Mass extinctions disrupt ecological communities. Although climate changes produce stress in ecological communities, few paleobiological studies have systematically addressed the impact of global climate changes on the fine details of community structure with a view to understanding how changes in community structure presage, or even cause, biodiversity decline during mass extinctions. Based on a novel Bayesian approach to biotope assessment, we present a study of changes in species abundance distribution patterns of macroplanktonic graptolite faunas (∼447-444 Ma) leading into the Late Ordovician mass extinction. Communities at two contrasting sites exhibit significant decreases in complexity and evenness as a consequence of the preferential decline in abundance of dysaerobic zone specialist species. The observed changes in community complexity and evenness commenced well before the dramatic population depletions that mark the tipping point of the extinction event. Initially, community changes tracked changes in the oceanic water masses, but these relations broke down during the onset of mass extinction. Environmental isotope and biomarker data suggest that sea surface temperature and nutrient cycling in the paleotropical oceans changed sharply during the latest Katian time, with consequent changes in the extent of the oxygen minimum zone and phytoplankton community composition. Although many impacted species persisted in ephemeral populations, increased extinction risk selectively depleted the diversity of paleotropical graptolite species during the latest Katian and early Hirnantian. The effects of long-term climate change on habitats can thus degrade populations in ways that cascade through communities, with effects that culminate in mass extinction.

Department of Earth Sciences Dalhousie University Halifax NS Canada B3H 4R2;

Department of Earth Sciences St Francis Xavier University Antigonish NS Canada B2G 2W5;

Department of Geology University at Buffalo The State University of New York Buffalo NY 14260;

Department of Physics Canisius College Buffalo NY 14208;

Institute of Geology The Czech Academy of Sciences 165 00 Prague 6 Czech Republic

Komentář v

Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):8349-51. doi: 10.1073/pnas.1608630113. PubMed

Zobrazit více v PubMed

Droser ML, Bottjer DJ, Sheehan PM, McGhee GR. Decoupling of taxonomic and ecologic severity of Phanerozoic marine mass extinctions. Geology. 2000;28(8):675–678.

McGhee GR, Jr, Clapham ME, Sheehan PM, Bottjer DJ, Droser ML. A new ecological-severity ranking of major Phanerozoic biodiversity crises. Palaeogeogr Palaeoclimatol Palaeoecol. 2013;370:260–270.

Brenchley PJ, Marshall JD, Underwood CJ. Do all mass extinctions represent an ecological crisis? Evidence from the Late Ordovician. Geol J. 2001;36(3-4):329–340.

Hull PM, Darroch SAF. 2013. Mass extinctions and the structure and function of ecosytems. Ecosystem Paleobiology and Geobiology, The Paleontological Society Short Course, October 26, 2013, Paleontological Society Papers, eds Bush AM, Pruss SB, Payne JL (Paleontol Soc, Boulder, CO), Vol 19, pp 1–42.

Solé RV, Saldaña J, Montoya JM, Erwin DH. Simple model of recovery dynamics after mass extinction. J Theor Biol. 2010;267(2):193–200. PubMed

Wagner PJ, Kosnik MA, Lidgard S. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science. 2006;314(5803):1289–1292. PubMed

Clémence M-E, Hart MB. Proliferation of Oberhauserellidae during the recovery following the Late Triassic extinction: Paleoecological implications. J Paleontol. 2013;87(6):1004–1015.

McElwain JC, Wagner PJ, Hesselbo SP. Fossil plant relative abundances indicate sudden loss of Late Triassic biodiversity in East Greenland. Science. 2009;324(5934):1554–1556. PubMed

Pandolfi JM, Lovelock CE. Ecology. Novelty trumps loss in global biodiversity. Science. 2014;344(6181):266–267. PubMed

Dornelas M, et al. Assemblage time series reveal biodiversity change but not systematic loss. Science. 2014;344(6181):296–299. PubMed

Melchin MJ, Mitchell CE, Naczk-Cameron A, Fan JX, Loxton J. Phylogeny and adaptive radiation of the Neograptina (Graptoloida) during the Hirnantian mass extinction and Silurian recovery. Proc Yorks Geol Soc. 2011;58(4):281–309.

