Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-30T15:08:25.742Z Has data issue: false hasContentIssue false
  • English
  • Français

Plankton ecology and the Proterozoic-Phanerozoic transition

Published online by Cambridge University Press:  08 February 2016

Nicholas J. Butterfield
Nicholas J. Butterfield*
Affiliation:
Department of Earth Sciences, University of Western Ontario, London, Ontario, N6A 5B7 Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Type
Articles
Information
Paleobiology , Volume 23 , Issue 2 , Spring 1997 , pp. 247 - 262
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Alldredge, A. L., and Silver, M. W. 1988. Characteristics, dynamics and significance of marine snow. Progress in Oceanography 20:41–82.CrossRefGoogle Scholar
Avnimelech, Y., Troeger, B. W., and Reed, L. W. 1982. Mutual flocculation of algae and clay: evidence and implications. Science 216:63–65.CrossRefGoogle ScholarPubMed
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 10:257–263.CrossRefGoogle Scholar
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 38:45–51.CrossRefGoogle Scholar
Berger, W. H., Smetacek, V. S., and Wefer, G. 1989a. Productivity of the ocean: present and past. Wiley, Chichester.Google Scholar
Berger, W. H., Smetacek, V. S., and Wefer, G. 1989b. Ocean productivity and palaeoproductivity—an overview. pp. 1–34 in Berger et al. 1989a.Google Scholar
Brasier, M. D. 1992. Nutrient-enriched waters and the early skeletal fossil record. Journal of the Geological Society of London 149:621–629.CrossRefGoogle Scholar
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 131:767–783.CrossRefGoogle Scholar
Brett, M. T., and Goldman, C. R. 1997. Consumer versus resource control in freshwater pelagic food webs. Science 275:384–386.CrossRefGoogle ScholarPubMed
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 75:2243–2254.CrossRefGoogle Scholar
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. 193–215in Berger et al. 1989a.Google Scholar
Bruton, D. L. 1991. Beach and laboratory experiments with the jellyfish Aurelia, and remarks on some fossil “medusoid” traces. pp. 125–129In Simonetta, A. M. and Conway Morris, S., eds. The early evolution of metazoa and the significance of problematic taxa. Cambridge University Press, Cambridge.Google Scholar
Butterfield, N. J. 1994. Burgess Shale-type fossils from a Lower Cambrian shallow shelf sequence in northwestern Canada. Nature 369:477–479.CrossRefGoogle Scholar
Butterfield, N. J., and Chandler, F. W. 1992. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35:943–957.Google Scholar
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 70:893–899.CrossRefGoogle Scholar
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata 34:1–84.CrossRefGoogle Scholar
Carpenter, S. R., and Kitchell, J. F. 1993. The trophic cascade in lakes. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology 29:423–467.Google Scholar
Cook, P. J., and Shergold, J. H. 1984. Phosphorus, phosphorites and skeletal evolution at the Precambrian-Cambrian boundary. Nature 308:231–236.CrossRefGoogle Scholar
Cyr, H., and Pace, M. L. 1993. Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150.CrossRefGoogle Scholar
Dodson, S. I. 1974. Adaptive change in plankton morphology in response to size-selective predation: a new hypothesis of cyclomorphosis. Limnology and Oceanography 19:721–729.CrossRefGoogle Scholar
Dorning, K. J. 1987. The organic palaeontology of Palaeozoic carbonate environments. pp. 256–265in Hart, M. B., ed. Micropalaeontology of carbonate environments. Ellis Horwood, Chichester.Google Scholar
Duan, Cheng-Hua. 1982. Late Precambrian algal megafossils Chuaria and Tawuia in some areas of eastern China. Alcheringa 6:57–68.Google Scholar
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 92:212–218.2.0.CO;2>CrossRefGoogle Scholar
Elser, J. J., and Goldman, C. R. 1991. Zooplankton effects on phytoplankton in lakes of contrasting trophic status. Limnology and Oceanography 36:64–90.CrossRefGoogle Scholar
Erwin, D. H. 1993. The origin of metazoan development: a palaeobiological perspective. Biological Journal of the Linnean Society 50:255–274.CrossRefGoogle Scholar
Evitt, W. R. 1963. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres and acritarchs, II. Proceedings of the National Academy of Sciences USA 49:298–302.CrossRefGoogle ScholarPubMed
Fedonkin, M. A. 1985. Precambrian metazoans: the problems of preservation, systematitics and evolution. Philosophical Transactions of the Royal Society of London B 311:27–45.Google Scholar
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 16:809–839.CrossRefGoogle Scholar
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.Google Scholar
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 57:13–33.Google Scholar
