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Fish hunting trace Osculichnus and the oldest Sinusichnus sinuosus from the Upper Devonian of South China
Palaeogeography, Palaeoclimatology, Palaeoecology 530 (2019) 103–112
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Fish hunting trace Osculichnus and the oldest Sinusichnus sinuosus from the Upper Devonian of South China
T
Ruo-ying Fan, Rui-wen Zong, Yi-ming Gong
⁎
State Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences, Wuhan 430074, China
ARTICLE INFO
ABSTRACT
Keywords: Praedichnia Jawed fish Wutong Formation Late Devonian South China
Trace fossils are special objects in the study of predator–prey interactions in the fossil record. Here we report on diverse morphological types of the gnathostome fish hunting trace Osculichnus from the Upper Devonian of South China. The studied Osculichnus specimens occur as groups of bilobate mounds on the sole of fine- to mediumgrained quartz sandstones from the estuarine-embayment depositional system of the Upper Devonian Wutong Formation in Wuhan city. The fish feeding trace Osculichnus is closely associated with the highly regular, branched sinuous trace Sinusichnus sinuosus on the bedding plane. Previously, Sinusichnus sinuosus has been typically reported from Late Cretaceous to Miocene marginal-marine sediments, with two records in the Lower and Middle Triassic of South China, and is generally regarded as the burrows of decapod crustaceans. The discovery of Sinusichnus sinuosus in the Upper Devonian, though of relatively small diameter (0.4–4.3 mm) than its Mesozoic and Cenozoic counterparts, extends its stratigraphical distribution and is suggestive of some primitive, small-sized decapod crustacean producers. The Osculichnus makers possibly preyed upon the Sinusichnus makers or other small invertebrates in the sediments. The overall shape and morphological details of the Late Devonian Osculichnus suggest lungfish as candidate trace makers. The fish hunting traces and associated trace fossils from South China thus provide unique insights into the palaeoecology of Late Devonian fishes.
1. Introduction Fishes are important vertebrate trace makers in the fossil record. The earliest vertebrate trace fossil is a Late Silurian fish swimming trace (Knaust and Minter, 2018). Various fish traces in the sediments have been recognized; by far the most frequently reported and extensively studied are fish locomotion traces like Undichna Anderson, 1976 (see review in Minter and Braddy, 2006) and less commonly Parundichna Simon et al., 2003, both of which, from a functional point, resulted from jawed fishes. Predator–prey interactions may be as old as life itself, yet complex food webs were only established with the advent of the Cambrian explosion (Bengtson, 2002; Vannier et al., 2007; Dunne et al., 2008). Predator–prey interactions play a significant role in determining the distribution and diversity of organisms, and have long been hypothesized as a driving force of the macroevolution of related clades (Vermeij, 1977; Kelley et al., 2003; Huntley and Kowalewski, 2007; Baumiller et al., 2010; Sallan et al., 2011; Gorzelak et al., 2012). The fossil record of predation has focused on trace fossils like bite marks, drill holes or repair scars found on organic substrates (skeletons or shells of animals) (Jensen, 1990; Kowalewski et al., 1998; Kelley et al., ⁎
2003), or stomach contents and excretes (i.e., coprolites, gastroliths, and regurgitalites, bromalites sensu Hunt, 1992; Zhu et al., 2004; Vannier and Chen, 2005). There is less attention on predatory behaviours taking place in the sediments that could be potentially recorded as biogenic sedimentary structures (e.g., trapping traces or irretichnia, proposed by Lehane and Ekdale, 2013). The Devonian is known as “the age of fishes” with pronounced radiation of jaw-bearing fish (Janvier, 1996). Fish predation in the fossil record has been recognized through bite marks, such as crinoids preyed upon by durophagous fishes (Gorzelak et al., 2011), but there is also evidence of fish predation recorded by interaction with sediments. For instance, Piscichnus Feibel, 1987, representing ray feeding depressions on the sediment floor, has been common since the Cretaceous (Gregory et al., 1979; Gregory, 1991; Uchman et al., 2018). Probably the most interesting evidence of the feeding and hunting behaviour of gnathostomes lies in the recently reported Osculichnus Demírcan and Uchman, 2010 (meaning “kissing” traces), which is commonly preserved as surface pits or hypichnial mounds of sandstone beds. They represent the bottom-feeding activities of gnathostomes preying on small endobenthic animals (Szrek et al., 2016). In this paper, we report on diverse morphological types of the fish hunting trace Osculichnus and associated Sinusichnus sinuosus from
Corresponding author. E-mail address: [email protected] (Y.-m. Gong).
https://doi.org/10.1016/j.palaeo.2019.05.045 Received 17 April 2019; Received in revised form 31 May 2019; Accepted 31 May 2019 Available online 04 June 2019 0031-0182/ © 2019 Elsevier B.V. All rights reserved.
Palaeogeography, Palaeoclimatology, Palaeoecology 530 (2019) 103–112
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Fig. 1. Location and geological map of the study area. A. Map of China, showing the general locality of the study area (magnified in B). B. The study area is located in Wuhan, the capital city of Hubei Province, at the confluence of the Yangtze and Hanjiang rivers. C. Simplified geological map of the study area (boxed area in B), the fish hunting trace Osculichnus was found in Huangjintang (HJT) and Guodingshan hill (GDS).
the Late Devonian marginal-marine environment of South China, with a discussion of the behaviour, ecology and possible identity of its gnathostome producers.
climates. The sandstones in the lower part of the Wutong Formation show several large-scale fining upward sequences, with locally parallel bedding, large-scale wedge-shaped and herringbone cross-beddings, as well as asymmetric ripple marks (see also Peng and Du, 2002); it yields the Frasnian plants Leptophloem rhombicum Dawson, Protopteriodophyton devonicum Li et Hsu, Chamaedendron multisporangiatum Schweitzer et Li, Sphinxiocarpon wuhanium (Li, Hilton et Hemsley) and diverse spores (Li, 2000; Xu et al., 2012), as well as the scorpion Hubeiscopio graciltarus Walossek, Li et Brauckmann (Walossek et al., 1990). The Wutong Formation grades in the upper part to brownish grey or purplish thin- to medium-bedded fine- to medium-grained micaceous quartz sandstones (locally laminated) intercalated by thin-bedded muddy siltstones (Fig. 2). The upper part of the Wutong Formation yields abundant plant fossils and spores of the Late Devonian Famennian age: Leptophloeum rhombicum Dawson, Cyclostigma kiltorkense Haughton, Sublepidodendron wusihense (Sze), Sphenophyllum sp. (Li, 2000). The high content of mica flakes indicates deposition in an environment less winnowed by waves and longshore currents. The poorly developed marine fauna suggests that the Wutong Formation was probably deposited under stressed conditions influenced by significant salinity fluctuations. Overall, the Wutong Formation represents deposition in an oxygenated shallow water depth during the Late Devonian transgressional period, very likely belonging to the estuarine-embayment depositional system or associated marginal- to shallow-marine facies (barrier-island systems, upper shoreface, foreshore, tidal flat). The Wutong Formation is overlain by the Early Carboniferous Gaolishan Formation by a paraconformity in the study area. The Gaolishan Formation is composed primarily of greyish or mottled claystones, with intercalations of lenticular quartz sandstones, coal measures, and siderite nodules, which probably belongs to the lagoon–tidal-flat–marsh environment in the
2. Geological setting and stratigraphy The fossil material was found in the upper part of the Upper Devonian Wutong Formation from Wuhan city of Hubei Province, China. In the study area, the Wutong Formation crops out as E-W trending ribbons (Fig. 1). The Wutong Formation separates from the underlying Llandovery Fentou Formation by a paraconformity (Zong et al., 2017). The Llandovery Fentou Formation is made up of primarily mudstones, silty mudstones, and siltstones, which hosts abundant brachiopods, bivalves, gastropods, trilobites, fish, and trace fossils (Zong et al., 2011). Sandstone intercalations increase towards the upper part of the Fentou Formation, showing a coarsening upwards sequence. Large pyrite concretions (up to 1 cm) and well-pyritized body fossils have been found in this formation. Recently, well-preserved eurypterids, complete echinoderms, and sponges of the Burgess Shale-type were found in the Fentou Formation; they were attributed to the Fentou Biota, representing an early Silurian exceptionally preserved biota in the shallow-marine (deltaic, probably distal delta-front or prodelta) environment (Zong et al., 2017). The Wutong Formation is composed of grey-whitish to brownish thick- to very thick-bedded quartz sandstones interbedded with thin layers of muddy siltstones or claystones in the lower part, with commonly a basal lag of conglomerates (Fig. 2). There are densely distributed semi-spherical, poorly cemented sandy sediment packages (commonly weathered out as elliptical hollows) immediately above the paraconformity, which suggest effective fluvial input under humid
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Fig. 2. Outcrops and lithology of the Upper Devonian Wutong Formation in Huangjintang, Wuhan, China. A. Outcrop view of the Huangjintang section, showing the thin- to mediumbedded sandstone beds in the upper part of the section where fish hunting traces were found (people standing, see close shot in B, corresponding to bed no. 12 in C). B. The successive three sandstone soles (numbered) yielding the fish hunting traces. C. Lithological column of the Huangjintang section, showing the generally fining-upward sequences of the Wutong Formation (vf. – very fine-grained; m. – mediumgrained; c. – coarse-grained; vc. – very coarse-grained; cg. – conglomerate) (the stratigraphic column shows the stacking style of beds, but not to scale).
