Hostname: page-component-745bb68f8f-5r2nc Total loading time: 0 Render date: 2025-01-24T21:54:18.216Z Has data issue: false hasContentIssue false
  • English
  • Français

Escargots through time: an energetic comparison of marine gastropod assemblages before and after the Mesozoic Marine Revolution

Published online by Cambridge University Press:  08 April 2016

Seth Finnegan ,
Craig M. McClain ,
Matthew A. Kosnik  and
Jonathan L. Payne
Seth Finnegan
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305. E-mail: [email protected]
Craig M. McClain
Affiliation:
National Evolutionary Synthesis Center, 2024 West Main Street, Suite A200 Durham, North Carolina 27705
Matthew A. Kosnik
Affiliation:
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Post Office Box 37012, NHB MRC 121, Washington, D.C. 20013-7012
Jonathan L. Payne
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305
Get access Rights & Permissions [Opens in a new window]

Abstract

The modern structure of marine benthic ecosystems was largely established during the Jurassic and Early Cretaceous (200–100 Ma), a transition that has been termed the Mesozoic Marine Revolution (MMR). Although it has been suggested that the MMR marks an increase in the average energy consumption of marine animal ecosystems, this hypothesis has not been evaluated quantitatively. In this study, we integrate body size and abundance data from the fossil record with physiological data from living representatives to estimate mean per capita metabolic rates of tropical to subtropical assemblages of shallow-marine gastropods—a major component of marine ecosystems throughout the Meso-Cenozoic—both before and after the MMR. We find that mean per capita metabolic rate rose by ∼150% between the Late Triassic and Late Cretaceous and remained relatively stable thereafter. The most important factor governing the increase in metabolic rate was an increase in mean body size. In principle, this size increase could result from secular changes in sampling and taphonomic biases, but these biases are suggested to yield decreases rather than increases in mean size. Considering that post-MMR gastropod diversity is dominated by predators, the net primary production required to supply the energetic needs of the average individual increased by substantially more than 150%. These data support the hypothesis that benthic energy budgets increased during the MMR, possibly in response to rising primary productivity.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 2 , Spring 2011 , pp. 252 - 269
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

