Biogeosciences 16 2501ndash2510 2019httpsdoiorg105194bg-16-2501-2019copy Author(s) 2019 This work is distributed underthe Creative Commons Attribution 40 License

The colonization of the oceans by calcifying pelagic algaeBaptiste Sucheacuteras-Marx1 Emanuela Mattioli23 Pascal Allemand2 Fabienne Giraud4 Bernard Pittet2Julien Plancq5 and Gilles Escarguel61Aix Marseille Universiteacute CNRS IRD INRA Coll France CEREGE Aix-en-Provence France2Universiteacute de Lyon UCBL ENSL CNRS LGL-TPE 69622 Villeurbanne France3Institut Universitaire de France Paris France4Universiteacute Grenoble Alpes Universiteacute Savoie Mont Blanc CNRS IRD IFSTTARISTerre 38000 Grenoble France5School of Geographical and Earth Sciences University of Glasgow Glasgow G12 8QQ UK6Universiteacute de Lyon UMR 5023 LEHNA UCBL CNRS ENTPE 69622 Villeurbanne FranceThese authors contributed equally to this work

Correspondence Baptiste Sucheacuteras-Marx (sucherasceregefr)and Emanuela Mattioli (emanuelamattioliuniv-lyon1fr)

Received 29 November 2018 ndash Discussion started 11 December 2018Revised 3 June 2019 ndash Accepted 4 June 2019 ndash Published 25 June 2019

Abstract The rise of calcareous nannoplankton in Meso-zoic oceans has deeply impacted ocean chemistry and con-tributed to shaping modern oceans Nevertheless the calcare-ous nannoplankton colonization of past marine environmentsremains poorly understood Based on an extensive compila-tion of published and unpublished data we show that theiraccumulation rates in sediments increased from the EarlyJurassic (sim 200 Ma) to the Early Cretaceous (sim 120 Ma) al-though these algae diversified up to the end of the Mesozoic(66 Ma) After the middle Eocene (sim 45 Ma) a decouplingoccurred between accumulation rates diversity and coccol-ith size The time series analyzed points toward a three-phase evolutionary dynamic An invasion phase of the open-ocean realms was followed by a specialization phase occur-ring along with taxonomic diversification ended by an estab-lishment phase where a few small-sized species dominatedThe current hegemony of calcareous nannoplankton in theworld ocean results from a long-term and complex evolu-tionary history shaped by ecological interactions and abioticforcing

1 Introduction

Calcifying pelagic algae also known as calcareous nanno-plankton are an important and globally distributed compo-nent of marine biota in terms of both abundance and diver-sity Calcareous nannoplankton is today mainly composedof coccolithophores which are unicellular Haptophyta algaeproducing microscopic (1ndash20 microm) calcite platelets the coc-coliths and occurring in the fossil record since the Late Tri-assic (sim 210 Ma Gardin et al 2012) Coccoliths togetherwith incertae sedis calcite remains are grouped into calcare-ous nannofossils and are abundantly recovered in Mesozoicand Cenozoic marine sediments Coccoliths are produced in-side the coccolithophore cell and are then extruded to forman extracellular mineralized coccosphere Although this cal-cification process requires energy from the cell the reasonwhy coccolithophores produce coccoliths remains uncertain(Monteiro et al 2016) In modern surface oceans coccol-ithophores perform sim 1 ndash10 of the total organic carbonfixation in some cases more than 50 while calcification ofcoccolithophores contributessim 1 ndash10 of the total carbonfixation (Poulton et al 2007) Nevertheless their contribu-tion to the carbon flux toward the ocean interior is twofoldsince calcite also acts as a ballast for the organic carbon(Klaas et al 2002) Eventually calcareous nannofossils rep-resent about half of the extant pelagic carbonate sediments

Published by Copernicus Publications on behalf of the European Geosciences Union

2502 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

in the oceanic realm (Baumann et al 2004 Broecker andClark 2009) and accounted for even more in Neogene sed-iments despite their small size (Sucheacuteras-Marx and Hen-deriks 2014) Conversely during the early coccolithophoreevolution they only represented a minor contribution to thetotal calcium carbonate in sediments with extremely lownannofossil accumulation rates in the Jurassic period (Mat-tioli et al 2009 Sucheacuteras-Marx et al 2012) There is thena transition from Jurassic calcareous nannofossil-poor toLate Cretaceous and Cenozoic calcareous nannofossil-richoceanic sediments which has shifted the carbonate accumu-lation sustained by benthic organisms from neritic environ-ments to an accumulation in pelagic environments supportedby planktic organisms This major carbonate system changeis known as the Kuenen event (Roth 1989) and has beentraced to a tectonically mediated intensification of the oceancirculation This event is concomitant with the developmentof several planktic groups (eg planktic foraminifera Hartet al 2003 diatoms Kooistra et al 2007) may be seenas a Mesozoic plankton revolution (derived from Vermeij1977) and thus is also dramatically related to plankton evo-lution The causes and consequences of this biotic revolutionhave been extensively discussed but the transition itself re-mains poorly documented most interpretations solely rely onspecies richness (Falkowski et al 2004 Knoll and Follows2016) which does not provide an exhaustive framework tofully appreciate the evolutionary history of calcareous nanno-plankton

Our working hypothesis is that this difference betweenJurassic and Cenozoic pelagic carbonate accumulation ratespoints toward a major change in the nannoplankton evolu-tionary dynamics through geological time rather than beingmerely due to environmental changes In order to test thishypothesis we analyzed in this study the sim 200 Myr longevolutionary history of calcareous nannoplankton based onan extensive compilation of both published and unpublishednannofossil accumulation rates (NARs Table S1 Fig 1)species richness (Bown 2005) and coccolith mean size (ieat the assemblage level Aubry et al 2005 Herrmann andThierstein 2012) The novelty of this study is the long-termreconstruction of NAR and its use as a proxy for assessingthe evolutionary dynamics of the calcareous nannoplanktonFossil-based quantification in the sedimentary record is mostoften overlooked in paleontological studies due to the unevencharacter of the fossil record but the continuous and abun-dant record of calcareous nannofossils and their taphonomicresilience compensates for most preservation and samplingissues Our approach therefore represents an unprecedentedadvance in understanding the evolutionary dynamics of a ma-jor planktic group We discuss the resulting pattern with re-spect to the microplankton evolutionary history and compareit with the long-term global climate oceanographic and en-vironmental changes known for this time interval

2 Materials and methods

21 Sample preparation of the compiled data

All the published and unpublished data of nannofossil abso-lute abundance (see Supplement) coming from samples ana-lyzed by the authors result from the preparation techniquedescribed by Geisen et al (1999) All the published datafrom the literature compiled (except one source) also usedthe same preparation technique The preparation consists ofa settling method where a known quantity (m 10ndash30 mg)of homogeneous rock powder is diluted in water and settledin the random settling device for 24 h on a cover slide situ-ated at a depth of 2 cm (h) within the random settling deviceWater is eventually evacuated from the settling boxes veryslowly in order to avoid turbulence and powder remobiliza-tion Finally cover slides are mounted on microscope slidesusing Rhodopas B (polyvinyl acetate) and studied under alight-polarized (linear) microscope with times1000 magnifica-tion Usually a minimum of 300 nannofossils per sample arecounted (n) or a minimum of 50 fields of view (fov) is ob-served depending on the concentration of particles on thecover slide The nannofossil absolute abundance is then cal-culated based on Eq (1)

X =(n times v)

(m times fov times a times h) (1)

where X is the nannofossil absolute abundance (nannofos-sil gbulk) n is the number of nannofossils counted v is thevolume of water in the device m is the mass of sediment insuspension (g) fov is the number of fields of view observeda is the surface area of one field of view (cm2) and h is theheight of the water column above the cover slide (cm)

The only study not using the random settling prepara-tion technique deals with the Polaveno section (Italy lateBerriasianndashearly Hauterivian) (Erba and Tremolada 2004)where nannofossils were quantified in thin sections thinnedto an average thickness of 7 microm Absolute abundances werethen obtained by counting all nannofossil specimens on1 mm2 of the thin section in a light polarized microscope withtimes1250 magnification

22 Accumulation rate calculation

The nannofossil accumulation rate is calculated using sedi-mentation rate following Eq (2)

NAR = NannoAb times SR times DBD (2)

where NAR is nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) NannoAb is the nannofossil absolute abun-dance (nannofossil gbulk) and SR is the sedimentation rate(m Myrminus1) DBD is the dry bulk density of the rock (g cmminus3)

Sedimentation rates have been calculated based on the In-ternational Chronostratigraphic Chart 2012 (Gradstein et al2012) When cyclostratigraphy was available we used the

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2503

cycles provided by authors after re-evaluation of at least oneanchor age (commonly a stage limit or a biostratigraphicdatum) When cyclostratigraphy was not available we usedanchored ages mostly based on biostratigraphic datums as-suming that the sedimentation rate was constant betweentwo datums The dry bulk density of rocks is missing inall but one Mesozoic studied sample (Sucheacuteras-Marx et al2012) A typical value at 27 g cmminus3 corresponding to the cal-cite density was set when density was missing this value isclose to the 255 g cmminus3 measured for Middle Jurassic rocks(Sucheacuteras-Marx et al 2012) leading to a negligible differ-ence in nannofossil accumulation rates

For the Polaveno section samples the calcareous nanno-fossil accumulation rates were calculated by the authors perunit area (1 mm2) and time (1 year) (Erba et al 2004) Thelatter was derived from sedimentation rates estimated for in-dividual magnetic polarity chrons (Channel et al 2000)

23 Dataset compilation

All data sources but one used the same preparation tech-nique (see details above) limiting the discrepancies due tomethodological differences All the sites considered for nan-nofossil accumulation rate compilation are presented on amap (Fig 1) The vast majority of the samples are from theNorthern Hemisphere and almost all samples for Jurassicand Cretaceous times are from western Europe outcrops ndash arelatively poor quantitative record of nannofossils exists out-side Europe and at oceanic sites issued from deep-sea drillingprograms Europe the North Sea Greenland and the NorthAtlantic represent 8116 of all compiled samples Thusresults based on NAR particularly for the Mesozoic whichrepresent 8431 of all samples compiled will be mostlybased on European and Atlantic localities and thus may de-scribe patterns that occurred mainly in the western Tethysand North Atlantic (see Supplement S3 and Fig S3) For theCenozoic the data are more widely distributed but the sam-ples per million years are less abundant than in the Meso-zoic (see Supplement S3 and Fig S3) All data compiled areprovided in an Excel file with one sheet per site or paper(Table S1 in the Supplement) for a total of 3895 data pointsacross 79 sites or papers Name location and associated ref-erences for each site are provided in the Supplement