Melchin MJ, Mitchell CE. 1991. Late Ordovician extinction in the Graptoloidea. Advances in Ordovician Geology, Geological Survey of Canada Papers, eds Barnes CR, Williams SH, (Geol Surv Canada, Ottawa), Vol 90-9, pp 143–156.

Xu C, Melchin MJ, Sheets HD, Mitchell CE, Fan J. Patterns and processes of latest Ordovician graptolite mass extinction and recovery based on data from South China. J Paleontol. 2005;79(5):842–861.

Goldman D, et al. Biogeography and mass extinction: Extirpation and re-invasion of Normalograptus species (Graptolithina) in the Late Ordovician palaeotropics. Proc Yorks Geol Soc. 2011;58(4):227–246.

Finney SC, Berry WBN, Cooper JD. The influence of denitrifying seawater on graptolite extinction and diversification during the Hirnantian (Latest Ordovician) mass extinction event. Lethaia. 2007;40(3):281–291.

Bapst DW, Bullock PC, Melchin MJ, Sheets HD, Mitchell CE. Graptoloid diversity and disparity became decoupled during the Ordovician mass extinction. Proc Natl Acad Sci USA. 2012;109(9):3428–3433. PubMed PMC

Crampton JS, Cooper RA, Sadler PM, Foote M. Greenhouse−icehouse transition in the Late Ordovician marks a step change in extinction regime in the marine plankton. Proc Natl Acad Sci USA. 2016;113(6):1498–1503. PubMed PMC

Finnegan S, Rasmussen CM, Harper DA. Biogeographic and bathymetric determinants of brachiopod extinction and survival during the late Ordovician mass extinction. Proc R Soc B. April 27, 2016 doi: 10.1098/rspb.2016.0007. PubMed DOI PMC

Cooper RA, Rigby S, Loydell DK, Bates DEB. Palaeoecology of the Graptoloidea. Earth Sci Rev. 2012;112(1-2):23–41.

Cooper RA, Sadler P. Facies preference predicts extinction risk in Ordovician graptolites. Paleobiology. 2010;32(2):167–187.

LaPorte DF, et al. Local and global perspectives on carbon and nitrogen cycling during the Hirnantian glaciation. Palaeogeogr Palaeoclimatol Palaeoecol. 2009;276(1-4):182–195.

Melchin MJ, Mitchell CE, Holmden C, Štorch P. Environmental changes in the Late Ordovician−Early Silurian: Review and new insights from black shales and nitrogen isotopes. Geol Soc Am Bull. 2013;125(11/12):1635–1670.

Trotter JA, Williams IS, Barnes CR, Lécuyer C, Nicoll RS. Did cooling oceans trigger Ordovician biodiversification? Evidence from conodont thermometry. Science. 2008;321(5888):550–554. PubMed

Finnegan S, et al. The magnitude and duration of Late Ordovician−Early Silurian glaciation. Science. 2011;331(6019):903–906. PubMed

Cooper RA, Sadler PM, Munnecke A, Crampton JS. Graptoloid evolutionary rates track Ordovician–Silurian global climate change. Geol Mag. 2014;151(2):349–364.

Brenchley PJ, et al. Bathymetric and isotopic evidence for a short-lived Late Ordovician glaciation in a greenhouse period. Geology. 1994;22(4):295–298.

Brenchley PJ. End Ordovician glaciation. In: Webby BD, Paris F, Droser ML, Percival IG, editors. The Great Ordovician Biodiversification Event. Columbia Univ Press; New York: 2004. pp. 81–83.

Jones DS, Fike DA. Dynamic sulfur and carbon cycling through the end-Ordovician extinction revealed by paired sulfate–pyrite δ34S. Earth Planet Sci Lett. 2013;363:144–155.

Zhou L, et al. Changes in marine productivity and redox conditions during the Late Ordovician Hirnantian glaciation. Palaeogeogr Palaeoclimatol Palaeoecol. 2015;420:223–234.

Rohrssen M, Love GD, Fischer W, Finnegan S, Fike DA. Lipid biomarkers record fundamental changes in the microbial community structure of tropical seas during the Late Ordovician Hirnantian glaciation. Geology. 2013;41(2):127–130.

