the paleocene–eocene thermal maximum as recorded by tethyan planktonic foraminifera in the forada...

64 (2007) 189–214www.elsevier.com/locate/marmicro

Marine Micropaleontology

The Paleocene–Eocene Thermal Maximum as recorded by Tethyanplanktonic foraminifera in the Forada section (northern Italy)

Valeria Luciani a,⁎, Luca Giusberti b, Claudia Agnini b, Jan Backman c,Eliana Fornaciari b, Domenico Rio b,d

a Dipartimento di Scienze della Terra, Polo Scientifico Tecnologico, University of Ferrara, Via G. Saragat 1, I-44100 Ferrara, Italyb Department of Geosciences, Via Giotto 1, University of Padova, Via Giotto1, I-35137 Padova, Italyc Department of Geology and Geochemistry, Stockholm University, SE-106 91 Stockholm, Sweden

d Institute of Geosciences and Earth Resources, CNR-Padova c/o Department of Geosciences, Padova University,Via Giotto 1, I-35137 Padova, Italy

Received 7 February 2007; received in revised form 26 April 2007; accepted 8 May 2007

Abstract

The Forada section in the Venetian Pre-Alps of northern Italy represents an expanded record of the Paleocene–Eocene ThermalMaximum (PETM) at a depositional paleodepth of about 1 km±0.5 km. High-resolution planktonic foraminiferal analysis of thissection, in a time interval of approximately 1.3 Myr across the Paleocene/Eocene boundary, reveals striking faunal changes thatallow the identification of eight phases (a–h). The late Paleocene was represented by stable, warm and oligotrophic surface waterconditions (phase a). Unstable environmental conditions start well before the onset of PETM (ca. 150 kyr, phase b) and involved achange towards eutrophy, as marked by the increase of Subbotina and the concomitant decrease of Morozovella. This step is alsocharacterized by enhanced fragmentation and dissolution.

The interval corresponding to the main body of the carbon isotope excursion (CIE) is characterized by a marked increase ofAcarinina, though with some differences in the species composition and relative abundance, both in high-and low-latitudes,particularly in the Tethyan area. Forada is no exception to this pattern. However, at Forada, two prominent peaks in abundance ofacarininids are recorded ca. 30 kyr prior to the onset of the CIE, thus suggesting an increase in temperature heralding the onset ofthe PETM (phase c). Interestingly, the lower peak in abundance of Acarinina just precedes the 1‰ carbon isotope negative shiftoccurring below the onset of the main CIE. The basalmost Eocene, corresponding to the lower part of CIE curve, is represented byintense planktonic foraminiferal dissolution, implying an extraordinary rise of the CCD. This interval has an estimated duration ofabout 16 kyr (phase d).

The dominance of acarininids in the lower part of the CIE (phase e, f; ca. 14 and 22.5 kyr) is interpreted as a consequence of theextreme warmth coupled with eutrophic conditions characterizing the Forada depositional environment at that time. Theseacarininids include at Forada also the temporally constrained Acarinina sibaiyaensis and A. africana. The morphological similaritybetween these peculiar species with the radially elongated chambered forms characterizing the Cretaceous anoxic events, suggeststhe hypothesis that depletion of oxygen in the upper water column might have been one of the factors causing their conspicuousoccurrence at the PETM.

The recovery in abundance of the specialized morozovellids and of other planktonic foraminiferal groups (e.g., biserials,globanomalinids, igorinids, planorotalids and pseudohastigerinids), occurring in the middle part of the CIE (ca. 30 kyr after theonset of the PETM), indicates an initial environmental recovery (phase g). A new stable state is definitely reached in the upper part

⁎ Corresponding author. Tel.: +39 532 974737; fax: +39 532 974767.E-mail address: [email protected] (V. Luciani).

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190 V. Luciani et al. / Marine Micropaleontology 64 (2007) 189–214

of the Forada section where the relative proportions of the main component of planktonic foraminiferal assemblages move towardsvalues similar to those of the late Paleocene conditions (phase h). However, the perturbation during the PETM produced significantchanges in the ocean geochemistry that endured after the PETM event, as testified by the prominent high carbonate dissolutioncharacterizing the marly levels, and the large variability in relative abundance among different components of the planktonicforaminiferal assemblages. These striking oscillations were not present in the latest Paleocene.© 2007 Elsevier B.V. All rights reserved.

Keywords: Planktonic foraminifera; Paleocene–Eocene Thermal Maximum; paleoecology; biostratigraphy; Tethys; Venetian Pre-Alps

1. Introduction

A continuous marine sedimentary section acrossthe Paleocene/Eocene boundary interval is preserved

Fig. 1. Location and paleogeographical context of the Forada section. (A) Simand Bosellini, 1987). (B) The main Late Cretaceous–Early Paleogene paleoge(C) The Piave River Valley in the Belluno Province. The asterisks indicate th

at Forada, near Belluno, in the Venetian Pre-Alps ofnorthern Italy (Fig. 1). The Forada section, spectacu-larly exposed, contains a high-quality and expandedrecord of the so-called Paleocene Eocene Thermal

plified geological scheme of the Southern Alps (adapted from Doglioniographic elements of the Southern Alps (adapted from Cati et al., 1989).e location of the Forada section (modified from Giusberti et al., 2007).

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Maximum (PETM; Zachos et al., 1993). This episodeof extreme warmth, occurred at about 55 Ma, hasrecently attracted large consideration by the scientificcommunity as recording one of the most dramatic andsudden global temperature increase of the entire Ceno-zoic. The warming of the today's climate, caused byintense anthropogenic emission of CO2 and its poten-tial consequences for the biosphere, led to explore thepast greenhouse events in ever increasing detail.Across the PETM, temperatures rose by 4–5 °C intropical surface waters as well as in the deep ocean(Zachos et al., 2005), and by 6–8 °C in higher latitudes(Thomas and Shackleton, 1996; Thomas et al., 2002).This warming was superimposed as a sharp peak eventon the more gradual long-term warming of the earlyPaleogene (Zachos et al., 2001). The transition to thisevent has been estimated to have occurred within a fewthousand years, the source and trigger of which stillremains unknown although several hypotheses arecurrently debated (e.g., Dickens et al., 1995; Kentet al., 2003; Svensen et al., 2004; Cramer and Kent,2005; Lourens et al., 2005; Tripati and Elderfield,2005; Higgins and Schrag, 2006).

The PETM is globally recognizable in both terrestrialand marine setting by the about 2–3‰ negative carbonisotope excursion (CIE) (e.g., Kennett and Stott, 1991;Zachos et al., 1993, 2001, 2003; Dickens et al., 1997).The CIE event is characterized by a massive, rapid inputof light carbon to the ocean–atmosphere system, as wellas a major acidification event in the oceans resulting in arapid shallowing on the order of several kilometers ofthe calcite compensation depth (CCD) (e.g. Zachoset al., 2005). The duration of the CIE, including the so-called recovery interval, which refers to a return ofcarbon stable isotopes to a new steady-state, is on theorder of 170–230 kyrs (Röhl et al., 2000; Giusberti et al.,2007; Sluijs et al., in press). The 2–3‰ negative δ13Cshift in both marine and continental environments at thevery base of the CIE is used to define the base of theEocene Series in the Dababiya Global StandardStratotype Section and Point (GSSP) in Egypt (Aubryet al., 2002; Dupuis et al., 2003; Ouda and Aubry, 2003).

Among the biotic modifications that typify the PETMevent there are the radiation and rapid spreadingamong non-marine mammals (Gingerich, 2001, 2003),the largest extinction in the past 90 Ma of deep-waterbenthonic foraminifera (benthonic extinction event,BEE) (Tjalsma and Lohmann, 1983; Speijer et al.,1996; Thomas, 1998), a transient proliferation of severalshort-lived ephemeral plankton groups, such as theplanktonic foraminifera excursion taxa (Kelly et al.,1996, 1998; Kelly, 2002), the calcareous nannofossil

excursion taxa (Aubry et al., 2002; Agnini et al., 2007)and the poleward migration of the subtropical dinofla-gellate Apectodinium (Bujak and Brinkhuis, 1998;Crouch et al., 2001, 2003; Sluijs et al., in press).

