Exceptional Preservation in the Later Cambrian: Insights into a Cryptic Phase of the Early Evolution of Animals
Palaeoscience Research Centre, School of Environmental and Rural Science, University of New England, Armidale NSW 2351, Australia.
The Cambrian system is unusually rich in Konservat-Lagerstätten (Allisson & Briggs, 1993; Muscente et al., 2017) — strata yielding fossils of both biomineralizing and non-biomineralizing organisms — which have dramatically improved our understanding of the Cambrian Explosion and the complexification of early marine ecosystems it was associated with. However, these remarkable deposits are not evenly distributed in space and time, most occurring within the preliminary Cambrian Series 2 and 3 (up to Drumian Stage) of North America (Laurentia) and South China (Fig. 1A). Elsewhere, the fossil record of non-or weakly-biomineralizing macroscopic animals for this lower-middle Cambrian interval is essentially restricted to the Emu Bay Shale biota (Stage 4) in Gondwana (Paterson et al., 2016) and the Sinsk biota (Stage 3/Stage 4 boundary) in Siberia (Ivantsov et al., 2005), while it is virtually inexistent in Baltica. Likewise, exceptional preservation is comparatively rare in the Terreneuvian and Furongian, although in the latter series this apparent rarity might in part be due to a lack of interest for the time interval it represents, the significance of which in the history of life being frequently underestimated.
This contribution will review the fossil record of non- or weakly-biomineralizing animals from the Guzhangian to the end of the Furongian, a time interval spanning the last 15 million years of the Cambrian and informally called the ‘later Cambrian' hereafter. Including the Guzhangian Stage in this review is motivated by the facts that 1) discussions on Cambrian exceptionally-preserved macrofaunas (EPFs) never consider post-Drumian data, and 2) this stage partially overlaps what used to be regarded by some workers as the basal part of the upper Cambrian Series in countries like Sweden or the U.S.A (Babcock et al., 2014). Likewise, exceptional preservation refers herein to the preservation of organisms either exclusively composed of labile tissues, or possessing weakly biomineralized skeletal elements easily disarticulated or fragmented after death in normal marine settings (e.g. aglaspidid arthropods, Lerosey-Aubril et al., 2017; palaeoscolecid worms, Martin et al., 2016).Lastly,EPFs(and by extension the Lagerstätten they originate from)are assigned to one of the following categories based on their richness in non- or weakly-biomineralizing species: limited (<10), diverse (10—100), and prolific (>100).
Figure 1 Stratigraphical and paleogeographical distributions of later Cambrian Lagerstätten. (A) Stratigraphical distribution of Lagerstätten in the early Palaeozoic,with a special emphasize on the later Cambrian (Guzhangian to Stage 10).The 3 categories of Lagerstätten (limited, diverse, and prolific) are represented by different line thicknesses. Lines extending throughout the later Cambrian correspond to strata with poorly constrained ages.(B)Palaeogeographical distribution of Lagerstätten in the later Cambrian. Note the essentially intertropical distribution of the localities. Question marks indicate strata with poorly constrained ages.
Exceptionally-preserved fossils are known from 17 later Cambrian deposits around the world(Fig.1).More than half of these Lagerstätten are in Laurentia(10),the remaining ones being evenly distributed between Gondwana (2), Siberia (3), and South China (2);once again, no macroscopic remarkable assemblage has been described from Baltica. Interestingly, later Cambrian Lagerstätten also share with pre-Guzhangian ones an essentially intertropical paleogeographic distribution (Fig. 1B), but this is where similarities end. In term of diversity, there is no equivalent to the Chengjiang or Burgess Shale faunas (i.e. prolific EPFs) in the later Cambrian, and only 3 EPFs of that age can be regarded as diverse:the Guzhangian Weeks fauna (USA; Lerosey-Aubril et al., 2014), and the Jiangshanian St. Lawrence (USA; Raasch, 1939; Hesselbo, 1992) and Guole (South China; Zhu et al., 2016) faunas. All the others are limited EPFs (for now! ) — several of them actually comprise a single ‘soft'-bodied species, in rare cases represented by a single specimen only (e.g. Beecher, 1901; Vaccari et al., 2004). A notable proportion of the later Cambrian Lagerstätten were deposited in more proximal environments(foreshore to upper offshore), and are composed of coarser-grained sediments compared to the typical outer-shelf/upper-slope Burgess Shale-type deposits of the Cambrian Series 2 and 3. However, these more distal depositional settings are also represented, for instances by the Weeks (Lerosey-Aubril et al., 2014), Sandu (Zhu et al., 2016), and Santa Rosita (Vaccari et al., 2004) formations or the lower McKay Group (Lerosey-Aubril et al., 2017). The preservation of most of these later Cambrian fossils has not been studied