Finney SC, Perry BD. 1991. Depositional setting and palaeogeography of Ordovician Vinini Formation, central Nevada. Paleozoic Paleogeography of the Western United States 2: Pacific Section, eds Cooper JD, Stevens CH (Soc Sed Geol, Pacific Sect, Los Angeles), Vol 2, pp 747−766.

Lenz AC, McCracken AD. The Ordovician−Silurian boundary, northern Canadian Cordillera: Graptolite and conodont correlation. Can J Earth Sci. 1982;19(6):1308–1322.

Loxton J, Melchin MJ, Mitchell CE, Senior SJH. Ontogeny and astogeny of the graptolite genus Appendispinograptus (Li and Li, 1985) Proc Yorks Geol Soc. 2011;58(4):253–260.

Holmden C, et al. Nd isotope records of late Ordovician sea-level change—Implications for glaciation frequency and global stratigraphic correlation. Palaeogeogr Palaeoclimatol Palaeoecol. 2013;386(18):131–144.

Harris MT, Sheehan PM. Carbonate sequences and fossil communities from the Upper Ordovician−Lower Silurian of the Eastern Great Basin. Brigham Young Univ Geol Stud. 1997;42(1):105–128.

Jones DS, Creel RC, Rios BA. Carbon isotope stratigraphy and correlation of depositional sequences in the Upper Ordovician Ely Springs Dolostone, eastern Great Basin, USA. Palaeogeogr Palaeoclimatol Palaeoecol. January 26, 2016 doi: 10.1016/j/palaeo.2016.01.036. DOI

Fortey RA, Cocks LRM. Late Ordovician global warming—The Boda event. Geology. 2005;33(5):405–408.

Armstrong HA, Baldini J, Challands TJ, Gröcke DR, Owen AW. Response of the Inter-tropical Convergence Zone to Southern Hemisphere cooling during Upper Ordovician glaciation. Palaeogeogr Palaeoclimatol Palaeoecol. 2009;284(3-4):227–236.

Jiménez-Sánchez A, Villas E. The bryozoan dispersion into the Mediterranean margin of Gondwana during the pre-glacial Late Ordovician. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;294(3-4):220–231.

Sadler PM, Cooper RA, Melchin MJ. Sequencing the graptoloid clade: Building a global diversity curve from local range charts, regional composites and global time-lines. Proc Yorks Geol Soc. 2011;58(4):329–343.

Štorch P, Mitchell CE, Finney SC, Melchin MJ. Uppermost Ordovician (upper Katian−Hirnantian) graptolites of north-central Nevada, U.S.A. Bull Geosci. 2011;86(2):301–386.

Jablonski D. Survival without recovery after mass extinctions. Proc Natl Acad Sci USA. 2002;99(12):8139–8144. PubMed PMC

Holland SM, Patzkowsky ME. The stratigraphy of mass extinction. Palaeontology. 2015;58(5):903–924.

Finnegan S, Heim NA, Peters SE, Fischer WW. Climate change and the selective signature of the Late Ordovician mass extinction. Proc Natl Acad Sci USA. 2012;109(18):6829–6834. PubMed PMC

Greenacre MJ. Theory and Applications of Correspondence Analysis. Academic; London: 1984.

Aikake H. 1973. Information theory and an extension of the maximum likelihood principle. Proceedings of the Second International Symposium on Information Theory, eds Petrov BN, Caski F (Akad Kiado, Budapest), pp 267−281.

Boyle JT, et al. A re-examination of the contributions of biofacies and geographic range to extinction risk in Ordovician graptolites. GFF. 2014;136(1):38–41.

Finney SC, et al. Late Ordovician mass extinction: A new perspective from stratigraphic sections in central Nevada. Geology. 1999;27(3):215–218.

Ruedemann R. Graptolites of North America. Mem Geol Soc Am. 1947;19:1–652.

Carter C, Churkin MJ. Ordovician and Silurian graptolite succession in the Trail Creek area, Central Idaho—A graptolite zone reference section. US Geol Surv Prof Pap. 1977;1020:1–37.