Although a relatively high data set has been generatedfrom the analysis of several successions, the true causalmechanisms leading to PETM have not been definitelyestablished and several aspects of this crucial event arestill a matter of intense scientific debate. High-resolutionanalyses of the marine plankton, extremely sensitive toenvironmental modifications, may improve the compre-hension of this episode of extraordinary warmth.

The PETM interval in the Forada section, deposited inabout 1 km±0.5 km paleo-water depth is characterizedby a continuous and expanded carbonate record, anda cyclostratigraphy inferred from precessional cyclicity(Giusberti et al., 2007). Probably because of therelatively shallow depositional depth above the CCD,dissolution was less severe and planktonic foraminiferaare present for most of the entire thickness of the CIE(ca. 4.8 m thick). Only the lowermost 50 cm of the CIEare virtually barren of these microfossils.

The Forada section is thus well suited to explore theresponse of planktonic foraminifera to the environmentalperturbations occurring during a major portion of thePETM. Documenting changes among planktonic fora-miniferal assemblages from the central western Tethyswill improve our understanding of how the pelagic eco-system responded to a brief episode of extreme warmth,with subtropical temperatures at the North Pole, at about55 million years ago (Tripati and Elderfield, 2005; Sluijset al., 2006). By investigating the planktonic foraminif-era assemblages from the Forada section, this paper isaimed (1) to establish a highly resolved biostratigraphyand biochronology, (2) to infer the paleoenviromentalconditions and changes, in a ca. 1.3 myr interval acrossthe PETM, on the basis of changes in composition andabundance and (3) to discuss the paleoecological mean-ing of planktonic foraminifera that so uniquely char-acterize the PETM, through its excursion taxa, usingavailable environmental information on the Foradapaleoceanographic setting during the PETM.

2. Setting, stratigraphy and lithology

The Forada section is located in the Venetian Pre-Alps of NE Italy. The Venetian Pre-Alps represent asector of the Southern Alps, a major structural elementof the Alpine Chain, interpreted as a south vergingthrust-and-fold belt (Channell et al., 1979; Doglioni andBosellini, 1987; Fig. 1A). This area was less severelyaffected by tectonic deformation than elsewhere in the


Alps and Apennines (Channell and Medizza, 1981),making the Pre-Alps suited for studies of the lowerPaleogene pelagic record as exposed in well-preservedon-land sections.

From a palaeogeographic point of view, the Foradasediments were deposited in the NE–SW orientedBelluno Basin, a unit bordered to the west by the shal-low sediments of the Lessini Shelf (Bosellini, 1989) orby the relatively deep deposits of the Trento Plateau(Winterer and Bosellini, 1981) and to the southeastby shallow areas of the Friuli Platform (Bernoulli andJenkyns, 1974; Bernoulli et al., 1979; Winterer andBosellini, 1981) (Fig. 1B).

The Forada section is exposed along the ForadaCreek, roughly 2 km east of the Lentiai village (Fig. 1C),and consists of ca. 62 m of pink-reddish limestones andmarly limestones, locally rhythmically organized, re-ferred to the Scaglia Rossa formation. It encompasses theinterval from the Upper Cretaceous to the lower Eocene(Agnini et al., 2005; Fornaciari et al., in press), outcropscontinuously, and is virtually unaffected by structuralcomplications.

The local late Paleocene–early Eocene succession ofindurate marls and limestones is interrupted by the claymarl unit (CMU), a striking feature in the Veneto regionthat marks the PETM and correlates with similarlithological anomalies observed worldwide (e.g.,Moore et al., 1984; Norris et al., 1998; Baceta et al.,2000; Schmitz et al., 2001; Bralower et al., 2002; Lyleet al., 2002; Hancock et al., 2003; Zachos et al., 2004,2005). The 3.4 m thick CMU of Forada correspondsexactly with the main excursion of the CIE and its basecoincides with the BEE. Several properties of the CMU(δ13C, radiolarians, carbonate and hematite content)oscillate in fashions that have a cyclical character sug-gesting that the main excursion of the CIE spans fivecomplete precession cycles. The overlying recovery in-terval of the CIE is composed of six distinct marly–limestone couplets, representing six precessional cycles.These eleven cycles, that allowed estimating a totalduration of the CIE of ca. 230 kyr (Giusberti et al., 2007),are reported in Figs. 2–6 of this paper. Detailed data onstable isotopes (C, O), element concentration andmineralogy of the Forada PETM are given in Giusbertiet al. (2007), whereas investigations on calcareous nan-nofossils are reported in Agnini et al. (2007).

3. Material and methods

Analysis of planktonic foraminifera has been carriedout on 102 samples from a 17 m thick interval straddlingthe PETM. A sampling interval of 2–5 cm is used across

the PETM; 25–50 cm sample intervals are used for theportions of the section below and above the PETM.

Foraminifera were extracted from most of theindurate marls and limestones using the “cold acetolyse”technique of Lirer (2000). According to this method, 50–100 grams of dry sediment were crushed into smallfragments of about 5 mm in diameter. These pieces werecovered with ethanoic acid, highly concentrated aceticacid, ca. 80%, until the rock assumed a characteristicmousse appearance. The samples were subsequentlywashed and sieved using a 63 μm mesh size. In mostcases gentle ultrasonic treatment of the residues in pureNeoDesogen, a surface tension-active chemical, wasused in order to improve the cleaning of the tests. The“cold acetolyse” method has been recently applied todisaggregate strongly lithified samples (e.g., Coccioniet al., 2004a; Fornaciari et al., in press). Foraminiferaextracted using this method are normally well preservedwith genera and species well represented. However,some reservation might exist on the possibility that partof the assemblages could have been removed by dis-solution. To test the reliability of the “cold acetolyse”method we have prepared a number of samples usingboth this as well as standard methods. Results show nodifferences in the assemblage composition whereas insome cases the cold acetolyse-derived foraminiferaexhibit better preserved tests. Soft marly samples weretreated using standard methods: disaggregation with 10–30% solutions of hydrogen peroxide (Appendix A).

Planktonic foraminifera have been analyzed in theN63 μm fraction by counting the relative abundance ofgenera and selected species (marker), based on counts ofabout 300 specimens. The Subbotina group includes,beside Subbotina, the ecologically similar genera Para-subbotina and Globorotaloides (see Table 1) that,however, constitute a minor component of this groupthroughout the section. Radiolarian abundances havebeen evaluated as relative percentage with respect toforaminifera by counting number of specimens on 300tests in the N63 μm fraction and as number of specimensper gram of sediment (fraction N125 μm; from Giusbertiet al., 2007).

A prominent feature of the PETM event is the strongcarbonate dissolution, involving also planktonic fora-miniferal assemblages, particularly within the basal partof the event (Zachos et al., 2005). This feature is evidentalso in the basal CMU at Forada (Giusberti et al., 2007).As carbonate dissolution within the lysocline common-ly causes fragmentation of foraminiferal tests, we haveestimated the degree of dissolution by counting thenumber of planktonic foraminiferal fragments or par-tially dissolved tests versus entire tests, using about 300

Fig. 2. Planktonic foraminiferal biostratigraphic scheme across the PETM at the Tethyan Forada section with main and additional events plottedagainst lithology. Cycles are from Giusberti et al. (2007). Zonal schemes are from Molina et al. (1999) and Berggren and Pearson (2005). Calcareousnannofossil biozones (Martini, 1971) are from Giusberti et al. (2007). CMU = Clay marl unit. PFDI = Planktonic foraminiferal dissolution interval.BEE = Benthonic extinction event.


foraminifera and fragments/dissolved tests, followingHancock and Dickens (2005). Fragmented foraminif-era include specimens showing notable deterioration,missing chambers and substantial breakage. For theForada section, dissolution is thus expressed in termsof a fragmentation index (F-Index). Results of thequantitative analyses are shown in Figs. 2–5. Ourestimates of fragmentation are considered to furthervalidate the reliability of the “cold acetolyse” tech-nique, because most of the samples that have been

prepared using that method show the lowest F-Index(Appendix A).

