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Life in the Cambrian shallows: Exceptionally preserved arthropod and mollusk microfossils from the early Cambrian of Sweden
Geology ( IF 5.8 ) Pub Date : 2024-04-01 , DOI: 10.1130/g51829.1 Ben J. Slater 1
Geology ( IF 5.8 ) Pub Date : 2024-04-01 , DOI: 10.1130/g51829.1 Ben J. Slater 1
Affiliation
Burgess Shale–type (BST) Lagerstätten record an exceptional variety of Cambrian soft-bodied fauna, yet these deposits are typically restricted to outboard depositional settings >1000 km from the paleocoastline. For shallow, well-oxygenated shelf environments, our knowledge of non-mineralized animals (the majority of diversity) is severely limited, giving rise to substantial bias in our perception of Cambrian biotas. An alternate means of detecting soft-bodied Cambrian fauna, independent of paleobathymetry, is to use acid maceration to extract microscopic organic remains of non-mineralized animals, known as “small carbonaceous fossils” (SCFs). Here, a hitherto unknown diversity of Cambrian arthropod and mollusk remains are reported from shallow-marine sediments (Cambrian Stage 3 Mickwitzia Sandstone, Sweden). These microfossils comprise a variety of arthropod cuticles preserving sub-micron-scale anatomy alongside abundant radular mouthparts from mollusks—among the oldest known arthropod and molluscan SCFs on record. Significantly, at least three distinct types of fossil radula are identifiable (uniseriate, distichous, and polystichous forms), revealing that substantial diversification of the basic molluscan radula had already taken place by the early Cambrian. These cryptic elements of the biota—otherwise undetectable in such deposits—offer novel insights into Cambrian primary consumers as well as aspects of the fauna that are absent from deeper-water BST deposits.Cambrian Burgess Shale–type (BST) sites preserve a remarkable variety of non-mineralizing organisms, offering critical insights into the initial radiation of animal life (Butterfield, 1995). Despite their importance, BST deposits seem to be strongly biased toward deeper-water, off-shelf paleoenvironments (Conway Morris, 1989; Gaines, 2014). Ichnofossils reveal that a rich diversity of benthic invertebrates inhabited shallow-water sandy substrates during the Cambrian (Mángano and Buatois, 2017). Yet such sediments are seldom rich in body fossils outside depauperate shelly biotas and occasional coquina concentrations. In Cambrian shallower-water depositional settings, preservation of non-mineralized tissues or integument is rare. One exception to this are Doushantuo-type deposits, which preserve even labile sub-cellular details via phosphate permineralization (Bengtson and Zhao, 1997). Nevertheless, these sites are restricted to unusual environments of phosphogenesis during the Ediacaran–lower Cambrian and so fail to capture the broader ecosystem recorded at BST sites. As a general rule, high-energy, well-oxygenated and coarse-grained siliciclastic substrates that typify non-carbonate shallow-marine settings preclude the fossilization of delicate extracellular organic structures. Consequently, beyond the tracks and trails of benthos, we know little of the soft-bodied faunas that inhabited littoral environments early in animal evolution. Ideally, what is needed is a means of accessing body fossils of non-mineralized Cambrian metazoans from shallow-water and nearshore environments—not least since these are among the most biodiverse habitats today, but also because the early Paleozoic was characterized by extensively developed shallow epeiric seas on the continents, meaning that such environments represent an enormous portion of the available habitat to early animals.Fortunately, there is a way of ascertaining at least some measure of BST diversity, even in shallow-marine paleoenvironments. Outside Lagerstätten conditions, the carcasses of non-mineralized Cambrian animals and other organisms would quickly disintegrate and decay—yet recalcitrant fragments of these larger organisms are potentially preserved among organic microfossils (Slater and Bohlin, 2022). These microscopic, organically preserved components are known as “small carbonaceous fossils” (SCFs) (Butterfield and Harvey, 2012). In contrast to the macroscopic form of BST