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Nannofossil carbonate fluxes during the Early Cretaceous:

Phytoplankton response to nutrification episodes,

atmospheric CO2, and anoxiaElisabetta Erba and Fabrizio TremoladaDipartimento di Scienze Della Terra A. Desio, Milan, Italy

Received 23 January 2003; revised 2 October 2003; accepted 31 October 2003; published 10 February 2004.

[1] Greenhouse episodes during the Valanginian and Aptian correlate with major perturbations in the C cycleand in marine ecosystems, carbonate crises, and widespread deposition of Corg-rich black shales. Quantitativeanalyses of nannofossil micrite were conducted on continuous pelagic sections from the Southern Alps (northernItaly), where high-resolution integrated stratigraphy allows precise dating of Early Cretaceous geological events.Rock-forming calcareous nannofloras were quantified in smear slides and thin sections to obtain relative andabsolute abundances and paleofluxes that are interpreted as the response of calcareous phytoplankton to globalchanges in the ocean-atmosphere system. Increased rates of volcanism during the formation of Ontong Java andManihiki Plateaus and the Parana-Etendeka large igneous province (LIP) are proposed to have caused thegeological responses associated with early Aptian oceanic anoxic event (OAE) 1a and the Valanginian event,respectively. Calcareous nannofloras reacted to the new conditions of higher pCO2 and fertility by drasticallyreducing calcification. The Valanginian event is marked by a 65% reduction in nannofossil paleofluxes thatwould correspond to a 23 times increase in pCO2 during formation of the Parana-Endenteka LIP. A 90%reduction in nannofossil paleofluxes, which occurred in a 1.5 myr-long interval leading into OAE1a, isinterpreted as the result of a 36 times increase in pCO2 produced by emplacement of the giant Ontong Java andManihiki Plateaus. High pCO2 was balanced back by an accelerated biological pump during the Valanginianepisode, but not during OAE1a, suggesting persisting high levels ofpCO2 in the late Aptian and/or the inabilityof calcareous phytoplankton to absorb excess pCO2 above threshold values. INDEX TERMS: 1040 Geochemistry:Isotopic composition/chemistry; 1050 Geochemistry: Marine geochemistry (4835, 4850); 1055 Geochemistry: Organic geochemistry;

1615 Global Change: Biogeochemical processes (4805); 1635 Global Change: Oceans (4203); KEYWORDS: Early Cretaceous,

nannofossil fluxes, global change

Citation: Erba, E., and F. Tremolada (2004), Nannofossil carbonate fluxes during the Early Cretaceous: Phytoplankton response tonutrification episodes, atmospheric CO2, and anoxia, Paleoceanography, 19, PA1008, doi:10.1029/2003PA000884.

1. Introduction

[2] In the present oceans, coccolithophores are primaryproducers that convert dissolved carbon dioxide into organicmatter and calcite, and consequently, calcareous nanno-

plankton are key organisms for understanding both the biological and the carbonate pumps. While investigationsof sediment traps and calcareous oozes are addressed tounderstanding surface ocean processes of primary produc-tion and fluxes of biogenic and inorganic particles, ancientsedimentary successions can be decoded for characteriza-

tion of paleobiological processes and paleofluxes.[3] Coccolithophores dominate phytoplankton assemblages in the open ocean, whereas they are subordinate tosiliceous (diatoms) and nonmineralizing (bacteria and dino-flagellates) phytoplankton in areas characterized by meso-trophic to eutrophic conditions. The understanding of howcarbonate and siliceous primary production functions andinteracts is fundamental for the interpretation of geochem-ical cycles of calcium and carbon dioxide. Coccolithophore

photosynthesis and biocalcification affect the organic and

inorganic carbon cycle as well as adsorption of atmosphericCO2 into the oceans. These biotic sinks for CO2 implynutrification events and interactions of the carbon cycle withother biogeochemical cycles.

[4] Recent studies of the effects of atmospheric CO2 onrates of organic matter and calcite production in extant

Emiliania huxleyi and Gephyrocapsa oceanica clearly indi-cate that increasing atmospheric CO2 induces reduced

biocalcification [ Riebesell et al., 2000; Zondervan et al.,2001]. Similar results were obtained for coral reefs [Gattusoet al., 1998; Gattuso and Buddemeier, 2000; Kleypas et al.,

1999; Langdon et al., 2000; Leclercq et al., 2000] and planktonic foraminifera [ Bijma et al., 1999; Barker andElderfield, 2002], further indicating that biocalcification isstrongly inhibited under high pCO2.

[5] Estimates of coccolith carbonate fluxes are crucial forquantitatively assessing the information preserved in thesediment record and for using coccolithophores as biotic

proxies of paleoceanographic and climate change. Calcare-ous nannofossils (coccoliths and nannoliths) have been the

principal contributors to pelagic micrites since the Jurassic.Because calcareous nannofossils constitute the bulk ofcalcareous oozes and micritic limestones, characterization

PALEOCEANOGRAPHY, VOL. 19, PA1008, doi:10.1029/2003PA000884, 2004

Copyright 2004 by the American Geophysical Union.0883-8305/04/2003PA000884$12.00

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(Figure 1), where the Lower Cretaceous pelagic successionis represented by the Maiolica Formation consisting of thin-

bedded calcilutites, with chert and black shale as minorlithologies. The Polaveno section is a continuous outcrop oflimestones with radiolarian-rich layers, chert nodules, lensesand beds, and black shales [ Erba and Quadrio, 1987;

Bersezio et al., 2002]. The detailed biostratigraphy, magne-tostratigraphy, and chemostratigraphy [Channell and Erba,

1992; Lini et al., 1992; Channell et al., 1993; 1995a; Bersezio et al., 2002] have been used for refinement ofchronostratigraphy and timescales [Channell et al., 1995a,1995b] and paleoceanographic reconstructions [ Lini et al.,1992; Channell et al., 1993; Weissert et al., 1998; Bersezioet al., 2002].