4. Results

4.1. Biostratigraphy

Taxonomic criteria are adopted from Olsson et al.(1999) and Pearson et al. (2006). The single exceptionis the species Acarinina berggreni, which we prefer to

Fig. 3. Relative abundances of planktonic foraminiferal species markers across the PETM plotted against lithology and biostratigraphy. Cycles and δ13C curve, measured on bulk rock samples, arefrom Giusberti et al. (2007). The shaded bands highlight the intervals of the main carbon isotope excursion (dark) and of the recovery of δ13C values (light). CMU = Clay marl unit. PFDI = Planktonicforaminiferal dissolution interval. BEE = Benthonic extinction event. For the lithology see Fig. 2.

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keep separated from A. wilcoxensis, according to Blow(1979) and differently from Pearson et al. (2006),who include the relatively compressed chambered mor-photypes of A. berggreni within the morphological var-iability of A. wilcoxensis.

The great interest dedicated in recent years to thePETM event has generated new, improved data regard-ing the distribution of planktonic foraminifera across thisinterval, which has increased the biostratigraphic res-olution of planktonic foraminifera. The late Paleocene–early Eocene interval, formerly attributed entirely toZone P5 (Morozovella velascoensis Zone) (Berggrenet al., 1995) was subdivided by Berggren and Pearson(2005) into three biozones: P5 (M. velascoensis), E1(A. sibaiyaensis), and E2 (P. wilcoxensis/M. velascoensis).All three biozones have been identified in the Foradasec-tion on the basis of (Fig. 2): highest occurrence (HO) ofGlobanomalina pseudomenardii, lowest occurrence(LO) of A. sibaiyaensis, LO of Pseudohastigerinawilcoxensis and HO of M. velascoensis. Molina et al.(1999) proposed a five-fold subdivision of Zone P5 thatincludes the Morozovella aequa Subzone, the Morozo-vella gracilis Subzone, the A. berggreni Subzone, the A.sibaiyaensis Subzone, and the P. wilcoxensis Subzone(Fig. 2). Berggren and Pearson (2005) could notsystematically apply the five biozones of Molina et al.(1999), in particular the three uppermost Paleocene bio-zones (M. aequa–A. berggreni). In the Forada section,however, we have identified the same order of events asdescribed by Molina et al. (1999), suggesting that a five-fold subdivision across the Paleocene–Eocene transitionappears applicable in the Tethyan domain. It is worthnoting that the local LO of the marker A. sibaiyaensis isinfluenced by the intensity and extension of the carbonatedissolution interval during the CIE. In Forada, A.sibaiyaensis and A. africana occur up to 305 and345 cm above the P/E boundary, respectively. Rarespecimens of both these species occur sporadically up to+599 cm. It appears probable that these occurrences,above the end of the continuous range, had to be con-sidered as reworked. Calcareous nannofossils also showminor reworking in this part of the record (Agnini et al.,2007).

The absence ofM. allisonensis, and the scattered, rareoccurrences of Globanomalina luxorensis, in the Foradasection indicate that these two taxa are not biostrati-graphically useful in this Tethyan setting. They seem tobe restricted to tropical assemblages and were hence notemployed in the new zonal scheme of Berggren andPearson (2005).

The LO of P. wilcoxensis has been generally observedjust above the main excursion interval of the CIE, coin-

cident with or immediately following the HO of theexcursion taxa A. africana and A. sibaiyaensis (e.g.,Arenillas and Molina, 1996; Molina et al., 1999; Pardoet al., 1999; Berggren and Ouda, 2003a,b; Ouda andBerggren, 2003; Ouda et al., 2003; Petrizzo, 2007).However, P. wilcoxensis has, at Forada, its LO in themiddle part of the CMU, in lower cycle 3 (Fig. 3). Thisposition of the P. wilcoxensis event is consistent with theobservation by Lu et al. (1998) from the Alamedillasection in Spain. In the Possagno section, however,located only a few tens of km away from the Foradasection, the LO of P. wilcoxensis has been reported tooccur, albeit with a discontinuous record, immediatelyabove the HO of A. sibaiyaensis (Arenillas et al., 1999).This apparent discrepancy could reflect minor paleo-biogeographic diachrony, even if differences in preser-vation and methods of investigation are considered tolargely influence the data. High-resolution sampling andthe investigation of also a smaller size fraction, N63 μmrather than N100 μm, appear to generate an earlierLO event of P. wilcoxensis, in the middle part of themain excursion event of the CIE and well prior to theextinction of the excursion taxa (A. sibaiyaensis). InForada, P. wilcoxensis is consistently smaller than100 μm and intermittently occurring in the lowest partof its range. Further analysis is needed to definitelyvalidate the use of this species as zonal marker on aglobal scale.

The relative abundance and stratigraphy of severalother planktonic foraminiferal marker species recordedin the Forada section are displayed in Figs. 2 and 3.Selected planktonic foraminiferal species are displayedin Plate 1.

4.2. Age model

The early Eocene chronology is based on the cyclo-stratigraphic age model developed by Giusberti et al.(2007). The duration of each precessional cycle has beenassumed to be 21 kyr. In the Paleocene portion of thesection, where lithological cycles have not been firmlyidentified (see lithology and CaCO3 curve in Fig. 5),sedimentation rates are interpolated between the baseof the PETM at ±0 cm and the lowest occurrence ofthe calcareous nannofossil Discoaster multiradiatus at−1218 cm (Giusberti et al., 2007), using an age spacingbetween these two events of 1.238 Myr (Westerholdet al., 2007).

The investigated segment of the Forada sectionextends from the late Paleocene calcareous nannofossilD. multiradiatus Zone (NP9) to the early Eocene Tri-brachiatus contortus Zone (NP10) of Martini (1971)


(Giusberti et al., 2007). The entire investigated sectionspans ca. 1.3 million years.

4.3. Changes in composition and abundance of planktonicforaminiferal assemblages

The planktonic foraminiferal assemblages at Foradashow prominent changes in composition and abundanceacross the ca. 17 m thick interval investigated. A majorpart of these changes is shown in Fig. 4. Other criticalvariations, which include the abundance of the so-calledexcursion taxa and the F-Index, are shown together withthe dominant genera and radiolarians in Fig. 5. All thesecharacteristics have been used to subdivide the Foradasection into eight different phases, representing theevolution of the paleoecological conditions, as well asthe development of the preservational status of the as-semblages, across the PETM. These phases are related tothe three major lithological intervals of the Foradasection. Phases a through c represent the latest Paleocene,pre-CIE situation, lithologically composed of calcareousmarls. Phases d through g represent the earliest Eocenesituation, which is expressed as the CMU at Foradaand corresponds exactly with the main excursioninterval of the CIE. Phase h represents the recoveryinterval and the nearest overlying post-excursion inter-val, lithologically expressed by the limestone–marlcouplet unit (Giusberti et al., 2007). The time span ofeach phase has been approximated according to theabove age model.