Fryer, G. 1991. Functional morphology and the adaptive radiation of the Daphniidae (Branchiopoda: Anomopoda). Philosophical Transactions of the Royal Society of London B 331:1–99.Google Scholar
Graf, G. 1992. Benthic-pelagic coupling: a benthic view. Oceanography and Marine Biology, Annual Review 30:149–190.Google Scholar
Hansen, B., Bj⊘rnsen, P. K., and Hansen, P. J. 1994. The size ratio between planktonic predators and their prey. Limnology and Oceanography 39:395–403.CrossRefGoogle Scholar
Hessen, D. O., and Van Donk, E. 1993. Morphological changes in Scenedesmus induced by substances released from Daphnia. Archiv für Hydrobiologie 127:129–140.CrossRefGoogle Scholar
Hofmann, H. J. 1985. The mid-Proterozoic Little Dal macrobiota, Mackenzie Mountains, north-west Canada. Palaeontology 28:331–354.Google Scholar
Horodyski, R. J. 1993. Paleontology of Proterozoic shales and mudstones: examples from the Belt Supergroup, Chuar Group and Pahrump Group, western USA. Precambrian Research 61:241–278.CrossRefGoogle Scholar
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 73:724–732.CrossRefGoogle Scholar
Jablonski, D., Sepkoski, J. J., Bottjer, D. J., and Sheehan, P. M. 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222:1123–1125.CrossRefGoogle ScholarPubMed
Jackson, G. A. 1990. A model of the formation of marine algal flocs by physical coagulation processes. Deep Sea Research 37:1197–1211.CrossRefGoogle Scholar
Kiørboe, T. 1993. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Advances in Marine Biology 29:1–72.CrossRefGoogle Scholar
Knoll, A. H. 1992. Biological and biogeochemical preludes to the Ediacaran radiation. pp. 53–84In Lipps, J. H. and Signor, P. W., eds. Origin and early evolution of the Metazoa. Plenum, New York.CrossRefGoogle Scholar
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences USA 91:6743–6750.CrossRefGoogle ScholarPubMed
Knoll, A. H., and Butterfield, N. J. 1989. New window on Proterozoic life. Nature 337:602–603.CrossRefGoogle ScholarPubMed
Knoll, A. H., and Vidal, G. 1980. Late Proterozoic vase-shaped microfossils from the Visingsö Beds, Sweden. Geologiska Föreningens i Stockholm Förhandlingar 102:207–211.CrossRefGoogle Scholar
Knoll, A. H., Barghoorn, E. S., and Awramik, S. M. 1978. New microorganisms from the Aphebian Gunflint Iron Formation, Ontario. Journal of Paleontology 52:976–992.Google Scholar
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 65:531–570.CrossRefGoogle ScholarPubMed
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 31:478–490.CrossRefGoogle Scholar
Lampitt, R. S., Noji, T., and von Bodungen, B. 1990. What happens to zooplankton faecal pellets? Implications for material flux. Marine Biology 104:15–23.Google Scholar
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 115:73–85.CrossRefGoogle Scholar
Legendre, L., and Le Fèvre, J. 1989. Hydrodynamical singularities as controls of recycled versus export production in oceans. pp. 49–63in Berger et al. 1989a.Google Scholar
Li, W. K. W. 1995. Composition of ultraphytoplankton in the central North Atlantic. Marine Ecology Progress Series 122:1–8.CrossRefGoogle Scholar
Logan, G. A., Hayes, J. M., Hieshima, G. B., and Summons, R. E. 1995. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376:53–56.CrossRefGoogle ScholarPubMed
Longhurst, A. R. 1991. Role of the marine biosphere in the global carbon cycle. Limnology and Oceanography 36:1507–1526.CrossRefGoogle Scholar
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 19:847–850.2.3.CO;2>CrossRefGoogle Scholar
McCave, I. N. 1975. Vertical flux of particles in the ocean. Deep-Sea Research 22:491–502.Google Scholar
Mendelson, C. V., and Schopf, J. W., 1992. Proterozoic and Early Cambrian acritarchs. pp. 219–232in Schopf and Klein 1992.Google Scholar
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 24:159–162.2.3.CO;2>CrossRefGoogle Scholar
Molyneux, S. G., Le Hérissé, A., and Wicander, R. 1996. Biostratigraphy of Cambrian acritarchs and prasinophytes. pp. 493–529In Jansonius, J. and McGregor, D. C., eds. Palynology: principles and applications, Vol. 2. American Association of Stratigraphic Palynologists Foundation, Houston.Google Scholar
Naganuma, T. 1996. Calanoid copepods: linking lower-higher trophic levels by linking lower-higher Reynolds numbers. Marine Ecology Progress Series 136:311–313.CrossRefGoogle Scholar
Nienhuis, P. H. 1981. Distribution of organic matter in living marine organisms. pp. 31–69In Duursma, E. K. and Dawson, R., eds. Marine organic chemistry—evolution, composition, interactions and chemistry of organic matter in seawater. Elsevier, Amsterdam.CrossRefGoogle Scholar
Norton, T. A. 1992. Dispersal by macroalgae. British Phycological Journal 27:293–301.CrossRefGoogle Scholar
