High stress late Maastrichtian paleoenvironment: inference

High stress late Maastrichtian paleoenvironment:inference from planktonic foraminifera in Tunisia

Sigal Abramovich *, Gerta KellerDepartment of Geosciences, Princeton University, Princeton, NJ 08544, USA

Received 10 July 1999; accepted 9 August 2001

Abstract

High resolution (V5^10 kyr) planktonic foraminiferal analysis at Elles, Tunisia, reveals major changes in thestructure of the Tethyan marine ecosystem during the upper Maastrichtian. During the first 1.5 Myr of the lateMaastrichtian (68.3^66.8 Ma) relatively stable environmental conditions and cool temperatures are indicated by diverseplanktonic foraminiferal populations with abundant intermediate and surface dwellers. A progressive cooling trendbetween V66.8^65.45 Ma resulted in the decline of globotruncanid species (intermediate dwellers). This groupexperienced a further decline at the climax of a rapid warm event about 300 kyr before the K^T boundary. At the sametime relative abundances of long ranging dominant species fluctuated considerably reflecting the high stressenvironmental conditions. Times of critical high stress environments during the late Maastrichtian, and particularly atthe K^T boundary, are indicated by low species diversity and blooms of the opportunistic genus Guembelitria at warm^cool transition intervals. During the last 100 kyr of the Maastrichtian rapid cooling is associated with acceleratedspecies extinctions followed by the extinction of all tropical and subtropical species at the K^T boundary. ß 2002Elsevier Science B.V. All rights reserved.

Keywords: planktonic foraminifera; biostratigraphy; upper Maastrichtian; Tunisia; paleoecology; paleoclimate

1. Introduction

Until recently most studies of Maastrichtianplanktonic foraminiferal populations that aimedto describe the nature of the Cretaceous^Tertiary(K^T) boundary mass extinction focused in extra-ordinary detail on the K^T transition itself, whichrepresents at best a few hundred thousand years(e.g. Smit, 1982, 1990; Keller, 1988, 1989a, 1993;

Canudo et al., 1991; Keller and Benjamini, 1991;Olsson and Liu, 1993; Keller et al., 1995, 1997;Pardo et al., 1996; Appellaniz et al., l997; Lucia-ni, 1997; Molina et al., 1998). During the last fewyears, it has become increasingly evident that thenature of this mass extinction cannot be e¡ec-tively addressed until the background variationsof populations and their relationship to environ-mental parameters in the Maastrichtian ecosystemare understood (e.g. Keller, 1996). To date, only afew stratigraphically well constrained studies of amore complete Maastrichtian faunal record havebeen published, and these concern faunas fromthe Brazos River, Texas (Keller, 1989b), Denmark

0031-0182 / 02 / $ ^ see front matter ß 2002 Elsevier Science B.V. All rights reserved.PII: S 0 0 3 1 - 0 1 8 2 ( 0 1 ) 0 0 3 9 4 - 7

* Corresponding author. Tel. : +1-609-258-4117;Fax: +1-609-258-1671.

E-mail address: [email protected] (S. Abramovich).

PALAEO 2753 1-5-02

Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 145^164

www.elsevier.com/locate/palaeo

(Schmitz et al., 1992), the Southern Ocean (Hu-ber, 1992), mid-latitude South Atlantic (Li andKeller, l998a), Tunisia (Li and Keller, 1998b),and the Negev, Israel (Abramovich et al., l998).

These studies have shown that the deteriorationof Cretaceous planktonic foraminiferal popula-tions began in the late Maastrichtian and acceler-ated over the last few hundred thousand years ofthe Maastrichtian. The onset of the decline wasaccompanied by blooms of the opportunistic ge-nus Guembelitria which demonstrate the instabil-ity of the pelagic ecosystem during the last fewmillion years of the Cretaceous (Abramovich etal., 1998). The faunal decline climaxed at the K^T boundary with the mass extinction of all speci-alized tropical^subtropical planktonic foramini-feral species, whereas the cosmopolitan and eco-logically generalist species survived into theDanian (for a summary see Keller et al., 2002).