4.3.1. Phase a — the late Paleocene conditionsThe late Paleocene conditions occur from the base of

the section at−687 cm to−137 cm (Figs. 4 and 5),with anestimated duration of about 540 kyr. The key character ofphase a is the relatively stable abundance relationshipsamong the three dominant genera, which are Morozo-vella, Acarinina and Subbotina. Morozovella speciesincludeM. acuta,M. aequa,M. apanthesma,M. occlusa,M. pasionensis, M. subbotinae, M. velascoensis andM. gracilis from−527.5 cm. The generaMorozovella andAcarinina are well diversified with a slight dominance ofMorozovella, having a relative abundance of up to 54%(mean value 43%). Acarinina species include A. coalin-gensis, A. esnaensis, A. soldadoensis and rare and un-evenly distributed A. subsphaerica. These species showfluctuations in abundances but no dominance of oneor more species (mean relative abundance 36%). Theacarininid abundance fluctuations are mainly out ofphase with those of the morozovellids. Members of theSubbotina group are also present but these forms aresubordinate relatively to the morozovellids and acarini-

nids (mean value 18%). The genera Chiloguembelina,Globanomalina, Igorina, Planorotalites and Zeauviger-ina occur as minor components of the assemblages(Fig. 4). The F-index displays low values (mean value8.9%) (Fig. 5). Five biohorizons occur within phase a(Fig. 2). They consist of: HO of G. pseudomenardii andthe LOs of Igorina lodoensis, M. gracilis, M. margin-odentata, Acarinina angulosa.

4.3.2. Phase b— the latest Paleocene Subbotina advanceand Morozovella decline

This phase is from −137 cm to −37 cm, with anestimated duration of about 120 kyr. The key charactersof phase b consist of a sharp decline of the genus Mor-ozovella (from 42.7% in phase a to 9.5% in phase b),coupled with a contrasting increase in the Subbotinagroup (up to 51.3%). Acarinina, on the other hand, doesnot show significant modifications in relative abun-dance. Another key character in phase b is the change inF-index mean values from 8.9% (phase a) to 41.6%(phase b), thus indicating a much stronger influence ofcarbonate dissolution in the latter phase (Fig. 5). A fewvariations in species composition with respect to theprevious phase consist of the LOs of A. berggreni andA. esnehensis (Fig. 2).

4.3.3. Phase c— the terminal Paleocene Acarinina peaksThis phase is from −38.5 cm to the ±0 level, with an

estimated duration of about 30 kyr. The key characterof this phase consists of the increase in mean relativenumbers of Acarinina members (Figs. 4 and 5),displayed as two prominent peaks in abundance at−34.5 cm (67%) and at −7.5 cm (66%). In particular, therobust A. coalingensis, A. esnaensis and A. soldadoensis,possessing well-developed muricae, are the species thatflourish during this phase whereas other Acarininaspecies are declining. The F-index increases to a meanvalue of 68.7%. At the −22 cm and −27 cm levels,however, the F-index shows a further rise with respectto the previous phase and reaches striking values of85–90%, corresponding exactly to a carbon isotopenegative shift of 1‰. Interestingly, the first Acarininapeak just precedes the 1‰ carbon isotope shift (Fig. 5).The two peaks in abundances of acarininids just belowthe onset of the CIE have not been recorded beforefrom Tethyan settings. A single peak has been observedin other Tethyan or neighboring Atlantic settings(Molina et al., 1999; Pardo et al., 1999; Arenillas andMolina, 2000).

The F-index reaches a value of 100% in the lastPaleocene sample at −1.5 cm, interpreted as the “burn-down layer” associated with the onset of the PETM

Fig. 4. Relative abundance of planktonic foraminiferal genera and group of genera across the PETM plotted against lithology and biostratigraphy. The Subbotina group includes, beside Subbotina, theecologically similar genera Parasubbotina and Globorotaloides (see Table 1) that, however, constitute a minor component of this group. See comment in the text. Cycles are from Giusberti et al.(2007). The shaded bands highlight the intervals of the main carbon isotope excursion (dark) and of the recovery of δ13C values (light). CMU = Clay marl unit. PFDI = Planktonic foraminiferaldissolution interval. BEE = Benthonic extinction event. For the lithology see Fig. 2.

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(Giusberti et al., 2007).Morozovella abundances, thoughshowing minor fluctuations and a slight increase inphase c (Fig. 5), remains low compared to the backgroundconditions of phase a. Subbotina members are still nu-merous but show a reduction where Acarinina showspeak abundances (Fig. 4). Five biohorizons events arerecorded within this interval and consist of the HO ofIgorina tadijistatensis and by the LOs of Subbotinahornibrooki, Parasubbotina varianta, Globorotaloidesquadrocameratus and Igorina broedermanni (Fig. 2).Parasubbotina and Globorotaloides however representminor components of the assemblages.

4.3.4. Phase d — the basal Eocene planktonicforaminiferal dissolution interval

This phase is from ±0 cm to ca. +50 cm, within theCMU, with an estimated duration of about 16 kyr. Thekey character of this phase is the virtual absence ofplanktonic foraminifera, except for the occurrence ofscattered, strongly dissolved and fragmented tests,mainly composed of not identifiable acarininids, whichreappear at +12.5 cm. Calcified radiolarians, particularlysphaerellarians, appear at about +20 cm and dominatethe microfossil assemblages (Fig. 5). They are abundantnot only in relation to planktonic foraminifera but alsoas total flux (see number of radiolarians per gram inFig. 5).

The benthonic extinction event (BEE) occurs be-tween the ±0 cm and the +12.5 cm levels, where Eocenecalcareous hyaline benthonic foraminifera appear in theN63 μm fraction, representing the single biohorizon inthis phase. The F-index is near to 100%.

4.3.5. Phase e— the early Eocene Acarinina supremacyin the CIE main interval

This phase is from +50 cm to +97.5 cm, within theCMU, with an estimated duration of about 14 kyr. Thekey characters of this phase are the consistent reappear-ance of entire, abundant tests of planktonic foraminifera,and the prominent decrease of F-index from 100% inphase d to 60% at the top of phase e. Themean F-index ofphase e is 77.5%. Planktonic foraminiferal assemblagesare almost entirely composed of acarininids, scoring amean relative abundance in excess of 90%. The so-called excursion taxa (A. sibaiyaensis, A. africana; Kellyet al., 1996, 1998) enter at +52.5 cm, at the beginningof phase e, and are abundant even if not dominant.Acarinina soldadoensis, A. coalingensis and A. berg-greni also contribute considerably to the bulk of theAcarinina assemblages (Figs. 2–5). Three biohorizonsoccur in this phase and comprise the LOs of A. africana,A. sibaiyaensis and A. pseudotopilensis (Fig. 2).

4.3.6. Phase f — the acme of the excursion taxa in theCIE main interval

This phase is from +97.5 cm to +177.5 cm, within theCMU, with an estimated duration of about 22.5 kyr. Thekey characters of this phase are the maximum abundanceof the excursion taxa, the decreasing F-index (mean value44%), and the beginning of the reduced abundance ofradiolarians. Moreover, Morozovella experienced arecovery in abundance, with a mean relative abundanceof 24% vs 6.9% in the previous phase e. The LOs ofParagloborotalia griffinoides and P. wilcoxensis are thebiohorizons recorded in this phase (Fig. 2).

4.3.7. Phase g — the initial early Eocene recovery ofthe planktonic foraminiferal assemblages

This phase is from +177.5 cm to +332 cm, within theCMU, with an estimated duration of 52.5 kyr. The keycharacter in this interval is that the assemblages arebeginning to approach a new steady state, graduallyreturning tomore diversified communities. However, theyare still dominated by the genus Acarinina (mean relativeabundance 61.9%). The excursion taxa A. sibaiyaensisand A. africana are still present at b5% of the totalassemblage (Figs. 3 and 5). At some levels, some spec-imens of A. sibaiyaensis and A. africana exhibit giantsizes, up to 450–500 μm, in contrast to most other sam-ples, which show considerably smaller sizes (Plate 1). Themean value of the F-index is 33%. A single biohorizonoccurs in this phase and consists of the highest continuousoccurrence of A. sibaiyaensis (Fig. 2).