[13] The Cismon Apticore is a reference Barremian-Aptian pelagic section owing to its completeness andrelatively high sedimentation rate and the good time control

based on integrated bio-magneto-chemo-cyclostratigraphy[Channell et al., 1979; Weissert et al., 1985; Bralower,1987; Weissert, 1989; Weissert and Lini, 1991; Herbert,1992; Erba, 1994; Menegatti et al., 1998; Erba et al., 1999;Channell et al., 2000; Opdyke et al., submitted manuscript,

2003]. The Hauterivian-Barremian interval at Cismon con-sists of dominant limestones with intercalated black shales;radiolarian-rich arenites are frequent. In the lower Aptian, amajor lithologic change from limestone to black shale andmarlstone corresponds to the Selli Level representing theOAE1a in the Tethys Ocean. The upper Aptian consists ofmarly limestone with radiolarian-rich layers and chert [Erbaand Larson, 1998].

2.2. Sample Preparation and Nannofossil Counts

[14] At Polaveno and Cismon, calcareous nannofossilswere quantified both in smear slides and thin sections by

light polarizing microscope at 1250 times magnification.Smear slides were prepared for limestones, marlstones, and

black shales, after powdering a small quantity of rock,without centrifuging and/or ultrasonic cleaning to retain theoriginal composition. Permanent slides were mounted with

Norland optical adhesive. Thin sections were prepared onlyfor hard lithologies. At Polaveno, a total of 372 samples(236 smear slides and 136 thin sections) were studied, with an

average sampling rate of 70 cm for limestones, correspondingto approximately 1 sample every $40 5 kyr, owing tovariable sedimentation rates. In the Cismon core, 641 smearslides were prepared every 10 cm, corresponding to approx-imately 1 sample every $10 2 kyr. A total of 293 thinsections were prepared from samples collected in hardlithologies every 40 cm, corresponding to approximately1 sample every $40 5 kyr, owing to variable sedimentationrates. In smear slides, nannofossil assemblages were quanti-fied by counting at least 300 specimens and then percentagesof single taxon with respect to the total nannoflora (relativeabundance) were calculated. Thin sections were thinned to anaverage thickness of 7 mm in order to have an adequate viewof nannofloras. Absolute abundances were obtained by

counting all nannofossil specimens in 1 mm2 of thin section.For each sample (smear slides and thin sections), counts wererepeated 3 times and the standard deviation averages +1.5%at the 95% confidence level.

2.3. Nannofossil Paleofluxes

[15] The Polaveno and Cismon pelagic successions aredated with a high-resolution biostratigrpahy, magnetostra-tigraphy, and chemostratigraphy that allows a precise esti-mate of sedimentation rates of the investigated intervals.

Nannofossil paleofluxes have been calculated for themicrite-constituting nannofossils, taking into account abso-

Figure 1. Paleogeographic reconstruction of the Southern Alps in the Early Cretaceous (modified afterWeissert and Lini [1991]). The studied sections are indicated as 1 = Polaveno (eastern Lombardian basin)and 2 = Cismon (Belluno Basin).

PA1008 ERBA AND TREMOLADA: EARLY CRETACEOUS NANNOFOSSIL FLUXES

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lute abundances of the most common taxa, volume/mass ofindividual taxon, unit area (1 mm2), and unit time (1 year).The latter was derived from sedimentation rates estimatedfor individual magnetic polarity chrons [Channell et al.,2000]. Depending on sedimentation rates, the thickness of

thin sections (= 7 mm) represents 714 months, and wenormalized all absolute abundances to 1 year.

[16] Previous calculation of volume and mass of Meso-zoic nannofossils was documented by Williams and

Bralower [1995], who estimated an averaged Cretaceousnannofossil with a volume of 14 mm3. For the presentstudy we adopt the results of the morphometric analysesconducted by Tremolada and Young [2002] on the mostcommon Early Cretaceous taxa in well-preserved materialrecovered at sections and oceanic sites with high-resolutionintegrated stratigraphy. For size determination, pictures ofnannofossils were captured using a digital image system[Young et al., 1996] at 1600 and 1250 times magnification;then the dimensions were measured using the software

National Institutes of Health (NIH)-Image adapted fornannoplankton analyses. For each taxon, at least 250 speci-mens were investigated to give the most accurate sizeestimate. In addition, measurements were carried out byscanning electron microscope (SEM) on selected taxa tocompare the results obtained by three-dimensional (3-D)and 2-D observations. Details of image analyses are givenin the work of Tremolada and Young [2002]. Volume andmass estimates of selected nannofossil taxa used in thisstudy are reported in Table 1.

[17] When nannoconids are overwhelming the assemblages, only large-sized nannoliths such as pentaliths,

Assipetra, and Rucinolithus are unequivocally detectableand quantifiable in thin sections. In fact, because nannoco-nids are large and thick, they tend to cover coccoliths thatare present. Therefore abundance of coccoliths is typicallyunderestimated in thin section of Lower Cretaceous lime-stones because they constitute a small fraction of the micritedominated by nannoconids [e.g., Erba, 1994]. Conversely,

nannoconids are underestimated in smear slides, essentiallyowing to mechanical breakage during powdering. In fact,their ultrastructure favors disintegration of single crystals[Noel and Melguen, 1978]. In order to have a more realisticestimate of coccolith distribution, although probably over-estimated, we calculated coccolith absolute abundances onthe basis of the proportion of single taxon versus nannoco-nids in smear slides and absolute abundance of nannoconidsin thin section as follows:

AAtaxon 1 %taxon1=% nannoconids AA nannoconids;

where

AAtaxon 1 absolute abundance of taxon 1;%taxon1 percentage of taxon 1 in smear slide;

%nannoconids percentage of nannoconids in smear slide;AAnannoconids absolute abundance of nannoconids in thin

section.

