Surfing in and on Microbial Mats: Oxygen-Related Behavior of A

https://doi.org/10.1130/G46474.1

Manuscript received 7 May 2019 Revised manuscript received 11 August 2019 Manuscript accepted 17 August 2019

Surfing in and on microbial mats: Oxygen-related behavior of a terminal Ediacaran bilaterian animal Shuhai Xiao1*, Zhe Chen2, Chuanming Zhou2 and Xunlai Yuan2* 1Department of Geosciences, Virginia Tech, Blacksburg, Virginia 24060, USA 2State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China

ABSTRACT and they are spaced with a gap in between Geochemical evidence suggests that terminal Ediacaran (ca. 551–539 Ma) oceans experi- (gap length 10.9–102.2 mm; Table DR1). Gaps enced expansive anoxia and dynamic redox conditions, which are expected to have impacted are featureless and flush with the bedding sur- animal distribution and behaviors. However, fossil evidence for oxygen-related behaviors of face. Segments are 13.0–84.0 mm in length terminal Ediacaran animals is poorly documented. Here, we report a terminal Ediacaran trace and 3.4–8.9 mm in maximum width, straight fossil that records redox-regulated behaviors. This trace fossil, Yichnus levis new ichnogenus (#1–2 in Fig. 2A) or slightly curved (arrow- and new ichnospecies, consists of short and uniserially aligned segments of horizontal burrows head in Fig. 2A), generally smooth (Figs. 2A that are closely associated with microbial mats. Thin-section analysis shows that the trace- and 3A), and taper on both ends. Although making animal moved repeatedly in and out of microbial mats, with mat-burrowing intervals segments can be curved, the ends of neigh- interspersed by epibenthic intermissions. This animal is hypothesized to have been a bilaterian boring segments in a chain match perfectly in exploring an oxygen oasis in microbial mats. Such intermittent burrowing behavior reflects orientation (#1–6 in Fig. 2B). challenging and dynamic redox conditions in both the water column and microbial mats, The segments are preserved as full reliefs highlighting the close relationship between terminal Ediacaran animals and redox dynamics. and can be split with the overlying or underly- ing beds, with the corresponding counterpart INTRODUCTION GSA Data Repository1 for the systematic preserving a negative mold (Figs. 2A, 2B, and Emerging geochemical data indicate an epi- paleontology; ZooBank urn:lsid:zoobank. 2E–2H). Observations made in longitudinal and sode of expansive oceanic anoxia in the terminal org:pub:991964F6-DB19–493A-A91D- transverse thin sections cut perpendicular to the Ediacaran Period (Evans et al., 2018; Tostevin BFB72973B6B1). Y. levis is preserved in bedding plane suggest (1) they are preserved in et al., 2018; Wei et al., 2018; Zhang et al., 2018), limestone of the terminal Ediacaran Shiban- close association with organic- and clay-rich cal- with spatially and temporally dynamic redox tan Member of the Dengying Formation at careous microlaminites interpreted as microbial conditions in shallow oceans (Wood et al., 2015). Wuhe in the Yangtze Gorges area of South mats (labeled “m” in Figs. 2E–2G and 3C–3F); It has been shown that such dynamic redox con- China (Fig. 1; Fig. DR1 in the Data Reposi- (2) they are filled with micritic and intraclastic ditions influenced the distribution of animals tory). Specimens were collected at two hori- sediments, but with a greater amount of cement (Tostevin et al., 2016). However, it has not been zons, ∼20 m and ∼70 m above the base of the than in the peloidal and intraclastic sediment in thoroughly investigated how terminal Ediacaran Shibantan Member. Y. levis is the only trace the matrix (Figs. 3C–3F); (3) they are circular to redox dynamics impacted animal behaviors. Ter- fossil thus far found at the lower horizon, but oblate in transverse cross section (Figs. 2H, 3C, minal Ediacaran ichnofossils are ideal to address it co-occurs with other as-yet-undescribed ich- and 3D), indicating that the burrows experienced this question because, as a record of animal be- notaxa at the upper horizon. Sedimentary fea- some degrees of postdepositional compaction; haviors (Buatois et al., 2016, 2017; Gehling and tures indicate that the Shibantan Member was and (4) there is no discernible lining or back- Droser, 2018), they are often exceptionally pre- deposited on a carbonate shelf, between fair- filled structures. served due to low levels of bioturbation (Droser weather and storm wave base (Meyer et al., To determine whether segments are con- et al., 2002). Here, we describe a new trace fossil 2014). Radiometric dates and biostratigraphic nected with each other through unexposed in- that bears on the behavior of terminal Ediacaran data constrain the Shibantan Member to be trastratal burrows, one of the specimens was bilaterian animals in response to redox dynamics. 551–538 Ma (see the Data Repository). cut across the gap between two segments. No Yichnus levis consists of disconnected fu- intrastratal structure was found in either the FOSSIL DESCRIPTION siform or spindle-shaped segments that are part or the counterpart slab (Figs. 2C and 2D). The fossil is described as Yichnus levis new either isolated (arrowhead in Fig. 2A) or This was also obvious upon close inspection of ichnogenus and new ichnospecies (see the aligned to form a curved uniserial chain (#1–6 the terminal ends of the segment: On both the in Figs. 2A and 2B). As many as six fusiform part and counterpart slabs, the segment appears *E-mails: [email protected]; [email protected]. segments are preserved in a chain (Fig. 2B), to direct away from the sediment (Figs. 2A and