24 Trend smoothing

For nannofossil accumulation rates and pCO2 values (partsper million and micro-atmospheres Foster et al 2017Witkowski et al 2018) (Figs 2 S1ndashS2 S4) a LOESSsmoothed curve was computed in order to capture long-termvariations and overlook short-term shifts that are more likelycontrolled by the number of studied sites sampling resolu-tion and nannofossil preservation or alternatively by localenvironmental conditions The data from Mejiacutea et al (2017)are excluded from the LOESS calculation due to the large un-

certainties presented by the authors See the Supplement fora discussion of the effect of the selected smoothing factor onthe inferred trend The curve was calculated using PAST324(Hammer et al 2001) The CO2 curve was calculated us-ing a smoothing factor of 01 and the nannofossil accumula-tion rate curve using a smoothing factor of 05 both associ-ated with a 95 bootstrapped confidence interval based on999 random replicates

25 Nannofossil accumulation rate paleomapconstruction

Maps of nannofossil accumulation rates (Fig 3 dataset inTable S2) have been drawn from the linear interpolation ofthe measurements performed at various sites using the dedi-cated MATLAB functions The geographical coordinates ofthe sites studied were first converted in a sinusoidal projec-tion that preserves distance ratios The maps were then pro-jected in a conformal Mercator projection in order to be moreeasily readable The distance from continental coasts and theexistence of islands in the area of interpolation were nottaken into account We used the hypothesis that the islandswere small enough not to spatially impact the calcareous nan-nofossil accumulation rates Continental coastlines were notused as a limit in the interpolation because they would havegenerated artificial variations due to the relatively high aver-age distance between sites

3 Results

Nannofossil accumulation rate (NAR) expressed as num-ber of specimens per square meter and per year stronglyvaries between sites but also stratigraphically within a sin-gle site (Fig 2) In this study we used a LOESS smoothing tocatch the long-term trend and overlook short-term variationsthat may be influenced by preservation or local environmen-tal conditions (Figs 2 S1) Clearly the resulting time se-ries of smoothed NAR shows two main successive intervals(i) an increase of 2 orders of magnitude during the Jurassicand Early Cretaceous (ie from sim 200 to sim 120 Ma) fol-lowed by (ii) a steady-state dynamic equilibrium up to end-Cenozoic times

Two time intervals are geographically well-documented(Fig S3) mostly at European sites the Toarcian (EarlyJurassic sim 183ndash174 Ma) and the Valanginian (Early Cre-taceous sim 140ndash133 Ma) NAR paleomaps have been con-structed based on averaged NAR values for each site in bothtime intervals During the Toarcian NAR is higher in north-ern shallow epicontinental seas than in southeastern Tethyanopen sea (Fig 3a) Conversely during the Valanginian NARis higher in tropical open seas than in northeastern Europeanepicontinental seas near the Viking Corridor (ie the connec-tion between Boreal and European seas Westermann 1993)(Fig 3bndashc) Finally the highest Toarcian NAR (located in

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2504 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 1 Location of the sites compiled for this study Colors indicate the age of the samples (Neogene yellow Paleogene orange Creta-ceous green Jurassic blue) Squares represent land outcrops and circles represent deep-sea drilling

France and Yorkshire) is similar to the lowest ValanginianNAR (located in Greenland North Sea and France) (Ta-ble S2) Compared to nannofossil species richness and coc-colith mean size these results open new insights into the evo-lution of calcareous nannoplankton over the past sim 200 MyrThree distinct phases can be observed

During the Jurassic and Early Cretaceous the smoothedNAR increased with species richness (Bown 2005) whilecoccolith size was steadily small and started to increaseat the JurassicndashCretaceous boundary (Aubry et al 2005)The beginning of this phase is marked by high calcareousnannoplankton production in epicontinental seas whereasthe end of this phase is marked by greater production in trop-ical open-ocean environments as shown by the NAR maps(Fig 3) Hence this invasion phase reflects a sim 80 Myr longgradual invasion of the western Tethys and Atlantic oceansby calcareous nannoplankton during the JurassicndashEarly Cre-taceous time interval Watznaueria barnesiae (ie a cos-mopolitan Mesozoic coccolithophore species) coccolith bio-metric data show only one size population between the west-ern Tethys (La Charce-Vergol France) and western Pantha-lassa (ODP1149 Nadezhda basin close to Japan) during theLower Cretaceous Thus mixing of coccolithophore popula-tions was effective at that time testifying for a continuousgenetic flux through the Tethys following a circum-globalcirculation (Gollain et al 2019) The genetic flux was prob-ably sustained for many calcareous nannoplankton betweenboth regions of the oceans at that time The Early Cretaceousinvasion phase observed in the Atlantic Ocean may have thushappened in all open oceans worldwide although our re-stricted EuropeanndashNorth Hemisphere dataset cannot corrob-orate it

An abrupt change in NAR dynamics which has beensteadily high since the Early Cretaceous (sim 120 Ma) accord-

ing to the LOESS trend marks the beginning of the secondphase From this point up to the end of the Cretaceous NARremained high but the nannofossil species richness and thecoccolith mean size have increased since the beginning ofthe Cretaceous following CopendashDepeacuteretrsquos rule (ie increasein coccolith size over evolutionary time Aubry et al 2005)As seen in the Valanginian NAR maps (Fig 3bndashc) by thistime the shift in calcareous nannoplankton production towardthe open seas was already accomplished This phase corre-sponds to the specialization phase where more and morespecies shared an increasingly filled ecospace through spe-cialization to particular ecological niches

After the CretaceousndashPaleogene (ie KndashPg) mass extinc-tion event calcareous nannoplankton recovered followingthe same two phases namely invasion and specialization buton a short time interval (less than 4 Myr) although our Pale-ocene NAR record is too limited to unambiguously confirmthis pattern Finally a last phase in the calcareous nanno-plankton evolution started in the Eocene (Figs 2 S3) withsmoothed NAR steadily high or slightly increasing (Figs 2S1) but the nannofossil species richness and coccolith meansize both tending to decrease This may correspond to an es-tablishment phase where fewer species with smaller sizespredominated This establishment phase reached a climaxin modern oceans with the dominance within the coccol-ithophore community of the iconic small-sized species Emil-iania huxleyi (eg Ziveri et al 2000 Baumann et al 2004)

4 Discussion

Extant calcareous nannoplankton is neither uniformly norrandomly dispersed in the global ocean (eg Winter et al1994) Its distribution in ecological niches is shaped by(i) abiotic parameters such as temperature salinity pH and

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2505

Figure 2 Evolution through time of nannofossil accumulation rate species richness and size (a) Compiled nannofossil accumulation rate(nannofossil mminus2 yrminus1) Black circles are samples from Europe North Sea Greenland and North Atlantic and grey circles are from therest of the world The LOESS trend (SF 05) was calculated with all samples (b) Nannofossil species richness (Bown 2005) (c) Coccolithmean size at the assemblage level during the Mesozoic (Aubry et al 2005) and the Cenozoic (Herrmann and Thierstein 2012) Mesozoiccoccolith mean size at the assemblage level is derived from a compilation of species sizes as published in the literature (original taxonomicdescriptions) to which the authors have added their own measurements of published material This record consists of measurements of lengthand width of 302 species which is about one-third of all the described Mesozoic coccolith species The grey area illustrates the minimum andmaximum size recorded Cenozoic coccolith mean size at the assemblage level is derived from measurements of entire coccolith assemblagesduring the last 66 Myr from a number of globally distributed deep-sea cores using automated scanning electron microscopy and imageanalysis processing (d) pCO2 through time with the Foster et al (2017 in parts per million) compilation represented by black filled circlesWitkowski et al (2018 in micro-atmospheres) represented by grey open squares and Miocene pCO2 decline from Mejiacutea et al (2017) inwhite open circles with the range of possible values in grey The LOESS trend was calculated on Fosterrsquos and Witkowskirsquos data assumingparts per million and micro-atmospheres are equivalent and is represented by a black line and grey envelope representing the 95 confidenceinterval around the calculated trend

water mixing but also by the availability of nutrients or light(eg Margalef 1978 Balch 2004) and (ii) by functionalinteractions with other organisms such as viruses (Frada etal 2008) phytoplankton and grazers (Litchman et al 2006)Extant coccolithophores are commonly viewed as ldquointerme-diaterdquo organisms in Margalefrsquos mandala (ie Fig 2 fromMargalef 1978) so basically transitional between K (cor-responding to organisms evolving in more stable predicableand saturated environments eg dinoflagellates) and r (or-ganisms living in unstable unpredictable and unsaturated en-

vironments eg diatoms) strategists (Reznick et al 2002)living in intermediate nutrient-concentrated waters turbu-lence and light availability (Margalef 1978 Balch 2004Tozzi et al 2004) Thus the integration of abiotic and bioticparameters explains the macroecological distribution of ex-tant calcareous nannoplankton Macroecological pattern maychange through time due to evolution And long-term evo-lution ndash macroevolution ndash is influenced by abiotic and bi-otic drivers that have given two evolutionary models RedQueen (Van Valen 1973) and Court Jester (Barnosky 2001)

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2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

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2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