Recent studies of the Maastrichtian stable iso-topic records from DSDP Sites 525A and 21 (Liand Keller, 1998a,c) leave no doubt that globalclimatic deterioration occurred during the Maas-trichtian, and was accompanied by signi¢cant sealevel £uctuations (see also Barrera, 1994; Barreraet al., 1997; Barrera and Savin, l999). Further-more, the timing of these events strongly suggeststhat the Late Cretaceous faunal decline was trig-gered by environmental changes. This suggeststhat a bolide impact at the K^T boundary wasnot the sole causal mechanism for the K^T massextinction. Further detailed high resolution re-cords that evaluate the Maastrichtian ecosystemstress are still needed if we are to understand therelationship between environment and biotic per-turbations leading up to the K^T boundary.Among the regions of high potential for obtaininghigh resolution records are the sections from thenorthern part of Tunisia.

The Upper Cretaceous sequence of northernTunisian was deposited in a series of basins whichsurrounds a tectonically emergent zone, the Kas-serine Island (Fig. 1), the major source for clasticmaterial into the basins (Adatte et al., 1998; Ben-salem, 1998). The sediments within the northwest-ern basin are characterized by abundant pelagicmicrofaunas deposited on the outer shelf to upperslope (Li and Keller, 1998b).

Most studies of Maastrichtian and Paleogenesections in Tunisia have concentrated on theK^T boundary transition at the El Kef stratotype(e.g. early studies summarized by Salaj (1980) andlater studies by Keller et al. (1995)). High resolu-tion microfossil and geochemical studies havegenerally focused on the 50^100-cm interval be-low and above the K^T boundary. Maastrichtianstudies are few and generally of a stratigraphicnature (Salaj, l980) with the exception of Neder-bragt (l991) who studied the Heterohelicidae atEl Kef. A more complete quantitative study ofthe entire Maastrichtian planktonic foraminiferalfauna and various geochemical analyses (stableisotopes, mineralogy, trace element geochemistry)at El Kef and Elles has recently been publishedby Li and Keller (1998b) and Li et al. (1999,2000).

The objective of this study is to evaluate thelate Maastrichtian faunal turnover at a sectionlocated near the hamlet of Elles in north-central

Fig. 1. Maastrichtian paleogeography of Tunisia (after Burol-let, 1967). Note the paleogeographic location of the Elles sec-tion between the emergent zone of the Kasserine Island andEl Kef section.

PALAEO 2753 1-5-02

S. Abramovich, G. Keller / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 145^164146

Tunisia (Fig. 1). In this section planktonic fora-miniferal populations were quantitatively ana-lyzed at 10^20-cm intervals, or on average onesample every V5^10 kyr, for the last millionyears of the Maastrichtian.

2. Location, lithology and methods

The Elles section is located in the Karma valleynear the hamlet of Elles, about 75 km southeastof the city of El Kef and the nearby K^T bound-ary stratotype section. The Maastrichtian se-quence exposed in the Karma valley was depos-ited at middle to outer shelf depths and relativelyclose to the emergent zone of the Kasserine Island(Fig. 1). This position explains the high terrige-nous content in Maastrichtian sediments at Elles,and the unusually high sedimentation rate (e.g.V4 cm/1000 yr, Li and Keller, 1998b; Adatte etal., 2002). The very high sediment accumulationrate at Elles, which exceeds that of the El Kefsection (Li and Keller, 1998b), has great potentialfor accurately evaluating the timing of environ-mental changes during the late Maastrichtianand particularly during the last million years ofthe Maastrichtian.

Lithologically, the upper Maastrichtian innorthern Tunisia is represented by the El HariaFormation. Upper Maastrichtian sediments at El-les consist of relatively uniform marly shales witha 25-cm-thick resistant layer of bioturbated marlylimestone at about 26 m below the K^T bound-ary. The K^T transition is marked by a 20-cm-thick channelized cross-bedded bioclastic layer(foraminiferal packstone), which underlies a 1-cm dark gray clay and thin rust-colored layer.The rusty layer contains an iridium anomalyand Ni-rich spinels which mark the K^T bound-ary (Adatte et al., 2002). A total of 191 sampleswere collected from the last 31 m of the Maas-trichtian. Samples were collected at 10-cm inter-vals between 31.2 and 26.5 m, and at 20-cm in-tervals through the rest of the section. However,near the boundary interval samples were collectedat 1-cm intervals.