3. Results

[18] In the Tethys Ocean, Lower Cretaceous Maiolicalimestones mainly consist of calcareous nannofossils, withonly minor contribution by calpionellids and foraminifers.

Nannofloras are usually dominated by Watznaueria (espe-cially W. barnesae) and nannoconids that together can

represent up to 90% of assemblages. Abundance of nanno-conids in smear slide is typically underestimated owing tomechanical breakage of specimens during rock powdering.This become obvious when quantitative data obtained insmear slide are compared with abundance derived from thinsection and SEM analyses [Erba and Quadrio, 1987; Erba,1994]. Therefore dominance of W. barnesae in most sam-

ples from both the Polaveno section and the Cismon core isinterpreted as an artifact of sample preparation. The onlyother genera showing relative abundances higher than 5%are Diazomatolithus,Assipetra,Rucinolithus, and the penta-lith group (Micrantholithus and Braarudosphera).

[19] In both the Polaveno section and the Cismon Apti-core, absolute abundances of nannofossils show changes

that are only partly similar to those documented in relativeabundances (compare Figures 25). Although the nanno-floral composition and common taxa are the same, thinsection investigation clearly demonstrates the dominance ofnannoconids, which are artificially reduced during smearslide preparation. As previously suggested, the micrite ofMaiolica limestone can be regarded as a nannoconite[Erba, 1994].

[20] In both the Polaveno and Cismon sections, preserva-tion is moderate to poor but comparable in all samples. In

particular, thin section analysis shows that the type anddegree of diagenesis is similar through the studied intervals.

Table 1. Volume (mm3) and Mass (pg CaCO3) of Common Taxa in

the Early Cretaceousa

Volume, mm3 Mass, pg Species Ratio, Taxon/ N. Steinmannii

Oligotrophic Species1245.9 3363.9 N. steinmannii 1

8 30.2 2 24 1.4 N. globulus 1.55 46.5 1 79 4.0 N. bucheri 1.8

340.7 920 N. truittii 3.6

Uncertain Paleoecological Affinity323 872 A. infr. larsonii 3.8270 729 R. ter. youngii 4.6157 424 M. obtusus 8

87 234 P. embergeri 14.338 103 M. hoschulzii 32.835.4 96 A. infracretacea 35.224.3 66 R. terebrodentarius 51.321 57 W. barnesae 59.314 39 R. asper 89

9.3 25 Z. diplogrammus 1345.4 14.6 Z. elegans 230.7

Mesotrophic and Eutrophic Species5.1 13.77 D. lehmanii 244.3

4 10.8 D. rotatorius 3113.2 8.6 B. constans 3900.8 2.2 Z. erectus 1557

aAfter Tremolada and Young [2002]. The right-hand column representsthe ratio between a single specimen of each species and a single specimenof Nannoconus steinmannii. This ratio represents the number of specimensof individual species required to equal the calcite in one specimen of

N. steinmannii.


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Consequently, although the original micrite compositionwas certainly altered during burial and lithification, varia-tions in nannofossil absolute abundances cannot result fromdifferential dissolution and/or overgrowth of taxa withvariable sensitivity to diagenesis. This is certainly true forthe rock-forming nannoconids that are considered diagene-

sis resistant forms (see discussion in the work of Erba[1994]).

3.1. Valanginian-Hauterivian Interval at Polaveno

[21] A decrease in nannoconid relative abundance (from25 50% to 0 10%) and a coeval increase in abundance ofW. barnesae (from 5060% to >80%) correlate with mag-netic chron CM12 (Figure 2). The interval corresponding tomagnetic chrons CM12 through CM10 is characterized byvery low percentages of nannoconids and corresponds to the

previously documented nannoconid decline [Channell etal., 1993; Erba, 1994; Weissert et al., 1998; Bersezio et al.,

2 00 2 ]. I n t hi s i nt erv al t h e Diazomatolithus group( D. lehmanii and D. subbeticus) becomes common, with

percentages up to 14%. Assipetra infracretacea is abundantin the black shales deposited during the d13Ccarb positiveexcursion. As reported by Bersezio et al. [2002], the intervalimmediately preceding the isotopic excursion is also char-

acterized by an abundance peak of pentaliths (Figure 2). Inthis interval, percentages as high as 8% were quantified;

Micrantholithus hoschulzii is the dominant form, withminor contribution by Braarudosphaera regularis and

Micrantholithus obtusus.[22] The interval following the C isotopic excursion

(highestd13Ccarb values in magnetic chron CM11n) containsnannofossil assemblages with unchanged relative abun-dance ofW. barnesae, narrow- and wide-canal nannoconidsand virtually absent pentaliths. Only the Diazomatolithusgroup gradually decreases in relative abundance, afterreaching maximum percentages at the climax of the d13C

Figure 2. Percentages of most abundant nannofossils in the Polaveno section plotted against biomagnetostratigraphy [Channell et al., 1993, 1995b; Bersezio et al., 2002] and C isotope stratigraphy[ Lini et al., 1992; Lini, 1994]. The base of the nannoconid decline is based at the level where thedecrease in relative abundance of nannoconids correlates with a major increase in relative abundance ofW. barnesae.


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excursion and returning to pre-excursion values by magneticchron CM10 time (Figure 2).