2502 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

in the oceanic realm (Baumann et al 2004 Broecker andClark 2009) and accounted for even more in Neogene sed-iments despite their small size (Sucheacuteras-Marx and Hen-deriks 2014) Conversely during the early coccolithophoreevolution they only represented a minor contribution to thetotal calcium carbonate in sediments with extremely lownannofossil accumulation rates in the Jurassic period (Mat-tioli et al 2009 Sucheacuteras-Marx et al 2012) There is thena transition from Jurassic calcareous nannofossil-poor toLate Cretaceous and Cenozoic calcareous nannofossil-richoceanic sediments which has shifted the carbonate accumu-lation sustained by benthic organisms from neritic environ-ments to an accumulation in pelagic environments supportedby planktic organisms This major carbonate system changeis known as the Kuenen event (Roth 1989) and has beentraced to a tectonically mediated intensification of the oceancirculation This event is concomitant with the developmentof several planktic groups (eg planktic foraminifera Hartet al 2003 diatoms Kooistra et al 2007) may be seenas a Mesozoic plankton revolution (derived from Vermeij1977) and thus is also dramatically related to plankton evo-lution The causes and consequences of this biotic revolutionhave been extensively discussed but the transition itself re-mains poorly documented most interpretations solely rely onspecies richness (Falkowski et al 2004 Knoll and Follows2016) which does not provide an exhaustive framework tofully appreciate the evolutionary history of calcareous nanno-plankton

Our working hypothesis is that this difference betweenJurassic and Cenozoic pelagic carbonate accumulation ratespoints toward a major change in the nannoplankton evolu-tionary dynamics through geological time rather than beingmerely due to environmental changes In order to test thishypothesis we analyzed in this study the sim 200 Myr longevolutionary history of calcareous nannoplankton based onan extensive compilation of both published and unpublishednannofossil accumulation rates (NARs Table S1 Fig 1)species richness (Bown 2005) and coccolith mean size (ieat the assemblage level Aubry et al 2005 Herrmann andThierstein 2012) The novelty of this study is the long-termreconstruction of NAR and its use as a proxy for assessingthe evolutionary dynamics of the calcareous nannoplanktonFossil-based quantification in the sedimentary record is mostoften overlooked in paleontological studies due to the unevencharacter of the fossil record but the continuous and abun-dant record of calcareous nannofossils and their taphonomicresilience compensates for most preservation and samplingissues Our approach therefore represents an unprecedentedadvance in understanding the evolutionary dynamics of a ma-jor planktic group We discuss the resulting pattern with re-spect to the microplankton evolutionary history and compareit with the long-term global climate oceanographic and en-vironmental changes known for this time interval

2 Materials and methods

21 Sample preparation of the compiled data

All the published and unpublished data of nannofossil abso-lute abundance (see Supplement) coming from samples ana-lyzed by the authors result from the preparation techniquedescribed by Geisen et al (1999) All the published datafrom the literature compiled (except one source) also usedthe same preparation technique The preparation consists ofa settling method where a known quantity (m 10ndash30 mg)of homogeneous rock powder is diluted in water and settledin the random settling device for 24 h on a cover slide situ-ated at a depth of 2 cm (h) within the random settling deviceWater is eventually evacuated from the settling boxes veryslowly in order to avoid turbulence and powder remobiliza-tion Finally cover slides are mounted on microscope slidesusing Rhodopas B (polyvinyl acetate) and studied under alight-polarized (linear) microscope with times1000 magnifica-tion Usually a minimum of 300 nannofossils per sample arecounted (n) or a minimum of 50 fields of view (fov) is ob-served depending on the concentration of particles on thecover slide The nannofossil absolute abundance is then cal-culated based on Eq (1)

X =(n times v)

(m times fov times a times h) (1)

where X is the nannofossil absolute abundance (nannofos-sil gbulk) n is the number of nannofossils counted v is thevolume of water in the device m is the mass of sediment insuspension (g) fov is the number of fields of view observeda is the surface area of one field of view (cm2) and h is theheight of the water column above the cover slide (cm)

The only study not using the random settling prepara-tion technique deals with the Polaveno section (Italy lateBerriasianndashearly Hauterivian) (Erba and Tremolada 2004)where nannofossils were quantified in thin sections thinnedto an average thickness of 7 microm Absolute abundances werethen obtained by counting all nannofossil specimens on1 mm2 of the thin section in a light polarized microscope withtimes1250 magnification

22 Accumulation rate calculation

The nannofossil accumulation rate is calculated using sedi-mentation rate following Eq (2)

NAR = NannoAb times SR times DBD (2)

where NAR is nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) NannoAb is the nannofossil absolute abun-dance (nannofossil gbulk) and SR is the sedimentation rate(m Myrminus1) DBD is the dry bulk density of the rock (g cmminus3)

Sedimentation rates have been calculated based on the In-ternational Chronostratigraphic Chart 2012 (Gradstein et al2012) When cyclostratigraphy was available we used the

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2503

cycles provided by authors after re-evaluation of at least oneanchor age (commonly a stage limit or a biostratigraphicdatum) When cyclostratigraphy was not available we usedanchored ages mostly based on biostratigraphic datums as-suming that the sedimentation rate was constant betweentwo datums The dry bulk density of rocks is missing inall but one Mesozoic studied sample (Sucheacuteras-Marx et al2012) A typical value at 27 g cmminus3 corresponding to the cal-cite density was set when density was missing this value isclose to the 255 g cmminus3 measured for Middle Jurassic rocks(Sucheacuteras-Marx et al 2012) leading to a negligible differ-ence in nannofossil accumulation rates

For the Polaveno section samples the calcareous nanno-fossil accumulation rates were calculated by the authors perunit area (1 mm2) and time (1 year) (Erba et al 2004) Thelatter was derived from sedimentation rates estimated for in-dividual magnetic polarity chrons (Channel et al 2000)

23 Dataset compilation

All data sources but one used the same preparation tech-nique (see details above) limiting the discrepancies due tomethodological differences All the sites considered for nan-nofossil accumulation rate compilation are presented on amap (Fig 1) The vast majority of the samples are from theNorthern Hemisphere and almost all samples for Jurassicand Cretaceous times are from western Europe outcrops ndash arelatively poor quantitative record of nannofossils exists out-side Europe and at oceanic sites issued from deep-sea drillingprograms Europe the North Sea Greenland and the NorthAtlantic represent 8116 of all compiled samples Thusresults based on NAR particularly for the Mesozoic whichrepresent 8431 of all samples compiled will be mostlybased on European and Atlantic localities and thus may de-scribe patterns that occurred mainly in the western Tethysand North Atlantic (see Supplement S3 and Fig S3) For theCenozoic the data are more widely distributed but the sam-ples per million years are less abundant than in the Meso-zoic (see Supplement S3 and Fig S3) All data compiled areprovided in an Excel file with one sheet per site or paper(Table S1 in the Supplement) for a total of 3895 data pointsacross 79 sites or papers Name location and associated ref-erences for each site are provided in the Supplement

24 Trend smoothing

For nannofossil accumulation rates and pCO2 values (partsper million and micro-atmospheres Foster et al 2017Witkowski et al 2018) (Figs 2 S1ndashS2 S4) a LOESSsmoothed curve was computed in order to capture long-termvariations and overlook short-term shifts that are more likelycontrolled by the number of studied sites sampling resolu-tion and nannofossil preservation or alternatively by localenvironmental conditions The data from Mejiacutea et al (2017)are excluded from the LOESS calculation due to the large un-

certainties presented by the authors See the Supplement fora discussion of the effect of the selected smoothing factor onthe inferred trend The curve was calculated using PAST324(Hammer et al 2001) The CO2 curve was calculated us-ing a smoothing factor of 01 and the nannofossil accumula-tion rate curve using a smoothing factor of 05 both associ-ated with a 95 bootstrapped confidence interval based on999 random replicates

25 Nannofossil accumulation rate paleomapconstruction

Maps of nannofossil accumulation rates (Fig 3 dataset inTable S2) have been drawn from the linear interpolation ofthe measurements performed at various sites using the dedi-cated MATLAB functions The geographical coordinates ofthe sites studied were first converted in a sinusoidal projec-tion that preserves distance ratios The maps were then pro-jected in a conformal Mercator projection in order to be moreeasily readable The distance from continental coasts and theexistence of islands in the area of interpolation were nottaken into account We used the hypothesis that the islandswere small enough not to spatially impact the calcareous nan-nofossil accumulation rates Continental coastlines were notused as a limit in the interpolation because they would havegenerated artificial variations due to the relatively high aver-age distance between sites

3 Results

Nannofossil accumulation rate (NAR) expressed as num-ber of specimens per square meter and per year stronglyvaries between sites but also stratigraphically within a sin-gle site (Fig 2) In this study we used a LOESS smoothing tocatch the long-term trend and overlook short-term variationsthat may be influenced by preservation or local environmen-tal conditions (Figs 2 S1) Clearly the resulting time se-ries of smoothed NAR shows two main successive intervals(i) an increase of 2 orders of magnitude during the Jurassicand Early Cretaceous (ie from sim 200 to sim 120 Ma) fol-lowed by (ii) a steady-state dynamic equilibrium up to end-Cenozoic times

Two time intervals are geographically well-documented(Fig S3) mostly at European sites the Toarcian (EarlyJurassic sim 183ndash174 Ma) and the Valanginian (Early Cre-taceous sim 140ndash133 Ma) NAR paleomaps have been con-structed based on averaged NAR values for each site in bothtime intervals During the Toarcian NAR is higher in north-ern shallow epicontinental seas than in southeastern Tethyanopen sea (Fig 3a) Conversely during the Valanginian NARis higher in tropical open seas than in northeastern Europeanepicontinental seas near the Viking Corridor (ie the connec-tion between Boreal and European seas Westermann 1993)(Fig 3bndashc) Finally the highest Toarcian NAR (located in

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2504 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 1 Location of the sites compiled for this study Colors indicate the age of the samples (Neogene yellow Paleogene orange Creta-ceous green Jurassic blue) Squares represent land outcrops and circles represent deep-sea drilling

France and Yorkshire) is similar to the lowest ValanginianNAR (located in Greenland North Sea and France) (Ta-ble S2) Compared to nannofossil species richness and coc-colith mean size these results open new insights into the evo-lution of calcareous nannoplankton over the past sim 200 MyrThree distinct phases can be observed