In the laboratory, samples were disaggregatedand washed through a s 63-Wm sieve until a

clean foraminiferal residue was recovered, whichwas oven-dried at 50‡C. Planktonic foraminiferaltests are recrystallized, but preservation of testmorphology is very good. Population counts forplanktonic foraminifera are based on randomsample splits using a micro-splitter. From eachsample approximately 250^300 planktonic fora-minifera were picked from each of two size frac-tions (s 63 Wm and s 150 Wm Background DataSet1). Only the larger s 150-Wm size fraction ofthe uppermost meter of the section was analyzedfor this report; the smaller s 63-Wm size fractionwas studied by Keller et al. (2002). These twosize fractions were analyzed in order to obtainstatistically signi¢cant representations of thesmaller and larger species. At the same time,the quantitative study of two population splitsreduces the bias in ¢rst and last appearancesdue to the Signor^Lipps e¡ect (Signor and Lipps,1982). Species identi¢cations are based on de-scriptions of Smith and Pessagno (1973), Robas-zynski et al. (1984), Caron (l985) and Nederbragt(1991).

3. Biostratigraphy

In previous studies, the upper Maastrichtian oflow to middle latitude was generally assigned tothe Abathomphalus mayaroensis Zone (Caron,l985; Robaszynski and Caron, 1995). More re-cently, the interval spanning the last 200^300kyr has been assigned to the Plummerita hantke-ninoides Zone (Masters, l984; Pardo et al., 1996).Li and Keller (l998a) have further subdivided thelate Maastrichtian A. mayaroensis Zone based onCretaceous planktonic foraminiferal assemblagesand the paleomagnetic time scale of DSDP Site525A, and applied this chronology to the Tuni-sian sections at El Kef and Elles (Li and Keller,1998b). Their zonal scheme subdivides the lateMaastrichtian into four zones labeled CF1 toCF4 (CF = Cretaceous Foraminifera) as appliedin this study (Fig. 2).

1 http://www.elsevier.com/locate/palaeo

PALAEO 2753 1-5-02

S. Abramovich, G. Keller / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 145^164 147

3.1. Plummerita hantkeninoides zone(CF1, 65^65.3 Ma)

This zone is de¢ned by the total range of thenominate species. The zone was ¢rst de¢ned byMasters (1984), based on sections in Egypt. Pardoet al. (1996) calibrated the age and the duration ofthis zone as spanning the last 200^300 kyr of theMaastrichtian based on the paleomagnetic recordat Agost, Spain. At Elles, biozone CF1 spans thetop 9.6 m of the Maastrichtian. This thicknessrepresents the highest sedimentation rate (V3.2cm/1000 yr) measured to date for this biozone.In contrast, zone CF1 at El Kef is 6 m thick, atAgost in Spain 3.8 m, and at Hor Hahar in the

Negev, Israel, 8 m (Canudo et al., l99l ; Abramo-vich et al., 1998).

3.2. Pseudoguembelina palpebra zone(CF2, 65.3^65.45 Ma)

The base of this zone is de¢ned by the LA (lastappearance) of Gansserina gansseri, and the topby the FA (¢rst appearance) of Plummerita hant-keninoides. At Elles zone CF2 spans 12 m (from21.6 to 9.6 m) and represents the highest sedimen-tation rate (V8 cm/1000 yr) measured to date forthis interval. At the nearby El Kef section zoneCF2 is only 3 m thick due to a local fault thattruncates the base of the zone (Li and Keller,

Fig. 2. Later Maastrichtian planktonic foraminiferal biozonation used in this study and comparison with the zonations of Li andKeller (l998b) and Robaszynski and Caron (l995).

Fig. 3. Planktonic foraminiferal species census data at Elles arranged in order of last appearances. Note that two-thirds of theupper Maastrichtian species are rare and sporadically present. These are tropical to subtropical species with large complex mor-phologies. Among these species, extinctions are progressive with 17 species disappearing during the late Maastrichtian. Sedimentreworking is evident within the 50^100 cm below the K^T boundary where 12 of these species temporarily reappear.

PALAEO 2753 1-5-02


PALAEO 2753 1-5-02


1998b). Based on the paleomagnetic records atSite 525A and Agost, Zone CF2 spans about150 kyr (Li and Keller, 1998a), though this corre-lation is tentative and needs further calibration atother localities.