preservation, SCFs have relatively relaxed biostratinomic demands. Because they are small particles and were produced in large numbers, they can be preserved in a wide array of paleoenvironments and do not require the special sedimentary conditions needed for fully articulated macrofossils (Harvey and Butterfield, 2008, 2022; Harvey et al., 2011; Smith et al., 2015; Slater et al., 2017, 2018, 2020; Wallet et al., 2021). The challenge is to detect instances of SCF preservation in shallow-marine siliciclastic strata, thereby gradually revealing a more detailed picture of Cambrian shallow-water faunal communities.The Mickwitzia Sandstone member (Schmidtiellus mickwitzi Zone, Cambrian Stage 3) of the File Haidar Formation is an ~10-m-thick package of shallow marine sandstones, well exposed in sections at Lugnåsberget, south-central Sweden (Fig. 1; Fig. S1 in the Supplemental Material1). Sediments consist of thinly bedded medium- to coarse-grained heterolithic sandstones with mud-silt-clay interbeds (2–10 cm thick). Interbeds have been interpreted as finer material that settled from storm suspension, with a higher component of organic material (Jensen, 1997). A variety of sedimentary structures are present, including flute casts, gutter casts, wind-faceted pebbles, interference ripples, straight-crested ripples, and tool marks (e.g., Eophyton). Desiccation cracks and possible raindrop impressions point to emergent intervals. Sedimentation likely occurred in well-oxygenated conditions (ripples), a factor also suggested by the particularly diverse ichnofossil assemblage, indicating a motile, active benthos (e.g., Cruziana, Rusophycus, Diplocraterion, Palaeophycus, Gyrolithes, Olenichnus, Treptichnus, Rosselia; Jensen, 1997; Kesidis et al., 2019). The few body fossils known comprise a handful of incertae sedis shelly taxa: tubular Volborthella and Torellella, and cap-shaped Mobergella (elsewhere, the brachiopod Mickwitzia is also found in this unit).Fourteen (14) samples from silty interbeds (Fig. 1, sampled horizons 1 and 2) and mud clasts (horizon 3) of the Mickwitzia Sandstone member at Lugnås were subjected to a gentle HF acid maceration procedure outlined in Butterfield and Harvey (2012). Processing recovered well-preserved acritarchs (acanthomorphs and sphaeromorphs) alongside fragments of brachiopod cuticle and abundant cyanobacterial remains. Microfossils are encrusted with pyrite euhedra and display a yellow-orange coloration, indicating minimal thermal alteration. Among these background elements were numerous minute organically preserved metazoan fragments sourced from at least one arthropod taxon and several molluscan taxa.Recovered SCFs include sections of cuticle bearing ≤10 parallel strap-shaped extensions (50–200 µm length, 5–18 µm wide) connected to a basal membrane (Figs. 2A–2L). Each strap has a sclerotized central ridge (darker toward the basal attachment point) and is thinner and filmy toward the margins. Where complete, each strap terminates in a spatulate, finely fringed plumose structure (Figs. 2C and 2G–2L), which is recurved with respect to the strap. A separate population of cuticle fragments are notable for their dense fringes or tufts of setae (Figs. 2N–2X). Each seta is a few microns thick and tapers to a sharp tip, though in a minority of specimens they bear truncated or lobe-shaped termini (Fig. 2X). Spine-shaped portions of cuticle were also found covered with small denticles (Fig. 2M). These more complex cuticular fragments co-occur with portions of cuticle with a densely reticulate ornamentation (Fig. 2Y), elongate conical spines (Fig. 2AB), and sections of pock-marked cuticle that may represent the basal attachment point of spines in life (Fig. 2AC).Comparisons can be drawn with various arthropod fragments detected among SCFs elsewhere. For instance, cuticles with clumps of setae are reminiscent of the setal fringes and tufts borne on Cambrian arthropod mandible SCFs (Wallet et al., 2021, their fig. 8; Harvey and Butterfield, 2022, their fig. 1; Fig. S2) but could equally be derived from other regions of an arthropod cuticle. For simpler scalid-like elements (Figs. 2M and 2N), a more generic ecdysozoan origin cannot be excluded (see Smith et al., 2015). The parallel composites of straps (Figs. 2A–2L) are