The shrimp-like Waptia is also present. The diversity and the identification of a modern higher crustacean family (Plenocaris, thoughtto be a member.
Proc. Natl. Acad. Sci. USA Vol. 82, pp. 5809-5813, September 1985 Evolution
Pellet microfossils: Possible evidence for metazoan life in Early Proterozoic time (Precambrian paleobiology/metazoan origins)
ELEANORA IBERALL ROBBINS*, KAREN GLAUS PORTERt, AND KURT A. HABERYANt *U.S. Geological Survey, National Center MS 956, Reston, VA 22092; tDepartment of Zoology, University of Georgia, Athens, GA 30602; and tDepartment of Zoology, Duke University, Durham, NC 27706
Communicated by G. E. Hutchinson, April 16, 1985
Microfossils resembling fecal pellets occur in ABSTRACT acid-resistant residues and thin sections of Middle Cambrian to Early Proterozoic shale. The cylindrical microfossils average 50 x 110 ,.m and are the size and shape of fecal pellets produced by microscopic animals today. Pellets occur in dark gray and black rocks that were deposited in the facies that also preserves sulfide minerals and that represent environments analogous to those that preserve fecal pellets today. Rocks containing pellets and algal microfossils range in age from 0.53 to 1.9 gigayears (Gyr) and include Burgess Shale, Greyson and Newland Formations, Rove Formation, and Gunflint IronFormation. Similar rock types of Archean age, ranging from 2.68 to 3.8 Gyr, were barren of pellets. If the Proterozoic microfossils are fossilized fecal pellets, they provide evidence of metazoan life and a complex food chain at 1.9 Gyr ago. This occurrence predates macroscopic metazoan body fossils in the Ediacaran System at 0.67 Gyr, animal trace fossils from 0.9 to 1.3 Gyr, and fossils of unicellular eukaryotic plankton at 1.4 Gyr.
Possible fossil microbes and biochemicals occur in highly metamorphosed metasediments as old as the 3.8-gigayear (Gyr) Isua Iron-Formation (Fm) (refs. 1-3, and unpublished observation). However, the earliest generally accepted evidence of life is siliceous stromatolites formed by littoral, benthic bacteria in cherts of the 3.5-Gyr Warrawoona Group (4). By 1.9 Gyr, a diverse prokaryotic microflora was established, which is preserved in cherts of the Gunflint Iron-Fm (5-9). The currently accepted date for the origin of unicellular eukaryotes is 1.4 Gyr (10); however, some diagnostic fossils in the Gunflint and its lateral equivalents suggest eukaryotic algae might have been in existence by 1.9 Gyr. Eosphaera in the carbonate facies of the Gunflint may be an ancestor of Volvox (11), the colonial -green alga. Organic-walled structures (12) in Michigamme Fm coal are probably Botryococcus,§ the colonial green alga that formed boghead coals since at least Late Proterozoic time (13). From 1.3 Gyr on, there is increasing evidence for periodic radiations of both eukaryotic and prokaryotic algae (14-16). The origin of metazoans, multicellular animals that relied on microbes as a food resource, is less well documented. The oldest proven metazoan body fossils are in the Ediacaran System (0.55-0.67 Gyr) of southeast Australia (17). The complexity and diversity of the fauna suggest that these animals had a history that extended further back than Ediacaran time. Furthermore, amino acid sequences in 02-binding proteins suggest the radiation of animals took place at or before 0.9-1 Gyr (18). Although older body fossils have not been identified, trace fossils such as tubes of benthic animals range to 2 Gyr (19), and fecal pellets,
burrows, and trails of benthic animals are widespread in rocks younger than 0.68 Gyr (20). Detection of the time of metazoan origin has several constraints. The first is ecological: the abundance of a consumer is less than its resource, suggesting that metazoans initially were rare. The probable small size and soft-bodied nature of early consumers is another constraint that likely resulted in poor preservation in the fossil record. Metazoans, just like algae, may have begun as plankton (10, 19, 21). Plankton are less likely than benthos to leave body fossils or traces because of their small size, light structure, and aquatic habitat. Today, remains of planktonic animals consist primarily of fecal pellets. Microcrustacean fecal pellets predominate in modem sediment, but pellets of microscopic worms and salps as well as bodies of ciliates that resemble fecal pellets also have been identified (refs. 22-26; M. Silver, personal communication). Pellets that are predominantly from copepods accumulate today in low-energy anoxic waters of either silled marine basins or rift-valley lakes (Fig. la) (27, 28). Body parts are rare both in modem sediments and in the fossil record, although there are exceptions such as those of the Ediacara and Burgess faunas. The usual explanation for their absence is that chitin is rapidly degraded (29-31). We confirmed this by aging modem copepod chitin under nonsterile and sterile conditions at 20'C and observed complete dissolution by 16 and 32 weeks, respectively. Therefore, the history of such animals is probably going to be written by their fossilized fecal pellets. In this study, we applied a palynological technique that isolates soft microfossils in our search for remains of the oldest metazoans. Instead of studying oxide, silicate, or carbonate facies rocks (32) sampled by earlier authors, we sampled the pyrite-bearing rocks of anoxic basins. We studied kerogen in the sulfide facies because anoxic basins are modern depositional analogues that enhance organic preservation in sediments (28, 33).
MATERIALS AND METHODS Samples. We solicited samples of dark gray and black laminated shale and slate from Cambrian, Proterozoic, and Archean rocks. These were from rocks that are thought to have been formed in anoxic, nonbioturbated environments. Table 1 shows ages, lithologies, and depositional environments of rocks used in this study. Acid Residues. Ten grams ofrock was crushed, treated with cold 10% HCl for 24 hr, and stirred several times. Samples with high carbonate content were allowed to settle, the acid was decanted, and 30% HCl was added. After 24 hr, all HCl was removed by aspiration. Each sample was washed three Abbreviations: Gyr, gigayear(s); Fm, Formation. §LaBerge, G. L., Robbins, E. I. & Schmidt, R. G. (1985) International Geological Congress, Moscow, Aug. 1984, Abstracts Vol. 1, p. 241.
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Evolution: Robbins et al.
Proc. Natl. Acad. Sci. USA 82 (1985)
Table 1. Lithology and depositional environment of material examined for pellet microfossils Age, Gyr Location Geologic name and lithology Depositional setting Refs. 0.53 British Columbia, Canada Burgess Shale, bk mass calc sh Shallow marine 34 0.68 Virginia Fauquier Fm, slate Fluvial/lacustrine 35, 36, *