[23] Thin section analyses revealed that through the upperBerriasian/lower Hauterivian, micrite consists of nannoco-nids dominated by the narrow-canal forms (Figure 3). In theupper Berriasian/lowermost Valanginian interval (magneticchrons CM16 through CM13), an average of 3500 speci-mens mm2 ofW. barnesae was calculated. In this interval,narrow- plus wide-canal nannoconids show absolute abun-

dances between 3500 and 4000 specimens mm2. In mag-netic chron CM12, a first decrease in nannoconid absoluteabundance (to approximately 2000 specimens mm2)is followed by a more severe decrease, characterized byvalues of 7001000 specimens mm2 in the intervalcorresponding to the upper part of magnetic chron CM12to the lower part of magnetic chron CM10N. The nanno-conid decrease in abundance, named the nannoconiddecline, is paralleled by a major increase of W. barnesaereaching values of 8000 specimens mm2.

[24] The onset of the nannoconid decline precedes thed13Ccarb excursion, and the lowest nannoconid abundances

correspond to the isotopic event. An increase in nannoconidabundance (average values of 1800 specimens/mm2) corre-lates with the upper part of CM10N and the end of theisotopic excursion (Figure 3). Within nannoconids the wide-canal ones show a minor increase in abundance in theinterval characterized by the d13Ccarb excursion and in theoverlying limestones.

[25] Two distinct abundance peaks of pentaliths areobserved in the uppermost Berriasian and the lower

Valanginian in the same intervals marked by highest per-centages. However, maxima in relative and absolute abun-dances do not coincide (compare Figures 2 and 3). As

previously reported by Bersezio et al. [2002], such pentalith peaks characterize lithozones with marly interbeds andblack shales.

[26] Absolute abundances of the Diazomatolithus groupmarkedly increase in the interval corresponding to magneticchrons CM12 to CM10N, with highest values during thed13Ccarb excursion. The symmetric increase and decrease arevery similar to those of percentages (Figure 2), but thinsection quantification revealed that the increase in absolute

Figure 3. Absolute abundances of most abundant nannofossils in the Polaveno section plotted against

biomagnetostratigraphy [Channell et al., 1993, 1995b; Bersezio et al., 2002] and C isotope stratigraphy[Lini et al., 1992; Lini, 1994]. Absolute abundances ofW. barnesae, Diazomatolithus spp., and pentalithswere calculated taking into account the proportion of single taxon versus abundance of nannoconids (seetext for details). Lithologic legend and nannoconid decline as in Figure 2.


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before OAE1a. Percentages up to 5% of pentaliths weredetected in two discrete intervals: one just below the SelliLevel and the other in the uppermost part of the of d13Ccarbexcursion (Figure 4).

[30] Thin section quantitative analyses showed that thenarrow-canal nannoconids dominate the micrite in the upperHauterivian/Barremian interval (magnetic chrons CM8 toCM1) with average values of 40006000 specimens mm2

(Figure 5). Absolute abundances of W. barnesae average

5000 specimens mm2

. Fluctuations in nannoconid absoluteabundance show higher amplitude than changes in relativeabundance. Their lowest values are observed in the intervalcorresponding to the Faraoni level [Cecca et al., 1996; Erbaand Larson, 1998; Erba et al., 1999] and in the black shalelayers in the upper part of magnetic chron CM3. Othernannoconid minima correlate with intervals of massivecherts in magnetic chron CM1 (at approximately 55 m)and black shales within magnetic chron CM1n (at approx-imately 42 m) (Figure 5): they are more pronounced than inthe distribution of relative abundance of narrow-canalnannoconids (Figure 4).

[31] A marked decrease in absolute abundance of narrow-canal nannoconids, from 7000 to 4000 specimens mm2,occurs below magnetic chron CM0 and is followed bya further decrease within magnetic chron CM0, wherethe wide-canal nannoconids become more numerous.These changes are coeval with sharp increases in absoluteabundance of W. barnesae to more than 10,000 specimensmm2 j u st b elo w m agn eti c ch ro n CM 0 an d m o rethan 15,000 specimens mm2 within magnetic chron

CM0.[32] The nannoconid crisis affects both the narrow- and

t he w i de- can al n ann o co ni d s, f o r w h ich a d r op t o250 specimens mm2 and 140 specimens mm2, respec-tively, was observed (Figure 5). Although the pentaliths

Assipetra and Rucinolithus are temporarily common, theirabsolute abundances are orders of magnitude lower thanthose of W. barnesae and nannoconids (Figure 5). Pentalith

peaks are visible in the upper Hauterivian, in the intervalbelow the Selli Level, and in the upper Aptian. Assipetraand Rucinolithus display highest absolute abundances in theOAE1a interval and in the overlying limestones, reaching

Figure 5. Absolute abundances of most abundant nannofossils in the Cismon core plotted against bio-

magneto-chemostratigraphy [ Erba et al., 1999; Channell et al., 2000]. Absolute abundances ofW. barnesae, Assipetra, Rucinolithus, and pentaliths were calculated taking into account the proportion ofsingle taxon versus abundance of nannoconids (see text for details). Lithologic legend as in Figure 4.


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values as high as 1000 specimens mm2

and an averageabundance of 500 specimens mm2.