1GSA Data Repository item 2019367, stratigraphic setting, methods, and systematic paleontology, is available online at http://www.geosociety.org/ datarepository/2019/, or on request from [email protected].

CITATION: Xiao, S., Chen, Z., Zhou, C., and Yuan, X., 2019, Surfing in and on microbial mats: Oxygen-related behavior of a terminal Ediacaran bilaterian animal: Geology, v. 47, p. 1054–1058, https://doi.org/10.1130/G46474.1

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/47/11/1054/4852010/1054.pdf by guest on 28 September 2021 111°E Shuijingtuo Fm surface, with segments exposed in troughs but N 526.4±5.4 Ma Cambrian SSFs buried beneath crests (e.g., Jensen, 1997, his Cam. Yanjiahe Fm Ediacaran-Cambrian Tarim boundary (~539 Ma) North figure 46A). Similarly, apparently disjointed China burrow segments could result from a continu-

Mbr ous intrastratal burrow undulating in and out of Baimatuo Sinotubulites Yangtze Cathaysia the plane of preservation; this model has been proposed to explain the apparently disjointed 31°10'N 111°15'E 31°10'N Vendotaenia sp. Ar-Pt burrows of Treptichnus (Archer and Maples,

Y. levis 1984; Buatois and Mángano, 1993; Jensen

Dengying Fm Ediacara-type fossils et al., 2000). When these continuous burrows are Huangling & trace fossils Shibantan Mbr split, they may appear disjointed (Figs. DR2A– anticline Y. levis DR2B). However, combined observation of the Ediacaran 31°N 31°N HMJ part and counterpart should still reveal a contin- 551.1±0.7 Ma Miaohe biota uous burrow, whereas our thin-section observa- Ar-Pt tion revealed that the burrow segments of Y. levis are genuinely disjointed. Thus, the stratinomic Acanthomorphic acritarchs models that could make continuous burrows ap- 632.5±0.5 Ma pear discontinuous can be conclusively ruled out 30°50'N Zigui 30°50'N Doushantuo Fm 635.2±0.6 Ma for Y. levis. A third possibility is that the burrow Wuhe . 50 m 10 km Yangtze Yichang Nantuo Fm segments of Y. levis were made discontinuous River Cry by erosional processes (Figs. DR2C–DR2D). 0 m However, erosion would likely partially or en- Ar-Pt tirely remove microbial mats surrounding the chert and dolostone diamictite Cryogenian- Huangling Archean- Fault phosphorite burrow, whereas Y. levis is surrounded by in- Ediacaran Granite Paleoproterozoic ABblack shale limestone tact microbial mats above and below. Also, if a burrow were erosionally exposed before it was Figure 1. Geological map and stratigraphic column. (A) Generalized geological map of filled, it would be cast from above and preserved Yangtze Gorges area, China, showing distribution of Ediacaran strata and fossil location at Wuhe (star). Inset map shows major tectonic units (Yangtze, Cathaysia, North China, and as semireliefs rather than full reliefs. Finally, Tarim cratons) and Yangtze Gorges area (rectangle). (B) Stratigraphic column of Ediacaran to completely remove a segment of horizontal Doushantuo and Dengying Formations, showing stratigraphic range of fossils. Stars mark burrow, several millimeters of strata would have stratigraphic horizons of Yichnus levis. Mbr—Member; Fm—Formation; HMJ—Hamajing been differentially eroded, considering the size Member; SSF—small shelly fossil; Cry.—Cryogenian; Cam.