in details, but a couple of observations are worth mentioning: 1) a true Burgess Shale-type preservation (i.e. as carbon-films, rather than pyrite or even more derived diagenetic products) has only been observed once in a comb jelly from the lower McKay Group (Lerosey-Aubril et al., 2017); 2) a specular ‘Ediacaran-type'preservation has been documented in 3 later Cambrian Lagerstätten representative of proximal, shallow-water settings (e.g. Collette & Hagadorn, 2010). As to the taxa preserved, a great majority of them are arthropods, which is not surprising considering that these organisms have been dominating virtually all ecosystems on the planet since the beginning of the Palaeozoic Era. Yet, the most commonly found exceptionally-preserved arthropods in these deposits are aglaspidids and euthycarcinoids, 2 groups that actually first evolved in the later Cambrian (Collette & Hagadorn, 2010; Lerosey-Aubril et al., 2013). These oldest euthycarcinoid occurrences are particularly interesting — one demonstrates that the group initially lived in open-marine habitats (Vaccari et al., 2004), while the others illustrate the very first attempts of animals to explore terrestrial environments (e.g. Collette & Hagadorn, 2010). As to aglaspidids, they document the presence of a second diversification pulse of artiopodan arthropods in the Cambrian, which is associated with the emergence of their superclass, the Vicissicaudata. Artiopodan diversification pattern is therefore unusual, for it comprises two diversification phases only separated by a ca.20 Ma interval(i.e.trilobites and allies in the Cambrian Series 2, vicissicaudatans in the later Cambrian), which is about twice less than the time interval separating the GOBE from the Cambrian Explosion. Resting trace fossils of chasmataspidids from the Hickory Sandstone of Texas (USA; Dunlop et al., 2004) also demonstrates that Euchelicerata (spiders and allies), the second most diverse arthropod group in modern-day ecosystems, likely evolved during Guzhangian times. Lastly, Furongian strata of the Wonewoc (? ) and St. Lawrence formations in Wisconsin (USA) have yielded the oldest phyllocarid malacostracan (Crustacea; Collette & Hagadorn, 2010), confirming that the later Cambrian was an important time of morphological innovation for the phylum Arthropoda. As to the other phyla represented in later Cambrian EPFs, cnidarians and priapulid worms (palaeoscolecids) are the most common after arthropods (e.g. Barskov & Zhuravlev, 1988 and references therein).
This rapid overview of exceptional preservation in later Cambrian speaks to the great potential of these strata for complementing our understanding of the evolution of non- or weakly-biomineralizing animals during the early Palaeozoic. Later Cambrian EPFs have been found in various countries worldwide (i.e. Argentina, Australia, Canada, China, Russia, USA), but most of these findings were made during early geological mapping works some 70 (or more) years ago, and the localities have remained virtually unvisited since then. As demonstrated by the recent discoveries of various Ordovician Lagerstätten (e.g. Van Roy et al., 2015), our understanding of exceptional preservation through time is largely the fruit of collecting effort, which is itself tightly related to the putative scientific significance of a time interval in the history of Life. Lying in-between the Cambrian Explosion and the GOBE, the later Cambrian is critical to our understanding of both the diversification dynamics of metazoans during the early Palaeozoic and the major transition between Cambrian and Palaeozoic Evolutionary Faunas. As illustrated above with arthropods, it was also a time of evolutionary experiments that led to the emergence of major components of the Palaeozoic Evolutionary Fauna, as well as groups with more limited evolutionary successes (e.g. Lerosey-Aubril, 2015). Lastly, the later Cambrian is associated with major ecological events, such as an important diversification of planktonic life (Servais et al., 2016) or the first incursions of animals on lands. These various aspects should motivate the search for the kind of high-resolution data only EPFs can provide, and the main goal of the present contribution is to provide a starting point for such investigations.
Acknowledgments My research on the Weeks Formation fauna was supported by the Committee for Research and Exploration of the National Geographic Society (No. 9567-14). I am particularly grateful to Zhang Yuandong and Zhu Xuejian for generously financing my participation to the annual meeting 2017 of the International Geoscience Programme (IGCP) Project 653. This is a contribution of the IGCP Project 653.
References
Allison, P. A., Briggs, D. E. G. 1993. Exceptional fossil record: distribution of soft-tissue preservation through the Phanerozoic. Geology, 21: 527—530.
Babcock, L. E., Baranoski, M. T., Cook, A. E. 2014. Cambrian (Guzhangian Stage) trilobites from Ohio,USA,and modification of the Cedaria Zone as used in Gondwana.GFF,136:6—15.
