.
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Some circular or near-circular patterned structures from the Upper Devonian Hongguleleng Formation in Xinjiang, Northwest China, are presented. Based on morphological analysis of these
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patterned structures and comparison with the modern patterned structures made by pufferfish for courtship, these patterned structures are considered as large radial trace fossils and may be made by male fish in the Devonian to attract females. These structures would be the first reported example of courtship behaviour in the trace fossils of fish. They suggest that animal courtship behaviour has existed at least since the Late Devonian, and provide new insight on the origin and evolution of courtship behaviour, as well as new material for research on the breeding strategies and sexual selection of Devonian animals.
ACCEPTED MANUSCRIPT Acknowledgments We thank Alfred Uchman, one anonymous reviewer and Editor-in-Chief Thomas J. Algeo for the constructive comments on the manuscript. We would like to thank Zhen Shen,Chao Guo and Junyan Dong, all from China University of Geosciences (Wuhan) for their help in the field work. We are also very grateful to Ruoying Fan, who give helpful advices on the early version of the manuscript. This work was supported by the Natural Science Foundation of China (Nos. 41702006, 41290260, 41472001), the Open Foundation of Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences (Nanjing Institute of Geology and Palaeontology) (No. 2017KF05) and China Postdoctoral Science Foundation (No. 2017M620342).
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ACCEPTED MANUSCRIPT Figure 1 A–B. Location map of the large radial trace fossils in western Junggar; C. Stratigraphical column of the Upper Devonian Hongguleleng Formation in the Yangzhuang section
Figure 2 Large radial trace fossil of the courtship behaviour of fish from the Upper Devonian Hongguleleng Formation in western Junggar
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A. Outcrop of trace fossils where they are preserved on the surfaces of fine and hard tuffites of the Hongguleleng Formation; B–E. Field photographs of four examples of the large trace fossil, their specimen numbers are Y-H-1, Y-H-2, Y-H-3 and Y-H-4, respectively.
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Figure 3 Morphological characteristics of a Late Devonian large radial trace fossil (Y-H-1)
A. Morphology of specimen Y-H-1; B. Schematic diagram of specimen Y-H-1 and transverse section of the radial
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grooves; C. Left enlarged view of figure A, showing the branching pattern of the radial grooves; D. Morphology of
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the end of a radial groove and its interior argillaceous fillings; E. Cross section of a radial groove and ridge.
Figure 4 Underwater patterned structure created by Torquigener albomaculosus on the seafloor near Amami-
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Oshima Island, Japan
A. The complete structure of the underwater patterned structure; B. Plan view of underwater patterned structure
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and the trace-making pufferfish (white arrow); C. Local enlargement of the “nest” in the central part of the patterned structure and the pufferfish (white arrow); D. Pufferfish building the patterned structure (modified after
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Kawase et al., 2013).
Figure 5 Reconstruction of the trace fossils of courtship behaviour of Late Devonian fish in western Junggar A. The fish uses its body to make the “convex concave” core on the surface of the sediments; B. The fish digs radial grooves by constantly swinging its fins over the surface of the sediments; C. Transverse grooves are excavated between adjacent pairs of radial grooves during swimming; D. After courtship failure, the patterned structures on the surface of the sediment is preserved, covered by sediment and becomes a trace fossil.
ACCEPTED MANUSCRIPT Highlights:
Some large radial trace fossils were presented from the Upper Devonian in NW China. These trace fossils may be patterned structures made by male fish to attract females. First reported example of courtship behaviour in the trace fossils of fish.
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Animal courtship behaviour has been existed at least since the Late Devonian.
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Figure 5