Aberhan, M., Kiessling, W., and Fürsich, F. T. 2006. Testing the role of biological interactions in the evolution of mid-Mesozoic marine benthic ecosystems. Paleobiology 32:259–277.CrossRefGoogle Scholar
Anbar, A. D., and Knoll, A. H. 2002. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297:1137–1142.CrossRefGoogle ScholarPubMed
Bambach, R. K. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372–397.CrossRefGoogle Scholar
Bambach, R. K. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131–144.CrossRefGoogle Scholar
Bambach, R. K. 2002. Supporting predators: changes in the global ecosystem inferred from changes in predator diversity. In Kowalewski, M. and Kelley, P. H., eds. The fossil record of predation. Paleontological Society Special Papers 8:319–352.CrossRefGoogle Scholar
Bandel, K. 1999. On the origin of the carnivorous gastropod group Naticoidea (Mollusca) in the Cretaceous with description of some convergent but unrelated groups. Greifswalder Geowissenschaftliche Beiträge 6:143–175.Google Scholar
Barkai, R., and Griffiths, C. L. 1988. An energy budget for the South African abalone Haliotis midae Linnaeus. Journal of Molluscan Studies 54:43–51.CrossRefGoogle Scholar
Beesley, P. L., Ross, G. J. B., and Wells, A., eds. 1998. Mollusca: the southern synthesis. CSIRO publishing, Melbourne.Google Scholar
Behrensmeyer, A. K., Kidwell, S. M., and Gastaldo, R. A. 2000. Taphonomy and paleobiology. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective Paleobiology 36(Suppl. to No. 4):103–147.CrossRefGoogle Scholar
Berner, R. A., and Kothavala, Z. 2001. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 301:182–204.CrossRefGoogle Scholar
Bouchet, P., Lozouet, P., Maestrati, P., and Heros, V. 2002. Assessing the magnitude of species richness in tropical marine environments: exceptionally high numbers of molluscs at a New Caledonia site. Biological Journal of the Linnean Society 75:421–436.CrossRefGoogle Scholar
Brayard, A., Nützel, A., Stephen, D. A., Bylund, K. G., Jenks, J., and Bucher, H. 2010. Gastropod counter-evidences for the Early Triassic Lilliput effect. Geology 38:147–150.CrossRefGoogle Scholar
Bromley, R. G. 2004. A stratigraphy of marine bioerosion. Geological Society of London Special Publication 228:455–479.CrossRefGoogle Scholar
Bush, A. M., Bambach, R. K., and Daley, G. M. 2007. Changes in theoretical ecospace utilization in marine fossil assemblages between the mid-Paleozoic and late Cenozoic. Paleobiology 33:76–97.CrossRefGoogle Scholar
Collins, L. S. 2005. Panama Paleontology Project faunal data files. Florida International University. http://www2.fju.edu/∼collinsl/pppdatabase.html Google Scholar
Collins, L. S., and Coates, A. G. 1999. A paleobiotic survey of Caribbean faunas from the Neogene of the Isthmus of Panama. Bulletins of American Paleontology 357:119–158.Google Scholar
Cooper, R. A., Maxwell, P. A., Crampton, J. S., Beu, A. G., Jones, C. M., and Marshall, B. A. 2006. Completeness of the fossil record: estimating losses due to small body size. Geology 34:241–244.CrossRefGoogle Scholar
Cummins, R. H., Powell, E. N., Stanton, R. J. Jr., and Staff, G. 1986. The size frequency distribution in paleoecology: the effects of taphonomic processes during formation of death assemblages in Texas bays. Paleontology 29:495–518.Google Scholar
Dodds, P. S., Rothman, D. H., and Weitz, J. S. 2001. Reexamination of the “3/4-law” of metabolism. Journal of Theoretical Biology 209:9–27.CrossRefGoogle ScholarPubMed
Falkowski, P. G., and Knoll, A. H., eds. 2007. Evolution of primary producers in the sea. Academic Press, London.Google Scholar
Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofield, O., and Taylor, F. J. R. 2004. The evolution of modern eukaryotic phytoplankton. Science 305:354–360.CrossRefGoogle ScholarPubMed
Finnegan, S., and Droser, M. L. 2008. Body size, energetics, and the Ordovician restructuring of marine ecosystems. Paleobiology 34:342–359.CrossRefGoogle Scholar
Fraiser, M. L., and Bottjer, D. J. 2004. The non-actualistic Early Triassic gastropod fauna: a case study of the Lower Triassic Sinbad Limestone member. Palaios 19:259–275.2.0.CO;2>CrossRefGoogle Scholar
Fraiser, M. L., Twitchett, R. J., and Bottjer, D. J. 2005. Unique microgastropod biofacies in the Early Triassic: indicator of long-term biotic stress and the pattern of biotic recovery after the end-Permian mass extinction. Comptes Rendus Palevol 4:475–484.CrossRefGoogle Scholar
Frankovitch, T. 2003. Gastropod biomass and densities found at Rabbit Key Basin, Florida Bay from March 2000 to April 2001. Florida Coastal Everglades LTER Program. http://fcelter.fiu.edu/data/core/metadata/?datasetid=ST_CD_Frankovich_001 Google Scholar