3.3. Nannofossil-Calcite Paleofluxes

[33] In the Valanginian-Hauterivian and Barremian-Aptian, nannofossil calcite fluxes are largely determined bynannoconids, while the contribution of W. barnesae tocarbonates is minor in terms of mass. Similarly, the othercommon to abundant taxa are negligible in nannofossilfluxes (Figures 6 and 7). Paleofluxes (expressed as gnannofossilCaCO3 10

6 mm2 year1), in fact, are controlled by absoluteabundances (number of nannofossils mm2 year1) ofvarious taxa and their volumes/mass (gCaCO3 10

9). Nanno-liths of the narrow-canal N. steinmannii steinmannii are,

by far, the forms with the highest volume/mass (Table 1) aswell as the most abundant nannofossils, and consequentlytheir paleofluxes are 520 times higher than those of anyother taxa in the Valanginian/lower Hauterivian interval(Figure 6). Even when nannoconid paleofluxes reach thelowest values during the Valanginian d13Ccarb excursion, theyare 5 times greater than those of dominant W. barnesae. Asimilar difference in magnitude between paleofluxes ofindividual species was detected in the Hauterivian-Aptianinterval of the Cismon core. Here the maximum values ofW. barnesae paleofluxes are only 1/5 of the lowest nanno-conid paleofluxes during the nannoconid crisis. Similar

proportions ofAssipetra and Rucinolithus versus nannoco-nids are detected even in the Selli interval, where they reachthe highest abundances (Figure 7).

[34] In the lower Valanginian, total fluxes of nannofossilsvary between 22 and 17 g 106 mm2 year1, with anaverage value of 20 g 106 mm2 year1 (Figure 8). A firstdecrease in paleofluxes to an average of 15 g 106 mm2

year1 correlates with magnetic chron CM12, and a morepronounced one (from 15 to 7 g 106 mm2 year1) occursin the uppermost part of magnetic chron CM12. The intervalcorresponding to magnetic chrons CM12 through CM10Nis characterized by constantly low fluxes of 7 g 106 mm2

year1 on average, reaching the minimum values of3 g 1 06 mm2 year1 at the climax of the C isotopic

excursion. Nannofossil fluxes increase to 9 g 106 mm2year1 in magnetic chron CM10N and then return to 15 g106 mm2 year1 in the upper part of magnetic chronCM10N and 20 g 106 mm2 year1 in magnetic chronCM10, respectively.

[35] At Cismon (Figure 9), nannofossil paleofluxes arerelatively low (310 g 106 mm2 year1) in the upperHauterivian, represented by condensed limestones. In theBarremian, paleofluxes are higher (average of 15 g 106

mm2 year1) and display a gradual increasing trend withmaximum values in the upper Barremian. Intervals withmassive cherts and/or Corg-rich black shales correlate

Figure 6. Nannofossil CaCO3 paleofluxes (g 106 mm2 year1) of most abundant taxa in the

Polaveno section. Lithologic legend and nannoconid decline as in Figure 2.


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with minima in nannofossil paleofluxes (close to 5 g 106

mm2 year1). The interval corresponding to the uppermost

part of magnetic chron CM1n is characterized by thehighest nannofossil paleofluxes, with values between 23and 28 g 106 mm2 year1 (Figure 9). In the lower Aptiana stepwise decrease in paleofluxes is marked by a firstchange from average values of 2518 g 106 mm2 year1,then within magnetic chron CM0 a further decrease toapproximately 10 g 106 mm2 year1 is recorded, fol-lowed by another drop to 5 g 106 mm2 year1. Thenannoconid crisis interval is characterized by paleofluxes of2 g 106 mm2 year1 on average; the minimum value of1 g 106 mm2 year1 correlates with the negative spike inthe C isotopic curve at the base of the Selli Level (Figure 9).

Values oscillate between 3 and 8 g 106 mm2 year1 in theterminal part of the C isotopic anomaly of early late Aptian

age (Figure 9).[36] A large reduction in nannofossil calcite fluxes of

approximately 65% (three steps of 25, 40, and 22%,respectively) correlates with onset and extent of the Val-anginian d13Ccarb excursion. After the perturbation, nanno-fossil paleofluxes record a 65% increase (again in threesteps of +22, +40, and +25%, respectively) reaching pre-Cisotopic excursion values (Figure 10).

[37] In the Barremian-Aptian interval a first 28% decreasein paleofluxes occurs just below the base of magnetic chronCM0, then during magnetic chron CM0 a two-step (44.5and 50%, respectively) reduction of 72% is recorded, and

Figure 7. Nannofossil CaCO3 paleofluxes (g 106 mm2 year1) of most abundant taxa in the Cismon

core. Lithologic legend as in Figure 4.


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a further 60% reduction culminates in the nannoconid crisis preceding the Selli Level black shales. A total decrease ofapproximately 90% in nannofossil paleofluxes occurred in a

1.5 myr long interval, at the onset of the early Aptian Cisotopic anomaly and OAE1a (Figure 10). Above the SelliLevel, nannofossil paleofluxes recover to average values of5 g 1 06 mm2 year1, corresponding to an increase ofapproximately 60%.

4. Discussion

[38] The Cretaceous was a time of exceptional warmthwith global deposition of organic carbon-rich sediments[Schlanger and Jenkyns, 1976; Arthur et al., 1985, 1987,1990; Sliter, 1989; Bralower et al., 1993, 1994], carbon and

strontium isotope excursions [Weissert and Lini, 1991; Bralower et al., 1997; Weissert et al., 1998; Jones andJenkyns, 2001], and major biotic changes in planktonic

communities [Tappan and Loeblich, 1973; Roth, 1987;Coccioni et al., 1992; Erbacher et al., 1996; Leckie et al.,2002]. Both the late early Aptian OAE1a and the Valangi-nian event represent times of carbonate crises in pelagic andneritic environments, enhanced productivity, and oceanicdysoxia/anoxia [Channell et al., 1993; Erba, 1994; Weissertet al., 1998].

[39] Quantitative studies of nannofossil micrite in thewell-dated Polaveno and Cismon sections reveal majorchanges in: (1) abundance of total nannofloras; (2) relativeand absolute abundances of single taxa with very differentultrastructure and mass/volume; and (3) nannofossil paleo-

Figure 8. Total nannofossil CaCO3 paleofluxes (g 106 mm2 year1) in the Valanginian interval of the

Polaveno section. Lithologic legend and nannoconid decline as in Figure 2.