Barskov, I. S., Zhuravlev, A. Y. 1988. Soft-bodied organisms from the Cambrian of the Siberian Platform. Paleontological Journal, 1: 3—9 (in Russian).
Beecher, C. E. 1901. Discovery of eurypterid remains in the Cambrian of Missouri. American Journal of Science, 12: 364—366.
Collette, J. H., Hagadorn, J. W. 2010. Three-dimensionally preserved arthropods from Cambrian Lagerstätten of Quebec and Wisconsin.Journal of Paleontology,84:646—667.
Dunlop,J.A.,Anderson,L.I.,Braddy,S.J.2004.A redescription of Chasmataspis laurencii Caster and Brooks, 1956 (Chelicerata: Chasmataspidida) from the Middle Ordovician of Tennessee, USA, with remarks on chasmataspid phylogeny. Transactions of the Royal Society of Edinburgh, Earth Sciences, 94: 207—225.
Hesselbo, S. P. 1992. Aglaspidida (Arthropoda) from the Upper Cambrian of Wisconsin. Journal of Paleontology, 66: 885—923.
Ivantsov, A. Y., Zhuravlev, A. Y., Leguta, A. V. 2005. Palaeoecology of the Early Cambrian Sinsk biota from the Siberian Platform. Palaeogeography, Palaeoclimatology, Palaeoecology, 220:69—88.
Lerosey-Aubril,R.2015.Notchia weugi gen.et sp.nov.:a new short-headed arthropod from the Weeks Formation Konservat-Lagerstätte (Cambrian; Utah). Geological Magazine, 152:351—357.
Lerosey-Aubril, R., Ortega-Hernández, J., Kier, C., Bonino, E. 2013. Occurrence of the Ordovician-type aglaspidid Tremaglaspis in the Cambrian Weeks Formation(Utah,USA). Geological Magazine, 150: 945—951.
Lerosey-Aubril, R., Hegna, T. A., Babcock, L. E., Bonino, E., Kier, C. 2014. Arthropod appendages from the Weeks Formation Konservat-Lagerstätte: new occurrences of anomalocaridids in the Cambrian of Utah, USA. Bulletin of Geosciences, 89: 269—282.
Lerosey-Aubril, R., Paterson, J. R., Gibb, S., Chatterton, B. D. E. 2017. Exceptionally-preserved late Cambrian fossils from the McKay Group (British Columbia, Canada) and the evolution of tagmosis in aglaspidid arthropods. Gondwana Research, 42: 264—279.
Martin, E. L. O., Lerosey-Aubril, R., Vannier, J. 2016. Palaeoscolecid worms from the Lower Ordovician Fezouata Lagerstätte, Morocco: Palaeoecological and palaeogeographical implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 460: 130—141.
Muscente, A. D., Schiffbauer, J. D., Broce, J., Laflamme, M., O'Donnell, K., Boag, T. H., Meyer, M., Hawkins, A. D., Huntley, J. W., McNamara, M., MacKenzie, L. A., Stanley, Jr., G. D., Hinman, N. W., Hofmann, M. H., Xiao, S. 2017. Exceptionally preserved fossil assemblages through geologic time and space. Gondwana Research, 48: 164—188.
Paterson, J. R., García-Bellido, D. C., Jago, J. B., Gehling, J. G., Lee, M. S. Y., Edgecombe, G. D.2016.The Emu Bay Shale Konservat-Lagerstätte:a view of Cambrian life from East Gondwana. Journal of the Geological Society, 173: 1—11.
Raasch, G. O. 1939. Cambrian Merostomata. Geological Society of America Special Papers, 16:1—146.
Servais, T., Perrier, V., Danelian, T., Klug, C., Martin, R. E., Munnecke, A., Nowak, H., Nützel, A., Vandenbroucke, T. R. A., Williams, M., Rasmussen, C. M. Ø. 2016. The onset of the ‘Ordovician Plankton Revolution' in the late Cambrian. Palaeogeography, Palaeoclimatology, Palaeoecology, 458: 12—28.
Vaccari, N. E., Edgecombe, G. D., Escudero, C. 2004. Cambrian origins and affinities of an enigmatic fossil group of arthropods. Nature, 430: 554—557.
Van Roy, P., Briggs, D. E. G., Gaines, R. R. 2015. The Fezouata fossils of Morocco: an extraordinary record of marine life in the Early Ordovician. Journal of the Geological Society, 172: 541—549.
Zhu, X. J., Peng, S. C., Zamora, S., Lefebvre, B., Chen, G. Y. 2016. Furongian (upper Cambrian) Guole Konservat-Lagerstätte from South China.Acta Geologica Sinica,90:30—37.