—Cambrian. Zircon U-Pb ages in Shuijingtuo Formation are from Okada et al. (2014), and those in Doushantuo Formation of Y. levis. However, there is no evidence for are from Condon et al. (2005). erosion of this magnitude; the bedding surface is flat and smooth, largely defined by microbial laminae undisrupted by erosion. Thus, the most 2B). In other words, the segment terminates uniserial chains, and when multiple chains are likely scenario is that the burrow segments were at both ends, rather than going off-plane into found in the same bedding surface, the chains originally disjointed when they were made (Fig. either the part or counterpart slab; the termi- do not have consistent orientation (Fig. 3A), DR2E). Such short burrow segments with an nation is also clearly seen in longitudinal thin inconsistent with cylindrical body fossils that opening to the water column can also be more sections (Figs. 3E and 3F). Thus, segments are would be oriented by waves or currents. Impor- easily filled and cast with sediments than long not physically connected through intrastratal tantly, although microbial laminae warp around and continuous burrows. burrows. the segments because of compaction, there are Finally, the consistent occurrence of Y. levis cases where microbial laminae are truncated by burrow segments with clay- and organic-rich mi- INTERPRETATION the segments (arrowhead in Fig. 3C), unambigu- crobial laminites indicates interactions between The segments of Y. levis are interpreted as ously supporting a trace fossil interpretation. the trace maker and microbial mat. Such an as- trace fossils, and specifically endogenic bur- These observations, when considered with the sociation is also seen in other burrows from the rows, rather than sedimentary structures or full-relief preservation, clearly identify the seg- Shibantan Member (e.g., Chen et al., 2013, their body fossils. Sedimentary structures such as ments as endogenic burrows. figures 2C–2I; Meyer et al., 2014, their figures syneresis cracks, tool marks, and some mi- The alignment of burrow segments suggests 5–8; Chen et al., 2018, their figure S1A). The crobially induced sedimentary structures can that a burrow chain was made by the same indi- observations that the burrow segments occur in be spindle in shape, but they tend to be pre- vidual animal, not by different individuals oper- millimeter-thick microlaminites (Figs. 2E–2F, served as semireliefs with a U- or V-shaped ating separately and autonomously. Further, the 3C, and 3D) and were originally disjointed sug- cross section. In contrast, Y. levis is preserved chain was probably produced by a bilaterian ani- gest that the trace maker interacted with live mi- as full reliefs with an oblate cross section. It mal capable of directional movement, perhaps crobial mats at or near the mat-water interface. is closely associated with microbial mats and within a relatively short amount of time given Taken together, our observations suggest filled with well-cemented sediment, identical the coherent course of the chain. that the trace maker must have surfed just below to documented trace fossil preservation in the We further interpret that the burrow segments and above the mat-water interface, rather than Shibantan Member (e.g., Chen et al., 2013, their were originally disjointed when they were pro- cruising intrastratally and deeply at the inter- figures 2C–2F; Meyer et al., 2014, their figures duced (Fig. DR2). Some continuous burrows face between a buried/dead microbial mat and 5–9; Chen et al., 2018, their figure S1). The bur- can appear disjointed due to biostratinomic or overlying layers of intraclastic sediment (as in row segments vary widely in length, inconsistent erosional processes. For example, continuous the case of Curvolithus; Buatois et al., 1998). with body fossils, which would have consistent horizontal burrows of Palaeophycus imbricatus The trace maker penetrated and burrowed into widths and lengths. They are aligned to form can appear discontinuous on rippled bedding live microbial mat, produced a short and unlined

