The rise and early evolution of animals: where do we stand from a trace-fossil perspective?

Abstract

The trace-fossil record provides a wealth of information to track the rise and early evolution of animals. It comprises the activity of both hard- and soft-bodied organisms, is continuous through the Ediacaran (635-539 Ma)- Cambrian (539-485 Ma) transition, yields insights into animal behaviour and their role as ecosystem engineers, and allows for a more refined characterization of palaeoenvironmental context. In order to unravel macroevolutionary signals from the trace-fossil record, a variety of approaches is available, including not only estimation of degree of bioturbation, but also analysis of ichnodiversity and ichnodisparity trajectories, and evaluation of the occupation of infaunal ecospace and styles of ecosystem engineering. Analysis of the trace-fossil record demonstrates the presence of motile benthic bilaterians in the Ediacaran, mostly feeding from biofilms. Although Ediacaran trace fossils are simple and emplaced at or immediately below the sediment surface, an increase in ichnofossil complexity, predation pressure, sediment disturbance and penetration depth is apparent during the terminal Ediacaran. Regardless of this increase, a dramatic rise in trace fossil diversity and disparity took place during the earliest Cambrian, underscoring that the novelty of the Fortunian (539-529 Ma) cannot be underestimated. The Fortunian still shows the persistence of an Ediacaran-style matground ecology, but is fundamentally characterized by the appearance of new trace-fossil architectural plans reflecting novel ways of interacting with the substrate. The appearance of Phanerozoic-style benthic ecosystems attests to an increased length and connectivity of the food web and improved efficiency in organic carbon transfer and nutrient recycling. A profound reorganization of the infaunal ecospace is recorded in both high-energy sand-dominated nearshore areas and low-energy mud-dominated offshore environments, during the early Cambrian, starting approximately during Cambrian Age 2 (529-521 Ma), but continuing during the rest of the early Cambrian. A model comprising four evolutionary phases is proposed to synthetize information from the Ediacaran-Cambrian trace-fossil record. The use of a rich ichnological toolbox; critical, systematic and comprehensive evaluation of the Ediacaran-Cambrian trace-fossil record; and high-resolution integration of the ichnological dataset and sedimentological information show that the advent of biogenic mixing was an important factor in fully marine environments at the dawn of the Phanerozoic.

Keywords: Ediacaran–Cambrian; bioerosion; bioturbation; evolutionary palaeoecology; macroevolution; trace fossils.

Figure 1.

Representative trace fossils of the White Sea assemblage. (a) Helminthopsis tenuis, (b) Gordia marina, (c) Epibaion costatus, represented by four overlapping resting trace fossils, associated with its producer, Dickinsonia costata. Photograph by Jakob Vinther. (d) Kimberichnus teruzzi associated with its producer, Kimberella quadrata. Photo from a cast at the exhibition Fossil Art. All photos are from specimens preserved as positive hyporelief, Ediacara Member, Rawnsley Quartzite, Flinders Ranges, South Australia. Images from [87] and reproduced with permission of Springer.

Figure 2.

Representative trace fossils of the Nama assemblage. (a) Treptichnids and possible minute grazing trails, preserved as positive hyporelief. Huns Member, Urusis Formation, Schwarzrand Subgroup, Nama Group, Arimas Farm, Namibia. Photograph by Sören Jensen of a specimen originally published in [156]. (b) Parapsammichnites pretzeliformis, preserved as positive hyporelief. Spitskop Member of the Urusis Formation, Schwarzrand Subgroup, Nama Group, Koelkramps, Namibia. (c) Oichnus isp. in the tubular fossil Cloudina hartmannae. Dengying Formation, Lijiagou, Shaanxi Province, China. Photograph by Stefan Bengtson of specimens previously illustrated in [167].

Figure 3.

