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Is biodiversity energy-limited or unbounded? A test in fossil and modern bivalves

Published online by Cambridge University Press:  27 March 2018

Craig R. McClain ,
Noel A. Heim ,
Matthew L. Knope  and
Jonathan L. Payne
Craig R. McClain
Affiliation:
Louisiana Universities Marine Consortium, 8124 Highway 56, Chauvin, Louisiana 70344, U.S.A. E-mail: cmcclain@lumcon.edu
Noel A. Heim
Affiliation:
Department of Geological Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305, U.S.A. E-mail: naheim@stanford.edu, jlpayne@stanford.edu
Matthew L. Knope
Affiliation:
Department of Biology, University of Hawaii, Hilo, 200 W. Kawili Street, Hilo, Hawaii 96720, U.S.A. E-mail: knope@hawaii.edu
Jonathan L. Payne
Affiliation:
Department of Geological Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305, U.S.A. E-mail: naheim@stanford.edu, jlpayne@stanford.edu
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Abstract

The quantity of biomass in an ecosystem is constrained by energy availability. It is less clear, however, how energy availability constrains taxonomic and functional diversity. Competing models suggest biodiversity is either resource-limited or far from any bound. We test the hypothesis that functional diversity in marine bivalve communities is constrained by energy availability, measured as particulate organic carbon (POC) flux, in the modern oceans. We find that POC flux predicts the relative prevalence of ecological modes in both the Atlantic and Pacific Oceans. Moreover, the associations of ecological modes with POC fluxes are similar between the Atlantic and Pacific despite being based on independent sets of species, indicating a direct causal relationship. We then use the relationship between POC flux and the prevalence of functional groups in the modern to test the hypothesis that the trend of increasing functional diversity in bivalves across the past 500 Myr has occurred in response to increased POC flux. We find no evidence that the earliest-appearing modes of life are preferentially associated with low-POC environments or that the mean POC flux experienced by marine bivalves has increased across geological time. To reconcile the close association between ecological mode and POC flux in the modern oceans with the lack of evidence for increasing POC fluxes across time, we propose that POC flux has not increased substantially over time but, rather, the increase in bivalve functional diversity enabled bivalves to become more abundant, to occupy a broader range of environments, and to capture a greater fraction of the total POC flux. The results here suggest at the geographic scale of oceans and through geologic time bivalve diversity was not bounded by food availability.

Type
Articles
Information
Paleobiology , Volume 44 , Issue 3 , August 2018 , pp. 385 - 401
Copyright
© 2018 The Paleontological Society. All rights reserved. 