regressive phase. Trace fossil assemblages of the Wutong Formation can be attributed to a mixed, depauperate Skolithos–Cruziana ichnofacies, including dwelling traces Arenicolites, Bifungites, arthropod locomotion/feeding/ resting traces Cruziana, Rusophycus, Diplichnites, Monomorphichnus, bivalve locomotion trace Protovirgularia, bivalve resting trace Lockeia, and locomotion/feeding traces of worm-like animals Gordia, ?Chondrites, ?Cochlichnus,?Margaritichnus (revised from Yang et al., 1987; Zhang et al., 1987). Additional elements Osculichnus, Sinusichnus, Rhizocorallium, and ?Undichna were discovered during investigation of this study.
measured the Huangjintang section; the well exposed sandstone soles in the upper part of this section provide the opportunity to study the morphology, size, and orientation of Osculichnus in situ (Fig. 2). A total of three sandstone soles with Osculichnus were recognized in Huangjintang, among which the lowermost sole exposes the best preserved Osculichnus and Sinusichnus specimens of this locality; the other two sandstone soles were observed from a distance since they are high above the ground. One of the authors (R.W. Zong) came across the fossil site at the Guodingshan hill, and provided photograph and specimen materials. The rapid civil construction completely destroyed outcrops of the two localities and the two fossil sites are no longer accessible. Effort has been made in search of good outcrops nearby, however, extensive bedding surfaces were not easily encountered. Therefore, further investigation is hampered. Most of the fish hunting trace fossils were photographed in the field due to the difficulty in separating them from the bulky quartz sandstone bed. And unfortunately, we have not got the opportunity to cast the Osculichnus specimens. Two specimens were collected from the Guodingshan hill and Huangjintang locality (one for
3. Materials and methods The fish hunting traces were found on the soles of grey or brownish sandstones (10–30 cm thick) in two localities (Huangjintang, GPS coordinates: 30°30′49.25″N, 114°31′53.54″E; Guodingshan hill, GPS coordinates: 30°34′12.11″N, 114°10′37.56″E). We systematically 105
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(with an average of 44.0 mm, N = 16), maximum height 17.9–69.4 mm (with an average of 38.8 mm), flatness ratio 0.83–1.70 (mean = 1.17) (Table 1). On the same sandstone sole as well as in the thin siltstone intercalation (about 1 cm thick) immediately below the sandstone sole, abundant sinusoid burrows 2.4–4.3 mm in diameter are present as hypichnial grooves, some grading to hypichnial ridge preservation (Fig. 4C–E, G, H). The average amplitude of the sinusoids is 2.8–4.0 mm, average wavelength 20.5–34.0 mm. The wavelength/amplitude ratio (λ/A) is 6.2–8.7 (with an average of 7.5) (Table 2). The sinuous burrow winds in a straight or gently curved way in various directions, with a tendency of anastomosing to form networks (Fig. 4G, H). The sinusoidal tunnels and the branching style are typical of Sinusichnus sinuosus de Gibert (1996). The second Osculichnus-bearing layer is restricted in exposure and only 5 specimens were recognized. Two specimens exhibit a central elliptical lobe between the outer lobes rather than a linear furrow (measurement for these two specimens was not allowed because the specimens were high above the ground). A peculiar scene of this sandstone sole is that two bilobate specimens of nearly identical size (32.7 × 35.9 mm and 30.7 × 32.2 mm, respectively) are immediately juxtaposed with each other (Fig. 4F). No associated trace fossils were found at this level. The third fossil-bearing level (~1 m2) exposes only 6 obscure Osculichnus specimens with hardly recognizable morphological details. Groove marks can be observed on the sandstone sole that imply strong bottom currents at the time of deposition, which may explain the poor preservation of Osculichnus specimens at this level. 4.2. The Guodingshan hill locality A total of 11 Osculichnus specimens are observed on the sandstone soles in the Guodingshan hill locality. Osculichnus specimens are more well-preserved in this locality and commonly exhibit a distinct, trapezoid or elliptical central depression or convex lobe between the two outer lobes (Fig. 5A). The central lobe may even superimpose on one of the outer lobes locally (Fig. 5A). One collected specimen shows an exaggerated lower lobe, with an irregular central cavity between the two lobes (Fig. 5B). The maximum width of Osculichnus in this locality is 18.9–41.3 mm (with an average of 31.7 mm, N = 11), maximum height 14.0–36.0 mm (with an average of 22.3 mm) (Table 1). The flatness ratio is 1.04–2.12 (mean = 1.49), suggesting essentially a flattened structure. On the same sandstone sole and in the sandstones of adjacent levels, the branched sinuous trace Sinusichnus sinuosus of various size (0.4–2.8 mm in diameter) occurs as hypichnial grooves or ridges (Fig. 5C, D). The average amplitude of the sinusoids is 0.7–1.3 mm, average wavelength 8.2–14.3 mm. The wavelength/amplitude ratio (λ/A) is 8.2–11.7 (with a mean of 10.3) (Table 2). Undulating burrows about 5 mm wide are closely associated with Osculichnus on the sandstone sole (Fig. 5A), however, they are interrupted by Osculichnus and the complete morphology is uncertain. In this case, they could be probably assigned to ?Sinusichnus isp.
Fig. 3. Morphometric parameters for Osculichnus and Sinusichnus. A. Maximum width and height as two parameters for Osculichnus size measurement. B. Diameter, amplitude, and wavelength for Sinusichnus size measurement.
each locality) and are deposited in the Laboratory of Geobiology, School of Earth Sciences, China University of Geosciences (Wuhan), with prefix WHYJ. The sizes of Osculichnus and associated Sinusichnus of the two fossil sites were measured by the software ImageJ using photographs shot perpendicular to the bedding plane or in the laboratory. For Osculichnus, we extracted the maximum width (along the direction of the central groove/lobe) and height (perpendicular to the direction of the central groove/lobe) of each specimen, and a flatness ratio was calculated by maximum width subdivided by maximum height (Fig. 3A). For Sinusichnus, several sinusoids of a single sinuous stretch were measured to calculate the average value for diameter, amplitude and wavelength (Fig. 3B). 4. Morphology of the fish hunting trace and associated trace fossils 4.1. The Huangjintang locality
5. Discussions
There are three sandstone soles with fish hunting trace Osculichnus in the Huangjintang locality. A total of 15 morphologically distinct Osculichnus specimens are preserved in the lowermost sandstone sole with an exposing area about 1 m2 (Fig. 4A). They appear as approximately ellipsoidal mounds which are divided into two lobes by a median groove (Fig. 4C–E). The two lobes in a single specimen may be similar (semi-symmetrical) in shape and size (Fig. 4D) or different, with a wider lobe enveloping the other one (Fig. 4C, E). The individual mounds are closely spaced locally (less than 4 cm apart from each other), and in one case, one larger mound is superimposed by a smaller one (Fig. 4B). The maximum width of Osculichnus is 23.5–59.3 mm
5.1. Morphological types and behavioural analysis of Osculichnus In previously reported forms of Osculichnus, they are described as essentially bilobate mounds separated by an undulating furrow and usually the two lobes are of different width (Demírcan and Uchman, 2010; Szrek et al., 2016). Osculichnus is produced by jawed fish given its commonly bilobate morphology that mimics the outline of the upper and lower jaws, as demonstrated by actualistic experiments (Demírcan and Uchman, 2010). Osculichnus represents a particular hunting behaviour of jawed vertebrates, in which the fish descended from the water
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Fig. 4. Typical morphology of the fish hunting trace Osculichnus and associated Sinusichnus sinuosus from the Upper Devonian Wutong Formation in Huangjintang, Wuhan, China. A. The lowermost sandstone sole with fish hunting traces, showing the extent of B, C, D, E by the dashed-line boxes. B. Dense distribution of hypichnial mounds (Osculichnus ispp.), showing the superimposition of two mounds (denoted by an arrow). C. Relatively well-preserved mounds of the enveloped bilobate morphology. D. Blurred preservation of a semi-symmetric bilobate mound in association with sinuous burrows (Sinusichnus sinuosus). E. Well-preserved enveloped bilobate mound, with sinuous burrows (part of Sinusichnus sinuosus) in the adjacent. F. Juxtaposed hypichnial mounds of similar size on the second sandstone sole. G. Abundant sinuous burrows Sinusichnus sinuosus on the first sandstone sole, showing the tendency of anastomosing to form networks; one specimen of Osculichnus is situated just at the end of one sinuous stretch. H. Fine details of the sinuous, branched Sinusichnus sinuosus, corresponding to the boxed area in G.
