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The Rise of Predators The rise of predators Susannah Porter Department of Earth Science, University of California−Santa Barbara, Santa Barbara, California 93106, USA Despite their abundance, diversity, and importance today, organisms Cryogenian Ediacaran C Mineralogy with mineralized skeletons are a relatively recent introduction. For the fi rst 800 Ma 700 600 phosphatic three billion years of its history, life was soft-bodied, inducing mineral- K? SMG siliceous scale microfossils ized structures passively, if at all. Beginning ca. 550 Ma, however, more calcareous ? Melicerion poikilon than two dozen clades—primarily animal, but also protistan—indepen- ? Tenuocharta cloudii agglutinated dently evolved mineralized skeletons within a geologically short interval ? sponge-like fossils Namacalathus of time (Fig. 1; Bengtson, 1992). Now a new report by Cohen et al. (2011; Cloudina p. 539 in this issue of Geology) describing beautifully intricate scale-like A BCNamapoikia microfossils from the Fifteenmile Group, Yukon Territory, provides defi ni- anabaritids hexactinellid sponges tive evidence for mineralized skeletons some 150–250 m.y. earlier. These radiolarians scale-like microfossils were fi rst reported over two decades ago (Allison foraminifera? chaetognaths and Hilgert, 1986), but neither their age nor their mineralogy were well cap-shaped fossils constrained. Work by Cohen and her colleagues has now shown that these coeloscleritophorans D E hyolithelminths scales (which perhaps enveloped a single-celled green alga) are between hyoliths ca. 717 and ca. 812 Ma in age and composed of primary phosphate (Mac- tommotiids/brachiopods donald et al., 2010; Cohen et al., 2011). This adds to earlier suggestive cambroclaves conulariids evidence for mineralization at this time: the ca. 770–742 Ma vase-shaped molluscs microfossil (VSM) Melicerion poikilon, interpreted on the basis of tapho- paracarinachitids coleolids nomic models to be a euglyphid amoeba whose organic-walled test was archaeocyaths embedded with mineralized scales, possibly siliceous (Figs. 1B and 1C; calcarean sponges F radiocyaths Porter and Knoll, 2000; Porter et al., 2003); the mid-Neoproterozoic Ten- bradoriids uocharta cloudii, a multicellular, sheet-like fossil whose calcareous cell G byroniids cribricyaths walls may refl ect primary (Horodyski and Mankiewicz, 1990) or early hydroconozoans diagenetic (Knoll, 2003) mineralization; and ca. 650 Ma millimeter- to echinoderms centimeter-scale asymmetric bodies permeated with a network of canals lobopods mobergellans and interpreted to be sponge-like organisms perhaps lightly mineralized paiutiids with carbonate (Maloof et al., 2010b). trilobites Numerous hypotheses have been posed to explain the sudden appear- Figure 1. Independent origins of mineralized skeletons during the ance of skeletons in the latest Ediacaran and early Cambrian (e.g., Wood, Cryogenian, Ediacaran, and early Cambrian (through the Atdaba- 2011), but the most widely favored is that they evolved for defense against nian) and images of selected skeletons (A−G). Ediacaran and Cam- macrophagous predators—animals capable of consuming large prey brian occurrences from Bengtson (1992), Maloof et al. (2010a), and Porter (2010). See text for Cryogenian references. K?—possible (e.g., Bengtson, 1994). Animals most likely weren’t around in the mid- Kaigas glaciation; S—Sturtian glaciation; M—Marinoan glaciation; Neoproterozoic, but single-celled predators were (herein the term preda- G—Gaskiers glaciation. Age constraints on glaciations are from tor refers to eukaryotes that eat other living organisms, including algae). Macdonald et al. (2010, and references therein). A: The scale micro- Given the strong selective infl uence protistan predators have on micro- fossil Characodictyon. B: The vase-shaped microfossil Melicerion bial communities today (e.g., Smetacek, 2001; Tillmann, 2004), and that poikilon, interpreted to be a euglyphid amoeba. C: Test of the mod- ern euglyphid amoeba Euglypha tuberculata. D: Silicifi ed tubes of the primary function of many protistan skeletons seems to be for defense Cloudina carinata. E: Chancelloriid sclerite (Coeloscleritophora), (e.g., Hamm et al., 2003; Tillmann, 2004), it is reasonable to think that one of many that covered the animal’s body like the spines of a cac- mineralized skeletons may have appeared ca. 750 Ma as a response to tus. F: Sclerite of the cambroclave Cambroclavus fangxianensis, protistan predation. Single-celled predators obtain their food by engulfi ng part of an array of interlocking sclerites. G: Internal mold of the mol- lusc Mellopegma georginense. Image in A is courtesy of P. Cohen; or piercing their prey, and the (modest) diversity of skeletons in mid-Neo- images in