During the Jurassic and Early Cretaceous the smoothedNAR increased with species richness (Bown 2005) whilecoccolith size was steadily small and started to increaseat the JurassicndashCretaceous boundary (Aubry et al 2005)The beginning of this phase is marked by high calcareousnannoplankton production in epicontinental seas whereasthe end of this phase is marked by greater production in trop-ical open-ocean environments as shown by the NAR maps(Fig 3) Hence this invasion phase reflects a sim 80 Myr longgradual invasion of the western Tethys and Atlantic oceansby calcareous nannoplankton during the JurassicndashEarly Cre-taceous time interval Watznaueria barnesiae (ie a cos-mopolitan Mesozoic coccolithophore species) coccolith bio-metric data show only one size population between the west-ern Tethys (La Charce-Vergol France) and western Pantha-lassa (ODP1149 Nadezhda basin close to Japan) during theLower Cretaceous Thus mixing of coccolithophore popula-tions was effective at that time testifying for a continuousgenetic flux through the Tethys following a circum-globalcirculation (Gollain et al 2019) The genetic flux was prob-ably sustained for many calcareous nannoplankton betweenboth regions of the oceans at that time The Early Cretaceousinvasion phase observed in the Atlantic Ocean may have thushappened in all open oceans worldwide although our re-stricted EuropeanndashNorth Hemisphere dataset cannot corrob-orate it

An abrupt change in NAR dynamics which has beensteadily high since the Early Cretaceous (sim 120 Ma) accord-

ing to the LOESS trend marks the beginning of the secondphase From this point up to the end of the Cretaceous NARremained high but the nannofossil species richness and thecoccolith mean size have increased since the beginning ofthe Cretaceous following CopendashDepeacuteretrsquos rule (ie increasein coccolith size over evolutionary time Aubry et al 2005)As seen in the Valanginian NAR maps (Fig 3bndashc) by thistime the shift in calcareous nannoplankton production towardthe open seas was already accomplished This phase corre-sponds to the specialization phase where more and morespecies shared an increasingly filled ecospace through spe-cialization to particular ecological niches

After the CretaceousndashPaleogene (ie KndashPg) mass extinc-tion event calcareous nannoplankton recovered followingthe same two phases namely invasion and specialization buton a short time interval (less than 4 Myr) although our Pale-ocene NAR record is too limited to unambiguously confirmthis pattern Finally a last phase in the calcareous nanno-plankton evolution started in the Eocene (Figs 2 S3) withsmoothed NAR steadily high or slightly increasing (Figs 2S1) but the nannofossil species richness and coccolith meansize both tending to decrease This may correspond to an es-tablishment phase where fewer species with smaller sizespredominated This establishment phase reached a climaxin modern oceans with the dominance within the coccol-ithophore community of the iconic small-sized species Emil-iania huxleyi (eg Ziveri et al 2000 Baumann et al 2004)

4 Discussion

Extant calcareous nannoplankton is neither uniformly norrandomly dispersed in the global ocean (eg Winter et al1994) Its distribution in ecological niches is shaped by(i) abiotic parameters such as temperature salinity pH and

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2505

Figure 2 Evolution through time of nannofossil accumulation rate species richness and size (a) Compiled nannofossil accumulation rate(nannofossil mminus2 yrminus1) Black circles are samples from Europe North Sea Greenland and North Atlantic and grey circles are from therest of the world The LOESS trend (SF 05) was calculated with all samples (b) Nannofossil species richness (Bown 2005) (c) Coccolithmean size at the assemblage level during the Mesozoic (Aubry et al 2005) and the Cenozoic (Herrmann and Thierstein 2012) Mesozoiccoccolith mean size at the assemblage level is derived from a compilation of species sizes as published in the literature (original taxonomicdescriptions) to which the authors have added their own measurements of published material This record consists of measurements of lengthand width of 302 species which is about one-third of all the described Mesozoic coccolith species The grey area illustrates the minimum andmaximum size recorded Cenozoic coccolith mean size at the assemblage level is derived from measurements of entire coccolith assemblagesduring the last 66 Myr from a number of globally distributed deep-sea cores using automated scanning electron microscopy and imageanalysis processing (d) pCO2 through time with the Foster et al (2017 in parts per million) compilation represented by black filled circlesWitkowski et al (2018 in micro-atmospheres) represented by grey open squares and Miocene pCO2 decline from Mejiacutea et al (2017) inwhite open circles with the range of possible values in grey The LOESS trend was calculated on Fosterrsquos and Witkowskirsquos data assumingparts per million and micro-atmospheres are equivalent and is represented by a black line and grey envelope representing the 95 confidenceinterval around the calculated trend

water mixing but also by the availability of nutrients or light(eg Margalef 1978 Balch 2004) and (ii) by functionalinteractions with other organisms such as viruses (Frada etal 2008) phytoplankton and grazers (Litchman et al 2006)Extant coccolithophores are commonly viewed as ldquointerme-diaterdquo organisms in Margalefrsquos mandala (ie Fig 2 fromMargalef 1978) so basically transitional between K (cor-responding to organisms evolving in more stable predicableand saturated environments eg dinoflagellates) and r (or-ganisms living in unstable unpredictable and unsaturated en-

vironments eg diatoms) strategists (Reznick et al 2002)living in intermediate nutrient-concentrated waters turbu-lence and light availability (Margalef 1978 Balch 2004Tozzi et al 2004) Thus the integration of abiotic and bioticparameters explains the macroecological distribution of ex-tant calcareous nannoplankton Macroecological pattern maychange through time due to evolution And long-term evo-lution ndash macroevolution ndash is influenced by abiotic and bi-otic drivers that have given two evolutionary models RedQueen (Van Valen 1973) and Court Jester (Barnosky 2001)

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2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

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2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2503

cycles provided by authors after re-evaluation of at least oneanchor age (commonly a stage limit or a biostratigraphicdatum) When cyclostratigraphy was not available we usedanchored ages mostly based on biostratigraphic datums as-suming that the sedimentation rate was constant betweentwo datums The dry bulk density of rocks is missing inall but one Mesozoic studied sample (Sucheacuteras-Marx et al2012) A typical value at 27 g cmminus3 corresponding to the cal-cite density was set when density was missing this value isclose to the 255 g cmminus3 measured for Middle Jurassic rocks(Sucheacuteras-Marx et al 2012) leading to a negligible differ-ence in nannofossil accumulation rates

For the Polaveno section samples the calcareous nanno-fossil accumulation rates were calculated by the authors perunit area (1 mm2) and time (1 year) (Erba et al 2004) Thelatter was derived from sedimentation rates estimated for in-dividual magnetic polarity chrons (Channel et al 2000)

23 Dataset compilation

All data sources but one used the same preparation tech-nique (see details above) limiting the discrepancies due tomethodological differences All the sites considered for nan-nofossil accumulation rate compilation are presented on amap (Fig 1) The vast majority of the samples are from theNorthern Hemisphere and almost all samples for Jurassicand Cretaceous times are from western Europe outcrops ndash arelatively poor quantitative record of nannofossils exists out-side Europe and at oceanic sites issued from deep-sea drillingprograms Europe the North Sea Greenland and the NorthAtlantic represent 8116 of all compiled samples Thusresults based on NAR particularly for the Mesozoic whichrepresent 8431 of all samples compiled will be mostlybased on European and Atlantic localities and thus may de-scribe patterns that occurred mainly in the western Tethysand North Atlantic (see Supplement S3 and Fig S3) For theCenozoic the data are more widely distributed but the sam-ples per million years are less abundant than in the Meso-zoic (see Supplement S3 and Fig S3) All data compiled areprovided in an Excel file with one sheet per site or paper(Table S1 in the Supplement) for a total of 3895 data pointsacross 79 sites or papers Name location and associated ref-erences for each site are provided in the Supplement

24 Trend smoothing

For nannofossil accumulation rates and pCO2 values (partsper million and micro-atmospheres Foster et al 2017Witkowski et al 2018) (Figs 2 S1ndashS2 S4) a LOESSsmoothed curve was computed in order to capture long-termvariations and overlook short-term shifts that are more likelycontrolled by the number of studied sites sampling resolu-tion and nannofossil preservation or alternatively by localenvironmental conditions The data from Mejiacutea et al (2017)are excluded from the LOESS calculation due to the large un-

certainties presented by the authors See the Supplement fora discussion of the effect of the selected smoothing factor onthe inferred trend The curve was calculated using PAST324(Hammer et al 2001) The CO2 curve was calculated us-ing a smoothing factor of 01 and the nannofossil accumula-tion rate curve using a smoothing factor of 05 both associ-ated with a 95 bootstrapped confidence interval based on999 random replicates

25 Nannofossil accumulation rate paleomapconstruction

Maps of nannofossil accumulation rates (Fig 3 dataset inTable S2) have been drawn from the linear interpolation ofthe measurements performed at various sites using the dedi-cated MATLAB functions The geographical coordinates ofthe sites studied were first converted in a sinusoidal projec-tion that preserves distance ratios The maps were then pro-jected in a conformal Mercator projection in order to be moreeasily readable The distance from continental coasts and theexistence of islands in the area of interpolation were nottaken into account We used the hypothesis that the islandswere small enough not to spatially impact the calcareous nan-nofossil accumulation rates Continental coastlines were notused as a limit in the interpolation because they would havegenerated artificial variations due to the relatively high aver-age distance between sites

3 Results

Nannofossil accumulation rate (NAR) expressed as num-ber of specimens per square meter and per year stronglyvaries between sites but also stratigraphically within a sin-gle site (Fig 2) In this study we used a LOESS smoothing tocatch the long-term trend and overlook short-term variationsthat may be influenced by preservation or local environmen-tal conditions (Figs 2 S1) Clearly the resulting time se-ries of smoothed NAR shows two main successive intervals(i) an increase of 2 orders of magnitude during the Jurassicand Early Cretaceous (ie from sim 200 to sim 120 Ma) fol-lowed by (ii) a steady-state dynamic equilibrium up to end-Cenozoic times

Two time intervals are geographically well-documented(Fig S3) mostly at European sites the Toarcian (EarlyJurassic sim 183ndash174 Ma) and the Valanginian (Early Cre-taceous sim 140ndash133 Ma) NAR paleomaps have been con-structed based on averaged NAR values for each site in bothtime intervals During the Toarcian NAR is higher in north-ern shallow epicontinental seas than in southeastern Tethyanopen sea (Fig 3a) Conversely during the Valanginian NARis higher in tropical open seas than in northeastern Europeanepicontinental seas near the Viking Corridor (ie the connec-tion between Boreal and European seas Westermann 1993)(Fig 3bndashc) Finally the highest Toarcian NAR (located in