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one of the juxtaposed Osculichnus specimens in the Huangjintang locality shows an elongated oval depression between the two outer lobes (Fig. 4F), which indicates a partially opened mouth (Fig. 6A). In the Guodingshan hill locality, Osculichnus with an oval spacing between the two lobes is also present (Fig. 5B). The preservation of an elevated central lobe rather than a central cavity (e.g., Fig. 5A) is probably related to taphonomic processes associated with sediment movement when the fish took out the head from the sediment surface and/or spat out sediments when it sorted out its prey. Gnathostome fish generally have upper jaw unified with the rest of the skull (fixed) while the lower jaw can move down and up (mobile) (Janvier, 1996). Therefore, the imprints of the upper jaw may display relatively constant morphologies as an essentially arched or U-shaped lobe, whereas the lower jaw impression may take a wide spectrum of shape depending on the facing angle of the lower jaw to the sediments (cf. Szrek et al., 2016). One of the benthic feeding behaviour observed in modern marine as well as fresh-water fishes is the “diggers” feeding type (Sazima, 1986), in which the fish plunges the protrusible mouth into the soft substrate, filling it with sediments, withdraw and then sort out food items inside the mouth. Such a feeding method fits into the scenario of Osculichnus makers. The central cavity/lobe preservation provides strong evidence that the Osculichnus maker reached the sediment floor with an opened mouth and probably scooped or sucked up sediments with potential prey from the substrate. The various opening states of the two lobes in specimens represent the snapshots of this coherent hunting process that probably took only several seconds. The varied morphological distinctiveness of Osculichnus is probably related to the substrate consistency where the actual plunge was made. The specimens displaying obscure lobe outlines and blurred median furrows were probably made in loose, muddy sediments, with possible current reworking, resulting in poorly defined facial impressions (e.g., Fig. 4D). The well-preserved specimens with fine morphological details (e.g., with distinct median furrow or central cavity/lobe and outer lobes, Fig. 4C, F, Fig. 5A) are supposed to have been made in relatively firm muddy substrates with a thin sandy cover, in which the fish explored the buried muddy sediments at the lithological boundaries (cf. Demírcan and Uchman, 2010). The numerous mounds of various size and morphology on a given sandstone sole may at first sight suggest a group of trace makers, yet more likely resulted from the different angle of attack and depth of penetration by a single trace maker. This is also supported by the largely concordant orientation of the Osculichnus specimens on the sandstone soles. Osculichnus specimens on the three successive beds in the Huangjintang locality are oriented mostly at a small angle (about 30°) to the prevailing current direction indicated by groove marks (Fig. 7), suggesting that the Osculichnus maker might have swum in the direction up flow in the feeding process. The peculiar “twin” mounds (Fig. 4F) and superimposed mounds (Fig. 4B) of Osculichnus possibly records successive attempts from a single trace maker. Since Osculichnus makers could feed on endobenthic prey, they were probably able to detect the presence of the “underground” preys using, for example, olfactory senses (chemoreception) (Fig. 8). A hypothetical reconstruction of the feeding process and ecology of Osculichnus makers is given in Fig. 8.
Table 1 Size measurement results of Osculichnus from the Huangjintang and Guodingshan hill localities. No.
Width (mm)
Height (mm)
Flatness ratio
Locality
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
45.2 46.6 40.7 56.9 46.8 46.9 35.2 51.3 59.3 26.5 57.6 38.6 23.5 41.8 48.7 38.4 32.7 30.7 29.8 30.1 18.9 24.0 25.9 39.6 41.0 28.5 31.1 38.7 41.3
42.1 39.6 36.9 33.5 32.9 43.8 31.2 43.6 49.9 20.0 69.4 33.6 17.9 46.6 44.8 35.6 35.9 32.2 16.7 22.4 14.0 15.4 15.4 24.6 33.8 27.3 14.7 24.6 36.0
1.07 1.18 1.10 1.70 1.42 1.07 1.13 1.18 1.19 1.33 0.83 1.15 1.31 0.90 1.09 1.08 0.91 0.95 1.78 1.34 1.35 1.56 1.68 1.61 1.21 1.04 2.12 1.57 1.15
HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole, WHYJ-2) HJT (2nd sole) HJT (2nd sole) GDS GDS GDS GDS GDS GDS GDS GDS GDS GDS GDS (WHYJ-1)
Table 2 Size measurement results of Sinusichnus from the Huangjintang and Guodingshan hill localities (see abbreviation in Fig. 3). No.
Ave-D
Ave-A
Ave-λ
Ave-λ/Ave-A
Locality
L1 L2 L3 L4 L5 L6 L7 L8 L9 L10 L11
2.4 3.3 3.7 4.3 3.9 2.0 2.6 2.7 0.4 2.8 1.2
3.8 3.5 4.0 3.9 3.5 3.9 2.8 3.3 0.7 1.3 1.1
32.7 23.7 29.3 34.0 22.8 33.3 20.6 20.5 8.2 14.3 9.0
8.6 6.8 7.3 8.7 6.5 8.5 7.4 6.2 11.7 11.0 8.2
HJT HJT HJT HJT HJT HJT HJT HJT GDS GDS GDS
column, facing downward, and grasped the prey in the surface sediments, leaving facial impressions in the sediments (Demírcan and Uchman, 2010). However, details about how the fish got its prey, i.e., whether the prey is epibenthic (so that caught by vision) or endobenthic (detected by chemoreception and intentionally sorted out by the fish), are lacking. Since the two outer lobes of Osculichnus represent the impressions of the upper and lower jaws, naturally the area of the median groove or central cavity/lobe indicates the openness of the fish mouth when it hit and/or pulled out from the substrate. Specimens of Osculichnus with a narrow median furrow thus represent impressions from an almost closed mouth (e.g., Fig. 4C–E, Fig. 6B, C). Osculichnus with a central cavity or lobe, which resulted from an opened mouth, has been noted in previous reports (e.g., fig. 4D in Demírcan and Uchman, 2010). Szrek et al. (2016) mentioned the presence of a trapezoidal depression instead of a furrow in certain Osculichnus specimens. More examples of such “open-mouth” impressions are discovered in this study. For instance,
5.2. Report of Sinusichnus sinuosus from the Late Devonian Osculichnus is closely associated with sinuous burrows (Sinusichnus sinuosus) at both the Huangjintang and Guodingshan hill localities. The hypichnial groove or ridge preservation on the sandstone soles is evidence of excavation at the lithological boundary between mudstone and sandstone, which is consistent with the implication that the Osculichnus trace maker would explore buried mudstones (Demírcan and Uchman, 2010). Generally, Sinusichnus is sparse and interrupted where there are
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Fig. 5. Typical morphology of the fish predation trace Osculichnus and associated Sinusichnus and ?Sinusichnus from the Upper Devonian Wutong Formation in the Guodingshan hill locality, Wuhan, China. A. Dense distribution of hypichnial mounds (Osculichnus ispp.) on the sandstone sole, showing Osculichnus with an elevated central lobe (denoted by white arrows); stretches of undulating burrows (?Sinusichnus isp.) are present nearby (indicated by yellow arrows). B. Detailed morphology of one collected specimen of Osculichnus, exhibiting an exaggerated lower lobe and an irregular central cavity, specimen no. WHYJ-1. C. Dense distribution of hypichnial burrows Sinusichnus sinuosus in various sizes. D. Enlarged picture of an exceptionally small Sinusichnus sinuosus in the boxed area of C, showing the enlarged branching point. E. Dense distribution of hypichnial burrow ?Sinusichnus, note the branching style as indicated by arrows. F. Hypichnial burrow ?Sinusichnus, note the winding style of the sinuous trace. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
numerous Osculichnus mounds while more morphologically distinct where there are few Osculichnus specimens, and locally (in the Huangjintang locality) Osculichnus is positioned just at the end of one stretch of the sinuous burrow (Fig. 4G). Therefore, the Osculichnus makers seemed to have completely churned up the sediments originally riddled with Sinusichnus. And it cannot be exempted that Sinusichnus trace makers could be one of the prey animals of Osculichnus makers. Sinusichnus sinuosus is a strikingly regular trace fossil that has been largely reported from marginal-marine, especially prodelta deposits of the Late Cretaceous to Miocene age (de Gibert et al., 1999; Buatois et al., 2009; Belaústegui et al., 2014), with only two records in the Lower and Middle Triassic of South China (Luo et al., 2018; Lijun Zhang, personal communication). Another ichnotaxa, Sinusichnus cf. seilacheri Knaust et al., 2016, attributed to isopod crustaceans, has been described from the Upper Ordovician (Knaust and Desrochers, 2019). Sinusichnus sinuosus is generally interpreted as the burrows of specific types of decapod crustaceans with highly sophisticated navigational
capabilities (de Gibert, 1996; Belaústegui et al., 2014). The Late Devonian specimens here represent probably the earliest burrows made by decapod crustaceans, whose body-fossil history started from the Late Devonian (Schram et al., 1978). The expansion of the stratigraphical range of Sinusichnus sinuosus to the Late Devonian opens up possibilities of an ancient root for the represented complex behaviour. The Late Devonian specimens here are generally smaller (0.4–4.3 mm wide) than the common range of the Mesozoic and Cenozoic counterparts (2–25 mm) (de Gibert, 1996; de Gibert et al., 1999). This may be explained by supposedly smaller crustacean progenitors in the Palaeozoic or stressed environmental conditions (brackish water) of the Wutong Formation. The varied sizes of Sinusichnus encountered in the Guodingshan hill (0.4–2.8 mm) possibly indicate the presence of a dynamic population composed of juveniles and adults, which is occasionally found in certain crustacean species that lack a planktonic larval stage (Forbes, 1973).
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5.3. Possible makers of Late Devonian Osculichnus Osculichnus discovered here in the Late Devonian is its second occurrence in the Palaeozoic since its report in the Early Devonian (Szrek et al., 2016). The Early Devonian Osculichnus has been assigned to lungfish based on its snout morphology in dorsal view, the deep, curved profile of the lower jaw in lateral view, and the presence of a pair of arches in the ventral margin of the upper lip (Szrek et al., 2016). Imprints of dentitions have not been observed in the Late Devonian Osculichnus from South China, especially for the well-preserved ones presumed to have been made firmer substrates in the Guodingshan hill locality. The deep, curved profile of the lower jaw is noted in certain cases (Fig. 4E), which resembles the Early Devonian ones (figs. 4, 5 in Szrek et al., 2016). The arched upper lobe, which is curved more steeply in the two sides (e.g., Fig. 5A), is indicative of a trapezoidal outline of the snout and a pair of arches in the ventral margin of the upper lip. The preservation locally of an exaggerated lower lobe (Fig. 5B) suggests essentially fleshy lips without prominent marginal dentition. These evidences fit into the morphological characteristics of extant lungfishes. Lobe-finned fishes (Sarcopterygii) were diversified in the Devonian and gave rise to tetrapods in the Late Devonian (Benton, 2005), with only a few extant aquatic examples (i.e., six species of lungfish and two species of Latimeria (coelacanths)). Modern lungfish are essentially
Fig. 6. The morphological types of Osculichnus from the Upper Devonian Wutong Formation in Wuhan, China. A–D represent Osculichnus with two elevated outer lobes and a central groove or cavity of various size, indicating probably the openness of the fish mouth; the two outer lobes may be similar in width (A and B) or in an enveloped style (C and D). E and F show Osculichnus with an elevated, trapezoidal or elliptical central lobe, in addition to the two elevated outer lobes; the central lobe may superimpose upon one of the outer lobes (F).