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[O2] of fully saturated Ediacaran seawater was comparable to that of oxygen minimum zones (OMZs) in modern oceans (Sperling et al., 2013). Such redox conditions can support many animals (Mills et al., 2014), but it would be a challenge for animals engaged in energetically demanding activities such as carnivorous predation and burrowing (Sperling et al., 2013). Furthermore, with >20% of ocean floor bathed in anoxic water (Tostevin et al., 2018; Zhang et al., 2018), a percentage that is two orders of magnitude greater than in the modern ocean (0.1%; Helly and Levin, 2004), significant por- tions of terminal Ediacaran continental shelves were likely affected by anoxia. As in the modern ocean, anoxic seawater likely periodically flooded terminal Ediacaran outer shelves that intersected with the OMZ. Indeed, anoxia and dynamic redox conditions have been documented in terminal Ediacaran shelf deposits (Wood et al., 2015), and they have been shown to limit animal distribution (Darroch et al., 2015; Wood et al., 2015; Tostevin et al., 2016). Thus, termi- Figure 2. Bedding surface and vertical cross-sectional views of Yichnus levis, Nanjing Institute nal Ediacaran animals were likely compelled to of Geology and Paleontology specimen NIGP-169664. (A,B) Bottom (A) and top (B) bedding explore O2 oasis in light of such redox dynamics surface views of part and counterpart slabs. Six straight or slightly curved burrow segments in the water column. (numbered) are aligned to form a uniserial chain. Isolated and curved burrow segment is also Cyanobacterial microbial mats could pro- present (arrowheads). Oblique lighting from top end of images. Dotted lines with labels mark approximate positions where vertical cross sections (C–E, G–H) were made. (C,D) Part and vide, if only temporally, an O2 oasis for these counterpart, showing no unexposed intrastratal burrow in the gap between neighboring burrow animals. However, only small and mobile ani- segments. Arrowhead in D points to burrow segment a short distance from the cut surface mals would have been able and compelled to (hence, out of focus). (E,H) Part and counterpart, showing full-relief preservation (arrowhead take advantage of this O2 oasis because of their in H) and close association with microbial laminae (“m”). (F) Magnification of rectangle in E, high body-mass-specific metabolic rate, as well showing details of microbial laminae (“m”) and peloidal/intraclastic layer (“p”). (G) Transverse section showing negative mold on the bed sole. Black arrowheads (in E and G) bracket burrow as the strong diurnal redox dynamics and mil- width. C and E–G are thin sections, and D and H are polished slabs. In Figures 2 and 3, red limeter thickness of microbial mats (Fig. 4). symbols next to the subpanel labels denote orientations (┴: bottom bedding surface view; ┬: Empirical measurements show that dissolved top bedding surface view; ↑: stratigraphic-up direction). [O2] in modern cyanobacterial mats can reach 4–8 PAL during the day, but it drops to es- tunnel within the mat, emerged out of the mat, interaction but the latter is animal-sediment in- sentially 0 PAL during the night, when a sul- and then swam or moved epibenthically on the teraction. In ecological terms, live mats offer fidic environment develops (Canfield and des mat, but left no discernible epigenic trails or food and a dynamic redox microenvironment Marais, 1993; Wieland and Kühl, 2006; Gingras tracks presumably because of its inability to related to the diurnal cycle of photosynthesis, et al., 2011). These remarkable redox dynamics

produce epigenic traces on the relatively thick whereas dead mats offer only food and prob- are also confirmed by the observation of [O2] and firm mat (Evans et al., 2019). This cycle ably a hostile redox microenvironment (Gingras bubbles in cyanobacterial mats during the day

may have been repeated to produce a chain of et al., 2011). (Bosak et al., 2010), which indicate [O2] > 5 burrow segments (Animation DR1). Because The nature of the animal-mat interaction rep- PAL, and by diffusion-reaction models param-

the burrows are unlined, they are regarded as resented by Y. levis is uncertain. Considering eterized with O2 production and consumption locomotion traces rather than stabilized dwell- that the Shibantan Member was deposited in the rates as measured in modern microbial mats ing structures. The pattern of movement, with photic zone (Meyer et al., 2014), the microbial (Revsbech et al., 1986). Thus, although cya-

the trace maker periodically moving in and out mat was probably constructed by O2-produc- nobacterial mats can provide sufficient 2O to of the microbial mat (hereafter “in-and-out be- ing cyanobacteria. We thus hypothesize that the support millimeter-sized mobile animals during havior”), represents relatively complex locomo- trace maker was mining the microbial mat pri- the day, they are a challenging microenviron-

tion behaviors and close ecological interactions marily for O2 (Meyer et al., 2014) and perhaps ment for any animals that need even a moderate

between terminal Ediacaran bilaterian animals secondarily for food (e.g., Gehling and Droser, amount of O2 throughout the light-dark cycle. and microbial mats. 2018), if the lack of back-filled structures and The combined redox challenges and dynamics burrow lining was a taphonomic artifact. in the water column and microbial mats may DISCUSSION We further hypothesize that the in-and-out have driven the in-and-out behavior as recorded Our interpretation of Y. levis suggests that behavior as recorded by Y. levis reflects the dy- by Y. levis. the trace maker had biotic interactions with live namic redox conditions in the water column microbial mats, rather than mining dead organic (Wood et al., 2015) and in the microbial mats CONCLUSIONS matter in buried microbial mats. This distinction (Gingras et al., 2011). Ediacaran atmospheric Building upon previous observations of the

is important because the former is animal-mat pO2 levels are uncertain, but they were likely close association between terminal Ediacaran