3.3. Pseudoguembelina hariaensis zone(CF3, 65.45^66.8 Ma)

This zone is de¢ned by the FA of Pseudoguem-belina hariaensis at the base and the LA of Gans-serina gansseri at the top. At the Elles section, theFA of P. hariaensis almost coincides with the LAof G. gansseri (20 cm below). The absence of theindex species may be interpreted as either repre-senting a hiatus, or ecological exclusion due toadverse environmental conditions. Since thereare no structural or sedimentological changes(fault, lithological changes, hardground, and bio-turbation), or abrupt faunal changes, indicative ofa hiatus, we prefer the latter explanation, thoughthe possibility of a hiatus cannot be excluded.This interpretation is supported by the rarity ofP. hariaensis in the part of its stratigraphic rangebelow Zone CF2, which was also observed at ElKef (Nederbragt, 1991; Li and Keller, 1998b).For this reason we have not subdivided ZonesCF3 and CF4 based on the FA of P. hariaensis.

3.4. Racemiguembelina fructicosa zone(CF4, 66.8^68.3 Ma)

This zone is de¢ned by the FA of Racemiguem-belina fructicosa at the base and the FA of Pseu-doguembelina hariaensis at the top. Only the upperpart of the Zone is included in this study. Thelower part of the zone was studied by Li andKeller (1998b).

4. Species ranges

The temporal range of a species is de¢ned fromits evolutionary ¢rst appearance to its last appear-ance or extinction. During its range, a species mayonly be intermittently or sporadically present, orhave a truncated range as compared with otherlocalities due to ecological, preservational or sed-

imentological factors. Outside its preferred habi-tat, ecological stress may result in shortened spe-cies ranges or sporadic occurrences. Species whichare rare and only sporadically present may not beencountered in standard biostratigraphic analysisand therefore result in bias towards shortenedspecies ranges, also known as the Signor^Lippse¡ect (Signor and Lipps, l982). But species rangesin the sediment record can also be biased towardsprolonged ranges beyond that of the biologicaloccurrence by bioturbation and reworking.

A total of 75 planktonic foraminiferal specieswere identi¢ed in upper Maastrichtian sedimentsat Elles. About 25 of these species have relativelycontinuous occurrences throughout the upperMaastrichtian (Fig. 3). They are generally abun-dant, small and simple morphotypes characteristicof ecological generalists that tolerate a wide rangeof environments across latitudes (e.g. hedbergell-ids, heterohelicids, guembelitrids). But two-thirdsof the species are only sporadically present andgenerally few in numbers. These species have gen-erally more complex morphologies (e.g. trochospi-ral, multiserial), narrow tolerance limits, and gen-erally restricted to lower latitude environments.Similar species range patterns were observed atEl Kef (Li and Keller, 1998b), and the Negev(Abramovich et al., 1998).

Of particular interest in the species census dataat Elles is the progressive disappearance of 17species (mostly globotruncanids) in the upperMaastrichtian preceding the K^T boundary ex-tinction event (e.g. Abathomphalus mayaroensis,Archaeoglobigerina blowi, Gansserina gansseri,Gansserina wiedenmayeri, Globotruncanita pettersi,Globotruncanita angulata, Globotruncana duepe-blei, Globotruncana falsostuarti, Globotruncana in-signis, Globotruncana ventricosa, Globigerinelloidesmultispina, Globotruncanella citae, Planoglobulinamulticamerata, Pseudoguembelina excolata, Rositacontusa, Rosita plicata, and Rosita wal¢shensis). Asimilar late Maastrichtian decrease in species rich-ness (presumably due to extinction or high stressenvironment) was observed at El Kef (Li and Kel-ler, 1998b) and the Negev (Abramovich et al.,1998). However, at Elles 12 of these species tem-porarily reappear in the uppermost meter of theMaastrichtian (upper Zone CF1, see Fig. 3), after

PALAEO 2753 1-5-02


prolonged absence. There are two likely explana-tions for this phenomenon. (1) The reappearanceof these species represents their true evolutionaryranges, whereas their observed early extinction isan artifact of rare species (e.g. Signor^Lipps ef-fect, rare and sporadic occurrences that could bemissed in the sample analyzed). This is a real pos-sibility for any environmentally sensitive speciesin stressed environments. (2) Sediment reworkingby currents and redeposition into younger sedi-ments is a very common way to produce the ob-served pattern of isolated species occurrences.