Fig. 7. Rose diagram showing the orientation of Osculichnus specimens in the Huangjintang locality. A. The three successive sandstone soles and groove marks on the third sandstone sole, the orientation of Osculichnus is measured by the direction perpendicular to the median groove. B. Rose diagram showing orientation of Osculichnus and its relationship with the flow direction, supposing that the main current direction had not much changed during the deposition of the three successive sandstone beds.
Fig. 8. Interpretation of the hunting and feeding process of the Late Devonian jawed fish based on fossil material from the Wutong Formation, Wuhan, China. A. The Osculichnus maker shows up-current swimming, successive plunging, and chemoreception of endobenthic prey. Sinusichnus sinuosus is abundant in the sediments, which are disturbed and interrupted by the fish plunges. B. The resulted preservation of hypichnial bilobate mounds and sinuous burrows on the sandstone sole. 110
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benthic omnivores, feeding on fish, insects, crustaceans, worms, mollusks, amphibians and plant matter based on their intestine or feacal materials (Kemp, 1986). Fossil lobe-finned fish probably also led a benthic living style according to the bedding surface scratches (Parundichna) made by swimming coelacanths (Simon et al., 2003). The feeding mechanism of Osculichnus makers here is similar to modern lungfish in adopting a suction feeding style for prey capture (Bemis and Lauder, 1986). In addition, body fossils of lungfish have been previously discovered in the Wutong Formation (Li et al., 1984). Therefore, lungfish may be promising candidates for Osculichnus producers in the Late Devonian, which is also evoked by Szrek et al. (2016) for Early Devonian Osculichnus. Osculichnus Demírcan and Uchman, 2010, along with the trapping and hunting traces like Piscichnus Feibel, 1987, represents unique fossil evidence of predator–prey interactions that take place near the sediment–water interface. With the discovery of more trace fossils exhibiting the hunting (praedichnia sensu Ekdale, 1985) and trapping (irretichnia sensu Lehane and Ekdale, 2013) behaviour, we may have a more comprehensive understanding of the repertoire of predator–prey interactions in the fossil record, which may help to get a fuller picture of the macroevolutionary trends of predator–prey interactions.
Belaústegui, Z., Gibert, J.M.D., López-Blanco, M., Bajo, I., 2014. Recurrent constructional pattern of the crustacean burrow Sinusichnus sinuosus from the Paleogene and Neogene of Spain. Acta Palaeontol. Pol. 59, 461–474. Bemis, W.E., Lauder, G.V., 1986. Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi). J. Morphol. 187, 81–108. Bengtson, S., 2002. Origins and early evolution of predation. Paleontol. Soc. Pap. 8, 289–318. Benton, M.J., 2005. Vertebrate Palaeontology, 3rd ed. Blackwell Publishing, Oxford. Buatois, L.A., Macsotay, O., Quiroz, L.I., 2009. Sinusichnus, a trace fossil from Antarctica and Venezuela: expanding the dataset of crustacean burrows. Lethaia 42, 511–518. de Gibert, J.M., 1996. A new decapod burrow system from the NW Mediterranean Pliocene. Rev. Esp. Paleontol. 11, 251–254. de Gibert, J.M., Jeong, K., Martinell, J., 1999. Ethologic and ontogenic significance of the Pliocene trace fossil Sinusichnus sinuosus from the northwestern Mediterranean. Lethaia 32, 31–40. Demírcan, H., Uchman, A., 2010. Kiss of death of a hunting fish: trace fossil Osculichnus labialis igen. et isp. nov. from late Eocene - early Oligocene prodelta sediments of the Mezardere Formation, Thrace Basin, NW Turkey. Acta Geol. Pol. 60, 29–38. Dunne, J.A., Williams, R.J., Martinez, N.D., Wood, R.A., Erwin, D.H., 2008. Compilation and network analyses of Cambrian food webs. PLoS Biol. 6, e102. Ekdale, A.A., 1985. Paleoecology of the marine endobenthos. Palaeogeogr. Palaeoclimatol. Palaeoecol. 50, 63–81. Feibel, C.S., 1987. Fossil fish nests from the Koobi Fora Formation (Plio-Pleistocene) of Northern Kenya. J. Paleontol. 61, 130–134. Forbes, A.T., 1973. An unusual abbreviated larval life in the estuarine burrowing prawn Callianassa kraussi (Crustacea: Decapoda: Thalassinidea). Mar. Biol. 22, 361–365. Gorzelak, P., Rakowicz, Ł., Salamon, M.A., Szrek, P., 2011. Inferred placoderm bite marks on Devonian crinoids from Poland. Neues Jahrb. Geol. Palaeontol. Abh. 259, 105–112. Gorzelak, P., Salamon, M.A., Baumiller, T.K., 2012. Predator-induced macroevolutionary trends in Mesozoic crinoids. Proc. Natl. Acad. Sci. U. S. A. 109, 7004–7007. Gregory, M.R., 1991. New trace fossils from the Miocene of Northland, New Zealand: Rorschachichnus amoeba and Piscichnus waitemata. Ichnos 1, 195–205. Gregory, M.R., Ballance, P.F., Gibson, G.W., Ayling, A.M., 1979. On how some rays (Elasmobranchia) excavate feeding depressions by jetting water. J. Sediment. Res. 49, 1125–1129. Hunt, A.P., 1992. Late Pennsylvanian coprolites from the Kinney Brick Quarry, central New Mexico, with notes on the classification and utility of coprolites. N. M. Bur. Mines Miner. Resour., Bull. 138, 221–229. Huntley, J.W., Kowalewski, M., 2007. Strong coupling of predation intensity and diversity in the Phanerozoic fossil record. Proc. Natl. Acad. Sci. U. S. A. 104, 15006–15010. Janvier, P., 1996. Early Vertebrates. Clarendon Press, Oxford. Jensen, S., 1990. Predation by early Cambrian trilobites on infaunal worms - evidence from the Swedish Mickwitzia Sandstone. Lethaia 23, 29–42. Kelley, P.H., Kowalewski, M., Hansen, T.A., 2003. Predator-prey interactions in the fossil record. In: Landman, N.H., Jor, D.S. (Eds.), Topics in Geobiology. Kluwer Academic/ Plenum Publishers, New York, pp. 464. Kemp, A., 1986. The biology of the australian lungfish, Neoceratodus forsteri (Krefft, 1870). J. Morphol. 190, 181–198. Knaust, D., Desrochers, A., 2019. The trace fossil Sinusichnus from the Upper Ordovician of Anticosti Island, eastern Canada. Lethaia (In press). Knaust, D., Minter, N.J., 2018. The fish swimming trace Undichna unisulca from the Silurian of Sweden: probably the oldest vertebrate locomotion trace fossil. Lethaia 51, 469–472. Knaust, D., Uchman, A., Hagdorn, H., 2016. The probable isopod burrow Sinusichnus seilacheri isp. n. from the Middle Triassic of Germany: an example of behavioral convergence. Ichnos 23, 138–146. Kowalewski, M., Dulai, A.d., Fürsich, F.T., 1998. A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26, 1091–1094. Lehane, J.R., Ekdale, A.A., 2013. Pitfalls, traps, and webs in ichnology: Traces and trace fossils of an understudied behavioral strategy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 375, 59–69. Li, C.-S., 2000. Devonian plants and stratum in Wuhan, Hubei Province. China. Chin. Bull. Bot. 17, 1–10. Li, X.-X., Cai, C.-Y., Ouyang, S., 1984. Recent advances in the study of the Wutong Formation of the lower Yangtze valley. Bull. Chin. Acad. Geol. Sci. 9, 119–133. Luo, M., Gong, Y.-M., Shi, G.-R., Chen, Z.-Q., Huang, J.-Y., Hu, S.-X., Feng, X.-Q., Zhang, Q.-Y., Zhou, C.-Y., Wen, W., 2018. Palaeoecological analysis of trace fossil Sinusichnus sinuosus from the Middle Triassic Guanling Formationin Southwestern China. J. Earth Sci. 29, 854–863. Minter, N.J., Braddy, S.J., 2006. The fish and amphibian swimming traces Undichna and Lunichnium, with examples from the Lower Permian of New Mexico, USA. Palaeontology 49, 1123–1142. Peng, B.-X., Du, Y.-S., 2002. Sedimentary facies and paleogeography of sandstones of Wutong Formation of the Late Devonian in eastern Hubei Province. J. Palaeogeogr. 4, 26–32. Sallan, L.C., Kammer, T.W., Ausich, W.I., Cook, L.A., 2011. Persistent predator–prey dynamics revealed by mass extinction. Proc. Natl. Acad. Sci. U. S. A. 108, 8335–8338. Sazima, I., 1986. Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities. J. Fish Biol. 29, 53–65. Schram, F.R., Feldmann, R.M., Copeland, M.J., 1978. The Late Devonian Palaeopalaemonidae and the earliest decapod crustaceans. J. Paleontol. 52, 1375–1387. Simon, T., Hagdorn, H., Hagdorn, M.K., Seilacher, A., 2003. Swimming trace of a coelacanth fish from the Lower Keuper of south-west Germany. Palaeontology 46, 911–926. Szrek, P., Salwa, S., Niedźwiedzki, G., Dec, M., Ahlberg, P.E., Uchman, A., 2016. A glimpse of a fish face — an exceptional fish feeding trace fossil from the Lower Devonian of the Holy Cross Mountains, Poland. Palaeogeogr. Palaeoclimatol. Palaeoecol. 454, 113–124.