Fürsich, F. T., and Jablonski, D. 1984. Late Triassic naticid drillholes: carnivorous gastropods gain a major adaptation but fail to radiate. Science 224:78–80.CrossRefGoogle Scholar
Gahn, F. J., and Baumiller, T. K. 2003. Infestation of Middle Devonian (Givetian) camerate crinoids by platyceratid gastropods and its implications for the nature of their biotic interaction. Lethaia 36:71–82.CrossRefGoogle Scholar
Gahn, F. J., Fabian, A., and Baumiller, T. K. 2003. Additional evidence for the drilling behavior of Paleozoic gastropods. Acta Palaeontologica Polonica 48:156–156.Google Scholar
Gillooly, J. F. 2001. Effects of size and temperature on metabolic rate. Science 293:2248–2251.CrossRefGoogle ScholarPubMed
Hendy, A. J. W. 2009. The influence of lithification on Cenozoic marine biodiversity trends. Paleobiology 35:51–62.CrossRefGoogle Scholar
Huebner, J. D., and Edwards, D. C. 1981. Energy budget of the predatory marine gastropod Polinices duplicatus . Marine Biology 61:221–226.CrossRefGoogle Scholar
Hughes, R. N. 1986. A functional biology of marine gastropods. Croom Helm, London.Google Scholar
Jahnke, R. A. 1996. The global ocean flux of particulate organic carbon: areal distribution and magnitude. Global Biogeochemical Cycles 10.CrossRefGoogle Scholar
Jung, P. 1965. Miocene Mollusca from the Paraguaná Peninsula, Venezuela. Bulletins of American Paleontology 49:387–644.Google Scholar
Jung, P. 1969. Miocene and Pliocene mollusks from Trinidad. Bulletins of American Paleontology 55:293–657.Google Scholar
Kase, T., and Ishikawa, M. 2003. Mystery of naticid predation history solved: evidence from a “living fossil” species. Geology 31:403–406.2.0.CO;2>CrossRefGoogle Scholar
Katz, M. E., Finkel, Z. V., Grzebyk, D., Knoll, A. H., and Falkowski, P. G. 2004. Evolutionary trajectories and biogeochemical impacts of marine eukaryotic phytoplankton. Annual Review of Ecology Evolution and Systematics 35:523–556.CrossRefGoogle Scholar
Katz, M. E., Wright, J. D., Miller, K. G., Cramer, B. S., Fennel, K., and Falkowski, P. G. 2005. Biological overprint of the geological carbon cycle. Marine Geology 217:323–338.CrossRefGoogle Scholar
Kerr, S. R., and Dickie, L. M. 2001. The biomass spectrum: a predator-prey theory of aquatic production. Columbia University Press, New York.Google Scholar
Kidwell, S. M. 2001. Preservation of species abundance in marine death assemblages. Science 294:1091–1094.CrossRefGoogle ScholarPubMed
Kidwell, S. M. 2002. Time-averaged molluscan death assemblages: palimpsests of richness, snapshots of abundance. Geology 30:803–806.2.0.CO;2>CrossRefGoogle Scholar
Kidwell, S. M., and Bosence, D. W. J. 1991. Taphonomy and time-averaging of marine shelly faunas.CrossRefGoogle Scholar
Kidwell, S. M., and Brenchley, P. J. 1996. Evolution of the fossil record: thickness trends in marine skeletal accumulations and their implications. Pp. 290–336 in Jablonski, D., Erwin, D. H., and Lipps, J. H., eds. Evolutionary paleobiology: essays in honor of James W. Valentine. University of Chicago Press, Chicago.Google Scholar
Kosnik, M. A. 2005. Changes in Late Cretaceous-early Tertiary benthic marine assemblages: analyses from the North American coastal plain shallow shelf. Paleobiology 31:459–479.CrossRefGoogle Scholar
Kosnik, M. A., Jablonski, D., Lockwood, R., and Novack-Gottshall, P. M. 2006. Quantifying molluscan body size in evolutionary and ecological analyses: maximizing the return on data collection efforts. Palaios 21:588–597.CrossRefGoogle Scholar
Kosnik, M. A., Hua, Q., Jacobsen, G. E., Kaufman, D. S., and Wüst, R. A. 2007. Sediment mixing and stratigraphic disorder revealed by the age-structure of Tellina shells in Great Barrier Reef sediment. Geology 35:811–814.CrossRefGoogle Scholar
Kosnik, M. A., Hua, Q., Kaufman, D. S., and Wüst, R. A. 2009. Taphonomic bias and time-averaging in tropical molluscan death assemblages: differential shell half-lives in Great Barrier Reef sediment. Paleobiology 34:565–586.CrossRefGoogle Scholar
Kowalewski, M. 1997. The reciprocal taphonomic model. Lethaia 30:86–88.CrossRefGoogle Scholar
Kozlowski, J., and Gawelczyk, A. T. 2002. Why are species' body size distributions usually skewed to the right? Functional Ecology 16:419–432.CrossRefGoogle Scholar
Krause, R. A., Stempien, J. A., Kowalewski, M., and Miller, A. I. 2007. Body size estimates from the literature: utility and potential for macroevolutionary studies. Palaios 22:60–73.CrossRefGoogle Scholar