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2504 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 1 Location of the sites compiled for this study Colors indicate the age of the samples (Neogene yellow Paleogene orange Creta-ceous green Jurassic blue) Squares represent land outcrops and circles represent deep-sea drilling

France and Yorkshire) is similar to the lowest ValanginianNAR (located in Greenland North Sea and France) (Ta-ble S2) Compared to nannofossil species richness and coc-colith mean size these results open new insights into the evo-lution of calcareous nannoplankton over the past sim 200 MyrThree distinct phases can be observed

During the Jurassic and Early Cretaceous the smoothedNAR increased with species richness (Bown 2005) whilecoccolith size was steadily small and started to increaseat the JurassicndashCretaceous boundary (Aubry et al 2005)The beginning of this phase is marked by high calcareousnannoplankton production in epicontinental seas whereasthe end of this phase is marked by greater production in trop-ical open-ocean environments as shown by the NAR maps(Fig 3) Hence this invasion phase reflects a sim 80 Myr longgradual invasion of the western Tethys and Atlantic oceansby calcareous nannoplankton during the JurassicndashEarly Cre-taceous time interval Watznaueria barnesiae (ie a cos-mopolitan Mesozoic coccolithophore species) coccolith bio-metric data show only one size population between the west-ern Tethys (La Charce-Vergol France) and western Pantha-lassa (ODP1149 Nadezhda basin close to Japan) during theLower Cretaceous Thus mixing of coccolithophore popula-tions was effective at that time testifying for a continuousgenetic flux through the Tethys following a circum-globalcirculation (Gollain et al 2019) The genetic flux was prob-ably sustained for many calcareous nannoplankton betweenboth regions of the oceans at that time The Early Cretaceousinvasion phase observed in the Atlantic Ocean may have thushappened in all open oceans worldwide although our re-stricted EuropeanndashNorth Hemisphere dataset cannot corrob-orate it

An abrupt change in NAR dynamics which has beensteadily high since the Early Cretaceous (sim 120 Ma) accord-

ing to the LOESS trend marks the beginning of the secondphase From this point up to the end of the Cretaceous NARremained high but the nannofossil species richness and thecoccolith mean size have increased since the beginning ofthe Cretaceous following CopendashDepeacuteretrsquos rule (ie increasein coccolith size over evolutionary time Aubry et al 2005)As seen in the Valanginian NAR maps (Fig 3bndashc) by thistime the shift in calcareous nannoplankton production towardthe open seas was already accomplished This phase corre-sponds to the specialization phase where more and morespecies shared an increasingly filled ecospace through spe-cialization to particular ecological niches

After the CretaceousndashPaleogene (ie KndashPg) mass extinc-tion event calcareous nannoplankton recovered followingthe same two phases namely invasion and specialization buton a short time interval (less than 4 Myr) although our Pale-ocene NAR record is too limited to unambiguously confirmthis pattern Finally a last phase in the calcareous nanno-plankton evolution started in the Eocene (Figs 2 S3) withsmoothed NAR steadily high or slightly increasing (Figs 2S1) but the nannofossil species richness and coccolith meansize both tending to decrease This may correspond to an es-tablishment phase where fewer species with smaller sizespredominated This establishment phase reached a climaxin modern oceans with the dominance within the coccol-ithophore community of the iconic small-sized species Emil-iania huxleyi (eg Ziveri et al 2000 Baumann et al 2004)

4 Discussion

Extant calcareous nannoplankton is neither uniformly norrandomly dispersed in the global ocean (eg Winter et al1994) Its distribution in ecological niches is shaped by(i) abiotic parameters such as temperature salinity pH and

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2505

Figure 2 Evolution through time of nannofossil accumulation rate species richness and size (a) Compiled nannofossil accumulation rate(nannofossil mminus2 yrminus1) Black circles are samples from Europe North Sea Greenland and North Atlantic and grey circles are from therest of the world The LOESS trend (SF 05) was calculated with all samples (b) Nannofossil species richness (Bown 2005) (c) Coccolithmean size at the assemblage level during the Mesozoic (Aubry et al 2005) and the Cenozoic (Herrmann and Thierstein 2012) Mesozoiccoccolith mean size at the assemblage level is derived from a compilation of species sizes as published in the literature (original taxonomicdescriptions) to which the authors have added their own measurements of published material This record consists of measurements of lengthand width of 302 species which is about one-third of all the described Mesozoic coccolith species The grey area illustrates the minimum andmaximum size recorded Cenozoic coccolith mean size at the assemblage level is derived from measurements of entire coccolith assemblagesduring the last 66 Myr from a number of globally distributed deep-sea cores using automated scanning electron microscopy and imageanalysis processing (d) pCO2 through time with the Foster et al (2017 in parts per million) compilation represented by black filled circlesWitkowski et al (2018 in micro-atmospheres) represented by grey open squares and Miocene pCO2 decline from Mejiacutea et al (2017) inwhite open circles with the range of possible values in grey The LOESS trend was calculated on Fosterrsquos and Witkowskirsquos data assumingparts per million and micro-atmospheres are equivalent and is represented by a black line and grey envelope representing the 95 confidenceinterval around the calculated trend

water mixing but also by the availability of nutrients or light(eg Margalef 1978 Balch 2004) and (ii) by functionalinteractions with other organisms such as viruses (Frada etal 2008) phytoplankton and grazers (Litchman et al 2006)Extant coccolithophores are commonly viewed as ldquointerme-diaterdquo organisms in Margalefrsquos mandala (ie Fig 2 fromMargalef 1978) so basically transitional between K (cor-responding to organisms evolving in more stable predicableand saturated environments eg dinoflagellates) and r (or-ganisms living in unstable unpredictable and unsaturated en-

vironments eg diatoms) strategists (Reznick et al 2002)living in intermediate nutrient-concentrated waters turbu-lence and light availability (Margalef 1978 Balch 2004Tozzi et al 2004) Thus the integration of abiotic and bioticparameters explains the macroecological distribution of ex-tant calcareous nannoplankton Macroecological pattern maychange through time due to evolution And long-term evo-lution ndash macroevolution ndash is influenced by abiotic and bi-otic drivers that have given two evolutionary models RedQueen (Van Valen 1973) and Court Jester (Barnosky 2001)

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2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

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2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

2504 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 1 Location of the sites compiled for this study Colors indicate the age of the samples (Neogene yellow Paleogene orange Creta-ceous green Jurassic blue) Squares represent land outcrops and circles represent deep-sea drilling

France and Yorkshire) is similar to the lowest ValanginianNAR (located in Greenland North Sea and France) (Ta-ble S2) Compared to nannofossil species richness and coc-colith mean size these results open new insights into the evo-lution of calcareous nannoplankton over the past sim 200 MyrThree distinct phases can be observed

During the Jurassic and Early Cretaceous the smoothedNAR increased with species richness (Bown 2005) whilecoccolith size was steadily small and started to increaseat the JurassicndashCretaceous boundary (Aubry et al 2005)The beginning of this phase is marked by high calcareousnannoplankton production in epicontinental seas whereasthe end of this phase is marked by greater production in trop-ical open-ocean environments as shown by the NAR maps(Fig 3) Hence this invasion phase reflects a sim 80 Myr longgradual invasion of the western Tethys and Atlantic oceansby calcareous nannoplankton during the JurassicndashEarly Cre-taceous time interval Watznaueria barnesiae (ie a cos-mopolitan Mesozoic coccolithophore species) coccolith bio-metric data show only one size population between the west-ern Tethys (La Charce-Vergol France) and western Pantha-lassa (ODP1149 Nadezhda basin close to Japan) during theLower Cretaceous Thus mixing of coccolithophore popula-tions was effective at that time testifying for a continuousgenetic flux through the Tethys following a circum-globalcirculation (Gollain et al 2019) The genetic flux was prob-ably sustained for many calcareous nannoplankton betweenboth regions of the oceans at that time The Early Cretaceousinvasion phase observed in the Atlantic Ocean may have thushappened in all open oceans worldwide although our re-stricted EuropeanndashNorth Hemisphere dataset cannot corrob-orate it

An abrupt change in NAR dynamics which has beensteadily high since the Early Cretaceous (sim 120 Ma) accord-

ing to the LOESS trend marks the beginning of the secondphase From this point up to the end of the Cretaceous NARremained high but the nannofossil species richness and thecoccolith mean size have increased since the beginning ofthe Cretaceous following CopendashDepeacuteretrsquos rule (ie increasein coccolith size over evolutionary time Aubry et al 2005)As seen in the Valanginian NAR maps (Fig 3bndashc) by thistime the shift in calcareous nannoplankton production towardthe open seas was already accomplished This phase corre-sponds to the specialization phase where more and morespecies shared an increasingly filled ecospace through spe-cialization to particular ecological niches

After the CretaceousndashPaleogene (ie KndashPg) mass extinc-tion event calcareous nannoplankton recovered followingthe same two phases namely invasion and specialization buton a short time interval (less than 4 Myr) although our Pale-ocene NAR record is too limited to unambiguously confirmthis pattern Finally a last phase in the calcareous nanno-plankton evolution started in the Eocene (Figs 2 S3) withsmoothed NAR steadily high or slightly increasing (Figs 2S1) but the nannofossil species richness and coccolith meansize both tending to decrease This may correspond to an es-tablishment phase where fewer species with smaller sizespredominated This establishment phase reached a climaxin modern oceans with the dominance within the coccol-ithophore community of the iconic small-sized species Emil-iania huxleyi (eg Ziveri et al 2000 Baumann et al 2004)

4 Discussion

Extant calcareous nannoplankton is neither uniformly norrandomly dispersed in the global ocean (eg Winter et al1994) Its distribution in ecological niches is shaped by(i) abiotic parameters such as temperature salinity pH and

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B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2505

