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Plankton ecology and the Proterozoic-Phanerozoic transition

  • Nicholas J. Butterfield (a1)

Most modern marine ecology is ultimately based on unicellular phytoplankton, yet most large animals are unable to graze directly on even relatively large net phytoplankton; the repackaging effected by herbivorous mesozooplankton thus represents a key link in marine metazoan food chains. Despite the deep taphonomic biases affecting plankton fossilization, there is a clear record of phytoplankton from at least 1800 m.y ago. Proterozoic plankton are represented by small-to medium-sized sphaeromorphic acritarchs and probably do not include many/most of the unusually large acritarchs that characterize the Neoproterozoic. The first significant shift in phytoplankton diversity was therefore the rapid radiation of small acanthomorphic acritarchs in the Early Cambrian. The coincidence of phytoplankton diversification with the Cambrian radiation of large animals points compellingly to an ecological linkage between the two, particularly in light of recently discovered filter-feeding mesozooplankton in the Early Cambrian. The introduction of planktic filter feeders would have established the second tier of the Eltonian pyramid, potentially setting off the “self-propagating mutual feedback system of diversification” now recognized as the Cambrian explosion (Stanley 1973, 1976).

By consuming significant percentages of net phytoplankton and suspending it as animal biomass and non-aggregating fecal pellets, mesozooplankton cause a net reduction in export production; a general introduction of zooplankton would therefore have reduced carbon burial and moderated the bloom and bust cycle that must have characterized Proterozoic populations of net phytoplankton. The effect of added trophic levels in Early Cambrian ecosystems can be viewed as a serial application of the trophic cascade process observed in modern lakes, whereby the introduction of higher trophic levels determines the accumulation of plant biomass at the base of the system. As such, the major biogeochemical perturbations that mark the onset of the Phanerozoic might be considered a consequence, rather than a cause, of the Cambrian explosion; reduced C export due to zooplankton expansion explains the otherwise anomalous drop in δ13C at the base of the Tommotian.

Cambrian acanthomorphic acritarchs likely derived from planktic leiosphaerids exposed to mesozooplanktic grazing pressure, the ornamentation effectively increasing vesicle size without compromising buoyancy or surface-area:volume ratios. Alternatively, they may represent an escape into the plankton through a miniaturization of the much larger Neoproterozoic acanthomorphs. An invasion of small benthic herbivores into the water column to exploit the phytoplankton accounts for the origin of the mesozooplankton and may have been the key innovation in the Cambrian explosion.

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Alldredge, A. L., and Silver, M. W. 1988. Characteristics, dynamics and significance of marine snow. Progress in Oceanography 20:4182.
Avnimelech, Y., Troeger, B. W., and Reed, L. W. 1982. Mutual flocculation of algae and clay: evidence and implications. Science 216:6365.
Azam, F., Fenchel, T., Gray, J. G., Meyer-Reil, L. A., and Thingstad, T. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10:257263.
Bathmann, U. V., Noji, T. T., Voss, M., and Peinert, R. 1987. Copepod fecal pellets: abundance, sedimentation and content at a permanent station in the Norwegian Sea in May/June 1986. Marine Ecology Progress Series 38:4551.
Berger, W. H., Smetacek, V. S., and Wefer, G. 1989a. Productivity of the ocean: present and past. Wiley, Chichester.
Berger, W. H., Smetacek, V. S., and Wefer, G. 1989b. Ocean productivity and palaeoproductivity—an overview. pp. 134 in Berger et al. 1989a.
Brasier, M. D. 1992. Nutrient-enriched waters and the early skeletal fossil record. Journal of the Geological Society of London 149:621629.
Brasier, M. D., Rozanov, A. Yu., Zhuravlev, A. Yu., Corfield, R. M., and Derry, L. A. 1994. A carbon isotope reference scale for the Lower Cambrian succession in Siberia: report of IGCP Project 303. Geological Magazine 131:767783.
Brett, M. T., and Goldman, C. R. 1997. Consumer versus resource control in freshwater pelagic food webs. Science 275:384386.
Brett, M. T., Wiackowski, K., Lubnow, F. S., Mueller-Solger, A., Elser, J. J., and Goldman, C. R. 1994. Species-dependent effects of zooplankton on planktonic ecosystem processes in Castle Lake, California. Ecology 75:22432254.
Bruland, K. W., Bienfang, P. K., Bishop, J. K. B., Eglinton, G., Ittekkot, V. A. W., Lampitt, R., Sarnthein, M., Thiede, J., Walsh, J. J., and Wefer, G. 1989. Group Report—Flux to the seafloor. pp. 193215in Berger et al. 1989a.