Madin, J. S., Alroy, J., Aberhan, M., Fürsich, F. T., Kiessling, W., Kosnik, M. A., and Wagner, P. J. 2006. Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates. Science 312:897–900.CrossRefGoogle ScholarPubMed
MARGO project members. 2009. Constraints on the magnitude and patterns of ocean cooling at the Last Glacial Maximum. Nature Geoscience 2:127–132.CrossRefGoogle Scholar
Martin, R. E. 1996. Secular increase in nutrient levels through the Phanerozoic: implications for productivity, biomass, and diversity of the marine biosphere. Palaios 11:209–219.CrossRefGoogle Scholar
McClain, C. R. 2004. Connecting species richness, abundance and body size in deep-sea gastropods. Global Ecology and Biogeography 13:327–334.CrossRefGoogle Scholar
McClain, C. R. 2005. Bathymetric patterns of morphological disparity in deep-sea gastropods from the western North Atlantic Basin. Evolution 59:1492–1499.Google ScholarPubMed
McClain, C. R., Johnson, N. A., and Rex, M. A. 2004. Morphological disparity as a biodiversity metric in lower bathyal and abyssal gastropod assemblages. Evolution 58:338–348.Google ScholarPubMed
McClanahan, , and McClanahan, T. 2002. A comparison of the ecology of shallow subtidal gastropods between western Indian Ocean and Caribbean coral reefs. Coral Reefs 21:399–406.CrossRefGoogle Scholar
Miller, A. I. 1988. Spatial resolution in subfossil molluscan remains; implications for paleobiological analyses. Paleobiology 14:91–103.CrossRefGoogle Scholar
Miller, A. I., Llewellyn, G., Parsons, K. M., Cummins, H., Boardman, M. R., Greenstein, B. J., and Jacobs, D. K. 1992. Effect of Hurricane Hugo on molluscan skeletal distributions, Salt River Bay, St. Croix, U.S. Virgin Islands. Geology 20:23–26.2.3.CO;2>CrossRefGoogle Scholar
Morton, B., and Chan, K. 1999. Hunger rapidly overrides the risk of predation in the subtidal scavenger Nassarius siquijorensis (Gastropoda: Nassariidae): an energy budget and a comparison with the intertidal Nassarius festivus in Hong Kong. Journal of Experimental Marine Biology and Ecology 240:213–228.CrossRefGoogle Scholar
Novack-Gottshall, P. M. 2008. Ecosystem-wide body size trends in Cambrian-Devonian marine invertebrate lineages. Paleobiology 34:210–228.CrossRefGoogle Scholar
Nützel, A., and Kiessling, W. 1997. Gastropoden aus dem Amaltheenton (oberes Pliensbachium) von Kalchreuth. Geologische Blätter für Nordost Bayern 47:381–414.Google Scholar
Nützel, A., Mannani, M., Senowbari-Daryan, B., and Yazdi, M. 2010. Gastropods from the Late Triassic Nayband Formation (Iran), their relationships to other Tethyan faunas and remarks on the Triassic gastropod body size problem. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 256:213–228.CrossRefGoogle Scholar
Olabarria, C., and Thurston, M. H. 2003. Latitudinal and bathymetric trends in body size of the deep-sea gastropod Troschelia berniciensis (King). Marine Biology 143:723–730.CrossRefGoogle Scholar
Paine, R. T. 1971. Energy flow in a natural population of the herbivorous gastropod Tegula funebralis . Limnology and Oceanography 16:86–98.CrossRefGoogle Scholar
Payne, J. L. 2005. Evolutionary dynamics of gastropod size across the end-Permian extinction and through the Triassic recovery interval. Paleobiology 31:269–290.CrossRefGoogle Scholar
Payne, J. L., and Finnegan, S. 2006. Controls on marine animal biomass through geological time. Geobiology 4:1–10.CrossRefGoogle Scholar
Payne, J. L., Lehrmann, D. J., Wei, J., and Knoll, A. H. 2006. The pattern and timing of biotic recovery from the end-Permian extinction on the Great Bank of Guizhou, Guizhou Province, China. Palaios 21:63–85.CrossRefGoogle Scholar
Ponder, W. F. and Lindberg, D. R., eds. 2005. Phylogeny and evolution of the Mollusca. University of California Press, Berkeley.Google Scholar
Powell, E. N., Cummins, R. H., Stanton, R. J. Jr., and Staff, G. 1984. Estimation of the size of molluscan larval sets using the death assemblage. Estuarine Coastal and Shelf Science 18:367–384.CrossRefGoogle Scholar
Powell, E. N., Staff, G. M., Stanton, R. J., and Callender, W. R. 2001. Application of trophic transfer efficiency and age structure in the trophic analysis of fossil assemblages. Lethaia 34:97–118.CrossRefGoogle Scholar
Powell, E. N., and Stanton, R. J. 1985. Estimating biomass and energy-flow of mollusks in paleo-communities. Paleontology 28:1–34.Google Scholar
Rex, M. A., Ron, J. E., Clain, A. J., and Hill, M. S. 1999. Bathymetric patterns of body size in deep-sea gastropods. Evolution 53:1298–1301.Google ScholarPubMed
Rosenberg, G. 2009. Malacolog 4.1.1: a database of Western Atlantic marine Mollusca. http://www.malacolog.org/ Google Scholar