Figure 2 Evolution through time of nannofossil accumulation rate species richness and size (a) Compiled nannofossil accumulation rate(nannofossil mminus2 yrminus1) Black circles are samples from Europe North Sea Greenland and North Atlantic and grey circles are from therest of the world The LOESS trend (SF 05) was calculated with all samples (b) Nannofossil species richness (Bown 2005) (c) Coccolithmean size at the assemblage level during the Mesozoic (Aubry et al 2005) and the Cenozoic (Herrmann and Thierstein 2012) Mesozoiccoccolith mean size at the assemblage level is derived from a compilation of species sizes as published in the literature (original taxonomicdescriptions) to which the authors have added their own measurements of published material This record consists of measurements of lengthand width of 302 species which is about one-third of all the described Mesozoic coccolith species The grey area illustrates the minimum andmaximum size recorded Cenozoic coccolith mean size at the assemblage level is derived from measurements of entire coccolith assemblagesduring the last 66 Myr from a number of globally distributed deep-sea cores using automated scanning electron microscopy and imageanalysis processing (d) pCO2 through time with the Foster et al (2017 in parts per million) compilation represented by black filled circlesWitkowski et al (2018 in micro-atmospheres) represented by grey open squares and Miocene pCO2 decline from Mejiacutea et al (2017) inwhite open circles with the range of possible values in grey The LOESS trend was calculated on Fosterrsquos and Witkowskirsquos data assumingparts per million and micro-atmospheres are equivalent and is represented by a black line and grey envelope representing the 95 confidenceinterval around the calculated trend

water mixing but also by the availability of nutrients or light(eg Margalef 1978 Balch 2004) and (ii) by functionalinteractions with other organisms such as viruses (Frada etal 2008) phytoplankton and grazers (Litchman et al 2006)Extant coccolithophores are commonly viewed as ldquointerme-diaterdquo organisms in Margalefrsquos mandala (ie Fig 2 fromMargalef 1978) so basically transitional between K (cor-responding to organisms evolving in more stable predicableand saturated environments eg dinoflagellates) and r (or-ganisms living in unstable unpredictable and unsaturated en-

vironments eg diatoms) strategists (Reznick et al 2002)living in intermediate nutrient-concentrated waters turbu-lence and light availability (Margalef 1978 Balch 2004Tozzi et al 2004) Thus the integration of abiotic and bioticparameters explains the macroecological distribution of ex-tant calcareous nannoplankton Macroecological pattern maychange through time due to evolution And long-term evo-lution ndash macroevolution ndash is influenced by abiotic and bi-otic drivers that have given two evolutionary models RedQueen (Van Valen 1973) and Court Jester (Barnosky 2001)

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2505

Figure 2 Evolution through time of nannofossil accumulation rate species richness and size (a) Compiled nannofossil accumulation rate(nannofossil mminus2 yrminus1) Black circles are samples from Europe North Sea Greenland and North Atlantic and grey circles are from therest of the world The LOESS trend (SF 05) was calculated with all samples (b) Nannofossil species richness (Bown 2005) (c) Coccolithmean size at the assemblage level during the Mesozoic (Aubry et al 2005) and the Cenozoic (Herrmann and Thierstein 2012) Mesozoiccoccolith mean size at the assemblage level is derived from a compilation of species sizes as published in the literature (original taxonomicdescriptions) to which the authors have added their own measurements of published material This record consists of measurements of lengthand width of 302 species which is about one-third of all the described Mesozoic coccolith species The grey area illustrates the minimum andmaximum size recorded Cenozoic coccolith mean size at the assemblage level is derived from measurements of entire coccolith assemblagesduring the last 66 Myr from a number of globally distributed deep-sea cores using automated scanning electron microscopy and imageanalysis processing (d) pCO2 through time with the Foster et al (2017 in parts per million) compilation represented by black filled circlesWitkowski et al (2018 in micro-atmospheres) represented by grey open squares and Miocene pCO2 decline from Mejiacutea et al (2017) inwhite open circles with the range of possible values in grey The LOESS trend was calculated on Fosterrsquos and Witkowskirsquos data assumingparts per million and micro-atmospheres are equivalent and is represented by a black line and grey envelope representing the 95 confidenceinterval around the calculated trend

water mixing but also by the availability of nutrients or light(eg Margalef 1978 Balch 2004) and (ii) by functionalinteractions with other organisms such as viruses (Frada etal 2008) phytoplankton and grazers (Litchman et al 2006)Extant coccolithophores are commonly viewed as ldquointerme-diaterdquo organisms in Margalefrsquos mandala (ie Fig 2 fromMargalef 1978) so basically transitional between K (cor-responding to organisms evolving in more stable predicableand saturated environments eg dinoflagellates) and r (or-ganisms living in unstable unpredictable and unsaturated en-

vironments eg diatoms) strategists (Reznick et al 2002)living in intermediate nutrient-concentrated waters turbu-lence and light availability (Margalef 1978 Balch 2004Tozzi et al 2004) Thus the integration of abiotic and bioticparameters explains the macroecological distribution of ex-tant calcareous nannoplankton Macroecological pattern maychange through time due to evolution And long-term evo-lution ndash macroevolution ndash is influenced by abiotic and bi-otic drivers that have given two evolutionary models RedQueen (Van Valen 1973) and Court Jester (Barnosky 2001)

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

2506 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

Figure 3 Maps of nannofossil accumulation rate (nannofos-sil mminus2 yrminus1) drawn from the linear interpolation of the measure-ments realized at various sites (Table S2) Emerged lands are drawnin white epicontinental seas are indicated in grey and open oceansare indicated in black (a) Toarcian in Europe 11 sites consid-ered namely Peniche (Portugal) Rabaccedilal (Portugal) La Cerradura(Spain) HTM-102 (France) Tournadous (France) Saint-Paul-des-Fonts (France) Yorkshire (UK) Dotternhausen (Germany) Somma(Italy) Chionistra (Greece) and Reacuteka Valley (Hungary) for a totalof 229 analyzed samples (b) Valanginian in Europe six sites con-sidered namely Perisphinctes ravine (Greenland) ODP638 (NorthAtlantic) Vergol-La Charce (France) Carajuan (France) BGS8143 (North Sea) and Polaveno (Italy) for a total of 371 ana-lyzed samples (c) Valanginian in Europe and the Atlantic Oceanadding three sites to the European ones DSDP535 (Mexico Gulf)DSDP534A (North Atlantic) and DSDP603B (North Atlantic) fora total of 517 analyzed samples Paleogeographic maps modifiedfrom Ziegler (1988) and Blakey (2008)

hypotheses The former states that biotic interactions driveevolutionary changes whereas the latter asserts that changesin physical environments initiate evolutionary changes Thedifferent phases observed here could be described in light ofmacroecological and macroevolutionary models

The invasion phase during the JurassicndashEarly Cretaceousis marked by both increasing NAR and nannoplanktonspecies richness indicating that the new occurring species in-creases the NAR without limiting the distribution of alreadyexisting species Hence the ecology of JurassicndashEarly Cre-taceous nannoplankton species was closer to the r strategistpole of density-independent selection (Reznick et al 2002)The invasion phase echoes the beginning of the diversifica-tion of various planktic organisms ndash the Mesozoic plankton

revolution Even if there is an important change in the or-ganization of the plankton community the invasion phase islikely driven by the Pangaea breakup This major tectonicevent gave rise to newly formed oceanic domains createdperennial connections between the Pacific Tethys and At-lantic oceans and initiated sea-level rise and flooding of con-tinental areas finally establishing more numerous and het-erogeneous ecological niches (Roth 1989 Katz et al 2004)The Mesozoic change in ocean chemistry with increases inCd Cu Mo Zn and nitrate availability linked to deep-oceanoxygenation would also have favored the development of thered lineage algae (ie using chlorophyll a with chlorophyllc and fucoxanthin as accessory pigments typical in Hapto-phyte) such as coccolithophores (Falkowski et al 2004) Al-though this Court Jester scenario most likely explains the in-vasion of the oceans by calcareous nannoplankton Sucheacuteras-Marx and co-workers pointed out that the increase in NARduring the early Bajocian (Middle Jurassicsim 170 Ma) couldalso have resulted from a more efficient exploitation of eco-logical niches by the newly originated species (Sucheacuteras-Marx et al 2015)

The following specialization phase is marked by cal-careous nannoplankton species having reached the maxi-mum production of platelets (on average sim 1011 nanno-fossils mminus2 yrminus1) but these were produced by an increas-ing number of species characterized by a higher coccol-ith size variance than in the previous phase (Fig 2) Thisrecord suggests that more and more species shared an in-creasingly filled ecospace therefore becoming more special-ized to peculiar ecological niches This specialization mightcorrespond to an adaptation of different species to a partic-ular ecological niche variable trophic levels (ie oligo- toeutrophic eg Herrle 2003 Lees et al 2005) temperatureconditions (eg Mutterlose et al 2014) or seasonality andblooming (eg Thomsen 1989) Consequently late Earlyand Late Cretaceous species were closer to the K strategistpole of density-dependent selection corresponding to organ-isms evolving closer to carrying capacity This time intervalwitnessed many drastic short-term climatic and environmen-tal perturbations such as oceanic anoxic events (OAEs) ther-mal optimums or cooling (Friedrich et al 2012) but alsosome relatively stable long-term physical conditions (egsea level Muumlller et al 2008) Despite some major short-termabiotic parameter changes this macroevolutionary phase ismore compatible with the Red Queen model This time inter-val is the paroxysm of the Mesozoic plankton revolution withthe first occurrence of diatoms a plateau of marine dinoflag-ellate species richness and the diversification of plankticforaminifera which together with calcareous nannoplank-ton (Falkowski et al 2004 Knoll and Follows 2016) con-tributed to form massive chalk deposits (Roth 1986) Thesevarious lines of evidence point toward an increase in inter-action and competition between plankton organisms Ulti-mately the Mesozoic plankton revolution led to a bottom-upcontrol of plankton on the entire marine ecosystem structure

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2507

(Knoll and Follows 2016) as revealed by the diversificationof spatangoids echinoids palaeocorystids crabs Ancylocer-atina ammonites (Fraaije et al 2018) and many other groupsduring the Mesozoic plankton revolution (Vermeij 1977) in-cluding highly diverse marine reptiles (Pyenson et al 2014)