Mitchell CE, Goldman D, Cone MR, Maletz J, Janousek H. 2003. Ordovician graptolites of the Phi Kappa Formation at Trail Creek, Central Idaho, USA: A revised biostratigraphy. Proceedings of the Seventh International Graptolite Conference, eds Ortega G, Aceñolaza FG (Inst Superior Correl Geol, San Miguel de Tucumán, Argentina), pp 69−72.

Goldman D, et al. Ordovician graptolites and conodonts of the Phi Kappa Formation in the Trail Creek region of central Idaho: A revised, integrated biostratigraphy. Acta Palaeontol Sin. 2007;46(Suppl):155–162.

Ross RB, Berry WBN. Ordovician graptolites of the Basin Ranges in California, Nevada, Utah and Idaho. US Geol Surv Bull. 1963;1134:1–177.

Melchin MJ. Upper Ordovician graptolites from the Cape Phillips Formation, Canadian Arctic Islands. Bull Geol Soc Den. 1987;35(3-4):191–202.

Melchin MJ, McCracken AD, Oliff FJ. The Ordovician−Silurian boundary on Cornwallis and Truro islands, Arctic Canada: Preliminary data. Can J Earth Sci. 1991;28(11):1854–1862.

Williams SH. The late Ordovician graptolite fauna of the Anceps bands at Dob’s Linn, southern Scotland. Geol Palaeontol. 1982;16:29–56.

Williams SH. The Ordovician−Silurian boundary graptolite fauna of Dob’s Linn, southern Scotland. Palaeontology. 1983;26(3):605–639.

Melchin MJ, Holmden C, Williams SH. Correlation of graptolite biozones, chitinozoan biozones, and carbon isotope curves through the Hirnantian. In: Albanesi GL, Beresi MS, Peralta SH, editors. Ordovician from the Andes. Inst Superior Correl Geol; San Miguel de Tucumán, Argentina: 2003. pp. 101–104.

Koren TN, Oradovskaya MM, Pylma LJ, Sobolevskaya RF, Chugaeva MN. 1983. The Ordovician and Silurian Boundary in the Northeast of the U.S.S.R. (Nauka, Leningrad, Russia). Russian.

Koren TN, Sobolevskaja RF. The regional stratotype section and point for the base of the Hirnantian Stage (the uppermost Ordovician) at Mirny Creek, Omulev Mountains, Northeast Russia. Est J Earth Sci. 2008;57(1):1–10.

Apollonov MK, Bandaletov SM, Nikitin JF. 1980. The Ordovician−Silurian Boundary in Kazakhstan (Kazakh SSR, Pechat, Kazakhstan). Russian.

Apollonov MK, Koren TN, Nikitin IF, Paletz LM, Tsai DT. Nature of the Ordovician-Silurian boundary in South Kazakhstan, U.S.S.R. In: Cocks LRM, Rickards RB, editors. A Global Analysis of the Ordovician−Silurian Boundary. Nat Hist Museum; London: 1988. pp. 145–154.

Chen X, et al. Late Ordovician to earliest Silurian graptolite and brachiopod biozonation from the Yangtze region, South China with a global correlation. Geol Mag. 2000;137(6):623–650.

Chen X, Fan JX, Melchin MJ, Mitchell CE. Hirnantian (Latest Ordovician) graptolites from the Upper Yantze region, China. Palaeontology. 2005;48(2):235–280.

Chen X, et al. The global boundary stratotype section and point (GSSP) for the base of the Hirnantian Stage (the uppermost of the Ordovician System) Episodes. 2006;29(3):183–197.

Fan JX, et al. Geobiodiversity Database (GBDB) in stratigraphic, palaeontological and palaeogeographic research: Graptolites as an example. GFF. 2014;136(1):70–74.

Brenchley PJ. Late Ordovician Extinction. In: Briggs DEG, Crowther PR, editors. Palaeobiology II. Blackwell; Oxford: 2001. pp. 220–223.

Harper DA, Hammarlund EU, Rasmussen CM. End Ordovician extinctions: A coincidence of causes. Gondwana Res. 2014;25(4):1294–1307.

Desrochers A, Farley C, Achab A, Asselin E, Riva JF. A far-field record of the end Ordovician glaciation: The Ellis Bay Formation, Anticosti Island, Eastern Canada. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;296(3-4):248–263.