Bruton, D. L. 1991. Beach and laboratory experiments with the jellyfish Aurelia, and remarks on some fossil “medusoid” traces. pp. 125129In Simonetta, A. M. and Conway Morris, S., eds. The early evolution of metazoa and the significance of problematic taxa. Cambridge University Press, Cambridge.
Butterfield, N. J. 1994. Burgess Shale-type fossils from a Lower Cambrian shallow shelf sequence in northwestern Canada. Nature 369:477479.
Butterfield, N. J., and Chandler, F. W. 1992. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35:943957.
Butterfield, N. J., and Nicholas, C. J. 1996. Burgess Shale-type preservation of both non-mineralizing and ‘shelly’ Cambrian organisms from the Mackenzie Mountains, northwestern Canada. Journal of Paleontology 70:893899.
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata 34:184.
Carpenter, S. R., and Kitchell, J. F. 1993. The trophic cascade in lakes. Cambridge University Press, Cambridge.
Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology 29:423467.
Cook, P. J., and Shergold, J. H. 1984. Phosphorus, phosphorites and skeletal evolution at the Precambrian-Cambrian boundary. Nature 308:231236.
Cyr, H., and Pace, M. L. 1993. Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148150.
Dodson, S. I. 1974. Adaptive change in plankton morphology in response to size-selective predation: a new hypothesis of cyclomorphosis. Limnology and Oceanography 19:721729.
Dorning, K. J. 1987. The organic palaeontology of Palaeozoic carbonate environments. pp. 256265in Hart, M. B., ed. Micropalaeontology of carbonate environments. Ellis Horwood, Chichester.
Duan, Cheng-Hua. 1982. Late Precambrian algal megafossils Chuaria and Tawuia in some areas of eastern China. Alcheringa 6:5768.
Dunbar, R. B., and Berger, W. H. 1981. Fecal pellet flux to modern bottom sediment of Santa Barbara Basin (California) based on sediment trapping. Geological Society of America Bulletin 92:212218.
Elser, J. J., and Goldman, C. R. 1991. Zooplankton effects on phytoplankton in lakes of contrasting trophic status. Limnology and Oceanography 36:6490.
Erwin, D. H. 1993. The origin of metazoan development: a palaeobiological perspective. Biological Journal of the Linnean Society 50:255274.
Evitt, W. R. 1963. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres and acritarchs, II. Proceedings of the National Academy of Sciences USA 49:298302.
Fedonkin, M. A. 1985. Precambrian metazoans: the problems of preservation, systematitics and evolution. Philosophical Transactions of the Royal Society of London B 311:2745.
Fortier, L., Le Fèvre, J., and Legendre, L. 1994. Export of biogenic carbon to fish and to the deep ocean: the role of large planktonic microphages. Journal of Plankton Research 16:809839.
Fortey, R. A. 1994. Adaptive deployment in feeding habits in Cambrian trilobites. Ecological Aspects of the Cambrian Radiation (IGCP 366). TERRA nova 6, abstract supplement 3:3.
Fortey, R. A., Briggs, D. E. G., and Wills, M. A. 1996. The Cambrian evolutionary ‘explosion': decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society 57:1333.
Fryer, G. 1991. Functional morphology and the adaptive radiation of the Daphniidae (Branchiopoda: Anomopoda). Philosophical Transactions of the Royal Society of London B 331:199.
Graf, G. 1992. Benthic-pelagic coupling: a benthic view. Oceanography and Marine Biology, Annual Review 30:149190.
Hansen, B., Bj⊘rnsen, P. K., and Hansen, P. J. 1994. The size ratio between planktonic predators and their prey. Limnology and Oceanography 39:395403.
Hessen, D. O., and Van Donk, E. 1993. Morphological changes in Scenedesmus induced by substances released from Daphnia. Archiv für Hydrobiologie 127:129140.
Hofmann, H. J. 1985. The mid-Proterozoic Little Dal macrobiota, Mackenzie Mountains, north-west Canada. Palaeontology 28:331354.
Horodyski, R. J. 1993. Paleontology of Proterozoic shales and mudstones: examples from the Belt Supergroup, Chuar Group and Pahrump Group, western USA. Precambrian Research 61:241278.
Hunter, M. D., and Price, P. W. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724732.
Jablonski, D., Sepkoski, J. J., Bottjer, D. J., and Sheehan, P. M. 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222:11231125.
Jackson, G. A. 1990. A model of the formation of marine algal flocs by physical coagulation processes. Deep Sea Research 37:11971211.
Kiørboe, T. 1993. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Advances in Marine Biology 29:172.
Knoll, A. H. 1992. Biological and biogeochemical preludes to the Ediacaran radiation. pp. 5384In Lipps, J. H. and Signor, P. W., eds. Origin and early evolution of the Metazoa. Plenum, New York.