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Figure 9. Total nannofossil CaCO3 paleofluxes (g 106 mm2 year1) in the uppermost Hauterivian/

upper Aptian interval of the Cismon core. Lithologic legend as in Figure 4.


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fluxes. Our results suggest that variations in relative abun-dances are only partially similar to changes in absoluteabundances and can give a quite distorted picture of actualincreases and decreases through time.

[40] Because calcareous nannoflora acts both as a biolog-

ical pump (photosynthesis) and a carbonate pump (biomi-neralization), coccolithophore blooms and crises affect theorganic and inorganic carbon cycles in addition to absorp-tion of atmospheric CO2 into the oceans. However, the totalnumber of nannofossils alone is not a measure of primary

productivity and/or carbonate production. Other parameters,such as absolute abundance, ultrastructure and mass/volumeof coccoliths/nannoliths produced by individual speciesshould be taken into account to decipher paleoceanographicchanges in temperature, nutrient content, light penetrationand stability of surface waters. In fact, research on livingnannoplankton indicates that coccolith/nannolith type,

abundance, and degree of biomineralization depend onchemico-physical-trophic conditions, as well as the gasexchange between surface seawaters and the atmosphere.

[41] At Polaveno and Cismon the documented changes innannofossil abundance and composition as well as in pale-

ofluxes can be interpreted as the response of calcareousnannoplankton to global changes in the ocean-atmospheresystem. Increased rates of volcanism during the formation ofOntong Java and Manihiki Plateaus and the Parana-EtendekaLIP are proposed to have caused the geological responsesassociated with OAE1a and the Valanginian event, respec-tively. High levels of volcanogenic CO2 in the atmosphere,most probably turned the climate into a greenhouse state,accelerated continental weathering and increased nutrientcontent in oceanic surface waters via river runoff [Weissert,1989; Erba, 1994; Jenkyns, 1999; Larson and Erba, 1999].Moreover, higher fertility might have been triggered directly

Figure 10. Synthesis of total nannofossil paleofluxes (g 106 mm2 year1) during the Valanginian andearly Aptian. Major decreases in biocalcification are interpreted as the response of calcareous

phytoplankton to excess CO2 during emplacement of the Parana-Etendeka and Ontog Java Plateau (OJP)LIPs. Timescale after Channell et al. [1995b]; d13Ccarb curve after Weissert et al. [1998] and Erba et al.[1999]; LIP radiometric ages after Renne et al. [2001] and Duncan [2002]; trace metal data after R. A.Duncan (personal communication, 2002).


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by biolimiting metals related to hydrothermal venting during plateau formation [Sinton and Duncan, 1997; Larson andErba, 1999; Leckie et al., 2002].

[42] Calcareous nannofloras reacted to these new condi-tions of higher pCO2 and nutrient content in surface waters

by drastically reducing calcification. The decrease in nan-noconid abundance and the shift from narrow- to wide-canal

forms are interpreted as a consequence of a shallow nutri-cline and excess CO2. Like in the modern oceans, increaseof nutrients in the upper photic zone would induce bloomsof nannoplankton producing small placoliths and inhibit thedeep-photic zone nannoconids [Erba, 1994].

4.1. Trophic Conditions

[43] Studies on functional morphology of extant calcare-ous nannoplankton suggest that coccolithophores (andconsequently their specific coccoliths/nannoliths) are geo-graphically distributed and fluctuate in abundance accordingto biotic and abiotic ecological factors. Most important aretrophic conditions: in waters with relatively high nutrientcontents (upwelling or coastal nutrification), small placoliths

are dominant and coccolithophores inhabiting the lowerphotic zone are virtually absent [Young, 1994]. AbundancesofFlorisphaera profunda and other taxa of the lower photiczone, relative to abundance of coccolithophores of the upper

photic zone, have been quantified in various oceanographicsettings from the Pacific, Atlantic, and Indian Oceans. Low

percentages of F. profunda indicate a shallow nutriclinefavoring coccolithophores inhabiting the upper photic zone[ Molfino and McIntyre, 1990; Okada and Matsuoka, 1996;

Beaufort et al., 1997; Hagino et al., 2000; Takahashi andOkada, 2000; Kinkel et al., 2000; Broerse et al., 2000a,2000b]. Nannoplankton producing heavily calcified cocco-liths are typical of oligotrophic stable surface waters, wherethe deep photic zone assemblage thrives close to the ther-

mocline. The so-called mixed group are common every-where and do not show specific environmental adaptations[Young, 1994]. The quantity of calcite produced by cocco-lithophores therefore seems inversely correlated with trophiclevels. Even if abundance of cells and coccoliths reachesenormous values during blooms, the small size and reducedvolume/mass of fertility-related placoliths do not necessarilyaffect biogenic calcite fluxes.

[44] For the Early Cretaceous, paleobiogeographic and paleoceanographic reconstructions allowed identification ofnannofossil indices with affinities for oligotrophic andmesotrophic conditions [Roth, 1981; Roth and Bowdler,1981; Roth and Krumbach, 1986; Erba, 1986, 1992a,1992b, 1994; Premoli Silva et al., 1989; Watkins, 1989;

Erba et al., 1992; Williams and Bralower, 1995; Herrle,2002]. It is clear that higher fertility-related nannofossils aresmall and contain far less calcite than the oligotrophic forms(Table 1). As a consequence, Cretaceous episodes/areas ofenhanced primary productivity are invariably characterized

by very low carbonate content, large quantities of organicmatter, and increased biogenic silica. This is the case forOAEs, paleoequatorial upwelling zones, and mesotrophic toeutrophic coastal areas. Detailed studies of diagenesis andnannofossil preservation demonstrated that these reductionsin carbonate content are not the result of dissolution [Roth

and Krumbach, 1986; Erba, 1992b, 1994; Bralower et al.,1993, 1994; Premoli Silva et al., 1989, 1999].