4.3.8. Phase h— the post-CMU early Eocene conditionsThis phase is from the base of the CIE recovery

interval at +332 cm to the top of the section at +1035 cm,with an estimated duration of about 600 kyr. The keycharacters of this phase are the attainment of a newsteady state of well diversified planktonic foraminiferalassemblages. Minor components such as chiloguembeli-nids, igorinids, globanomalinids, pseudohastigerinids andplanorotalids (Fig. 4) increase in abundance, and Acari-nina suffered a decline with respect to the previous phasereaching a mean relative abundance similar to the latePaleocene conditions of phase a (37.7% vs 36.3%).Furthermore, the Subbotina group exhibits an increasewith respect to the previous phase. The increase of sub-surface, low-oxygen tolerant groups (chiloguembelinids,globanomalinids) within the recovery of δ13C, is a featurecommon in many Tethyan sections (Lu et al., 1998;Molina et al., 1999), recorded also in the Paratethys(Pardo et al., 1999). Planktonic foraminiferal abundancefluctuations in this interval appear lithologically modu-lated, a feature especially evident in the lower part of the

Fig. 5. Relative abundance of main planktonic foraminiferal genera and group of genera across the PETM. The cumulative percentage of the excursion taxa A. sibaiyaensis and A. africana is also plotted. Eight phases (a to h) have been identified on the basis of the prominentchanges displayed by the components of assemblages. The fragmentation index (F-index in the text) curve is reported as signal of dissolution (see discussion in the text). Cycles, δ13C (measured on bulk rock samples) and CaCO3 curves are from Giusberti et al. (2007). TheSubbotina group includes, beside Subbotina, the ecologically similar genera Parasubbotina and Globorotaloides (see Table 1) that, however, constitute a minor component of this group. Radiolarian abundances are expressed both as relative percentage with respect toforaminifera (by counting number of specimens on 300 tests in the N63 μm fraction; this paper) and as number of specimens per gram of sediment (fraction N125 μm; from Giusberti et al., 2007). The shaded bands highlight the intervals of the main carbon isotope excursion(dark) and of the recovery of δ13C values (light). CMU = Clay marl unit. PFDI = Planktonic foraminiferal dissolution interval. BEE = Benthonic extinction event. For the lithology see Fig. 2.

pp. 199–202V. Luciani et al. / Marine Micropaleontology 64 (2007) 189–214

Table 1Inferred life strategies and depth ranking of late Paleocene–early Eoceneplanktonic foraminifera derived from latitudinal distribution,environmental inferences (morphology, biogeographic distribution)and stable isotope data

Data are according to: Boersma and Shackleton (1977), Douglas andSavin (1978), Boersma et al. (1979, 1987), Boersma and Premoli Silva(1983, 1988), Poore and Matthews (1984), Shackleton et al. (1985),Premoli Silva and Boersma (1989), Corfield (1987), D'Hondt et al.(1994), Van Eijden and Ganssen (1995), Bralower et al. (1995),Norris (1996), Lu and Keller (1996), Berggren and Norris (1997),Kelly et al. (1998), Corfield and Norris (1998), Kelly (1999), Kelly(2002), Quillévéré and Norris (2003), Wade et al. (2006), this work.


phase having distinct lithological couplets. Members ofthe Subbotina group and Chiloguembelina become lessabundant within the marly intervals whereas the muricateforms (Acarinina and Morozovella) increase. In thelimestone/marly–limestone horizons, on the contrary,the Subbotina group, Chiloguembelina, Globanomalina,Pseudohastigerina and Planorotalites increase. The F-index shows marked variations in phase with the li-thology: high values were observed in the marls (up to63%) in contrast to the limestone/marly–limestone levels(16.5%). Seven biohorizons occur in this phase (highestcontinuous occurrence of Acarinina africana, LO ofMorozovella edgari, HOs of Morozovella apanthesma,M. velascoensis, M. acuta, M. occlusa, M. pasionensis)(Fig. 2).

5. Discussion: inferred paleoenvironmental scenariosbased on planktonic foraminiferal assemblages

The results based on compositional and abundancechanges among the planktonic foraminifera suggest anenvironmental interpretation for the three major litholog-ical intervals of the Forada section, each characterized bya distinct set of changes: the pre-CIE conditions of the latePaleocene (phases a–c), the main CIE interval of theearliest Eocene (phase d), and the subsequent carbonisotope recovery interval together with the initial post-recovery interval (phases e–g). Life strategies of earlyPaleogene planktonic foraminiferal genera and specieshave been discussed at length in numerous papers andthey are summarized in Table 1. The main inferred paleo-environmental conditions are summarized in Fig. 6.

5.1. The pre-CIE conditions of the late Paleocene(phases a–c)

The late Paleocene was characterized by highly di-versified assemblages, implying that a full set of ecol-ogical niches were occupied both in surface and sub-surface waters. Low abundances of biserial formsindicate a weakly developed oxygen minimum zone(Table 1). The relative dominance of morozovellids andacarininids, with respect to subbotinids, implies rela-tively warm, stable and oligotrophic conditions through-out phase a.

Significant changes in abundances of the planktonicforaminifera begin prior to the onset of the CIE, duringphase b. These changes involve a clear decline of Mor-ozovella, a specialized surface water dweller preferringwarmer waters, and a marked increase of the opportunistSubbotina group, which is considered to prefer deeper,colder and more eutrophic waters. The decline among

the morozovellids suggests critical conditions for thisgroup that can be represented either by increasing eu-trophic conditions or lower temperatures of the surfacewaters. Subbotinids, in contrast, may have benefitedfrom both these conditions.

The relatively high F-index during phase b indicatesintensified dissolution. As Subbotina is a more dissolu-tion-susceptible species, in comparison to Morozovella(Petrizzo, 2007), this suggests that the increase in Sub-botina and the concomitant decrease of Morozovelladuring phase b was authentic indeed and not caused bycarbonate dissolution. This abundance reversal thusrather suggests a genuine change of the trophic structuretowards eutrophy. The combination of the increase inSubbotina and decrease of Morozovella in phase b canhence be explained if surface waters were undergoing

Fig. 6. Summary of the major changes in planktonic foraminiferal assemblages across the PETM at the Forada section (phases a to h) andpaleoenvironmental interpretation plotted against lithology, stable carbon isotope curve (δ13C, measured on bulk rock samples) and dissolution,expressed as Fragmentation index. For discussion see the text. CMU = Clay marl unit. PFDI = Planktonic foraminiferal dissolution interval. BEE =Benthonic extinction event. For the lithology see Fig. 2.


a change towards more eutrophic conditions, about150 kyr prior to the onset of the CIE. Moreover, anotherchange in surface water conditions occurred at about30 kyr (phase c) prior to the CIE, as indicated by themarked increase in Acarinina abundance that may beinterpreted as a warm signal. The lowest Acarininaspike, in particular, for its stratigraphic position below alightening of 1‰ in the δ13C, may provide significantimplications for estimate triggering mechanisms. Theplanktonic foraminiferal assemblages thus indicate thatsurface water conditions changed in two steps in thelatest Paleocene, first towards eutrophy which was fol-lowed, several tens of thousands of years, by increasingtemperatures.

Finally, the virtual absence of planktonic foraminif-era in the phase d at the very base of the CIE prevent apaleoecological interpretation based on this group andindicate the rapid and impressive shallowing of the CCDcaused by acidification of the oceans that is a commonfeature of the PETM (Dickens et al., 1997; Zachos et al.,2005) except for the ODP Site 690 in the SouthernOcean (Kennett and Stott, 1991; Kelly et al., 2005).

5.2. Reading the Acarinina dominance within the CIE(phases e–f)

During the earliest Eocene, represented by the low-ermost part of the main excursion of the CIE (phase e),


the planktonic foraminiferal response is similar in Foradato what has been recorded at several other sites, fromTethyan as well as high latitude environments. Thisinterval is characterized by a marked increase of Acari-nina, though with some differences in the speciescomposition and relative abundance (Canudo andMolina, 1992a,b; Kelly et al., 1996, 1998; Lu et al.,1996; Schmitz et al., 1997; Arenillas et al., 1999; Pardoet al., 1999; Kelly, 2002; Ernst et al., 2006).