Though it is often di⁄cult to separate reworkedspecies, especially if reworking of extant species isinvolved, there are some clues, including poorpreservation as compared with in situ specimens,occurrences restricted to speci¢c intervals markedby bioturbation, hardground, and lithologicalchanges. In addition, reworked sediments gener-ally preserve large, robust and thick-shelled speci-mens as a result of transport and winnowing. Incontrast, isolated occurrences due to the Signor^Lipps e¡ect show no preservation preference ^large and small, fragile and robust specimens

Fig. 4. Planktonic foraminiferal species richness patterns of the late Maastrichtian at Elles, in terms of cumulative and non-cumu-lative species richness (black line marks ¢ve points running average). Non-cumulative species richness is further divided based onthree depth ranked foraminiferal groups: surface, intermediate, and deep dwellers. Cumulative species richness shows a gradualdecline with accelerated species extinctions during the last meter below the K^T boundary, and re£ects the evolutionary responseto global environmental stress. Non-cumulative species richness shows a decreasing trend with strong sinusoidal variations mainlywithin intermediate dwellers that re£ect the local response to changes in climate and watermass strati¢cation.

PALAEO 2753 1-5-02


Table 1Relative percent abundances of planktonic foraminifera in the 63^150-Wm size fraction at Elles, Tunisia

Depth (m) below the KTB 4.20 4.00 3.80 3.60 3.40 3.20 3.00 2.80 2.60 2.40 2.20 2.00 1.80 1.60 1.40 1.20Biozones CF1

A. blowiA. cretaceaGuembelitria cretacea 1 6 6 2 3 5 7 3 4 4 1 1 2 5 1 1G. trifolia 1 3 4 x 6 4 4 1 6 4 2 1 3 1 1Globigerinelloides aspera 1 2 x x 2 1 1 3 1 x 1 2 1 1 1 1G. prehillensis x 1 x x xG. volutus x 1 1G. subcarinatus 1 2 3 x 3 2 1 3 2 x x 1 x 1 1G. rosebudensis x x 2 1 1 1 1 1 x x 1G. multispinaG. yaucoensis 4 2 2 4 3 2 1 2 2 2 2 2 2 2 1 1Abathomphalus mayaroensisGlobotruncana aegyptica x 1 xG. orientalis x 1 x 1G. arca x 1 xG. esnehensis x xG. falsostuartiG. mariei x 1 x 1 xG. insignis xG. ventricosaG. rosetta x xGlobotruncanita conicaG. angulataG. pettersiG. stuartiG. stuartiformis xG. petaloidea x x x xG. citaeG. havanensis x 1 2 1 x x 1 x 1 1 xGublerina cuvilieri xG. acutaGansserina gansseriG. wiedenmayeriHedbergella 4 9 8 8 5 6 9 7 5 10 4 5 8 6 5 4L. glabrans 2 2 1 3 1 2 4 4 3 3 2 2 x 2 2 3H. globulosa 28 20 19 19 12 19 18 22 22 18 18 16 13 16 24 29H. carinata 6 2 4 4 1 4 1 4 5 3 4 3 3 4 4 5H. labellosa x x x 1 x x 1H. navarroensis 10 19 17 16 18 15 23 9 17 14 11 8 21 15 7 10H. dentata 15 15 15 11 19 11 15 15 14 14 21 25 30 23 28 13H. planata 1 1 1 2 2 x 1 1H. punctulataPlummerita hantkeninoides 1 x x x 1 xP. reicheliPseudoguembelina costulata 16 13 14 20 17 16 13 18 15 19 28 19 16 16 16 22P. hariaensis x 1 x x x 1P. kempensis 2 1 1 1 2 1 1 2 1 2 1 1 2 1 1 1P. palpebra x x x x xPseudotextularia deformis 1 x x xP. intermediaP. elegans x 1 1 1 2 x 1 x x x 1 1 1Rugoglobigerina hexacamerata 1 x 1 1 1 1 1 x x 1 2 x 1

PALAEO 2753 1-5-02


should be represented. Most of the suspect spe-cies, which are reappearing in the uppermostmeter at Elles well after their last continuousoccurrences, show characteristics of reworkedspecimens. In addition, ¢eld and laboratory sed-imentological and mineralogical observations in-dicate various features characteristic of reworkingand current transport, including cross-bedding,size gradation, and the presence of a foraminiferalpackstone (see Adatte et al., 2002). These featuresstrongly indicate that the reappearance of the sus-pect species (stippled interval, Fig. 3) is an artifactof sediment reworking.