broadly comparable to the overall morphology exhibited in SCF “crustacean” filter plates (Wallet et al., 2021, their figs. 8A–8C; Harvey and Butterfield, 2022, their figs. 11B, 11C, 12C, and 12D; compare also the distal tips to Harvey and Butterfield, 2022, their figs. 12I and 12J; Fig. S2). If they are filter plates, they are unusual in that they are entirely blunt, lacking setae except for the distalmost tip. Alternatively, these arrays may represent clusters of sensory setae. The examples here substantially expand the known paleogeographic range of microscopic arthropod SCFs—the current scattering of reports being exclusively restricted to the paleocontinent Laurentia (Harvey and Butterfield, 2008, 2022; Harvey et al., 2012; Harvey and Pedder, 2013; Nowak et al., 2018; Wallet et al., 2021; Table S1).Acid extraction also produced SCFs that appear to represent three distinct morphologies of molluscan radula, comprising uniseriate, distichous, and polystichous types. The most common form (n = >30) consists of a uniseriate arc (80–350 µm length) of ≤7 blade-shaped teeth (Figs. 3J–3G). The teeth range in size between 5 and 290 µm and increase in size toward the anterior. Each tooth is connected to adjacent teeth by knob-shaped extensions at the base (Figs. 3L, 3O, 3R, and 3AB). Similar fossil radulae have been described among SCFs from younger Wuliuan-age strata, where they have been closely compared to the characteristic radulae of extant sacoglossan heterobranch gastropods (Slater, 2023). The older examples here push back the known range of such distinctive uniseriate radulae by ~10 m.y. and, along with the other radula types detected here, represent the oldest known radulae on record (though see Nagovitsin, 2011, his figure 25K, which appears to be an undescribed radula fragment from Terreneuvian strata).Co-occurring with the uniseriate forms are carbonaceous straps (n = 11; 5–12 µm wide, up to 220 µm length) fringed by a row of equally spaced teeth along a single margin (Figs. 3A–3G). The teeth range from 5 to 10 µm from base to tip and are 5–45 µm wide at the base and vary between hook-shaped (Fig. 3F) to recumbent blade-shaped forms (Fig. 3A), but each isolated strap bears teeth of a consistent morphology. In one specimen, two adjacent straps are seen in articulation (Fig. 3G). In terms of affinity, these microfossils resemble dispersed fragments of a compound radula, whereby each of the serrated straps represent a disarticulated column of teeth sourced from a polystichous molluscan radula, in this case adapted for deposit feeding via rasping and/or scraping (Pastorino and Scarabino, 2008, their figs. 15–18; Montroni et al., 2019, their figs. 4 and 5A).A third, rarer morphotype (n = 2) comprises what appear to be semi-articulated portions of a distichous radula (Figs. 3H and 3I). The closest comparison is found among the distichous hooks seen in extant neomenioid aplacophoran radulae (e.g., Scheltema et al., 2003, their fig. 11C). SCFs described as “triaxial elements” from the Cambrian Mahto Formation (Alberta, Canada; Butterfield, 2008, his figs. 8.1 and 8.2) exhibit a somewhat similar construction but form much larger arrays.From an evolutionary perspective, shallow-marine environments are interesting because they appear to have functioned as “cradles” for the evolution of clades that only later expanded to deeper waters—for instance, Phanerozoic marine communities show a distinct pattern of nearshore origination followed by offshore displacement (Jablonski et al., 1983). Shallow-marine settings are typified by higher nutrient input, high productivity (photic zone), and heterogeneous benthic settings (macroalgae, and, in carbonate settings, reefs). Animals living there must contend with UV exposure, tides, storms, and desiccation—factors that mean Cambrian shallow-marine faunas are likely to differ from those found in off-shelf BST Lagerstätten.Evidently, the depositional environments reflected among BST Lagerstätten vary to some degree—for example, core material from the Yu’anshan Formation (China) adjacent to the Chengjiang biota has recently been interpreted to represent offshore-directed hyperpycnal flows, presumably sourced from deltaic muds (Saleh et al., 2022). Even so, recovery of microscopic arthropod and molluscan