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References

Literature Cited

Aava, B. 2001. Primary productivity can affect mammalian body size frequency distributions. Oikos 93:205–212.Google Scholar
Abrams, P. A. 1993. Effect of increased productivity on the abundance of trophic levels. American Naturalist 141:351–271.Google Scholar
Alexander, R. M. 2005. Models and the scaling of energy costs for locomotion. Journal of Experimental Biology 208:1645–1652.Google Scholar
Allen, J. A. 2008. Bivalvia of the deep Atlantic. Malacologia 50(1−2), 57–173.Google Scholar
Andrew, M. E., Wulder, M. A., Coops, N. C., and Baillargeon, G.. 2012. Beta-diversity gradients of butterflies along productivity axes. Global Ecology and Biogeography 21:352–364.Google Scholar
Bambach, R. K. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372–397.Google Scholar
Bambach, R. K. 1999. Energetics in the global marinefauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131–144.Google Scholar
Bambach, R. K., Bush, A. M., and Erwin, D. H.. 2007. Autecology and the filling of ecospace: key metazoan radiations. Paleontology 50:1–22.Google Scholar
Beesley, P. L., Ross, G. J. B., and Wells, A., eds. 1998. Mollusca: the southern synthesis, Part B. Australian Biological Reserve, Canberra.Google Scholar
Blackburn, T. M., and Gaston, K. J.. 1996. Spatial patterns in the body sizes of bird species in the New World. Oikos 77:436–446.Google Scholar
Brault, S., Stuart, C., Wagstaff, M., McClain, C. R., Allen, J. A., and Rex, M. A.. 2013. Contrasting patterns of α- and β-diversity in deep-sea bivalves of the eastern and western North Atlantic. Deep-Sea Research II 92:157–164.Google Scholar
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.Google Scholar
Buckley, L. B., Davies, T. J., Ackerly, D. D., Kraft, N. J. B., Harrison, S. P., Anakcer, B. L., Cornell, H. V., Damschen, E. I., Grytnes, J.-A., Hawkins, B. A., McCain, C. M., Stephens, P. R., and Wiens, J. J. 2010. Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals. Proceeding of the Royal Society of London B 277:2131–2138.Google Scholar
Bush, A. M., and Bambach, R. K 2011. Paleoecologic megatrends in marine metazoa. Annual Review of Earth and Planetary Sciences 39:241–269.Google 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.Google Scholar
Carbone, C., Teacher, A., and Rowcliff, J. M. 2007. The cost of carnivory. PLoS Biology 5:e22.Google Scholar
Clarke, A., and Gaston, K. J. 2006. Climate, energy and diversity. Proceedings of the Royal Society of London B 273:2257–2266.Google Scholar
Coan, E. V., Scott, P. V., and Bernard, F. R. 2000. Bivalve seashells of Western North America. Santa Barbara Museum of Natural History, Santa Barbara, Calif.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.Google Scholar
DeAngelis, D. L. 1994. Relationships between the energetics of species and large-scale species richness. Pp 263–272. in C. G. Jones, and J. H. Lawton, eds. Linking species and ecosystems. Chapman & Hall, New York.Google Scholar
Desbruyeres, D., Hashimoto, J., and Fabri, M. 2006. Composition and biogeography of hydrothermnal vent communities in Western Pacific Back-Arc Basins. Pp 215–234. in Back-arc spreading systems: geological, biological, chemical, and physical interactions. American Geophysical Union, Washington, D.C.Google Scholar
Evans, K. L., Warren, P. H., and Gaston, K. J. 1999. Species–energy relationships at the macroecological scale: a review of the mechanisms. Biological Reviews 80:1–25.Google Scholar
Evans, K. L., Greenwood, J. J. D., and Gaston, K. J. 2005. Dissecting the species–energy relationship. Proceeding of the Royal Society of London B 272:2155–2163.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 5682:354–360.Google Scholar
Finnegan, S., McClain, C. R., Kosnik, M., and Payne, J. L. 2011. Escargot through time: an energetic comparison of marine gastropods assemblages beofore and after the Mesozoic Marine Revolution. Paleobiology 37:252–269.Google Scholar
Harmon, L. J., and Harrison, S. 2015. Species diversity is dynamic and unbounded at local and continental scales. American Naturalist 185:584–593.Google Scholar
Hawkins, B. A., Diniz-Filho, J. A. F., Jaramillo, C. A., and Soeller, S. A. 2007. Climate, niche conservatism, and the global bird diversity gradient. American Naturalist 170:S16–S27.Google Scholar