The occurrence of the initial CIE peak of acarininidsin widely separated geographic areas such as the Tethysand the Southern Ocean, points to a common paleoeco-logical advantage during severely stressed surface waterconditions. The extreme warmth during the CIE clearlywas responsible for the strong reduction of the coldindices Subbotina at Forada, and for the concomitanthuge increase of the warm indicator Acarinina. How-ever, this scenario at Forada, is not consistent with thedistinct decline of the thermophile morozovellids, whichshould have benefited of warm conditions and henceincreased their abundance. An increase in morozovellidshas been observed from the equatorial Pacific Ocean(Kelly et al., 1996, 1998; Petrizzo, 2007). An increasedabundance of Morozovella implies both warming andoligotrophy, a situation recorded in the open oceanequatorial Pacific, whereas the reduction of this genus inForada appears to be caused by eutrophy coupled withthe concomitant temperature increase.

This scenario is consistent with the abundance behaviorof the oligotrophic calcareous nannofossil Sphenolithusthat records a marked decline comparable with that ofmorozovellids (Agnini et al., 2007).However, it is possiblethat changes in geochemistry and salinity of surface watersmight have influenced the morozovellids crisis as well,though a lower salinity in surfacewaters is not indicated bythe low-salinity calcareous nannofossils indices (Agnini etal., 2007). It is not excluded that the Morozovella declinemight have been related to a crisis of its symbionts,possibly different from those hosted by Acarinina, able tothrive in stressful, eutrophic, surface-water conditions(Guasti, 2005).Amulti-chambered variety ofA. sibaiyaen-sis, the dominant taxon at Dababiya (Egypt) in the lowerCIE interval, has been considered by Ernst et al. (2006) tohave flourished under nutrient-rich conditions.

The increased nutrient supply in the western Tethys atForada is caused by the accelerated hydrological cycle.This was triggered by an extremely warm, humid climateand enhanced weathering, intensifying the siliciclasticpump which, in turn, resulted in a huge increase interrigenous input (Giusberti et al., 2007). The closecorrelation between mineralogical/geochemical data andcalcareous nannofossil fluctuations appears to confirm

this hypothesis (Agnini et al., 2007). The fact that sedi-mentation rates increased by a factor of five during theCMU and that a pulse of reworked calcareous nanno-fossils occurs in the CMU is coherent with the proposedscenario (Giusberti et al., 2007). Moreover, the greatabundance of radiolarians within the CMU is yet anotherindicator of increased eutrophy of the surface waters(e.g., Roth and Krumbach, 1986; Hallock, 1987; Jarviset al., 1988; Robaszynski et al., 1990, 1993).

Higher trophic levels could have been induced at alarger scale, besides the enhanced hydrological cycles,by hydrothermal inputs of biolimiting metals (e.g. Fe,Zn) during the accelerated production of oceanic crustrelated to the large northeast Atlantic spreading (Reaet al., 1990; Eldholm and Thomas, 1993; Svensen et al.,2004) or the circum-Caribbean explosive volcanism(Bralower et al., 1997). Similar mechanisms have beeninvoked to explain increased input of nutrient during theOAEs, particularly the OAE1a (e. g., Wilson and Norris,2001; Bice and Poulsen, 2002). In addition, the Foradasection is located in a submarine volcanic provinceactive during the Paleogene (e.g. De Vecchi et al., 1976;De Vecchi and Sedea, 1995; Beccaluva et al., 2007).

5.3. The latest part of the main interval of the CIE(phase g)

Sharp and strongly reduced abundance of excursiontaxa and radiolarians togetherwith a sharp improvement inpreservation imply that water conditions were radicallychanged towards a less extreme environment. Thissignificant change is not apparently linked to any majorvariability in the δ13C record (Fig. 5). How-ever, environmental conditions continued to be stressedthroughout the main CIE interval as indicated by thedominance of Acarinina (phase g). Increasing carbonateconcentration and decreasing F-index witness aboutsteadily and gradually improved preservation of theforaminiferal assemblages throughout this phase, indicat-ing a gradually deepening of the lysocline and the CCD.Interestingly, the response time of calcareous nannofossils(Agnini et al., 2007) and planktonic foraminifera differs,in that the recovery of the former plankton group coincideswith the onset of the δ13C recovery interval correspondingto the phase h, whereas the planktonic foraminifera showan earlier start of their recovery in phase g.

5.4. The recovery interval of the CIE and the initialpost-recovery interval (phase h)

In the upper part of the Forada section, the relativeproportions of the main components of the foraminiferal


assemblages move towards a new stable state, becomingsimilar to the late Paleocene conditions during phase a(Fig. 5). A similar trend is observed for the minor con-stituents, such as biserial forms and deeper dwelling

taxa. These changes coincide with the onset of therecovery of δ13C values and document the relative pro-gressive cooling following the extreme warmth duringthe main CIE interval, indicating a water column


structure that becomes progressively more stratified andthus permitting a great number of ecological niches to beoccupied. However, the perturbation during the PETMproduced significant changes in the ocean geochemistrythat lasted after this event as testified by the prominentcarbonate dissolution and fragmentation of the plank-tonic foraminiferal assemblages characterizing the marlylevels and the large variability in the relative abundanceamong the different species and genera. These strikingoscillations have not been recorded among the latePaleocene assemblages.

5.5. Chamber elongation, oxygen contents and foodsupply in surface waters

A. sibaiyaensis, A. africana and M. allisonensisflourished during the main interval of the CIE (Canudoand Molina, 1992a,b; Canudo et al., 1995; Kelly et al.,1996, 1998; Lu et al., 1996; Arenillas et al., 1999; Pardoet al., 1999). Forada is no exception to this pattern(Figs. 3 and 5), except forM. allisonensis, that is absent.A. sibaiyaensis and A. africana are a conspicuouscomponent of the assemblages within phase e–f, andthen decrease in abundance during phase g. A progres-sive increase of other planktonic foraminiferal speciesoccurs concomitantly with the decrease of the excursiontaxa.

Considering the so-called excursion taxa A. sibaiyaen-sis and A. africana exclusively from a morphologicalperspective, it is evident that these forms exhibit,with respect to other components of this genus, a radialelongation of chambers. This is particularly obvious inA. africana (Plate 1). Morphotypes of Parasubbotina andGlobanomalina with elongated chambers also occur inthe interval where both A. sibaiyaensis and A. africanahave their highest abundance (Plate 1). Specimens ofSubbotina patagonica also show elongation of the lastchamber from the identical interval at Forada. It appears

Plate 1. 1–20: Selected planktonic foraminifera from the late Paleocene–earlvelascoensis; 1: ventral view, 2: profile, −261.5 cm, P5 Zone, late PaleocenPaleocene; 4,7, 8—Morozovella aequa, 5: ventral view, 7: dorsal view, 8: pro5: ventral view, −27 cm, P5 Zone, late Paleocene, 6: profile, +182,5 cm, eaP5 Zone, late Paleocene, 10: profile, +112,5 cm, E1 Zone, early Eocene; 11, 1dorsal view, +182.5 cm, E1 Zone, 14: dorsal view, +202.5 cm, E2 Zone, 15: d12, 13— Pseudohastigerina wilcoxensis, profile, +325 cm, E2 Zone, early Eelongation of the chambers, +167.5 cm, E1 Zone, early Eocene; 16, 18, 19—18: ventral view, +82.5 cm, E1 Zone; 19: ‘giant’ specimen, +285 cm, E2 Zoanoxic event (OAEs) (Coccioni et al., 2006) exhibiting morphological simielongation of the chambers; 21: Globigerinelloides blowi lobatulus Verga andPremoli Silva (2005); 22: Pseudoschackoina saundersiVerga and Premoli Silv(2005); 23: Muricohedbergella simplex (Morrow, 1934), Pueblo section,Longoria, 1974, Rio Argos section (Spain), after Coccioni et al. (2004b). Sca

as if the clavate body plan developed because of thestressed ecological conditions that occurred during themain excursion interval of the CIE.