B, C, and E are reprinted with permission from the Journal proterozoic rocks might refl ect a comparable diversity of predation styles. of Paleontology; image in D is courtesy of I. Cortijo; image in F is Scale microfossils, in particular Characodictyon, with its central, pronged courtesy of J. Moore. Scale bar equals 5 µm in A, 50 µm in B, 35 µm shaft (Fig. 1A), might have restricted the ability of single-celled predators in C, 10 mm in D, 100 µm in E, 150 µm in F, and 500 µm in G. to engulf the cell by effectively increasing its size, and VSM tests—both those with mineralized scales and those that are entirely organic-walled— might have deterred predators that used pseudopods to pierce their prey algae) involved the host cell engulfi ng another cell. The absence of pro- (e.g., Old, 1978). The earliest direct fossil evidence for protistan predators tistan predators in older rocks probably refl ects (at least in part) the lim- are the VSMs themselves (Porter et al., 2003), as well as biomarkers of ited preservation potential of many protozoan groups. However, it is also the same age thought to be derived from ciliates (Summons et al., 1988). possible that the appearance of protistan skeletons in the mid-Neoprotero- Fossils of eukaryotic algae as old as 1200 Ma (Butterfi eld, 2000) provide zoic refl ects a shift in the taxonomic contributors to primary productivity indirect evidence for the presence of protistan predators much earlier, how- (Knoll, 2007). Both biomarker ratios and body fossils suggest increasing ever, as the origin of plastids (the sites of photosynthesis in eukaryotic dominance of eukaryotic algae from the early Mesoproterozoic to the late © 2011 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected]. GEOLOGY,Geology, June June 2011; 2011 v. 39; no. 6; p. 607–608; doi: 10.1130/focus062011.1. 607 Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/39/6/607/3541164/607.pdf by guest on 29 September 2021 Neoproterozoic, perhaps caused by a change from euxinic, nitrogen-poor shells provide effective mechanical protection: Nature, v. 421, p. 841–843, oceans to increasingly oxic oceans richer in nitrogen (Knoll, 2007). Pro- doi:10.1038/nature01416. tistan predators thus may have been common in Mesoproterozoic oceans, Horodyski, R.J., and Mankiewicz, C., 1990, Possible Late Proterozoic skeletal algae from the Pahrump Group, Kingston Range, southeastern California: but primarily feeding on bacteria. As eukaryotic algae began to increase American Journal of Science, v. 290-A, p. 149–169. in abundance, however, more protistan predators would have become Javaux, E.J., and Marshal, C.P., 2006, A new approach in deciphering early pro- adapted to eating eukaryotes, and eukaryotic algae would have responded tist paleobiology and evolution: Combined microscopy and microchemistry by evolving a variety of defenses, including skeletons. The ability to engulf of single Proterozoic acritarchs: Review of Palaeobotany and Palynology, v. 139, p. 1–15, doi:10.1016/j.revpalbo.2006.01.005. large prey (eukaryotes tend to be much larger than bacteria) also meant that Knoll, A.H., 2003, Biomineralization and evolutionary history, in Dove, P.M., protistan predators would have had the capacity to consume other protistan et al., eds., Biomineralization: Reviews in Minerology and Geochemistry, predators, which in turn would have evolved defenses of their own (or sto- v. 54, p. 329–356. len them from their prey: some modern testate ameobae incorporate into Knoll, A.H., 2007, The geological succession of primary producers in the oceans, in their own tests mineralized scales they acquired from the tests of their prey Falkowski, P.G., and Knoll, A.H., eds., The Evolution of Primary Pro- ducers in the Sea: Burlington, Massachusetts, Elsevier Academic Press, [e.g., Ogden, 1991]). Some protistan skeletons could also have evolved p. 133–163. to function in predation; some radiolarians, for example, use their spiny Leander, B.S., 2008, A hierarchical view of convergent evolution in microbial skeletons both for protection and for mechanical support as they extend eukaryotes: The Journal of Eukaryotic Microbiology, v. 55, p. 59–68, pseudopods to ensnare prey (Anderson, 1983). The convergent evolution doi:10.1111/j.1550-7408.2008.00308.x. Macdonald, F.A., Schmitz, M.D., Crowley, J.L., Roots, C.F., Jones, D.S., Maloof, of macroscopic size and multicellularity in numerous clades in the early A.C., Strauss, J.V., Cohen, P.A., Johnston, D.T., and Schrag, D.P., 2010, Ediacaran (e.g., Yuan et al., 2011; Xiao and Lafl amme, 2009) could also Calibrating the Cryogenian: Science, v. 327, p. 1241–1243, doi:10.1126/ refl ect increasing predation pressure by protists, as large size is one form science.1183325. of defense against
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