fossils here shows that SCF sampling can reveal cryptic non-mineralized aspects of the fauna in shallow-water and littoral depositional environments that are simply not captured in Cambrian BST deposits. In particular, sampling has uncovered an unexpected diversity of molluscan benthic herbivores, which are major primary consumers in modern trophic systems but are currently dramatically underrepresented in Cambrian BST sites globally (Vermeij and Lindberg, 2000). Indeed, the relative rarity of primary consumers from BST sites may simply reflect a tendency for grazers to have lived in well-oxygenated, shallow waters, where the photosynthetic autotrophs they fed upon were abundant.Detection of these exceptionally preserved Cambrian animal remains raises the question of why such detailed fossilization of non-mineralized organisms occurs within what is otherwise a poorly fossiliferous, coarse-grained sandstone. A shallow burial depth and quiescent tectonic history has meant these sediments have been subject to remarkably little thermal alteration (a prerequisite of organic preservation). Yet there is little to distinguish this unit from other Paleozoic marine sandstones. Notably, however, the silty partings from which the microfossils were extracted are particularly rich in the clay mineral kaolinite (Lindström and Vortisch, 1978). At Lugnås, the Mickwitzia Sandstone rests directly upon a kaolinized gneissic basement, and although the sandstone beds are relatively clean, finer-grained interbeds are rich in this clay material. Kaolinite is noteworthy for its association with the macroscopic variety of BST preservation (Butterfield, 1995; Anderson et al., 2021; Woltz et al., 2023) and has been documented to produce an early diagenetic tanning effect on cuticular tissues in actualistic taphonomic experiments (Wilson and Butterfield, 2014). Moreover, the paleotropical distribution of BST sites has been linked to kaolinite production in tropical weathering regimes (Anderson et al., 2021), yet, curiously, Sweden sat at high southern paleolatitudes during the Cambrian within the paleocontinent Baltica (Slater et al., 2017). Organic microfossils and BST macrofossils are both essentially carbonaceous compressions, albeit at different scales, and their preservation may therefore share certain features (Anderson et al., 2011; Slater and Bohlin, 2022). It is plausible that at Lugnås, this clay matrix was responsible for postponing autolytic degradation (Butterfield, 1995; Wilson and Butterfield, 2014), facilitating the preservation of delicate carbonaceous integuments, including animal mouthparts and cuticles.SCFs offer a fresh perspective on shallow-marine ecosystems from a time when Phanerozoic-style ecology was first emerging. In contrast to BST Lagerstätten, SCFs appear to preserve across an exceedingly broad paleobathymetric range, including even mud-cracked shales (Pika Formation, Alberta, Canada; Butterfield and Harvey, 2011; Smith et al., 2015). Low-manipulation SCF processing of the lower Cambrian Mickwitzia Sandstone has yielded exceptionally preserved microanatomical remains of soft-bodied arthropods as well as the feeding apparatus of at least three types of mollusk. Though current records represent only a limited sampling, recovered SCFs already allude to important faunal differences between Cambrian ecosystems in epeiric, littoral settings and those of the better-known deeper-water biotas documented in deposits like the Burgess Shale. For instance, an early Cambrian diversification of molluscan feeding ecologies is not apparent from contemporaneous BST deposits. Understanding how shallow-marine ecosystems developed in the earliest Phanerozoic requires enhanced accounting of the non-mineralized aspects of the fauna. Clearly, the discovery of non-mineralized metazoan remains in clay-rich interbeds here provides a useful search image and opens up the prospect of exploring soft-bodied biotas in equivalent shallow-water sandstone packages that are common throughout the Cambrian System globally.Slater is supported by the Swedish Research Council (VR 2020-03314). I thank Thomas Harvey (Leicester University) and three anonymous reviewers for detailed, helpful reviews.
更新日期：2024-04-05
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