[45] Morphometric analyses conducted on common EarlyCretaceous nannofossil taxa [ Tremolada and Young,2002] indicate that mass/volumes of fertility-related taxa(Zeughrabdotus erectus, Biscutum constans, Discorhabdusrotatorius and Diazomatolithus lehmanii) are very small

and that their contribution to calcite in pelagic carbonates isorders of magnitude lower than those of medium- to large-sized coccoliths/nannoliths of the oligotrophic forms (nan-noconids and W. barnesae) (Table 1). Therefore an increasein abundance of the fertility-related coccoliths equal to 102103 is required to produce the same quantity of calcitecontained in one nannofossil of the oligotrophic forms.

[46] The change in composition of nannofossil assemb-lages and carbonate crises documented for both theValanginian and the early Aptian events can be explainedas a nannoplankton response to global nutrification epi-sodes, directly or indirectly linked to major igneous/tectonic events [Channell et al., 1993; Erba, 1994;

Larson and Erba, 1999; Leckie et al., 2002]. In both

cases, global change in nannofossil-carbonate abundancecorrelates with an increase in deposition of biogenic silicaand Corg-rich black shales and precedes the C isotopicexcursions, suggesting that planktonic communitiesreacted to the early changes in trophic and climaticconditions and then persisted during the perturbation. Ashift to mesotrophic/eutrophic conditions is further sug-gested by changes in radiolarian and planktonic forami-niferal assemblages [Coccioni et al., 1992; Erbacher etal., 1996; Premoli Silva et al., 1999; Leckie et al., 2002;

Erba et al., 2004]. Higher nutrient contents might beintroduced in surface waters by accelerated continentalweathering and runoff under greenhouse conditions[Weissert, 1989; Lini et al., 1992; Channell et al.,1993; Erba, 1994; Weissert et al., 1998; Jenkyns, 1999;

Larson and Erba, 1999; Premoli Silva et al., 1999; Bellanca et al., 2002; Bersezio et al., 2002] and or (volcanogenic) upwelling [Vogt, 1989; Arthur et al.,1990; Bralower et al., 1994, 1999; Premoli Silva et al.,1999]. Moreover, hydrothermal megaplumes related toformation of oceanic plateaus are potentially responsiblefor rapid introduction of enormous concentrations ofdissolved and particulate biolimiting metals into theoceans [Sinton and Duncan, 1997; Larson and Erba,1999; Snow and Duncan, 2002; Erba and Duncan,2002; Leckie et al., 2002].

4.2. Atmospheric CO2

[47] Although the link between photosynthesis and calci-fication in coccolithophores has long been known, mecha-nisms involved are not fully understood. The relationship is

probably based on the energetic needs of calcification. Lightand photosynthesis facilitate coccolith production by pro-viding adenosine triphosphate (ATP) as energy source forion transport and synthesis of organic matrix. However,experimental results suggest that calcification can take placein absence of light, and photosynthesis is not required ifCO2 diffuses sufficiently rapidly from the site of calcitedeposition [Simkiss and Wilbur, 1989].


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[48] The effects of increased atmospheric CO2 have beentested on extant Emiliania huxleyi and Gephyrocapsaoceanica, both in laboratory cultures and on incubationsof natural nannoplankton assemblages from the NorthPacific [ Riebesell et al., 2000]. Nannoplankton calciumcarbonate interacts with marine carbon cycling and ocean-atmosphere CO2 exchange. According to Riebesell et al.

[2000], increased CO2 concentrations result in decreasedcalcification and lower ratio of calcification to particulateorganic carbon (POC) production (calcite/POC). Undertriple preindustrial CO2 levels, decreases of 15.7 and44.7% in rate of calcification and decreases of 21 and52.5% in calcite/POC ratio were recorded. Such changesare extremely important in marine ecosystems dominated bycalcareous nannoplankton.

[49] Increases in atmospheric CO2 levels would/couldlessen coccolith/nannolith production because coccolithsecretion might represent a strategy to produce, directlywithin the cell, the waste-product CO2 reducing the energycost of photosynthesis [Paasche, 1962; Young, 1994].Therefore excess CO2 would make calcification less indis-

pensable to coccolithophore life because surface waters arealready (over) saturated with carbon dioxide.

[50] We speculate that during the Early Cretaceous, highlycalcified coccoliths/nannoliths were secreted when atmo-spheric CO2 was low in order to sustain photosynthesis incalcareous nannoplankton. Conversely, during times ofvolcanogenic emissions of CO2, biocalcification was ham-

pered while organic matter production was emphasized. Ifthis interpretation is correct, then we can use changes innannofossil paleofluxes to estimate atmospheric CO2increases and decreases by analogy with experiments con-ducted on extant coccolithophores [ Riebesell et al., 2000;

Zondervan et al., 2001].[51 ] T he Valang in ian event i s m ar ked b y a 6 5%

reduction in nannofossil paleofluxes that would corre-spond to a 23 times increase in CO 2 during formationof the Parana-Etendeka LIP (Figure 10). High carbondioxide content in the atmosphere-ocean system was

balanced back to pre-event values after 2 million years.Our data also suggest that blooms of r-selected (calcar-eous) phytoplankton were able to absorb excess CO2 byreducing calcification and enhancing production of organicmatter.