Chamber elongation is a recurring morphologicalcharacter in Cretaceous and Cenozoic planktonic for-aminiferal evolution, which developed independentlyfrom wall-texture features or size. Cretaceous sedimentscontaining increased concentrations of organic car-bon that record the effects of Oceanic Anoxic Events(OAEs, Schlanger and Jenkyns, 1976) show, in severalcases, planktonic foraminiferal assemblages enriched informs having radially elongated chambers (see review inCoccioni et al., 2006). Thus, chamber elongation hasbeen interpreted as an adaptation to low oxygen levels inthe upper water column (e.g., Boudagher-Fadel et al.,1997; Magniez-Jannin, 1998; Aguado et al., 1999;Premoli Silva et al., 1999; Bellanca et al., 2002; Coccioniand Luciani, 2004, 2005; Coccioni et al., 2006).Moreover, their morphological similarity with Eocenehantkeninids, known to live at, or near, oxygen-depletedsea surface waters (Boersma et al., 1987; Coxall et al.,2000, 2002), is consistent with this hypothesis.

The radially extended, perforate chambers imply anincreased surface/volume ratio. By doing this, theradially elongated forms may represent an adaptation tofacilitate oxygen uptake in a poorly oxygenated envi-ronment. Moreover, it is possible that the clavatechambers functioned as anchors to large radial rhizopods,enabling the foraminifera to graze a larger volume ofwater at minimal metabolic cost (Boudagher-Fadel et al.,1997; Magniez-Jannin, 1998; Premoli Silva et al., 1999;Premoli Silva and Sliter, 1999; Coxall et al., 2000, 2002;Coccioni and Luciani, 2004; Coccioni et al., 2006).

It is not surprising that the extraordinary, rapid tem-perature increase occurring across the CIE could havedecreased the solubility of oxygen. Furthermore, theassumed enhanced photosynthetic activity in surfacewaters may have favored a decrease in oxygen content

y Eocene Tethyan Forada section (northern Italy). 1,2 — Morozovellae; 3 — Acarinina soldadoensis, ventral view, −137cm, P5 Zone, latefile, −591 cm, P5 Zone, late Paleocene; 5,6—Morozovella subbotinae,rly Eocene. 9, 10 — Acarinina berggreni, 9: ventral view, −34,5 cm,4, 15, 20— Acarinina sibaiyaensis, early Eocene, 11: ‘giant’ specimen,orsal view, +172.5 cm, E1 Zone, 20: dorsal view, +142,5 cm, E1 Zone;ocene; 17: Planoglobulina sp., specimen showing a tendency of radialAcarinina africana, early Eocene, 16: dorsal view, +295 cm, E2 Zone,ne, early Eocene. 21–24: Cretaceous species typical of the Cretaceouslarities with A. sibaiyaensis and A. africana in the tendency of radialPremoli Silva 2005, Lesches en Diois section, France, after Verga anda 2005, Lesches en Diois section, France, after Verga and Premoli SilvaColorado, after Keller and Pardo (2004); Hedbergella semielongatale bar=100 μm.


in sub-surface waters. The different proportion ofA. africana and A. sibaiyaensis in different geographicareas might imply different degrees of local oxygenationof the water column and/or different amount of nutrientavailability. Less severe environmental conditions at thePETM, with respect to the main Cretaceous OAEs (earlylate Aptian Selli and latest Cenomanian Bonarellievents), both in terms of oxygen condition of watercolumn and eutrophy, may have hampered the evolu-tionary control to produce taxa showing the “extreme”morphological character of the tubulospine, even if theabove mentioned events share greenhouse conditionsand a sensationally intense warmth.

Apart from the chamber elongation, the compressedtests of A. sibaiyaensis and A. africana are anothermorphological similarity with the planispiral/low trochos-piral Cretaceous and Eocene Leupoldina, Schackoina,Pseudoschackoina and Hantkenina. A low trochospire-compressed test is a feature common to the radiallyelongated Cretaceous hedbergellids. Among the clavatechambered forms, A. sibaiyaensis and A. africana areexclusive in having a muricate wall, which otherwise isgenerally related to symbiont-bearing adaptation (e. g.,Quillévéré et al., 2001). Strict relationships between walltextures and habitat, largely used as a taxonomic criterion,are not always straightforward as suspected by Sextonet al. (2006). It cannot be excluded that the excursion taxa,considering their short range during extremely stressedenvironmental conditions, may have been forced to de-velop different feeding strategies. This assumption mayperhaps also explain the large differences in size displayedby the species involved (Plate 1).

In the case that low oxygen content would have beenone of the most important controlling-factor in the upperpart of the water column during the CIE, one may expectan increase of biserial forms and globanomalinids, char-acterized by their tolerance for low oxygen conditions,in the lower part of the CMU (=lower CIE) at Forada.However, these forms are typically very rare in thisinterval. Biserial forms are nevertheless cooler indiceswith respect to acarininids (Table 1), suggesting that hightemperatures during the CIE hampered development ofbiserial forms.

The palaeoecological significance of planktonicforaminifera that occasionally develop radially elongat-ed chambers remains however puzzling. Several linesof evidence suggest that oxygenation cannot havebeen the single controlling factor governing the de-velopment of elongate chambers. The availability offood and the nature of the food available appear to beunderestimated with regard to possible casual mechan-isms that are driving chamber elongation. It is most

likely that the interplay of several influential physical,chemical, and ecological factors, for example, temper-ature, dissolved oxygen concentration, Ph, salinity,nutrients, type of food, trace elements, were responsiblefor such a morphological adaptation (Coccioni et al.,2006).

6. Conclusions

The high-resolution planktonic foraminiferal analysisperformed at the expanded PETM from the centralwestern Tethyan Forada section highlights several eventsand striking changes in abundance and compositionwithin the assemblages that represent ecological andevolutionary responses to this brief episode of extremewarmth. These changes clearly outline a complex paleo-environmental evolution in the western central Tethysacross the PETM (Fig. 6).

One of the most significant features provided by theForada record is the clear signal of a marked environ-mental instability starting well before the onset of thePETM. In fact, the relatively stable, warm and oligo-trophic surface water conditions of the late Paleocene(phase a) changed distinctly in two steps, at ca. 150 kyrand 30 kyr, prior to the onset of the CIE (phase b–c). Thefirst step (phase b) involved a change towards eutrophy,as marked by the advance of Subbotina group and theconcomitant decline of Morozovella. This step is alsocharacterized by enhanced fragmentation and dissolu-tion. The second step (phase c) is marked by an increasein surface water temperatures, suggested by the highabundances of Acarinina. Interestingly, the lower peakin abundance of Acarinina is just below the 1‰ negativecarbon isotope shift occurring before the onset of themain CIE, stimulating the intriguing hypothesis that theintense warming preceded the giant release of CO2. Itremains however unclear whether or not these pre-CIEsteps represent global or regional events, although anincrease inAcarinina has been observed in other Tethyanas well as open ocean sites suggesting a possible globalprelude to the PETM.