Kiessling W, Martin A. Environmental determinants of marine benthic biodiversity dynamics through Triassic−Jurassic time. Paleobiology. 2007;33(3):414–434.

Simpson C, Paul GH. Assessing the role of abundance in marine bivalve extinction over the post-Paleozoic. Paleobiology. 2009;35(4):631–647.

Hopkins MJ, Simpson C, Kiessling W. Differential niche dynamics among major marine invertebrate clades. Ecol Lett. 2014;17(3):314–323. PubMed PMC

Foote M. Environmental controls on geographic range size in marine animal genera. Paleobiology. 2014;40(3):440–458.

Connolly SR, Miller AI. Joint estimation of sampling and turnover rates from fossil databases: Capture-mark-recapture methods revisited. Paleobiology. 2001;27(4):751–767.

Foote M. Inferring temporal patterns of preservation, origination, and extinction from taxonomic survivorship analysis. Paleobiology. 2001;27(4):602–630.

Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E. Equations of state calculations by fast computing machines. J Chem Phys. 1953;21(6):1087–1092.

Hastings WK. Monte Carlo sampling methods using Markov chains and their applications. Biometrika. 1970;57(1):97–109.

Wartenberg D, Ferson S, Rohlf FJ. Putting things in order: A critique of detrended correspondence analysis. Am Nat. 1987;129(3):434–448.

Miller AI, Holland SM, Meyer DL, Dattilo BF. The use of faunal gradient analysis for intraregional correlation and assessment of changes in sea‐floor topography in the type Cincinnatian. J Geol. 2001;109(5):603–613.

Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica. 2001;4(1):4.

Chen Q, Fan JX, Melchin MJ, Zhang L. Temporal and spatial distribution of the Wufeng Formation black shales (Upper Ordovician) in South China. GFF. 2014;136(1):55–59.

Chen X, Rong JY, Li Y, Boucot AJ. Facies patterns and geography of the Yangtze region, South China, through the Ordovician and Silurian transition. Palaeogeogr Palaeoclimatol Palaeoecol. 2004;204(3):353–372.

Yan D, et al. Organic matter accumulation of Late Ordovician sediments in North Guizhou Province, China: Sulfur isotope and trace element evidences. Mar Pet Geol. 2015;59:348–358.

Shannon CE, Weaver W. The Mathematical Theory of Communication. Univ Illinois Press; Urbana, IL: 1949.

Heip CHR, Herman PMJ, Soetaert K. Indices of diversity and evenness. Oceanis. 1998;24(4):61–87.

Kosnik MA, Wagner PJ. Effects of taxon abundance distributions on expected numbers of sampled taxa. Evol Ecol Res. 2006;8(2):195–211.

Magurran AE. Measuring Biological Diversity. Blackwell Sci; Oxford: 2004.

McGill BJ, et al. Species abundance distributions: Moving beyond single prediction theories to integration within an ecological framework. Ecol Lett. 2007;10(10):995–1015. PubMed

Mathworks (2013) MATLAB Release 2013b (MathWorks, Natick, MA)

Root RB. The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Monogr. 1967;37(4):317–350.

Laland KN, Odling-Smee FJ, Feldman MW. Evolutionary consequences of niche construction and their implications for ecology. Proc Natl Acad Sci USA. 1999;96(18):10242–10247. PubMed PMC

Frontier S. Diversity and structure in aquatic ecosystems. Oceanogr Mar Biol Ann Rev. 1985;23:253–312.

Gray JS. In: Species Abundance Patterns in Organization of Communities Past and Present. Gee JHR, Gillier PS, editors. Blackwell; Oxford: 1987. pp. 53–67.

Cooper RA, Sadler PM, Hammer Ø, Gradstein FM. The Ordovician Period. In: Gradstein FM, Ogg JG, Schmitz MD, Ogg GM, editors. The Geological Timescale 2012. Vol 1. Elsevier; Amsterdam: 2012. pp. 489–523.

Chen X, et al. Biostratigraphy of the Hirnantian Substage from the Yangtze region. J Stratigr. 2000;21(1):169–175.

Zhang L, Fan JX, Chen Q, Melchin MJ. Geographic dynamics of some major graptolite taxa of the Diplograptina during the Late Ordovician mass extinction in South China. GFF. 2014;136(1):327–332.