6. Conclusions Osculichnus from the Upper Devonian Wutong Formation occurs as hypichnial bilobate mounds with two elevated outer lobes and a central groove/depression or convex lobe of various size. There is considerable morphological variety among Osculichnus specimens. Osculichnus is interpreted as the imprints of the upper and lower jaws of gnathostome makers when plunging into the sediments for endobenthic prey. The morphological characteristics (highly arched, U-shaped upper lobe and exaggerated lower lobe) of Osculichnus from South China indicate a trapezoidal outline of the snout and smooth, fleshy lips without prominent marginal dentition of the fish makers, which suggest lungfish as possible trace makers. The direction perpendicular to the central groove of Osculichnus specimens are oriented mostly at a small angle (about 30°) to the current flow indicated by groove marks, implying that the gnathostome fish maker of Osculichnus probably swam in the direction up flow. Osculichnus is in close association with the sinuous, branched trace Sinusichnus sinuosus. Late Devonian Sinusichnus sinuosus in this study is probably the oldest reported to date, with diameter 0.4–4.3 mm, wavelength 8.2–34.0 mm, amplitude 0.7–4.0 mm, which is generally smaller than Late Cretaceous to Miocene examples. Its trace maker is supposed to be some primitive, small decapod crustaceans that inhabited the stressed, brackish water of the estuarine environment of the Wutong Formation. Acknowledgements This work was supported by the National Natural Science Foundation of China [grant numbers 41290260, 41872034, 41702006] and the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan) [grant number 162301182730]. We thank Zhao Zhao and Zhen Shen from China University of Geosciences for their assistance in the field. We appreciate much the constructive and critical comments from Alfred Uchman and an anonymous reviewer, which aid in the further improvement of the manuscript. The Editor in Chief Thomas Algeo is acknowledged for suggestions on the manuscript. References Anderson, A.M., 1976. Fish trails from the early Permian of South Africa. Palaeontology 19, 397–409. Baumiller, T.K., Salamon, M.A., Gorzelak, P., Mooi, R., Messing, C.G., Gahn, F.J., 2010. Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution. Proc. Natl. Acad. Sci. U. S. A. 107, 5893–5896.
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R.-y. Fan, et al. Uchman, A., Torres, P., Baptista, L., Madeira, P., Cordeiro, R., Ávila, S.P., Berning, B., Melo, C.S., Rebelo, A.C., Johnson, M.E., Ramalho, R.S., 2018. Feeding traces of recent ray fish and occurrences of the trace fossil Piscichnus waitemata from the Pliocene of Santa Maria Island, Azores (Northest Atlantic). Palaios 33, 361–375. Vannier, J., Chen, J.-Y., 2005. Early Cambrian food chain: new evidence from fossil aggregates in the Maotianshan Shale Biota, SW China. Palaios 20, 3–26. Vannier, J., Steiner, M., Renvoisé, E., Hu, S.-X., Casanova, J.-P., 2007. Early Cambrian origin of modern food webs: evidence from predator arrow worms. Proc. R. Soc. B 274, 627–633. Vermeij, G.J., 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258. Walossek, D., Li, C.-S., Brauckmann, C., 1990. A scorpion from the Upper Devonian of Hubei Province, China (Arachnida, Scorpionida). Neues Jahrb. Geol. Palaeontol. Abh. 3, 169–180. Xu, H.-H., Zong, R.-W., Wang, Q., 2012. New materials of Sphinxiocarpon, a seed-like
organ of putative lycopsid affinity, from the Late Devonian of Hubei, China. Palaeoworld 21, 131–136. Yang, S.-P., Hu, C.-M., Sun, Y.-C., 1987. Discovery of Late Devonian trace fossils from Guodingshan district, Hanyang, China and its significance. J. Earth Sci. 12, 1–8. Zhang, G.-D., Zhu, J.-C., Wang, Y.-Y., Zhang, S.-L., 1987. Marine transgression and depositional environments of the Late Devonian Wutong Formation in the Jiangsu–Anhui region. Geol. Rev. 33, 69–77. Zhu, M.-Y., Vannier, J., Iten, H.V., Zhao, Y.-L., 2004. Direct evidence for predation on trilobites in the Cambrian. Proc. R. Soc. B 271, S277–S280. Zong, R.-W., Liu, Q., Gong, Y.-M., 2011. Fossil association and sedimentary environments of the Lower Silurian Fentou Formation in Wuhan, Hubei Province. J. Palaeogeogr. 13, 299–308. Zong, R.-W., Liu, Q., Wei, F., Gong, Y.-M., 2017. Fentou Biota: a Llandovery (Silurian) shallow-water exceptionally preserved biota from Wuhan, Central China. J. Geol. 125, 469–478.
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Fish hunting trace Osculichnus and the oldest Sinusichnus sinuosus from the Upper Devonian of South China
T
Ruo-ying Fan, Rui-wen Zong, Yi-ming Gong
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State Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences, Wuhan 430074, China
ARTICLE INFO
ABSTRACT
Keywords: Praedichnia Jawed fish Wutong Formation Late Devonian South China
Trace fossils are special objects in the study of predator–prey interactions in the fossil record. Here we report on diverse morphological types of the gnathostome fish hunting trace Osculichnus from the Upper Devonian of South China. The studied Osculichnus specimens occur as groups of bilobate mounds on the sole of fine- to mediumgrained quartz sandstones from the estuarine-embayment depositional system of the Upper Devonian Wutong Formation in Wuhan city. The fish feeding trace Osculichnus is closely associated with the highly regular, branched sinuous trace Sinusichnus sinuosus on the bedding plane. Previously, Sinusichnus sinuosus has been typically reported from Late Cretaceous to Miocene marginal-marine sediments, with two records in the Lower and Middle Triassic of South China, and is generally regarded as the burrows of decapod crustaceans. The discovery of Sinusichnus sinuosus in the Upper Devonian, though of relatively small diameter (0.4–4.3 mm) than its Mesozoic and Cenozoic counterparts, extends its stratigraphical distribution and is suggestive of some primitive, small-sized decapod crustacean producers. The Osculichnus makers possibly preyed upon the Sinusichnus makers or other small invertebrates in the sediments. The overall shape and morphological details of the Late Devonian Osculichnus suggest lungfish as candidate trace makers. The fish hunting traces and associated trace fossils from South China thus provide unique insights into the palaeoecology of Late Devonian fishes.
1. Introduction Fishes are important vertebrate trace makers in the fossil record. The earliest vertebrate trace fossil is a Late Silurian fish swimming trace (Knaust and Minter, 2018). Various fish traces in the sediments have been recognized; by far the most frequently reported and extensively studied are fish locomotion traces like Undichna Anderson, 1976 (see review in Minter and Braddy, 2006) and less commonly Parundichna Simon et al., 2003, both of which, from a functional point, resulted from jawed fishes. Predator–prey interactions may be as old as life itself, yet complex food webs were only established with the advent of the Cambrian explosion (Bengtson, 2002; Vannier et al., 2007; Dunne et al., 2008). Predator–prey interactions play a significant role in determining the distribution and diversity of organisms, and have long been hypothesized as a driving force of the macroevolution of related clades (Vermeij, 1977; Kelley et al., 2003; Huntley and Kowalewski, 2007; Baumiller et al., 2010; Sallan et al., 2011; Gorzelak et al., 2012). The fossil record of predation has focused on trace fossils like bite marks, drill holes or repair scars found on organic substrates (skeletons or shells of animals) (Jensen, 1990; Kowalewski et al., 1998; Kelley et al., ⁎
2003), or stomach contents and excretes (i.e., coprolites, gastroliths, and regurgitalites, bromalites sensu Hunt, 1992; Zhu et al., 2004; Vannier and Chen, 2005). There is less attention on predatory behaviours taking place in the sediments that could be potentially recorded as biogenic sedimentary structures (e.g., trapping traces or irretichnia, proposed by Lehane and Ekdale, 2013). The Devonian is known as “the age of fishes” with pronounced radiation of jaw-bearing fish (Janvier, 1996). Fish predation in the fossil record has been recognized through bite marks, such as crinoids preyed upon by durophagous fishes (Gorzelak et al., 2011), but there is also evidence of fish predation recorded by interaction with sediments. For instance, Piscichnus Feibel, 1987, representing ray feeding depressions on the sediment floor, has been common since the Cretaceous (Gregory et al., 1979; Gregory, 1991; Uchman et al., 2018). Probably the most interesting evidence of the feeding and hunting behaviour of gnathostomes lies in the recently reported Osculichnus Demírcan and Uchman, 2010 (meaning “kissing” traces), which is commonly preserved as surface pits or hypichnial mounds of sandstone beds. They represent the bottom-feeding activities of gnathostomes preying on small endobenthic animals (Szrek et al., 2016). In this paper, we report on diverse morphological types of the fish hunting trace Osculichnus and associated Sinusichnus sinuosus from
Corresponding author. E-mail address: [email protected] (Y.-m. Gong).
https://doi.org/10.1016/j.palaeo.2019.05.045 Received 17 April 2019; Received in revised form 31 May 2019; Accepted 31 May 2019 Available online 04 June 2019 0031-0182/ © 2019 Elsevier B.V. All rights reserved.