5. Species richness

Species richness, or the number of speciespresent within a sample, is the simplest measureof diversity and an important tool for understand-ing £uctuations in the structure of an ecosystem.There are two measures of species richness: simplespecies richness and cumulative species richness.Simple species richness is the number of speciesphysically present in any given sample. It measuresthe species £ux in and out of a given ecosystem. Assuch it is a measure of ecological variability, ofclimatic changes, of short-term availability of nu-trients, of oxygen and salinity £uctuations. Inshort, it is an index of climatic, ecological, geo-graphic and overall environmental variability. Incontrast, cumulative species richness is the numberof species theoretically present in any given sample.It assumes that a species is present from its ¢rstevolutionary appearance to its extinction andignores any temporary absence in the sediment rec-

ord due to adverse environmental £uctuations.Cu mulative species richness thus expresses the evo-lutionary response of species to long-term changesin the environment over time.

5.1. Cumulative species richness

The cumulative species richness pattern at Ellesshows a gradual decline through the upper Maas-trichtian followed by accelerated species extinc-tions during the top 1 m below the K^T boundary(Fig. 4). The lower part of the section (lowerCF4^3 interval, part I) shows a diverse planktonicforaminiferal community with a maximum of 63species. This species community gradually de-creased to 53 species by the upper Zone CF2(part II). Species richness remained low duringthe transition between CF2 and CF1 (part III)and decreased by three species in the middle toupper Zone CF1 (part IV). A rapid decrease inspecies richness by 18 species occurred in theuppermost Maastrichtian, last meter below theK^T boundary (part V), followed by the extinc-tion of all remaining tropical and subtropical spe-cies at or near the K^T boundary (Fig. 4, Tables 1and 2 Background Data Set1). This cumulativespecies richness pattern re£ects the decreased evo-lutionary diversity during the late Maastrichtianand the accelerated rate of extinction approachingthe K^T boundary event. Similar patterns wereobserved from sections at El Kef and the Negev,Israel (Li and Keller, l998b; Abramovich et al.,l998). High biotic stress induced by rapidly chang-ing climatic conditions near the end of the Maas-tricthian are the likely causal factors for this spe-cies richness decrease (Li and Keller, l998c).

Table 1 (continued)

Depth (m) below the KTB 4.20 4.00 3.80 3.60 3.40 3.20 3.00 2.80 2.60 2.40 2.20 2.00 1.80 1.60 1.40 1.20Biozones CF1

R. macrocephala x xR. rotundataR. pennyiR. rugosa 2 2 1 1 1 3 1 2 1 1 2 4 x 3 3 3R. scotti x xx 1 1 x 1 x 1 1 1R. cf scottiTotal number counted 412 264 331 339 325 241 270 302 331 229 323 299 270 554 335 336

x = 6 1%, xx = very rare.

PALAEO 2753 1-5-02


Table 2Relative percent abundances of planktonic foraminifera in the size fraction s 150 Wm at Elles, Tunisia

Depth (m) below the KTB 0.18 0.13 0.08 0.04 0.03 0.02 0.01 0.00Biozones CF1

Archaeoglobigerina blowi x x x x xA. cretaceaGlobigerinelloides aspera 1 1 1 1 x 1G. prehillensis x 4 x xG. rosebudensis xG. multispinaG. subcarinatus x x 1 xG. volutusG. yaucoensis 2 x xAbathomphalus mayaroensisGlobotruncana aegyptica 1 1 1 1 x 1 2G. arca 2 2 3 2 3 5 5 7G. orientalis 3 1 1 1 2 3 2 2G. dupeublei x x x x x xG. esnehensis x 1 1 1 1 2 1 1G. ventricosa x 1 1 x x 1G. angulata x x 1G. falsostuarti x x x x 1G. mariei 4 3 1 1 2 3 3 2G. insignis x x x xG. rosetta 1 1 1Globotruncanita conica 1 x 1 1 1G. pettersi x x xG. stuarti x 1 1 x x 1 1G. stuartiformis 2 x 2 1 x 4 x 2G. petaloidea 1 1 1 1 x x x xG. citaeG. havanensis 3 1 2 3 2 3 3Gublerina cuvilieri 1 xGublerina acuta 1Gansserina gansseriG. wiedenmayeri x x x xHeterohelix globulosa 34 38 37 46 37 28 35 30H. punctulata x 1 x xH. labellosa 4 3 2 2 4 4 6 8L. glabrans 1 1 1 1 x xPlanoglobulina brazoensis x 1 1P. carseyae x 1 x 1P. acervulinoides x x xP. multicamerata x x x xPlummerita hantkeninoides x 1 xP. reicheli xPseudoguembelina costulata 5 8 7 6 4 2 3 4P. excolataP. hariaensis 3 3 2 4 5 4 3 2P. kempensis 1 x x 1 1 xP. palpebra 3 1 1 2 2 3 2 1Pseudotextularia deformis 3 1 3 3 6 7 7 7P. intermedia x 1 x 1 xP. elegans 8 7 12 8 8 6 4 4Racemiguembelina fructicosa 1 x x 1R. powelli 1 1 x 1 2 1 1