Roy, K. 2002. Bathymetry and body size in marine gastropods: a shallow water perspective. Marine Ecology Progress Series 237:143–149.CrossRefGoogle Scholar
Sanders, H. L. 1968. Benthic marine diversity: a comparative study. American Naturalist 102:660–668.CrossRefGoogle Scholar
Schubert, S., Gründel, J., and Nützel, A. 2008. Early Jurassic (Upper Pliensbachian) gastropods from the Herforder Liasmulde (Bielefeld, Northwest Germany). Paläontologische Zeitschrift 82:17–30.CrossRefGoogle Scholar
Seibel, B. A. 2007. On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca). Journal of Experimental Biology 210:1–11.CrossRefGoogle ScholarPubMed
Sepkoski, J. J. Jr. 2002. A compendium of fossil marine animal genera. Bulletins of American Paleontology 363:560.Google Scholar
Sessa, J. A., Patzkowsky, M. E., and Bralower, T. J. 2009. The impact of lithification on the diversity, size distribution, and recovery dynamics of marine invertebrate assemblages. Geology 37:115–118.CrossRefGoogle Scholar
Sohl, N. F. 1987. Cretaceous gastropods: contrasts between Tethys and the temperate provinces. Journal of Paleontology 61:1085–1111.CrossRefGoogle Scholar
Staff, G. M., Stanton, R. J. Jr., Powell, E. N., and Cummins, H. 1986. Time-averaging, taphonomy, and their impact on paleocommunity reconstruction; death assemblages in Texas bays. Geological Society of America Bulletin 97:428–443.2.0.CO;2>CrossRefGoogle Scholar
Sterner, R. W., and Elser, J. J. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, N.J. Google Scholar
Sutton, M. D., Briggs, D. E. G., and Siveter, D. J. 2006. Fossilized soft tissues in a Silurian platyceratid gastropod. Proceedings of the Royal Society of London B 273:1039–1044.Google Scholar
Thayer, C. W. 1979. Biological bulldozers and the evolution of marine benthic communities. Science 203:458–461.CrossRefGoogle ScholarPubMed
Thayer, C. W. 1983. Sediment-mediated biological disturbance and the evolution of marine benthos. Pp. 649–669 in Tevesz, M. J. S. and McCall, P. L., eds. Biotic interactions in Recent and fossil benthic communities. Plenum, New York.Google Scholar
Todd, J. A. 2000. NMITA gastropod diets database.Google Scholar
Todd, J. A., Fortunato, H., Jackson, J. B. C., and Jung, P. 2006. Neogene marine biota of North America: gastropods. University of Iowa.Google Scholar
Valentine, J. W. 1973. Evolutionary paleoecology of the marine biosphere. Prentice-Hall, Englewood Cliffs, N.J. Google Scholar
Van Valen, L. 1976. Energy and evolution. Evolutionary Theory 1:179–229.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution; evidence from snails, predators and grazers. Paleobiology 3:245–258.CrossRefGoogle Scholar
Vermeij, G. J. 1978. Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge.Google Scholar
Vermeij, G. J. 1983. Shell-breaking predation through time. Pp. 649–669 in Tevesz, M. J. S. and McCall, P. L., eds. Biotic interactions in Recent and fossil benthic communities. Plenum, New York.CrossRefGoogle Scholar
Vermeij, G. J. 1987. Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J. CrossRefGoogle Scholar
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125–152.CrossRefGoogle Scholar
Vermeij, G. J. 2002. Evolution in the consumer age: predators and the history of life. Paleontological Society Papers 8:375–393.CrossRefGoogle Scholar
Vermeij, G. J. 2004. Nature: an economic history. Princeton University Press, Princeton, N.J. CrossRefGoogle Scholar
Vladimirova, I. G. 2001. Standard metabolic rate in Gastropoda Class. Biology Bulletin, 28:163–169.CrossRefGoogle Scholar
Wagner, P. J., Kosnik, M. A., and Lidgard, S. 2006. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:1289–1292.CrossRefGoogle ScholarPubMed
Weisbord, N. E. 1962. Late Cenozoic gastropods from northern Venezuela. Bulletins of American Paleontology 42:672.Google Scholar
Woodring, W. P. 1928. Miocene mollusks from Bowden, Jamaica, Part II. Gastropods and discussion of results. Carnegie Institution of Washington Publication 385:564.Google Scholar
Woodring, W. P. 1957–1982. Geology and paleontology of Canal Zone and adjoining parts of Panama. United States Geological Survey Professional Paper 306A-E:1–759.Google Scholar
Zardini, R. 1978. Fossili cassiani (Trias Medio-Superiore). Atlantae dei gastropodi della formazione di S. Cassiano raccolti nella regione dolomitica attorno a Cortina d'Ampezzo. Ghedina, Cortina d'Ampezzo.Google Scholar
Supplementary material: File

Finnegan et al. supplementary material

Appendix 1

Download Finnegan et al. supplementary material(File)
File 163.8 KB