The Court Jester model applies to the KndashPg mass extinc-tion (66 Ma) well This mass extinction event is related toabiotic perturbation ie the Deccan traps volcanism (Cour-tillot et al 1986) and an asteroid impact (Alvarez et al1980) This event had a catastrophic impact on calcareousnannoplankton diversity with a species turnover of up to80 during the crisis (Bown 2005) The KndashPg crisis almostshut down pelagic production with raw NAR values return-ing to Lower Jurassic ones (107ndash108 nannofossils mminus2 yrminus1Fig 2) (Hull et al 2011) Our record of the aftermath ofthe KndashPg event indicates that the NAR recovered to pre-extinction levels in less than 4 Myr (Fig 2) Associated withthis Paleocene post-crisis NAR increase which was followedby a steady production for the rest of this Epoch an increasein coccolith mean size and in species richness is observed(Fig 2) At a much shorter timescale the Paleocene there-fore appears similar to the JurassicndashCretaceous interval inthat a first invasion phase (the post-crisis biotic recovery)and the origination of new calcareous nannoplankton fami-lies (Bown 2005) is followed by a period of species diversifi-cation and ecological specialization ndash a specialization phase

Eventually at the end of the Paleogene and during theNeogene calcareous nannoplankton experienced a third evo-lutionary phase ndash the establishment ndash characterized by highraw NAR and lower species richness involving smaller-sizedspecies than in the Cretaceous This last phase may havebeen driven by combined abiotic and biotic changes Firstthe decrease in pCO2 below a threshold throughout the Neo-gene could have driven the decrease in coccolithophore cellsize (Hannisdal et al 2012) based on estimation of coccol-ith size decrease (Bolton et al 2016) The carbon supply tococcolithophore cells is indeed sustained by CO2 diffusionthrough the cellular membrane and depends on the cell sur-face volume ratio which is in turn controlled by cell sizeIn many coccolithophores there is a linear (isometric) rela-tion between coccolith size and cell size (Henderiks 2008)Consequently the fitness decrease in large-sized species re-lated to the pCO2 drawdown led to a reduction in speciesrichness Secondly diatoms tremendously diversified due toincrease in silicic acid input to the oceans during this time in-terval (Spencer-Cervato 1999 Cermentildeo et al 2015) locallyoutcompeting calcareous nannoplankton and only the mostcompetitive coccolithophore species continued to proliferateA habitat partitioning resulted with calcareous nannoplank-ton dominating the open-ocean oligotrophic areas whereasdiatoms thrived in meso-eutrophic coastal regions (Margalef1978) Nevertheless modern-day calcareous nannoplanktonis still more abundant in eutrophic upwelling regions than inopen oceans (Baumann et al 2004) underscoring a complex

rearrangement of microplankton community rather than asimple replacement of calcareous nannoplankton by diatoms

5 Conclusions

Coccolithophores represent about half of the calcium car-bonate in late Holocene deep-sea sediments but they wereless abundant at the onset of calcareous nannoplankton evo-lution Since the first occurrence of calcareous nannoplank-ton in the Late Triassic the colonization of the oceans was along-lasting and gradual process which can be separated intothree successive phases based on comparison of the nanno-fossil accumulation rate species richness and coccolith meansize variations The first phase from Early Jurassic to EarlyCretaceous corresponds to the nannoplankton oceansrsquo inva-sion This phase is marked by an increasing NAR trend inspecies richness along with a steady to slight increase incoccolith mean size In this time interval our results sug-gest that the nannofossil accumulation almost exclusivelyoccurred in epicontinental seas By the Early Cretaceous aphase of specialization started NAR attained the highest val-ues while species richness and coccolith mean size continuedto increase Moreover NAR became highest in open-oceantropical environments During this second phase an increas-ing number of species tended to specialize and to more ef-ficiently share the available ecospace After the KndashPg massextinction that led to a new and brief invasion and special-ization phase a third and ongoing phase began during theEocenendashOligocene It is marked by a steady NAR but re-duced species richness and coccolith mean size A smallernumber of species characterized by smaller size produce asmany fossil coccoliths as before pointing toward an increasein absolute abundances at least for some species This estab-lishment phase may be simultaneously related to the diversi-fication and competitive interaction of diatoms and to a de-crease in atmospheric pCO2 Finally the long-term calcare-ous nannoplankton evolution over the past 200 Myr appearsas a gradual colonization of almost all marine environmentswithin the world ocean Such colonization was successivelyshaped by abiotic and biotic factors ultimately pointing to-ward the Court Jester and the Red Queen macroevolutionarymodels as likely scenarios of the invasion and specializationphases respectively and both models apply to the more re-cent establishment phase

Data availability Data are available in the Supplement in two Ex-cel files Table S1 gathered the dataset of nannofossil accumula-tion rate in the different settings studied in this work sorted inchronological order Each sheet presents the location of the sitethe age (relative and absolute) the nannofossil absolute abundancethe sedimentation rate the nannofossil accumulation rate and otherinformation such as the sample name height in the section and thepublished reference Table S2 gathered the datasets of nannofossilaccumulation rate used to construct Fig 3 The table presents for

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

2508 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

both considered geological stages (ie Toarcian and Valanginian)the location of each site their mean nannofossil absolute abun-dance and mean nannofossil accumulation rate and the numberof samples per site The data used in the paper are available athttpsdoiorg101594PANGAEA902908 (Sucheacuteras-Marx et al2019)

Sample availability Slides made by BSM and EM for the calcare-ous nannofossil study are curated at the Collections de Geacuteologie deLyon de lrsquoUniversiteacute Lyon 1 (collection code FSL)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194bg-16-2501-2019-supplement

Author contributions BSM and EM contributed equally to thiswork BSM and EM designed the study and compiled the data BPprovided accumulation rates BSM performed the calculations PAconstructed the maps EM FG and JP provided unpublished dataBSM EM and FG devised the model with advice from GE BSMEM FG and GE wrote the text with significant inputs from all otherauthors

Competing interests The authors declare that they have no conflictof interest

Acknowledgements Emanuela Mattioli acknowledges fundingfrom INSU SYSTER 2011ndash2012 and INTERRVIE 2014ndash2015Baptiste Sucheacuteras-Marx kindly thanks Jorijntje Henderiks for con-structive comments on a previous version of the dataset Bap-tiste Sucheacuteras-Mar thanks the team Climat at Cerege

Review statement This paper was edited by Jack Middelburg andreviewed by Nina Keul and one anonymous referee

References

Alvarez L W Alvarez W Asaro F and Michel H V Extrater-restrial cause for the Cretaceous-Tertiary extinction Science208 1095ndash1108 httpsdoiorg101126science208444810951980

Aubry M-P Bord D Beaufort L Kahn A andBoyd S Trends in size changes in the coccol-ithophorids calcareous nannoplankton during the Meso-zoic A pilot study Micropaleontology 51 309ndash318httpsdoiorg102113gsmicropal514309 2005

Balch W M Re-evaluation of the physiological ecology ofcoccolithophores in Coccolithophores From molecular pro-cesses to global impact edited by Thierstein H R andYoung J R Springer-Verlag Heidelberg Germany 165ndash190httpsdoiorg101007978-3-662-06278-4_7 2004

Barnosky A D Distinguishing the effects of the RedQueen and Court Jester on Miocene mammal evo-lution in the northern Rocky Mountains J VertebrPaleontol 21 172ndash185 httpsdoiorg1016710272-4634(2001)021[0172DTEOTR]20CO2 2001

Baumann K-H Boumlckel B and Frenz M Coccolith contributionto South Atlantic carbonate sedimentation in CoccolithophoresFrom molecular processes to global impact edited by Thier-stein H R and Young J R Springer-Verlag Heidelberg Ger-many 367ndash402 httpsdoiorg101007978-3-662-06278-4_142004

Blakey R C Gondwana paleogeography from assembly tobreakup ndash A 500 my odyssey Geol Soc Am Spec Paper 4411ndash28 httpsdoiorg10113020082441(01) 2008

Bolton C T Hernandez-Sanchez M T Fuertes M-AGonzalez-Lemos S Abrevaya L Mendez-Vicente AFlores J-A Probert I Giosan L Johnson J andStoll H M Decrease in coccolithophore calcification andCO2 since the middle Miocene Nat Commun 7 10284httpsdoiorg101038ncomms10284 2016

Bown P R Calcareous nannoplankton evolution atale of two oceans Micropaleontology 51 299ndash308httpsdoiorg102113gsmicropal514299 2005

Broecker W S and Clark E Ratio of coccolithCaCO3 to foraminifera CaCO3 in late Holocenedeep sea sediments Paleoceanography 24 PA3205httpsdoiorg1010292009PA001731 2009

Cermentildeo P Falkowski P G Romero O E Schaller M Fand Vallina S M Continental erosion and the Cenozoic riseof marine diatoms P Natl Acad Sci USA 112 4239-4244httpsdoiorg101073pnas1412883112 2015

Channel J E T Erba E Muttoni G and Tremolada F EarlyCretaceous magnetic stratigraphy in the APTICORE drill coreand adjacent outcrop at Cismon (Southern Alps Italy) and thecorrelation to the proposed BarremianAptian boundary strato-type Geol Soc Am Bull 112 1430ndash1443 2000

Courtillot V Besse J Vandamme D Montigny R JaegerJ-J and Cappetta H Deccan flood basalts at the Creta-ceousTertiary boundary Earth Planet Sc Lett 80 361ndash374httpsdoiorg1010160012-821X(86)90118-4 1986

Erba E and Tremolada F Nannofossil carbonate fluxes duringthe Early Cretaceous phytoplankton response to nutrificationepisodes atmospheric CO2 and anoxia Paleoceanography 19PA1008 httpsdoiorg1010292003PA000884 2004

Falkowski P G Katz M E Knoll A H Quigg A RavenJ A Schofield O and Taylor F J R The evolutionof modern eukaryotic phytoplankton Science 305 354ndash360httpsdoiorg101126science1095964 2004

Foster G L Royer D L and Lunt D J Future climate forc-ing potentially without precedent in the last 420 million yearsNat Commun 8 14845 httpsdoiorg101038ncomms148452017

Fraaije R H B Van Bakel B W M Jagt J W M and Vie-gas P A The rise of a novel plankton-based marine ecosystemduring the Mesozoic a bottom-up model to explain new higher-tier invertebrate morphotypes B Soc Geol Mex 70 187ndash2002018

Frada M Probert I Allen M J Wilson W H andde Vargas C The ldquoCheshire Catrdquo escape strategy of