PALAEO 2753 1-5-02


5.2. Non-cumulative species richness(total number)

The non-cumulative species richness (totalnumber) shows a very di¡erent pattern fromthat of the cumulative species richness (Fig. 4).Where the latter shows a linear acceleration ofthe evolutionary decrease, the former shows a de-creasing trend with strong sinusoidal variations.The maximum species diversity (V50^54 species)is found in the lowermost part of the CF4^3 in-terval, but decreased rapidly to 37^40 species inthe upper CF4^3. In the lower part of Zone CF2,species richness values at ¢rst increased by sevenspecies, then decreased to 32^35 species in theupper CF2 to lower CF1 Zones. In the lower-middle CF1, species richness temporarilyincreased by ¢ve species, and then decreased rap-idly to 30^35 species towards the K^T boundaryprior to the extinction of all tropical and subtrop-ical forms (for changes across the K^T transitionsee Keller et al., 2002). These broad-based sinus-oidal variations likely re£ect changes in climateand watermass strati¢cation, though no climatedata based on stable isotopes are available atthis time.

5.3. Non-cumulative species richness(depth ranked)

More environmental information can be gained

by evaluating the non-cumulative species richnesspatterns based on groups living at speci¢c depthhabitats (e.g. surface mixed layer, intermediate orthermocline depth, and deep dwellers below ther-mocline, Fig. 4). Depth habitats of planktonicforaminifera, inferred from stable isotopic dataof individual species, provide a solid basis forreconstructing species life habitats and strati¢ca-tion of the water column (D’Hondt and Arthur,l995; Li and Keller, 1998b). Species richnessdepth habitat patterns show that surface anddeeper dwellers remained relatively stablethroughout the upper Maastrichtian. Though atthe end of the Maastrichtian (uppermost meter),the species richness of surface dwellers decreased.Thus, the non-cumulative diversity £uctuationsnoted above primarily occurred within the inter-mediate dwellers which lived within the thermo-cline layer. In today’s oceans a well-developedthermocline layer characterized by high produc-tivity supports the highest diversity of planktonicforaminifera. This is largely due to the high nu-trient content recycled from deeper waters, andhence an abundant food supply (e.g. phytoplank-ton and other zooplankton, Hemleben et al.,1989). The strength of the thermocline layer pri-marily depends on the temperature gradient andtherefore re£ects mostly climate and oceanic cir-culation. The depth ranked species richness curvesthus also re£ect signi¢cantly accelerating bioticstress induced by climate changes.

Table 2 (continued)

Depth (m) below the KTB 0.18 0.13 0.08 0.04 0.03 0.02 0.01 0.00Biozones CF1

Rosita contusa xR. patelliformisR. plicataR. wal¢schensis xRugoglobigerina hexacamerata 2 3 x 1 1 1 4 2R. miliamerensis x 1R. macrocephala 3 1 2 1 2 1 3 2R. rotundata 1 1 1 1 1R. pennyi x x 1R. rugosa 8 13 12 10 11 10 6 5R. scotti 5 3 2 4 3 2 4 5R. cf scotti 1Total number counted 314 351 330 312 309 269 272 293