The dominance of acarininids in the lower part of theCIE at Forada (phase e, f; ca. 14 and 22.5 kyr) is inter-preted as a consequence of exceptional warmth coupledwith eutrophic conditions in the upper water column.The enhanced fertility would have been induced byglobal mechanisms such as accelerated hydrologicalcycle due to the expanded greenhouse effect and con-sequent input of nutrients. The Forada section, located ina geological setting adjacent to land masses, records alarge terrigenous input that caused the increase innutrient availability. The high abundance of radiolarians


and the sharp decrease in abundance exhibited by thecalcareous nannofossil oligotrophic taxa are consistentwith this scenario. All these evidences of increasedeutrophy at Forada are independent clues that Acarininawas able to tolerate and thrive within eutrophic envi-ronments under extreme warmth. The genus Morozo-vella, that suffered the most consistent reduction inabundance across the PETM, is confirmed to be the mostspecialized group among the planktonic foraminifera.Moreover, the relative abundance of this genus isfrequently out of phase with that of the genus Acari-nina, further indicating that dissimilarities in the ecol-ogical preferences of the two muricate genera have beenpreviously underestimated. Acarininids, with respect tomorozovellids, were probably able to temporarilycolonize warm deeper water occupying ecologicaldepth niches previously inhabited by the cold Subbo-tina. At the same time, acarininids tolerated relativelyhigh eutrophic conditions which suppressed the abun-dances of Morozovella.

The excursion taxa A. sibaiyaensis and A. africanaexhibit radially elongated chambers, a feature partic-ularly evident in the latter species. This peculiar mor-phology has been repeatedly employed by planktonicforaminifera during Cretaceous and Paleogene times(e.g., Leupoldina, Schackoina, clavate hedbergellidsand Hantkenina). Specifically, the Cretaceous OAEsare characterized by flourishing of this morphologicaladaptation to stressed surface water conditions. Themorphological similarity between the excursion taxaand the Cretaceous and Eocene radially-elongatedchambered forms, is a stimulating hypothesis for thecomprehension of the ecology of these short-livedspecies that represent an optimal adaptation to theextremely perturbed environmental conditions duringthe PETM event. These stressed conditions mayinclude reduced oxygen concentration, availabilityand nature of food, temperature, salinity, traceelements or a combination of these parameters.Although the general geological and paleoceano-graphic contexts are sensibly different, the PETMevent and the Cretaceous OAEs are both related toextreme greenhouse conditions and intense volcanicactivities.

The initial amelioration of surface water conditionsat Forada is marked by a drastic decrease of theexcursion taxa, a marked improvement in planktonicforaminiferal diversity and preservation, and a declinein radiolarian abundance. These changes, starting ca.52.5 kyr after the onset of the CIE and representing thelate part of the main excursion (phase h), areconsidered to be caused by a global deepening of the

CCD and a gradual return to less eutrophic conditionsat Forada.

A new steady state is definitely reached in the upperpart of the Forada section, corresponding to the CIErecovery and the following initial CIE post-recoveryintervals (phase h), where relative proportions of themain components of the planktonic foraminiferal as-semblages move towards those of the Paleocene(phase a). However, the large variability in relativeabundance of genera and species in this interval, togetherwith prominent carbonate dissolution in the marly levels,strongly suggests that the perturbed conditions intro-duced during the PETM continued to influence surfacewater conditions, to some degree, also during the initialpost-recovery interval.

No major biotic extinctions occurred among thecalcareous plankton although the PETM represents anextraordinary event that induced severely stressed sur-face water environments. On the contrary, severalplanktonic foraminiferal first appearances are recordedand may give the opportunity for future finest subdivi-sions of this crucial interval. The new taxa mainlybelong to the thermophilic acarininids, which wererelatively tolerant to eutrophy. On the other hand, alsocooler and deep dwelling taxa originated across thePETM event. The environmental perturbations duringthis event had, therefore, positive effects on theplanktonic foraminiferal assemblages and stimulatedspeciation. The micro-evolutionary patterns in plank-tonic foraminifera have been generally related to astable ocean and to depth-related specializations(Pearson et al., 2006). The link between new speciesand the PETM episode of stress, demonstrates howincomplete our knowledge is about evolutionarymechanisms.

Acknowledgements

This work was financially supported by MIUR/PRIN COFIN 2003–2005 (D. Rio), by the Universityof Ferrara (FAR) to V. Luciani, by the University ofPadova to E. Fornaciari and by the Stockholm Universityto J. Backman. This paper benefited from the constructivecomments of R. Olsson, E. Guasti and A. Mackensen.

Thanks are also due to Lorenzo Franceschin forprocessing samples for micropaleontological analyses.

Appendix A. Supplementary data

Supplementary data associated with this articlecan be found, in the online version, at doi:10.1016/j.marmicro.2007.05.001.

http://dx.doi.org/doi:10.1016/j.marmicro.2007.05.001

http://dx.doi.org/doi:10.1016/j.marmicro.2007.05.001


Appendix B. Planktonic foraminifera: list of citedtaxa in alphabetical order

Acarinina africana (El Naggar) = Globorotaliaafricana El Naggar, 1966Acarinina angulosa (Bolli) = Globigerina solda-doensis angulosa Bolli, 1957Acarinina berggreni (El naggar) = Globorotaliaberggreni El Naggar 1966;Globorotalia (Acarinina)wilcoxensis berggreni El Naggar in Blow (1979)Acarinina coalingensis (Cushman and Hanna) =Globigerina coalingensis Cushman and Hanna, 1927Acarinina esnaensis (Le Roy) = Globigerina esnaen-sis Le Roy, 1953Acarinina esnehensis (Nakkady) = Globigerinacretacea d’Orbigny var. esnehensis Nakkady, 1950Acarinina sibaiyaensis (El Naggar) = Globorotaliasibaiyaensis El Naggar, 1966Acarinina soldadoensis (Brönnimann) = Globiger-ina soldadoensis Brönnimann, 1952Acarinina subsphaerica (Subbotina) = Globigerinasubsphaerica Subbotina, 1947Globanomalina luxorensis (Nakkady) = Anomalinaluxorensis Nakkady, 1950Globanomalina pseudomenardii (Bolli) = Globoro-talia pseudomenardii Bolli, 1957Globorotaloides quadrocameratus Olsson, Pearsonand Huber, 2006Igorina broedermanni (Cushman and Bermudez) =Globorotalia broedermanni Cushman and Bermu-dez, 1949Igorina convexa (Subbotina) = Globorotalia convexaSubbotina, 1953Igorina tadjikistanensis (Bykova) = Globorotaliatadjikistanensis Bykova, 1953Morozovella acuta (Toulmin) = Globorotalia wilcox-ensis Cushman and Ponton var. acuta Toulmin, 1941Morozovella aequa (Cushman and Renz) = Globor-otalia crassata var. aequa Cushman and Renz, 1942Morozovella allisonensis Kelly, Bralower andZachos, 1998Morozovella apanthesma (Loeblich and Tappan) =Globorotalia apanthesma Loeblich and Tappan,1957Morozovella edgari (Premoli Silva and Bolli) =Globorotalia edgari Premoli Silva and Bolli, 1973Morozovella gracilis (Bolli) = Globorotalia formosagracilis Bolli, 1957Morozovella marginodentata (Subbotina) = Globor-otalia marginodentata Subbotina, 1953Morozovella occlusa (Loeblich and Tappan) = Glo-borotalia occlusa Loeblich and Tappan, 1957

Morozovella pasionensis (Bermudez) = Pseudoglo-borotalia pasionensis Bermudez, 1961Morozovella subbotinae (Morozova) = Globorotaliasubbotinae Morozova, 1939Morozovella velascoensis (Cushman) = Pulvinulinavelascoensis Cushman, 1925Paragloborotalia griffinoides Olsson and Pearson,n. sp., 2006Parasubbotina varianta (Subbotina) = Globigerinavarianta Subbotina, 1953Pseudohastigerina wilcoxensis (Cushman and Pon-ton) = Nonion wilcoxensis Cushman and Ponton,1932Subbotina hornibrooki (Brönnimann) = Globigerinahornibrooki Brönnimann, 1952Subbotina patagonica Todd and Kniker = Globi-gerina patagonica Todd and Kniker 1952

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the paleocene–eocene thermal maximum as recorded by tethyan planktonic foraminifera in the forada...

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