Huber, M. 2010. Compendium of bivalves. A full-color guide to 3,300 of the world’s marine bivalves. A status on Bivalvia after 250 years of research. ConchBooks, Hackenheim, Germany.Google Scholar
Hurlbert, A. H., and Stegen, J. C. 2014. When should species richness be energy limited, and how would we know? Ecology Letters 17:401–413.Google Scholar
Hutchinson, G. E. 1959. Homage to Santa Rosalia, or why are there so many kinds of animals. American Naturalist 93:145–159.Google Scholar
Kidwell, S. M. 2005. Shell composition has no net impact on large-scale evolutionary patterns in mollusks. Science 309:914–917.Google Scholar
Knope, M. L., Heim, N. A., Frishkoff, L. O., and Payne, J. L. 2015. Limited role of functional differentiation in early diversification of animals. Nature Communications 6:6455.Google Scholar
Lutz, M. J., Caldiera, K., Dunbar, R. B., and Behrenfeld, M. J. 2007. Seasonal rhythms of net primary production and particulate organic carbon flux describes biological pump efficiency in the global ocean. Journal of Geophysical Research 112:C10011.Google Scholar
Marra, J., Weibe, P. H., Bishop, J. B., and Stepien, J. C. 1987. Primary production and grazing in the plankton of the Panama Bight. Bulletin of Marine Science 40:255–270.Google Scholar
Marshall, D. J., Krug, P. J., Kupriyanova, E., Byrne, M., and Emlet, R. B. 2012. The biogeography of marine invertebrate life histories. Annual Review of Ecology, Evolution, and Systematics 43:97–114.Google Scholar
Martin, R. 2003. The fossil record of biodiversity: nutrients, productivity, habitat area and differential preservation. Lethaia 36:179–193.Google Scholar
McClain, C. R., and Lundsten, L. 2015. Assemblage structure is related to slope and depth on a deep offshore Pacific seamount chain. Marine Ecology 36:210–220.Google Scholar
McClain, C. R., and Rex, M. A. 2015. Toward a conceptual understanding of β-diversity in the deep-sea benthos. Annual Review of Ecology, Evolution, and Systematics 46:623–642.Google Scholar
McClain, C. R., and Schlacher, T. 2015. On some hypotheses of diversity of animal life at great depths on the seafloor. Marine Ecology 36:849–872. doi: 10.1111/maec.12288.Google Scholar
McClain, C. R., Gullet, T., Jackson-Ricketts, J., and Unmack, P. J. 2012a. Increased energy promotes size-based niche availability in marine mollusks. Evolution 66:2204–2215.Google Scholar
McClain, C. R., Stegen, J. C., and Hurlbert, A. H. 2012b. Dispersal, niche dynamics, and oceanic patterns in beta-diversity in deep-sea bivalves. Proceedings of the Royal Society of London B 279:1933–2002.Google Scholar
McClain, C. R., Filler, R., and Auld, J. R. 2014. Does energy availaiblity predict gastropod reproductive strategies? Proceeding of the Royal Society of London B 281:20140400.Google Scholar
McClain, C. R., Barry, J. P., Eernisse, D., Horton, T., Judge, J., Kakui, K., Mah, C. L., and Waren, A. 2016. Multiple processes generate productivity−diversity relationships in experimental wood-fall communities. Ecology 97:885–898. doi: 10.1890/15-1669.1.Google Scholar
Melo, A. S., Rangel, T. F. L. V. B., and Diniz-Filho, J. A. F. 2009. Environmental drivers of beta-diversity patterns in New-World birds and mammals. Ecography. 32:226–236.Google Scholar
Meyers, K. M., Ridgewell, A., and Payne, J. L. 2016. The influence of the biological pump on ocean chemistry: implications for long-term trends in marine redox chemistry, the global carbon cycle, and marine animal ecosystems. Geobiology 14:207–219.Google Scholar
Moen, J., and Collins, S. L. 1996. Trophic interactions and plant species richness along a productivity gradient. Oikos 76:603–607.Google Scholar
Mönkkönen, M., Forsman, J. T., and Bokma, F. 2006. Energy availability, abundance, energy‐use and species richness in forest bird communities: a test of the species–energy theory. Global Ecology and Biogeography 15:290–302.Google Scholar
Okie, J. G., and Brown, J. H. 2009. Niches, body sizes, and the disassembly of mammal communities on the Sunda Shelf islands. Proceedings of the National Academy of Sciences USA 106 (Suppl. 2), 19679–19684. https://doi.org/10.1073/pnas.0901654106.Google Scholar
Parolo, G., Rossi, G., and Ferrarini, A. 2009. Toward improved species niche modelling: Arnica montana in the Alps as a case study. Journal of Applied Ecology 45:1410–1418.Google Scholar