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Fig. 1. Location and geological map of the study area. A. Map of China, showing the general locality of the study area (magnified in B). B. The study area is located in Wuhan, the capital city of Hubei Province, at the confluence of the Yangtze and Hanjiang rivers. C. Simplified geological map of the study area (boxed area in B), the fish hunting trace Osculichnus was found in Huangjintang (HJT) and Guodingshan hill (GDS).
the Late Devonian marginal-marine environment of South China, with a discussion of the behaviour, ecology and possible identity of its gnathostome producers.
climates. The sandstones in the lower part of the Wutong Formation show several large-scale fining upward sequences, with locally parallel bedding, large-scale wedge-shaped and herringbone cross-beddings, as well as asymmetric ripple marks (see also Peng and Du, 2002); it yields the Frasnian plants Leptophloem rhombicum Dawson, Protopteriodophyton devonicum Li et Hsu, Chamaedendron multisporangiatum Schweitzer et Li, Sphinxiocarpon wuhanium (Li, Hilton et Hemsley) and diverse spores (Li, 2000; Xu et al., 2012), as well as the scorpion Hubeiscopio graciltarus Walossek, Li et Brauckmann (Walossek et al., 1990). The Wutong Formation grades in the upper part to brownish grey or purplish thin- to medium-bedded fine- to medium-grained micaceous quartz sandstones (locally laminated) intercalated by thin-bedded muddy siltstones (Fig. 2). The upper part of the Wutong Formation yields abundant plant fossils and spores of the Late Devonian Famennian age: Leptophloeum rhombicum Dawson, Cyclostigma kiltorkense Haughton, Sublepidodendron wusihense (Sze), Sphenophyllum sp. (Li, 2000). The high content of mica flakes indicates deposition in an environment less winnowed by waves and longshore currents. The poorly developed marine fauna suggests that the Wutong Formation was probably deposited under stressed conditions influenced by significant salinity fluctuations. Overall, the Wutong Formation represents deposition in an oxygenated shallow water depth during the Late Devonian transgressional period, very likely belonging to the estuarine-embayment depositional system or associated marginal- to shallow-marine facies (barrier-island systems, upper shoreface, foreshore, tidal flat). The Wutong Formation is overlain by the Early Carboniferous Gaolishan Formation by a paraconformity in the study area. The Gaolishan Formation is composed primarily of greyish or mottled claystones, with intercalations of lenticular quartz sandstones, coal measures, and siderite nodules, which probably belongs to the lagoon–tidal-flat–marsh environment in the
2. Geological setting and stratigraphy The fossil material was found in the upper part of the Upper Devonian Wutong Formation from Wuhan city of Hubei Province, China. In the study area, the Wutong Formation crops out as E-W trending ribbons (Fig. 1). The Wutong Formation separates from the underlying Llandovery Fentou Formation by a paraconformity (Zong et al., 2017). The Llandovery Fentou Formation is made up of primarily mudstones, silty mudstones, and siltstones, which hosts abundant brachiopods, bivalves, gastropods, trilobites, fish, and trace fossils (Zong et al., 2011). Sandstone intercalations increase towards the upper part of the Fentou Formation, showing a coarsening upwards sequence. Large pyrite concretions (up to 1 cm) and well-pyritized body fossils have been found in this formation. Recently, well-preserved eurypterids, complete echinoderms, and sponges of the Burgess Shale-type were found in the Fentou Formation; they were attributed to the Fentou Biota, representing an early Silurian exceptionally preserved biota in the shallow-marine (deltaic, probably distal delta-front or prodelta) environment (Zong et al., 2017). The Wutong Formation is composed of grey-whitish to brownish thick- to very thick-bedded quartz sandstones interbedded with thin layers of muddy siltstones or claystones in the lower part, with commonly a basal lag of conglomerates (Fig. 2). There are densely distributed semi-spherical, poorly cemented sandy sediment packages (commonly weathered out as elliptical hollows) immediately above the paraconformity, which suggest effective fluvial input under humid
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Fig. 2. Outcrops and lithology of the Upper Devonian Wutong Formation in Huangjintang, Wuhan, China. A. Outcrop view of the Huangjintang section, showing the thin- to mediumbedded sandstone beds in the upper part of the section where fish hunting traces were found (people standing, see close shot in B, corresponding to bed no. 12 in C). B. The successive three sandstone soles (numbered) yielding the fish hunting traces. C. Lithological column of the Huangjintang section, showing the generally fining-upward sequences of the Wutong Formation (vf. – very fine-grained; m. – mediumgrained; c. – coarse-grained; vc. – very coarse-grained; cg. – conglomerate) (the stratigraphic column shows the stacking style of beds, but not to scale).
regressive phase. Trace fossil assemblages of the Wutong Formation can be attributed to a mixed, depauperate Skolithos–Cruziana ichnofacies, including dwelling traces Arenicolites, Bifungites, arthropod locomotion/feeding/ resting traces Cruziana, Rusophycus, Diplichnites, Monomorphichnus, bivalve locomotion trace Protovirgularia, bivalve resting trace Lockeia, and locomotion/feeding traces of worm-like animals Gordia, ?Chondrites, ?Cochlichnus,?Margaritichnus (revised from Yang et al., 1987; Zhang et al., 1987). Additional elements Osculichnus, Sinusichnus, Rhizocorallium, and ?Undichna were discovered during investigation of this study.
measured the Huangjintang section; the well exposed sandstone soles in the upper part of this section provide the opportunity to study the morphology, size, and orientation of Osculichnus in situ (Fig. 2). A total of three sandstone soles with Osculichnus were recognized in Huangjintang, among which the lowermost sole exposes the best preserved Osculichnus and Sinusichnus specimens of this locality; the other two sandstone soles were observed from a distance since they are high above the ground. One of the authors (R.W. Zong) came across the fossil site at the Guodingshan hill, and provided photograph and specimen materials. The rapid civil construction completely destroyed outcrops of the two localities and the two fossil sites are no longer accessible. Effort has been made in search of good outcrops nearby, however, extensive bedding surfaces were not easily encountered. Therefore, further investigation is hampered. Most of the fish hunting trace fossils were photographed in the field due to the difficulty in separating them from the bulky quartz sandstone bed. And unfortunately, we have not got the opportunity to cast the Osculichnus specimens. Two specimens were collected from the Guodingshan hill and Huangjintang locality (one for
3. Materials and methods The fish hunting traces were found on the soles of grey or brownish sandstones (10–30 cm thick) in two localities (Huangjintang, GPS coordinates: 30°30′49.25″N, 114°31′53.54″E; Guodingshan hill, GPS coordinates: 30°34′12.11″N, 114°10′37.56″E). We systematically 105
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(with an average of 44.0 mm, N = 16), maximum height 17.9–69.4 mm (with an average of 38.8 mm), flatness ratio 0.83–1.70 (mean = 1.17) (Table 1). On the same sandstone sole as well as in the thin siltstone intercalation (about 1 cm thick) immediately below the sandstone sole, abundant sinusoid burrows 2.4–4.3 mm in diameter are present as hypichnial grooves, some grading to hypichnial ridge preservation (Fig. 4C–E, G, H). The average amplitude of the sinusoids is 2.8–4.0 mm, average wavelength 20.5–34.0 mm. The wavelength/amplitude ratio (λ/A) is 6.2–8.7 (with an average of 7.5) (Table 2). The sinuous burrow winds in a straight or gently curved way in various directions, with a tendency of anastomosing to form networks (Fig. 4G, H). The sinusoidal tunnels and the branching style are typical of Sinusichnus sinuosus de Gibert (1996). The second Osculichnus-bearing layer is restricted in exposure and only 5 specimens were recognized. Two specimens exhibit a central elliptical lobe between the outer lobes rather than a linear furrow (measurement for these two specimens was not allowed because the specimens were high above the ground). A peculiar scene of this sandstone sole is that two bilobate specimens of nearly identical size (32.7 × 35.9 mm and 30.7 × 32.2 mm, respectively) are immediately juxtaposed with each other (Fig. 4F). No associated trace fossils were found at this level. The third fossil-bearing level (~1 m2) exposes only 6 obscure Osculichnus specimens with hardly recognizable morphological details. Groove marks can be observed on the sandstone sole that imply strong bottom currents at the time of deposition, which may explain the poor preservation of Osculichnus specimens at this level. 4.2. The Guodingshan hill locality A total of 11 Osculichnus specimens are observed on the sandstone soles in the Guodingshan hill locality. Osculichnus specimens are more well-preserved in this locality and commonly exhibit a distinct, trapezoid or elliptical central depression or convex lobe between the two outer lobes (Fig. 5A). The central lobe may even superimpose on one of the outer lobes locally (Fig. 5A). One collected specimen shows an exaggerated lower lobe, with an irregular central cavity between the two lobes (Fig. 5B). The maximum width of Osculichnus in this locality is 18.9–41.3 mm (with an average of 31.7 mm, N = 11), maximum height 14.0–36.0 mm (with an average of 22.3 mm) (Table 1). The flatness ratio is 1.04–2.12 (mean = 1.49), suggesting essentially a flattened structure. On the same sandstone sole and in the sandstones of adjacent levels, the branched sinuous trace Sinusichnus sinuosus of various size (0.4–2.8 mm in diameter) occurs as hypichnial grooves or ridges (Fig. 5C, D). The average amplitude of the sinusoids is 0.7–1.3 mm, average wavelength 8.2–14.3 mm. The wavelength/amplitude ratio (λ/A) is 8.2–11.7 (with a mean of 10.3) (Table 2). Undulating burrows about 5 mm wide are closely associated with Osculichnus on the sandstone sole (Fig. 5A), however, they are interrupted by Osculichnus and the complete morphology is uncertain. In this case, they could be probably assigned to ?Sinusichnus isp.