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1 ater column

0 tW ive ma tical scale (mm)

r -1 tL Ve

-2

night day -3 Sediment or dead ma 0 0.1 1.0 10 Dissolved [O2], PAL

Figure 4. Schematic diagram showing diur-

nal change in dissolved [O2] profiles within a live cyanobacterial mat based on empirical measurements (Canfield and des Marais, 1993; Wieland and Kühl, 2006; Gingras et al.,

2011), adjusted to ambient pO2 = 0.1 present atmospheric level (PAL) in Ediacaran (Lu et al., 2018) and mat thickness of 1 mm. Redox con- dition is more favorable in mat during day and in water column during night. Spatial and tem- poral redox dynamics of water column (Wood et al., 2015; Tostevin et al., 2016) are not shown in diagram, but such dynamics mean that simple diurnal migration in and out of microbial mat is not expected for trace maker of Yichnus levis. Figure 3. Bedding surface and vertical cross-sectional views of Yichnus levis, Nanjing Institute of Geology and Paleontology specimen NIGP-169665. (A) Top bedding surface view. Oblique lighting from top left of image. At least 13 burrow segments (numbered) are seen on this slab. ACKNOWLEDGMENTS Some burrow segments (#10) are curved, whereas others are mostly straight (#4) or slightly This research was funded by the National Science curved (#7). Segments 1–2, 4–6, and 11–12 appear to form three uniserial chains, which do not Foundation (EAR-1528553), the National Geographic share a preferred orientation. (B) Enlarged view of rectangle in A. (C–F) Thin-section images Society (9564–14), and the Chinese Academy of Sci- of cross sections cut perpendicular to bedding surface and along labeled dotted lines in B, ences (XDB18000000, QYZDJ-SSW-DQC009, and showing transverse sections of burrow segments 1 and 4, as well as longitudinal sections of XDB26000000). We thank Xiang Chen for field assis- burrow segments 1 and 3. Burrow segments end terminally (black arrowheads in E–F) and do tance, and three anonymous reviewers for constructive not continue as unexposed intrastratal burrows. Microbial laminae are truncated by burrows comments. (black arrowhead in C). REFERENCES CITED Archer, A.W., and Maples, C.G., 1984, Trace-fossil burrows and microbial mats (Meyer et al., could be mitigated by mobile bilaterians with distribution across a marine-to-nonmarine gradi- 2014), we show that uniserially aligned burrows the capability to explore dynamic and localized ent in the Pennsylvanian of southwestern Indiana: of Yichnus levis were produced by a bilaterian O2 oases, which together with the heterogenic Journal of Paleontology, v. 58, p. 448–466. animal that developed an in-and-out behavior, distribution of food (Budd and Jensen, 2017), Boag, T.H., Stockey, R.G., Elder, L.E., Hull, P.M., interacted with live microbial mats, and repeat- may have been a stimulus for the evolution of and Sperling, E.A., 2018, Oxygen, temperature and the deep-marine stenothermal cradle of Edia- edly burrowed into and emerged out of live mi- animal mobility. This hypothesis can be fur- caran evolution: Proceedings, Biological Scienc- crobial mats. We hypothesize that the in-and-out ther tested through a comprehensive analysis es, v. 285, p. 20181724, https://doi.org/10.1098/ behavior was an evolutionary innovation driven of terminal Ediacaran trace fossils exhibiting rspb.2018.1724. by the dynamic redox conditions in both the potential signs of in-and-out behavior (Jensen Bosak, T., Bush, J.W.M., Flynn, M.R., Liang, B., Ono, S., Petroff, A.P., and Sim, M.S., 2010, Formation water column and the microbial mat. Dynamic et al., 2000; Jensen and Runnegar, 2005; Meyer and stability of oxygen-rich bubbles that shape redox conditions were a challenge for early et al., 2014) to demonstrate the global scale of photosynthetic mats: Geobiology, v. 8, p. 45–55, animals (Boag et al., 2018), but this challenge this innovation. https://doi.org/10.1111/j .1472-4669.2009.00227.x .

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