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences USA 91:67436750.
Knoll, A. H., and Butterfield, N. J. 1989. New window on Proterozoic life. Nature 337:602603.
Knoll, A. H., and Vidal, G. 1980. Late Proterozoic vase-shaped microfossils from the Visingsö Beds, Sweden. Geologiska Föreningens i Stockholm Förhandlingar 102:207211.
Knoll, A. H., Barghoorn, E. S., and Awramik, S. M. 1978. New microorganisms from the Aphebian Gunflint Iron Formation, Ontario. Journal of Paleontology 52:976992.
Knoll, A. H., Swett, K., and Mark, J. 1991. Paleobiology of a Neoproterozoic tidal flat/lagoonal complex: the Draken Conglomerate Formation, Spitsbergen. Journal of Paleontology 65:531570.
Lampert, W., Fleckner, W., Rai, H., and Taylor, B. E. 1986. Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnology and Oceanography 31:478490.
Lampitt, R. S., Noji, T., and von Bodungen, B. 1990. What happens to zooplankton faecal pellets? Implications for material flux. Marine Biology 104:1523.
Landry, M. R., Lorenzen, C. J., and Peterson, W. K. 1994. Mesozooplankton grazing in the Southern California Bight. II. Grazing impact and particulate flux. Marine Ecology Progress Series 115:7385.
Legendre, L., and Le Fèvre, J. 1989. Hydrodynamical singularities as controls of recycled versus export production in oceans. pp. 4963in Berger et al. 1989a.
Li, W. K. W. 1995. Composition of ultraphytoplankton in the central North Atlantic. Marine Ecology Progress Series 122:18.
Logan, G. A., Hayes, J. M., Hieshima, G. B., and Summons, R. E. 1995. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376:5356.
Longhurst, A. R. 1991. Role of the marine biosphere in the global carbon cycle. Limnology and Oceanography 36:15071526.
Margaritz, M., Kirschvink, J. L., Latham, A. J., Zhuravlev, A. Yu., and Rozanov, A. Yu. 1991. Precambrian/Cambrian boundary problem: Carbon isotope correlations for Vendian and Tommotian time between Siberia and Morocco. Geology 19:847850.
McCave, I. N. 1975. Vertical flux of particles in the ocean. Deep-Sea Research 22:491502.
Mendelson, C. V., and Schopf, J. W., 1992. Proterozoic and Early Cambrian acritarchs. pp. 219232in Schopf and Klein 1992.
Moldowan, J. M., Dahl, J., Jacobson, S. R., Huizinga, B. J., Fago, F. J., Shetty, R., Watt, D. S., and Peters, K. E. 1996. Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology 24:159162.
Molyneux, S. G., Le Hérissé, A., and Wicander, R. 1996. Biostratigraphy of Cambrian acritarchs and prasinophytes. pp. 493529In Jansonius, J. and McGregor, D. C., eds. Palynology: principles and applications, Vol. 2. American Association of Stratigraphic Palynologists Foundation, Houston.
Naganuma, T. 1996. Calanoid copepods: linking lower-higher trophic levels by linking lower-higher Reynolds numbers. Marine Ecology Progress Series 136:311313.
Nienhuis, P. H. 1981. Distribution of organic matter in living marine organisms. pp. 3169In Duursma, E. K. and Dawson, R., eds. Marine organic chemistry—evolution, composition, interactions and chemistry of organic matter in seawater. Elsevier, Amsterdam.
Norton, T. A. 1992. Dispersal by macroalgae. British Phycological Journal 27:293301.
Paul, C. R. C., and Mitchell, S. F. 1994. Is famine a common factor in marine mass extinctions? Geology 22:679682.
Pauly, D., and Christensen, V. 1995. Primary production required to sustain global fisheries. Nature 374:255257.
Peinert, R., von Bodungen, B., and Smetacek, V. S. 1989. Food web structure and loss rate. pp. 3548in Berger et al. 1989a.
Pilskaln, C. H., and Honjo, S. 1987. The fecal pellet fraction of biogeochemical particle fluxes to the deep sea. Global Biogeochemical Cycles 1:3148.
Porter, K. G. 1977. The plant-animal interface in freshwater ecosystems. American Scientist 65:159170.
Porter, K. G., and Robbins, E. I. 1981. Zooplankton fecal pellets link fossil fuel and phosphate deposits. Science 212:931933.
Riebesell, U. 1991. Particle aggregation during a diatom bloom. II. Biological aspects. Marine Ecology Progress Series 69:281291.
Rigby, S., and Milsom, C. 1996. Benthic origins of zooplankton: An environmentally determined macroevolutionary effect. Geology 24:5254.