Fig. 3. Morphometric parameters for Osculichnus and Sinusichnus. A. Maximum width and height as two parameters for Osculichnus size measurement. B. Diameter, amplitude, and wavelength for Sinusichnus size measurement.
each locality) and are deposited in the Laboratory of Geobiology, School of Earth Sciences, China University of Geosciences (Wuhan), with prefix WHYJ. The sizes of Osculichnus and associated Sinusichnus of the two fossil sites were measured by the software ImageJ using photographs shot perpendicular to the bedding plane or in the laboratory. For Osculichnus, we extracted the maximum width (along the direction of the central groove/lobe) and height (perpendicular to the direction of the central groove/lobe) of each specimen, and a flatness ratio was calculated by maximum width subdivided by maximum height (Fig. 3A). For Sinusichnus, several sinusoids of a single sinuous stretch were measured to calculate the average value for diameter, amplitude and wavelength (Fig. 3B). 4. Morphology of the fish hunting trace and associated trace fossils 4.1. The Huangjintang locality
5. Discussions
There are three sandstone soles with fish hunting trace Osculichnus in the Huangjintang locality. A total of 15 morphologically distinct Osculichnus specimens are preserved in the lowermost sandstone sole with an exposing area about 1 m2 (Fig. 4A). They appear as approximately ellipsoidal mounds which are divided into two lobes by a median groove (Fig. 4C–E). The two lobes in a single specimen may be similar (semi-symmetrical) in shape and size (Fig. 4D) or different, with a wider lobe enveloping the other one (Fig. 4C, E). The individual mounds are closely spaced locally (less than 4 cm apart from each other), and in one case, one larger mound is superimposed by a smaller one (Fig. 4B). The maximum width of Osculichnus is 23.5–59.3 mm
5.1. Morphological types and behavioural analysis of Osculichnus In previously reported forms of Osculichnus, they are described as essentially bilobate mounds separated by an undulating furrow and usually the two lobes are of different width (Demírcan and Uchman, 2010; Szrek et al., 2016). Osculichnus is produced by jawed fish given its commonly bilobate morphology that mimics the outline of the upper and lower jaws, as demonstrated by actualistic experiments (Demírcan and Uchman, 2010). Osculichnus represents a particular hunting behaviour of jawed vertebrates, in which the fish descended from the water
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Fig. 4. Typical morphology of the fish hunting trace Osculichnus and associated Sinusichnus sinuosus from the Upper Devonian Wutong Formation in Huangjintang, Wuhan, China. A. The lowermost sandstone sole with fish hunting traces, showing the extent of B, C, D, E by the dashed-line boxes. B. Dense distribution of hypichnial mounds (Osculichnus ispp.), showing the superimposition of two mounds (denoted by an arrow). C. Relatively well-preserved mounds of the enveloped bilobate morphology. D. Blurred preservation of a semi-symmetric bilobate mound in association with sinuous burrows (Sinusichnus sinuosus). E. Well-preserved enveloped bilobate mound, with sinuous burrows (part of Sinusichnus sinuosus) in the adjacent. F. Juxtaposed hypichnial mounds of similar size on the second sandstone sole. G. Abundant sinuous burrows Sinusichnus sinuosus on the first sandstone sole, showing the tendency of anastomosing to form networks; one specimen of Osculichnus is situated just at the end of one sinuous stretch. H. Fine details of the sinuous, branched Sinusichnus sinuosus, corresponding to the boxed area in G.
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one of the juxtaposed Osculichnus specimens in the Huangjintang locality shows an elongated oval depression between the two outer lobes (Fig. 4F), which indicates a partially opened mouth (Fig. 6A). In the Guodingshan hill locality, Osculichnus with an oval spacing between the two lobes is also present (Fig. 5B). The preservation of an elevated central lobe rather than a central cavity (e.g., Fig. 5A) is probably related to taphonomic processes associated with sediment movement when the fish took out the head from the sediment surface and/or spat out sediments when it sorted out its prey. Gnathostome fish generally have upper jaw unified with the rest of the skull (fixed) while the lower jaw can move down and up (mobile) (Janvier, 1996). Therefore, the imprints of the upper jaw may display relatively constant morphologies as an essentially arched or U-shaped lobe, whereas the lower jaw impression may take a wide spectrum of shape depending on the facing angle of the lower jaw to the sediments (cf. Szrek et al., 2016). One of the benthic feeding behaviour observed in modern marine as well as fresh-water fishes is the “diggers” feeding type (Sazima, 1986), in which the fish plunges the protrusible mouth into the soft substrate, filling it with sediments, withdraw and then sort out food items inside the mouth. Such a feeding method fits into the scenario of Osculichnus makers. The central cavity/lobe preservation provides strong evidence that the Osculichnus maker reached the sediment floor with an opened mouth and probably scooped or sucked up sediments with potential prey from the substrate. The various opening states of the two lobes in specimens represent the snapshots of this coherent hunting process that probably took only several seconds. The varied morphological distinctiveness of Osculichnus is probably related to the substrate consistency where the actual plunge was made. The specimens displaying obscure lobe outlines and blurred median furrows were probably made in loose, muddy sediments, with possible current reworking, resulting in poorly defined facial impressions (e.g., Fig. 4D). The well-preserved specimens with fine morphological details (e.g., with distinct median furrow or central cavity/lobe and outer lobes, Fig. 4C, F, Fig. 5A) are supposed to have been made in relatively firm muddy substrates with a thin sandy cover, in which the fish explored the buried muddy sediments at the lithological boundaries (cf. Demírcan and Uchman, 2010). The numerous mounds of various size and morphology on a given sandstone sole may at first sight suggest a group of trace makers, yet more likely resulted from the different angle of attack and depth of penetration by a single trace maker. This is also supported by the largely concordant orientation of the Osculichnus specimens on the sandstone soles. Osculichnus specimens on the three successive beds in the Huangjintang locality are oriented mostly at a small angle (about 30°) to the prevailing current direction indicated by groove marks (Fig. 7), suggesting that the Osculichnus maker might have swum in the direction up flow in the feeding process. The peculiar “twin” mounds (Fig. 4F) and superimposed mounds (Fig. 4B) of Osculichnus possibly records successive attempts from a single trace maker. Since Osculichnus makers could feed on endobenthic prey, they were probably able to detect the presence of the “underground” preys using, for example, olfactory senses (chemoreception) (Fig. 8). A hypothetical reconstruction of the feeding process and ecology of Osculichnus makers is given in Fig. 8.
Table 1 Size measurement results of Osculichnus from the Huangjintang and Guodingshan hill localities. No.
Width (mm)
Height (mm)
Flatness ratio
Locality
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
45.2 46.6 40.7 56.9 46.8 46.9 35.2 51.3 59.3 26.5 57.6 38.6 23.5 41.8 48.7 38.4 32.7 30.7 29.8 30.1 18.9 24.0 25.9 39.6 41.0 28.5 31.1 38.7 41.3
42.1 39.6 36.9 33.5 32.9 43.8 31.2 43.6 49.9 20.0 69.4 33.6 17.9 46.6 44.8 35.6 35.9 32.2 16.7 22.4 14.0 15.4 15.4 24.6 33.8 27.3 14.7 24.6 36.0
1.07 1.18 1.10 1.70 1.42 1.07 1.13 1.18 1.19 1.33 0.83 1.15 1.31 0.90 1.09 1.08 0.91 0.95 1.78 1.34 1.35 1.56 1.68 1.61 1.21 1.04 2.12 1.57 1.15
HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole) HJT (1st sole, WHYJ-2) HJT (2nd sole) HJT (2nd sole) GDS GDS GDS GDS GDS GDS GDS GDS GDS GDS GDS (WHYJ-1)
Table 2 Size measurement results of Sinusichnus from the Huangjintang and Guodingshan hill localities (see abbreviation in Fig. 3). No.