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019

B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae 2509

the coccolithophore Emiliania huxleyi in response to vi-ral infection P Natl Acad Sci USA 105 15944ndash15949httpsdoiorg101073pnas0807707105 2008

Friedrich O Norris R D and Erbacher J Evolution of middle toLate Cretaceous oceans-A 55 my record of Earthrsquos temperatureand carbon cycle Geology 40 107ndash110 2012

Gardin S Krystyn L Richoz S Bartolini A and GalbrunB Where and when the earliest coccolithophores Lethaia45 507ndash523 httpsdoiorg101111j1502-3931201200311x2012

Geisen M Bollmann J Herrle J O Mutterlose J and YoungJ R Calibration of the random settling technique for calculationof absolute abundances of calcareous nannoplankton Micropale-ontology 45 437ndash442 httpsdoiorg1023071486125 1999

Gollain G Mattioli E Kenjo S Bartolini A and Reboulet SSize patterns of the coccolith Watznaueria barnesiae in the lowerCretaceous Biotic versus abiotic forcing Mar Micropaleontolhttpsdoiorg101016jmarmicro201903012 2019

Gradstein F M Ogg J G Schmitz M D and Ogg G MThe Geologic Time Scale 2012 Elsevier Amsterdam 1144 pp2012

Hammer Oslash Harper D A T and Ryan P D PAST paleontolog-ical statistics software package for education and data analysisPalaeontol Electronica 4 1ndash9 2001

Hannisdal B Henderiks J and Liow L H Long-term evolu-tionary and ecological responses of calcifying phytoplankton tochanges in atmospheric CO2 Glob Change Biol 18 3504ndash3516 httpsdoiorg101111gcb12007 2012

Hart M B Hylton M D Oxford M J Price G D Hud-son W and Smart C W The search for the origin of theplanktic foraminifera J Geol Soc London 160 341ndash343httpsdoiorg1011440016-764903-003 2003

Henderiks J Coccolithophore size rules ndash Reconstructingancient cell geometry and cellular calcite quota fromfossil coccoliths Mar Micropaleontol 67 143ndash154httpsdoiorg101016jmarmicro200801005 2008

Herrle J O Reconstructing nutricline dynamics of mid-Cretaceous oceans evidence from calcareous nannofossils fromthe Niveau Paquier black shale (SE France) Mar Micropaleon-tol 47 307ndash321 2003

Herrmann S and Thierstein H R Cenozoic coc-colith size changesndashevolutionary andor ecologicalcontrols Palaeogeogr Palaeocl 333334 92ndash106httpsdoiorg101016jpalaeo201203011 2012

Hull P M Norris R D Bralower T J and SchuethJ D A role for chance in marine recovery from theendndashCretaceous extinction Nat Geosci 4 856ndash860httpsdoiorg101038ngeo1302 2011

Katz M E Finkel Z V Grzebyk D Knoll A Hand Falkowski P G Evolutionary trajectories andbiogeochemical impacts of marine eukaryotic phyto-plankton Annu Rev Ecol Evol S 35 523ndash556httpsdoiorg101146annurevecolsys351122021301372004

Klaas C and Archer D E Association of sinking organic mat-ter with various types of mineral ballast in the deep sea Im-plications for the rain ratio Global Biogeochem Cy 16 1116httpsdoiorg1010292001GB001765 2002

Knoll A H and Follows M J A bottom-up perspective onecosystem change in Mesozoic oceans P Roy Soc B-Biol Sci283 20161755 httpsdoiorg101098rspb20161755 2016

Kooistra W H C F Gersonde R Medlin L K and Mann DG The origin and evolution of the diatoms their adaptation to aplanktonic existence in evolution of primary producers in thesea edited by Falkowski P G and Knoll A H AcademicPress Burlington USA 207ndash249 httpsdoiorg101016B978-012370518-150012-6 2007

Lees J A Bown P R and Mattioli E Problems with proxiesCautionary tales of calcareous nannofossil paleoenvironmentalindicators Micropaleontol 51 333ndash343 2005

Litchman E Klausmeier C A Miller J R Schofield O M andFalkowski P G Multi-nutrient multi-group model of presentand future oceanic phytoplankton communities Biogeosciences3 585ndash606 httpsdoiorg105194bg-3-585-2006 2006

Margalef R Life-forms of phytoplankton as survival alternativesin an unstable environment Oceanol Acta 1 493ndash509 1978

Mattioli E Pittet B Petitpierre L and Mailliot S Dramatic de-crease of pelagic carbonate production by nannoplankton acrossthe Early Toarcian anoxic event (T-OAE) Glob Planet Change65 134ndash145 httpsdoiorg101016jgloplacha2008100182009

Mejiacutea L M Meacutendez-Vicente A Abrevaya L Lawrence K TLadlow C Bolton C Cacho I and Stoll H A diatom recordof CO2 decline since the late Miocene Earth Planet Sc Lett479 18ndash33 httpsdoiorg101016jepsl201708034 2017

Monteiro F M Bach L T Brownlee C Bown P R RickabyR E M Poulton A J Tyrrell T Beaufort L Dutkiewicz SGibbs S J Gutowska M A Lee R Riebesell U YoungJ R and Ridgwell A Why marine phytoplankton calcifySci Adv 2 e1501822 httpsdoiorg101126sciadv15018222016

Muumlller R D Sdrolias M Gaina C Steinberger Band Heine C Long-term sea-level fluctuations drivenby ocean basin dynamics Science 319 1357ndash1362httpsdoiorg101126science1151540 2008

Mutterlose J Bottini C Schouten S and Sinninghe DamsteacuteJS High sea-surface temperatures during the early AptianOceanic Anoxic Event 1a in the Boreal Realm Geology 42439ndash442 httpsdoiorg101130g353941 2014

Poulton A J Adey T R Balch W M and Holligan PM Relating coccolithophore calcification rates to phytoplank-ton community dynamics Regional differences and implica-tions for carbon export Deep-Sea Res Pt 2 54 538ndash557httpsdoiorg101016jdsr2200612003 2007

Pyenson N D Kelley N P and Parham J F Marine tetra-pod macroevolution Physical and biological drivers on 250 Maof invasions and evolution in ocean ecosystems PalaeogeogrPalaeocl 400 1ndash8 2014

Reznick D Bryant M J and Bashey F r- andK-selection revis-ited the role of population regulation in lifendashhistory evolutionEcology 83 1509ndash1520 2002

Roth P H Mesozoic paleoceanography of the North Atlantic andTethys Oceans in North Atlantic Paleoceanography edited bySummerhayes C P and Shackleton N J Geol Soc Spec PublLond 21 299ndash320 1986

Roth P H Ocean circulation and calcareous nannoplank-ton evolution during the Jurassic and Cretaceous Palaeo-

wwwbiogeosciencesnet1625012019 Biogeosciences 16 2501ndash2510 2019

2510 B Sucheacuteras-Marx et al The colonization of the oceans by calcifying pelagic algae

geogr Palaeocl 74 111ndash126 httpsdoiorg1010160031-0182(89)90022-9 1989

Spencer-Cervato C The Cenozoic deep sea microfossil recordexplorations of the DSDPODP sample set using the Neptunedatabase Palaeontol Electronica 2 1ndash270 1999

Sucheacuteras-Marx B and Henderiks J Downsizing thepelagic carbonate factory Impacts of calcareous nanno-plankton evolution on carbonate burial over the past17 million years Glob Planet Change 123 97ndash109httpsdoiorg101016jgloplacha201410015 2014

Sucheacuteras-Marx B Guihou A Giraud F Leacutecuyer C Alle-mand P Pittet B and Mattioli E Impact of theMiddle Jurassic diversification of Watznaueria (coccolithndashbearing algae) on the carbon cycle and δ13C of bulkmarine carbonates Glob Planet Change 86ndash87 92ndash100httpsdoiorg101016jgloplacha201202007 2012

Sucheacuteras-Marx B Giraud F Mattioli E and EscarguelG Paleoenvironmental and paleobiological origins of coc-colithophorid genus Watznaueria emergence during theLate AalenianndashEarly Bajocian Paleobiology 41 415ndash435httpsdoiorg101017pab20158 2015

Sucheacuteras-Marx B Mattioli E Allemand P Giraud F Pit-tet B Plancq J Escarguel G Calcareous nannofos-sils absolute abundance and accumulation rates PANGAEAhttpsdoiorg101594PANGAEA902908 last access 24 June2019

Thomsen E Seasonal variation in boreal Early Cretaceouscalcareous nannofossils Mar Micropaleontol 15 123ndash152httpsdoiorg1010160377-8398(89)90008-X 1989

Tozzi S Schofield O M and Falkowski P G Historical cli-mate change and ocean turbulence as selective agents for twokey phytoplankton functional groups Mar Ecol Prog Ser 274123ndash132 httpsdoiorg103354meps274123 2004

Van Valen L A A new evolutionary law Evol Theor 1 1ndash301973

Vermeij G J The Mesozoic marine revolution evidencefrom snails predators and grazers Paleobiology 3 245ndash258httpsdoiorg101017S0094837300005352 1977

Westermann G E G Global bio-events in mid-Jurassic am-monites controlled by seaways in The Ammonoidea environ-ment ecology and evolutionary change edited by House M RThe Systematics Association Special Volume Oxford UniversityPress UK 187ndash226 1993

Winter A Jordan R W and Roth P H Biogeography of livingcoccolithophores in ocean waters in Coccolithophores editedby Winter A and Siesser W G Cambridge University PressCambridge UK 161ndash178 1994

Witkowski C R Weijers J W H Blais B Schouten S andSinninghe Damsteacute J S Molecular fossils from phytoplanktonreveal secular pCO2 trend over the Phanerozoic Sci Adv 4eaat4556 httpsdoiorg101126sciadvaat4556 2018

Ziegler P A Evolution of the ArcticndashNorth Atlantic and the West-ern Tethys Am Assoc Pet Geol Memoir 43 164ndash196 1988

Ziveri P Rutten A de Lange G J Thomson J and CorselliC Present-day coccolith fluxes recorded in central easternMediterranean sediment traps and surface sediments Palaeo-geogr Palaeocl 158 175ndash195 httpsdoiorg101016S0031-0182(00)00049-3 2000

Biogeosciences 16 2501ndash2510 2019 wwwbiogeosciencesnet1625012019