Robbins, E. I., Porter, K. G., and Haberyan, K. A. 1985. Pellet microfossils: possible evidence for metazoan life in Early Proterozoic time. Proceedings of the National Academy of Sciences USA 82:58095813.
Rothhaupt, K. O., and Güde, H. 1992. The influence of spatial and temporal concentration gradients on phosphate partitioning between different size fractions of plankton: further evidence and possible causes. Limnology and Oceanography 37:739749.
Schopf, J. W., and Klein, C. 1992. The Proterozoic biosphere. Cambridge University Press, Cambridge.
Sepkoski, J. J. 1992. Proterozoic-Early Cambrian diversification of metazoans and metaphytes. pp. 553561in Schopf and Klein 1992.
Sheehan, P. M., and Hansen, T. A. 1986. Detritus feeding as a buffer to extinction at the end of the Cretaceous. Geology 14:868870.
Sherr, E. B., and Sherr, B. F. 1991. Planktonic microbes: tiny cells at the base of the oceans's food webs. Trends in Recent Ecology and Evolution 6:5054.
Signor, P. W., and Vermeij, G. J. 1994. The plankton and the benthos: origins and early history of an evolving relationship. Paleobiology 20:297319.
Smayda, T. J. 1970. The suspension and sinking of phytoplankton in the sea. Oceanography and Marine Biology Annual Review 8:353414.
Smetacek, V. 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Marine Biology 84:239251.
Smith, S. V. 1981. Marine macrophytes as a global carbon sink. Science 211:838840.
Sogin, M. L. 1989. Evolution of eukaryotic microorganisms and their small subunit ribosomal RNAs. American Zoologist 29:487499.
Spjeldnaes, N. 1963. A new fossil (Papillomembrana sp.) from the upper Precambrian of Norway. Nature 200:6364.
Stanley, S. M. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences USA 70:14861489.
Stanley, S. M. 1976. Ideas on the timing of metazoan diversification. Paleobiology 2:209219.
Strauss, H., Des Marais, D. J., Hayes, J. M., and Summons, R. E. 1992. Concentrations of organic carbon and maturities and elemental compositions of kerogens. pp. 9599in Schopf and Klein 1992.
Summons, R. E., Thomas, J., Maxwell, J. R., and Boreham, C. J. 1992. Secular and environmental constraints on the occurrence of dinosterane in sediments. Geochimica et Cosmochimica Acta 56:24372444.
Tollrian, R. 1995. Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia 101:151155.
Turner, T. T., and Ferrante, J. G. 1979. Zooplankton fecal pellets in aquatic ecosystems. Bioscience 29:670677.
Vanni, M. J., Luecke, C., Kitchell, J. F., Allen, Y., Temte, J., and Magnuson, J. J. 1990. Effects on lower trophic levels of massive fish mortality. Nature 344:333335.
van Waveren, I. M., and Marcus, N. H. 1993. Morphology of recent copepod egg envelopes and their implication for acritarch affinity. Special Papers in Palaeontology 48:111125.
van Waveren, I. M., and Visscher, H. 1994. Analysis of the composition and selective preservation of organic matter in surficial deep-sea sediments from a high productivity area (Banda Sea, Indonesia). Palaeogeography, Palaeoclimatology, Palaeoecology 112:85111.
Verity, P. G., and Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series 130:277293.
Vermeij, G. J. 1989. The origin of skeletons. Palaios 4:585589.
Vidal, G. 1990. Giant acanthomorph acritarchs from the upper Proterozoic in Southern Norway. Palaeontology 33:287298.
Vidal, G., and Moczydlowska, M. 1992. Patterns of phytoplankton radiation across the Precambrian-Cambrian boundary. Journal of the Geological Society of London 149:647654.
Walossek, D. 1993. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils and Strata 32:1202.
Walter, M. 1995. Faecal pellets in world events. Nature 376:1617.
Welschmeyer, N. A., and Lorenzen, C. J. 1985. Chlorophyll budgets: zooplankton grazing and phytoplankton growth in a temperate fjord and the Central Pacific Gyres. Limnology and Oceanography 30:121.
Woodwell, G. M., Whittaker, R. H., Reiners, W. A., Likens, G. E., Delwiche, C. C., and Botkin, D. B. 1978. The biota and the world carbon budget. Science 199:141146.
Wray, G. A., Levinton, J. S., and Shapiro, L. H. 1996. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274:568573.
Zachos, J. C., Arthur, M. A., and Dean, W. E. 1989. Geochemical evidence for suppression of pelagic marine productivity at the Cretaceous/Tertiary boundary. Nature 337:6164.
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