Ave-D
Ave-A
Ave-λ
Ave-λ/Ave-A
Locality
L1 L2 L3 L4 L5 L6 L7 L8 L9 L10 L11
2.4 3.3 3.7 4.3 3.9 2.0 2.6 2.7 0.4 2.8 1.2
3.8 3.5 4.0 3.9 3.5 3.9 2.8 3.3 0.7 1.3 1.1
32.7 23.7 29.3 34.0 22.8 33.3 20.6 20.5 8.2 14.3 9.0
8.6 6.8 7.3 8.7 6.5 8.5 7.4 6.2 11.7 11.0 8.2
HJT HJT HJT HJT HJT HJT HJT HJT GDS GDS GDS
column, facing downward, and grasped the prey in the surface sediments, leaving facial impressions in the sediments (Demírcan and Uchman, 2010). However, details about how the fish got its prey, i.e., whether the prey is epibenthic (so that caught by vision) or endobenthic (detected by chemoreception and intentionally sorted out by the fish), are lacking. Since the two outer lobes of Osculichnus represent the impressions of the upper and lower jaws, naturally the area of the median groove or central cavity/lobe indicates the openness of the fish mouth when it hit and/or pulled out from the substrate. Specimens of Osculichnus with a narrow median furrow thus represent impressions from an almost closed mouth (e.g., Fig. 4C–E, Fig. 6B, C). Osculichnus with a central cavity or lobe, which resulted from an opened mouth, has been noted in previous reports (e.g., fig. 4D in Demírcan and Uchman, 2010). Szrek et al. (2016) mentioned the presence of a trapezoidal depression instead of a furrow in certain Osculichnus specimens. More examples of such “open-mouth” impressions are discovered in this study. For instance,
5.2. Report of Sinusichnus sinuosus from the Late Devonian Osculichnus is closely associated with sinuous burrows (Sinusichnus sinuosus) at both the Huangjintang and Guodingshan hill localities. The hypichnial groove or ridge preservation on the sandstone soles is evidence of excavation at the lithological boundary between mudstone and sandstone, which is consistent with the implication that the Osculichnus trace maker would explore buried mudstones (Demírcan and Uchman, 2010). Generally, Sinusichnus is sparse and interrupted where there are
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Fig. 5. Typical morphology of the fish predation trace Osculichnus and associated Sinusichnus and ?Sinusichnus from the Upper Devonian Wutong Formation in the Guodingshan hill locality, Wuhan, China. A. Dense distribution of hypichnial mounds (Osculichnus ispp.) on the sandstone sole, showing Osculichnus with an elevated central lobe (denoted by white arrows); stretches of undulating burrows (?Sinusichnus isp.) are present nearby (indicated by yellow arrows). B. Detailed morphology of one collected specimen of Osculichnus, exhibiting an exaggerated lower lobe and an irregular central cavity, specimen no. WHYJ-1. C. Dense distribution of hypichnial burrows Sinusichnus sinuosus in various sizes. D. Enlarged picture of an exceptionally small Sinusichnus sinuosus in the boxed area of C, showing the enlarged branching point. E. Dense distribution of hypichnial burrow ?Sinusichnus, note the branching style as indicated by arrows. F. Hypichnial burrow ?Sinusichnus, note the winding style of the sinuous trace. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
numerous Osculichnus mounds while more morphologically distinct where there are few Osculichnus specimens, and locally (in the Huangjintang locality) Osculichnus is positioned just at the end of one stretch of the sinuous burrow (Fig. 4G). Therefore, the Osculichnus makers seemed to have completely churned up the sediments originally riddled with Sinusichnus. And it cannot be exempted that Sinusichnus trace makers could be one of the prey animals of Osculichnus makers. Sinusichnus sinuosus is a strikingly regular trace fossil that has been largely reported from marginal-marine, especially prodelta deposits of the Late Cretaceous to Miocene age (de Gibert et al., 1999; Buatois et al., 2009; Belaústegui et al., 2014), with only two records in the Lower and Middle Triassic of South China (Luo et al., 2018; Lijun Zhang, personal communication). Another ichnotaxa, Sinusichnus cf. seilacheri Knaust et al., 2016, attributed to isopod crustaceans, has been described from the Upper Ordovician (Knaust and Desrochers, 2019). Sinusichnus sinuosus is generally interpreted as the burrows of specific types of decapod crustaceans with highly sophisticated navigational
capabilities (de Gibert, 1996; Belaústegui et al., 2014). The Late Devonian specimens here represent probably the earliest burrows made by decapod crustaceans, whose body-fossil history started from the Late Devonian (Schram et al., 1978). The expansion of the stratigraphical range of Sinusichnus sinuosus to the Late Devonian opens up possibilities of an ancient root for the represented complex behaviour. The Late Devonian specimens here are generally smaller (0.4–4.3 mm wide) than the common range of the Mesozoic and Cenozoic counterparts (2–25 mm) (de Gibert, 1996; de Gibert et al., 1999). This may be explained by supposedly smaller crustacean progenitors in the Palaeozoic or stressed environmental conditions (brackish water) of the Wutong Formation. The varied sizes of Sinusichnus encountered in the Guodingshan hill (0.4–2.8 mm) possibly indicate the presence of a dynamic population composed of juveniles and adults, which is occasionally found in certain crustacean species that lack a planktonic larval stage (Forbes, 1973).
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5.3. Possible makers of Late Devonian Osculichnus Osculichnus discovered here in the Late Devonian is its second occurrence in the Palaeozoic since its report in the Early Devonian (Szrek et al., 2016). The Early Devonian Osculichnus has been assigned to lungfish based on its snout morphology in dorsal view, the deep, curved profile of the lower jaw in lateral view, and the presence of a pair of arches in the ventral margin of the upper lip (Szrek et al., 2016). Imprints of dentitions have not been observed in the Late Devonian Osculichnus from South China, especially for the well-preserved ones presumed to have been made firmer substrates in the Guodingshan hill locality. The deep, curved profile of the lower jaw is noted in certain cases (Fig. 4E), which resembles the Early Devonian ones (figs. 4, 5 in Szrek et al., 2016). The arched upper lobe, which is curved more steeply in the two sides (e.g., Fig. 5A), is indicative of a trapezoidal outline of the snout and a pair of arches in the ventral margin of the upper lip. The preservation locally of an exaggerated lower lobe (Fig. 5B) suggests essentially fleshy lips without prominent marginal dentition. These evidences fit into the morphological characteristics of extant lungfishes. Lobe-finned fishes (Sarcopterygii) were diversified in the Devonian and gave rise to tetrapods in the Late Devonian (Benton, 2005), with only a few extant aquatic examples (i.e., six species of lungfish and two species of Latimeria (coelacanths)). Modern lungfish are essentially
Fig. 6. The morphological types of Osculichnus from the Upper Devonian Wutong Formation in Wuhan, China. A–D represent Osculichnus with two elevated outer lobes and a central groove or cavity of various size, indicating probably the openness of the fish mouth; the two outer lobes may be similar in width (A and B) or in an enveloped style (C and D). E and F show Osculichnus with an elevated, trapezoidal or elliptical central lobe, in addition to the two elevated outer lobes; the central lobe may superimpose upon one of the outer lobes (F).
Fig. 7. Rose diagram showing the orientation of Osculichnus specimens in the Huangjintang locality. A. The three successive sandstone soles and groove marks on the third sandstone sole, the orientation of Osculichnus is measured by the direction perpendicular to the median groove. B. Rose diagram showing orientation of Osculichnus and its relationship with the flow direction, supposing that the main current direction had not much changed during the deposition of the three successive sandstone beds.
Fig. 8. Interpretation of the hunting and feeding process of the Late Devonian jawed fish based on fossil material from the Wutong Formation, Wuhan, China. A. The Osculichnus maker shows up-current swimming, successive plunging, and chemoreception of endobenthic prey. Sinusichnus sinuosus is abundant in the sediments, which are disturbed and interrupted by the fish plunges. B. The resulted preservation of hypichnial bilobate mounds and sinuous burrows on the sandstone sole. 110
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benthic omnivores, feeding on fish, insects, crustaceans, worms, mollusks, amphibians and plant matter based on their intestine or feacal materials (Kemp, 1986). Fossil lobe-finned fish probably also led a benthic living style according to the bedding surface scratches (Parundichna) made by swimming coelacanths (Simon et al., 2003). The feeding mechanism of Osculichnus makers here is similar to modern lungfish in adopting a suction feeding style for prey capture (Bemis and Lauder, 1986). In addition, body fossils of lungfish have been previously discovered in the Wutong Formation (Li et al., 1984). Therefore, lungfish may be promising candidates for Osculichnus producers in the Late Devonian, which is also evoked by Szrek et al. (2016) for Early Devonian Osculichnus. Osculichnus Demírcan and Uchman, 2010, along with the trapping and hunting traces like Piscichnus Feibel, 1987, represents unique fossil evidence of predator–prey interactions that take place near the sediment–water interface. With the discovery of more trace fossils exhibiting the hunting (praedichnia sensu Ekdale, 1985) and trapping (irretichnia sensu Lehane and Ekdale, 2013) behaviour, we may have a more comprehensive understanding of the repertoire of predator–prey interactions in the fossil record, which may help to get a fuller picture of the macroevolutionary trends of predator–prey interactions.
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6. Conclusions Osculichnus from the Upper Devonian Wutong Formation occurs as hypichnial bilobate mounds with two elevated outer lobes and a central groove/depression or convex lobe of various size. There is considerable morphological variety among Osculichnus specimens. Osculichnus is interpreted as the imprints of the upper and lower jaws of gnathostome makers when plunging into the sediments for endobenthic prey. The morphological characteristics (highly arched, U-shaped upper lobe and exaggerated lower lobe) of Osculichnus from South China indicate a trapezoidal outline of the snout and smooth, fleshy lips without prominent marginal dentition of the fish makers, which suggest lungfish as possible trace makers. The direction perpendicular to the central groove of Osculichnus specimens are oriented mostly at a small angle (about 30°) to the current flow indicated by groove marks, implying that the gnathostome fish maker of Osculichnus probably swam in the direction up flow. Osculichnus is in close association with the sinuous, branched trace Sinusichnus sinuosus. Late Devonian Sinusichnus sinuosus in this study is probably the oldest reported to date, with diameter 0.4–4.3 mm, wavelength 8.2–34.0 mm, amplitude 0.7–4.0 mm, which is generally smaller than Late Cretaceous to Miocene examples. Its trace maker is supposed to be some primitive, small decapod crustaceans that inhabited the stressed, brackish water of the estuarine environment of the Wutong Formation. Acknowledgements This work was supported by the National Natural Science Foundation of China [grant numbers 41290260, 41872034, 41702006] and the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan) [grant number 162301182730]. We thank Zhao Zhao and Zhen Shen from China University of Geosciences for their assistance in the field. We appreciate much the constructive and critical comments from Alfred Uchman and an anonymous reviewer, which aid in the further improvement of the manuscript. The Editor in Chief Thomas Algeo is acknowledged for suggestions on the manuscript. References Anderson, A.M., 1976. Fish trails from the early Permian of South Africa. Palaeontology 19, 397–409. Baumiller, T.K., Salamon, M.A., Gorzelak, P., Mooi, R., Messing, C.G., Gahn, F.J., 2010. Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution. Proc. Natl. Acad. Sci. U. S. A. 107, 5893–5896.
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