Paul, C. R. C., and Mitchell, S. F. 1994. Is famine a common factor in marine mass extinctions? Geology 22:679–682.2.3.CO;2>CrossRefGoogle Scholar
Pauly, D., and Christensen, V. 1995. Primary production required to sustain global fisheries. Nature 374:255–257.CrossRefGoogle Scholar
Peinert, R., von Bodungen, B., and Smetacek, V. S. 1989. Food web structure and loss rate. pp. 35–48in Berger et al. 1989a.Google Scholar
Pilskaln, C. H., and Honjo, S. 1987. The fecal pellet fraction of biogeochemical particle fluxes to the deep sea. Global Biogeochemical Cycles 1:31–48.CrossRefGoogle Scholar
Porter, K. G. 1977. The plant-animal interface in freshwater ecosystems. American Scientist 65:159–170.Google Scholar
Porter, K. G., and Robbins, E. I. 1981. Zooplankton fecal pellets link fossil fuel and phosphate deposits. Science 212:931–933.CrossRefGoogle ScholarPubMed
Riebesell, U. 1991. Particle aggregation during a diatom bloom. II. Biological aspects. Marine Ecology Progress Series 69:281–291.CrossRefGoogle Scholar
Rigby, S., and Milsom, C. 1996. Benthic origins of zooplankton: An environmentally determined macroevolutionary effect. Geology 24:52–54.2.3.CO;2>CrossRefGoogle Scholar
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 82:5809–5813.CrossRefGoogle ScholarPubMed
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 37:739–749.CrossRefGoogle Scholar
Schopf, J. W., and Klein, C. 1992. The Proterozoic biosphere. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Sepkoski, J. J. 1992. Proterozoic-Early Cambrian diversification of metazoans and metaphytes. pp. 553–561in Schopf and Klein 1992.Google Scholar
Sheehan, P. M., and Hansen, T. A. 1986. Detritus feeding as a buffer to extinction at the end of the Cretaceous. Geology 14:868–870.2.0.CO;2>CrossRefGoogle Scholar
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 6:50–54.CrossRefGoogle ScholarPubMed
Signor, P. W., and Vermeij, G. J. 1994. The plankton and the benthos: origins and early history of an evolving relationship. Paleobiology 20:297–319.CrossRefGoogle Scholar
Smayda, T. J. 1970. The suspension and sinking of phytoplankton in the sea. Oceanography and Marine Biology Annual Review 8:353–414.Google Scholar
Smetacek, V. 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Marine Biology 84:239–251.CrossRefGoogle Scholar
Smith, S. V. 1981. Marine macrophytes as a global carbon sink. Science 211:838–840.CrossRefGoogle ScholarPubMed
Sogin, M. L. 1989. Evolution of eukaryotic microorganisms and their small subunit ribosomal RNAs. American Zoologist 29:487–499.CrossRefGoogle Scholar
Spjeldnaes, N. 1963. A new fossil (Papillomembrana sp.) from the upper Precambrian of Norway. Nature 200:63–64.CrossRefGoogle Scholar
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 70:1486–1489.CrossRefGoogle ScholarPubMed
Stanley, S. M. 1976. Ideas on the timing of metazoan diversification. Paleobiology 2:209–219.CrossRefGoogle Scholar
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. 95–99in Schopf and Klein 1992.Google Scholar
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 56:2437–2444.CrossRefGoogle Scholar
Tollrian, R. 1995. Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia 101:151–155.CrossRefGoogle ScholarPubMed
Turner, T. T., and Ferrante, J. G. 1979. Zooplankton fecal pellets in aquatic ecosystems. Bioscience 29:670–677.CrossRefGoogle Scholar
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 344:333–335.CrossRefGoogle Scholar
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 48:111–125.Google Scholar
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 112:85–111.CrossRefGoogle Scholar
Verity, P. G., and Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series 130:277–293.CrossRefGoogle Scholar
Vermeij, G. J. 1989. The origin of skeletons. Palaios 4:585–589.CrossRefGoogle Scholar
Vidal, G. 1990. Giant acanthomorph acritarchs from the upper Proterozoic in Southern Norway. Palaeontology 33:287–298.Google Scholar
Vidal, G., and Moczydlowska, M. 1992. Patterns of phytoplankton radiation across the Precambrian-Cambrian boundary. Journal of the Geological Society of London 149:647–654.CrossRefGoogle Scholar
Walossek, D. 1993. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils and Strata 32:1–202.CrossRefGoogle Scholar
Walter, M. 1995. Faecal pellets in world events. Nature 376:16–17.CrossRefGoogle Scholar
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 30:1–21.CrossRefGoogle Scholar
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 199:141–146.CrossRefGoogle ScholarPubMed
Wray, G. A., Levinton, J. S., and Shapiro, L. H. 1996. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274:568–573.CrossRefGoogle Scholar
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 337:61–64.CrossRefGoogle Scholar