Payne, J. L., Heim, N. A., Knope, M. L., and McClain, C. R. 2014. Metabolic dominance of bivalves predates brachiopod diversity decline by more than 150 million years. Proceeding of the Royal Society of London B 281:20133122.Google Scholar
Peters, S. E. 2007. The problem with the Paleozoic. Paleiobiology 33:165–181.Google Scholar
Post, D. M. 2002a. The long and short of food-chain length. Trends in Ecology and Evolution 17:269–277.Google Scholar
Post, D. M. 2002b. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.Google Scholar
Rabosky, D. L., and Hurlbert, A. H. 2015. Species richness at continental scales is dominated by ecological limits. American Naturalist 185:572–583.Google Scholar
Rex, M. A., and Etter, R. J. 2010. Deep-sea biodiversity: pattern and scale. Harvard University Press, Cambridge.Google Scholar
Rosenberg, G. 2009. Malacolog 4.1.1: A Database of Western Atlantic Marine Mollusca. http://www.malacolog.org, accessed 20 August 2009.Google Scholar
Rosenzweig, M. L., and Abramsky, Z. 1993. How are diversity and productivity related?. Pp 52–65. in R. E. Ricklefs, and D. Schluter, eds. Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago.Google Scholar
Schoener, T. W. 1976. Alternatives to Lotka-Volterra competition: models of intermediate complexity. Theoretical Population Biology 10:309–333.Google Scholar
Sepkoski, J. J. Jr. 1984. A kinetic model of phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology 10:246–267.Google Scholar
Sepkoski, J. J. Jr., and Miller, A. I. 1985. Evolutionary faunas and the distribution of Paleozoic benthic communities in space and time. Pp 153–190. in J. W. Valentine, ed. Phanerozoic diversity patterns: profiles in macroevolution. AAAS, Pacific Division, and Princeton University Press, Princeton, N.J.Google Scholar
Smith, C. R., and Rabouille, C. 2002. What controls the mixed-layer depth in deep-sea sediments? The importance of POC flux. Limnology and Oceanography 47:418–426.Google Scholar
Srivastava, D. S., and Lawton, J. H. 1998. Why more productive sites have more species: an experimental test of theory using tree-hole communities. American Naturalist 152:510–529.Google Scholar
Stanley, S. M. 2007. Memoir 4: an analysis of the history of marine animal diversity. Paleobiology 33:1–55.Google Scholar
Taylor, C. R., Schmidt-Nielsen, K., and Raab, J. L. 1970. Scaling of energetic costs of running to body size in mammals. American Journal of Physiology 219:1104–1107.Google Scholar
Terribile, L. C., Olalla-Tarraga, M. A., Diniz-Filho, J. A. F., and Rodriguez, M. A. 2009. Ecological and evolutionary components of body size: geographic variation of venomous snakes at the global scale. Biological Journal of the Linnean Society 98:94–109.Google Scholar
Tilman, D. 1982. Resource competition and community structure. Princeton University Press, Princeton, N.J.Google Scholar
Tomašových, A. 2006. Brachiopod and bivalve ecology in Late Triassic (Alps, Austria): onshore–offshore replacements caused by variations in sediment and nutrient supply. Palaios 21:344–368.Google Scholar
Trueman, E. R. 1983. Locomotion in molluscs. Pp 155–198. in A. S. M. Saleuddin, and K. M. Wilbur, eds. The Mollusca: physiology, Part 1. Academic Press, New York.Google Scholar
Tukey, J. W. 1949. Comparing individual means in the analysis of variance. Biometrics 5:99–114.Google Scholar
Veech, J. A., and Crist, T. O. 2007. Habitat and climate heterogeneity maintain beta-diversity of birds among landscapes within ecoregions. Global Ecology and Biogeography 16:652–656.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3:245–258.Google Scholar
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125–152.Google Scholar
Vladimirova, I. G. 2001. Standard metabolic rate in Gastropoda class. Biology Bulletin 28:163–169.Google Scholar
Vladimirova, I. G., Kleimenov, S. Y., and Radzinskaya, L. I. 2003. The relation of energy metabolism and body weight in bivalves (Mollusca: Bivalvia). Biology Bulletin 30:392–399.Google Scholar
Waltari, E., Hijmans, R. J., Peterson, A. T., Nyari, A., Perkins, S. L., and Guralnick, R. P. 2007. Locating Pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS One 2:e563.Google Scholar
Wright, D. H. 1983. Species–energy theory: an extension of species–area theory. Oikos 41:496–506.Google Scholar
Wright, D. H., Currie, D. J., and Maurer, B. A. 1993. Energy supply and patterns of species richness on local and regional scales. Pp 66–74. in. Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago.Google Scholar