[52] A much more drastic increase in CO2 must have been produced by emplacement of the giant Ontong Java andManihiki Plateaus and formation of the Nova Canton troughsystem. In the lowermost Aptian a 90% reduction innannofossil paleofluxes occurred in a 1.5 myr long intervalleading into OAE1a (Figure 10). In this case a 36 timesincrease in volcanogenic CO2 is estimated. The return ofnannoconids above the Selli Level only partially counter-

balanced (increase of approximately +60% in nannofossil paleofluxes) the drop in biocalcification of the 1.25 myr-long nannoconid crisis interval. The relatively low nanno-fossil paleofluxes during the late Aptian is not surprisingsince atmospheric CO2 most probably remained high as aresult of emplacement of the Kerguelen LIP [Duncan, 2002;

Erba, 2002] and accelerated ocean crust production at mid-ocean ridges [Larson, 1991a, 1991b]. Our data might also

be indicative of inability of phytoplankton to absorb excessCO2 above threshold values.

[53] If increases of atmospheric CO2 were the cause ofreduced rates in nannoplankton biocalcification, then theabundance peaks of Assipetra and Rucinolithus duringOAE1a are puzzling. Normal- and large-sized morphotypesof Assipetra and Rucinolithus [Tremolada and Erba, 2002]

are in fact quite big and heavily calcified (Table 1). Theirvolume/mass and ultrastructure are also totally differentfrom those of the generally accepted nannofossil indicesof higher fertility. An alternative explanation might be that

Assipetra and Rucinolithus are not fossil remains of cocco-lithophores, as further suggested by lacking documentationof their coccospheres/xenospheres. These peculiar nanno-liths might represent CaCO3 precipitates and/or biocalcifi-cation by bacteria under extreme paleoenvironmentalconditions, including massive methane release into theoceans [Opdyke et al., 1999, submitted manuscript, 2003;Tremolada and Erba, 2002; Bellanca et al., 2002; Beerlinget al., 2002].

4.3. Anoxia-Dysoxia[54] The late Valanginian event and early Aptian OAE1a

are marked by pronounced positive carbon isotopic excur-sions, typically 2% higher than background levels (seeWeissert et al. [1998] for a synthesis) recorded at a globalscale. The OAE1a was also a time of widespread anoxia/dysoxia documented by burial of organic carbon at low andhigh latitudes and in all oceans. Sedimentological evidence(Corg-rich black shales) for an OAE in the Valanginian islimited. However, recent recovery of organic carbonenriched sediments of Valanginian age from the ShatskyRise in the North Pacific Ocean [ Bralower et al., 2002]suggests that also this time interval was characterized byglobal anoxia/dysoxia [Erba et al., 2004].

[55] Recently, Leckie et al. [2002] discussed planktonevolution in the mid-Cretaceous trying to unravel the bioticresponse of planktonic communities to enhanced primary

productivity associated with OAEs. Accelerated evolutionaryrates in calcareous nannoplankton, planktonic foraminifera,and radiolaria are interpreted as the result of higher fertilityand global warming triggered by submarine volcanism.

[56] When high-resolution stratigraphy is available,anoxic/dysoxic conditions during OAEs clearly postdatethe biotic response. This is certainly the case for the Valan-ginian and early Aptian since the nannoconid crises precedeOAEs by some thousands years. Similarly, the documenteddrops in nannofossil paleofluxes anticipate the C isotopicanomalies and associated black shales. Therefore anoxia per

se did not affect nannofloral abundance and composition, butconversely, the shift in (phyto) plankton dominance con-trolled the abundance and type of biogenic carbonate aswell as organic matter produced in surface waters andsubsequently incorporated in the geological record.

5. Conclusions

[57] Relative and absolute abundances of calcareousnannofossils are suggestive of paleoenvironmental globalchanges. Despite the close-sum problem, percentages of


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individual taxa can be used to trace major paleocean-ographic modifications. However, absolute abundances aremuch more reliable and can be used for calculations ofnannofossil paleofluxes, when high-resolution (integrated)stratigraphy is available. Our study pointed out that:

[58] 1. Morphometric analyses allow quantification ofcalcite contained in single coccoliths/nannoliths of individ-

ual species and estimates of nannofossil paleofluxes whenabsolute abundances are available.

[59] 2. CaCO3 per se is not a reliable measure of biogeniccarbonate production, especially under oligotrophic condi-tions inducing blooms of k-selected highly calcified cocco-liths/nannoliths.

[60] 3. Fluctuations in pelagic biogenic carbonates can beused to reconstruct paleofertility and paleoCO2 contents insurface waters.

[61] We interpret the nannoconid decline (Valanginian)and crisis (early Aptian) as the results of combined higherfertility and higher atmospheric CO2, both favoring small-sized coccoliths/nannoliths and, in general, r-selected

phytoplankton. The Early Cretaceous biologic and carbon-ate pump could counterbalance the nutrification event andatmospheric CO2 increase at the onset of and during theValaginian episode but only partially mitigated the muchmore severe conditions of the Aptian OAE1a.

[62] Additional nannofossil paleofluxes on well-datedsuccessions, in combination with other proxies for paleo-

CO2, will improve modeling of the paleobiological andpaleocarbonate pump. Detailed reconstruction of nannofos-sil paleofluxes might also allow the identification of thresh-old values of pCO2 in the past, enabling more realistic

predictions of timing and type of environmental modifica-tions induced by future global change.

[63] Acknowledgments. We are very grateful to Helmi Weissert, BobDuncan, Hugh Jenkyns, Jim Channell, Isabella Premoli Silva, and RogerLarson for interesting discussions. The manuscript benefited from thereview by Mark Leckie, an anonymous reviewer, and Lisa Sloan: theirconstructive criticism and valuable suggestions were very helpful. Thisresearch was supported by COFIN 2001 to I. Premoli Silva.

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E. Erba and F. Tremolada, Dipartimento diScienze Della Terra A. Desio, via Mangiagalli

34, I-20133 Milan, Italy. ([email protected])


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