Representative trace fossils of the Fortunian. (a) Oldhamia alata, preserved as positive hyporelief. Puncoviscana Formation, El Mollar, Quebrada del Toro, northwest Argentina. (b) Gyrolithes scintillus, vertical cross-section view. Member 2, Chapel Island Formation, Fortune Head, Burin Peninsula, Newfoundland, Canada. Image from [47] and reproduced with permission of Springer. (c) Psammichnites isp., preserved as negative epirelief. Member 3, Chapel Island Formation, Grand Bank Head, Burin Peninsula, Newfoundland, Canada. (d) Cochlichnus anguineus, preserved as positive hyporelief. Member 2, Chapel Island Formation, Grand Bank Head, Burin Peninsula, Newfoundland, Canada. (e) Monomorphichnus isp., preserved as positive hyporelief. Chapel Island Formation, Lewin's Cove, Burin Peninsula, Newfoundland, Canada. (f) Tasmanadia cachii, preserved as positive hyporelief. Puncoviscana Formation, Cachi, northwest Argentina. (g) Treptichnus pedum, preserved as positive hyporelief. Lower Member, Wood Canyon Formation, Death Valley, western USA.

Figure 4.

Representative trace fossils and ichnofabrics of Cambrian Stage 2 and Series 2. (a) Skolithos linearis forming a typical piperock, vertical cross-section view. Lake O'Hara Member, St Piran Formation, Gog Group, Lake O'Hara, Canadian Rockies. Photograph by Patricio Desjardins. (b) Rosselia isp. vertical cross-section view. Lake O'Hara Member, St Piran Formation, Gog Group, Lake Magog, Canadian Rockies. Photograph by Patricio Desjardins. Image from [47] and reproduced with permission of Springer. (c) Diplocraterion parallelum, vertical cross-section view. Dividalen Group, Imobekken, northern Norway. Image from [47] and reproduced with permission of Springer. (d) Psammichnites gigas, as seen on a sandstone base. Shiyantou Formation, Meishucun, Yunnan Province, China. (e) Teichichnus rectus (arrowed) superimposed on typical mixed-layer burrow mottling. Member 5, Chapel Island Formation, Little Dantzic Cove, Burin Peninsula, Newfoundland, Canada. Photograph by Romain Gougeon. (f) Dense occurrence of Thalassinoides isp. ichnofabrics, vertical cross-section view. Zhushadong Formation, Guankou, Henan Province.

Figure 5.

Summary of ichnodiversity and ichnodisparity changes during the Ediacaran–Cambrian Series 2, and iconic representation of evolutionary phases (modified from [12]). Phase 1 (Ediacaran) shows the earliest ichnological evidence of locomotion by bilaterians. Simple grazing trails are dominant (e.g. Gordia, Helminthoidichnites, Helminthopsis), but other classic members of the Ediacara biota also record motility (e.g. resting traces of dickinsonids: Epibaion). This phase is typically illustrated by the White Sea assemblage, but the oldest deposits representative of the Nama assemblage are part of this phase as well. Phase 2 (Ediacaran) records a prelude to the Cambrian explosion, as evidenced by the appearance of more complex and penetrative burrows (treptichnids), trace fossils of bulldozers (Parapsammichnites) and drilling predation in Cloudina (Oichnus). Patches of more bioturbated sediment are apparent in shallow, fully marine settings. This phase is recorded in strata corresponding to the youngest representatives of the Nama assemblage. Both phases 1 and 2 are clearly manifested in environments between the fair-weather and storm wave bases (i.e. offshore). Phase 3 (Fortunian) is characterized by the appearance of novel architectures reflecting the evolution of novel body plans, significantly euarthropods (e.g. Diplichnites isp., Rusophycus avalonensis), more penetrative burrows (e.g. Treptichnus pedum, various ichnospecies of Gyrolithes) and patterned feeding strategies (e.g. various ichnospecies of Oldhamia) that allowed more efficient exploitation of fine-grained sediment and microbial mats. Although most of the ichnologic information comes from offshore settings, evidence of colonization of very shallow intertidal settings and deep-marine environments is recorded. Phase 4A (Cambrian Age 2) is signalled by an increase in depth and extent of bioturbation. Nearshore areas were colonized by a deep-tier, suspension-feeding (e.g. Skolithos, Diplocraterion) and detritus-feeding (e.g. Rosselia) infauna, and offshore environments by a stationary and vagile deposit- and detritus-feeder benthos. Phase 4B (Cambrian Ages 3–4) is similar to the previous one, but recording a renewed diversification at ichnogenus level and more extensive colonization of agitated nearshore settings as shown by the widespread occurrence of Skolithos piperock.