x = 6 1%

PALAEO 2753 1-5-02


PALAEO 2753 1-5-02


6. Relative abundance changes

6.1. Heterohelicids

The planktonic foraminiferal populations of theupper Maastrichtian at Elles are typical of theTethyan pelagic upper slope and outer shelf envi-ronments (Figs. 5 and 6). Long-ranging biserialheterohelicid species dominate (generally s 70%)in the two size fractions analyzed (s 63 Wm ands 150 Wm). Heterohelicid populations in thesmaller (s 63 Wm) size fraction comprise mainlyfour species (Heterohelix globulosa, Heterohelixdentata, Heterohelix navarroensis, and Pseudo-guembelina costulata), whereas in the larger(s 150 Wm) size fraction three species dominate(H. globulosa, Pseudotextularia elegans, and Pseu-dotextularia deformis). Hence, with the exceptionof H. globulosa, heterohelicid species are speci¢cto the smaller size fraction. All other Maastrich-tian taxa are much less abundant, especially in thesmaller (s 63 Wm) size fraction (Fig. 5).

Within the heterohelicids of the s 63 Wm sizefraction, Heterohelix dentata gradually decreasedin the lower part of Zone CF2 (from V30% toV10%), and increased again towards the upperpart of CF1 (V30%). Pseudoguembelina costulatadecreased in the upper part of CF4^3 (V30 toV10%, Fig. 5), and increased again (V30%) inthe lower part of CF2. Heterohelix navarroensissigni¢cantly increased from the lower to the upperpart of CF4^3 (from V5% to V20%, Fig. 5). Therelative abundance of Heterohelix globulosa £uc-tuated in Zone CF4^3, and stabilized in CF2 withhigh average values of V40%. The terminal de-cline of H. globulosa began in the upper part ofCF1 (V20%). In the larger (s 150 Wm) size frac-tion the most signi¢cant biotic change within theheterohelicids is the sharp abundance decline ofPseudotextularia deformis in the upper part ofCF2 which coincided with the sharp increase inPseudotextularia elegans (Fig. 6).

6.2. Guembelitrids

Two separate Guembelitria blooms (G. cretaceaand G. trifolia) occurred in the upper Maas-trichtian as observed in the s 63-Wm size fraction(Fig. 5). The ¢rst Guembelitria bloom occurred inthe interval between the upper part of Zone CF4^3 and the lower part of Zone CF2, with the com-bined relative abundance of the two species reach-ing a maximum of 8.5% (see Fig. 7). The secondGuembelitria bloom occurred in Zone CF1 whereit reached a maximum level of 13.6%. Theseblooms are not observed at the nearby El Kefsection (Li and Keller, 1998b), probably due tothe lower sample resolution.

In previous studies of the Maastrichtian, Guem-belitria has been reported in low abundances inouter shelf and deep sea environments (D’Hondtand Keller, 1991; Keller, 1996), and relativelyhigh abundances in shallow shelf regions (e.g.Brazos River (Keller, 1989a,b), Stevns Klint(Schmitz et al., 1992), Seldja, Tunisia (Keller etal., 1998). High Guembelitria abundances in thepelagic marine environment have been describedso far only from the earliest Danian (Smit, 1982,1990; Keller and Benjamini, 1991; Schmitz et al.,1992; Keller et al., 1993, 1995; Pardo et al.,1996), and in the upper Maastrichtian of the Ne-gev (Abramovich et al., 1998).

Guembelitria are ecological opportunists as in-dicated by the very low N

13C values associatedwith the early Danian blooms that indicate adrastic reduction in primary productivity (Keller,1996; Keller et al., 2002). The presence of twoGuembelitria blooms in the upper Maastrichtianat Elles re£ects the instability of the planktonicpopulation structure at this time. The relativestrength of environmental stress is indicated bythe magnitude of the Guembelitria blooms. Bythis measure, the environmental stress at Elles islower than in the Negev where coeval Guembeli-tria blooms reached a maximum of V80% as

Fig. 5. Relative abundances of planktonic foraminifera in the smaller (s 63 Wm) size fraction at Elles. Note that only about ¢vespecies dominate the assemblages and four of these species are biserial morphotypes and the ¢fth is a hedbergellid. There areshort-term (Milankovitch) £uctuations and long-term trends. Intervals of environmental crises during the late Maastrichtian canbe identi¢ed based on two separate blooms of the opportunistic Guembelitria species (G. cretacea, and G. trifolia) in zones CF1and CF3^4.

PALAEO 2753 1-5-02


PALAEO 2753 1-5-02


compared with 13.6% at Elles (Abramovich et al.,1998). Thus the biotic response to the environ-mental stress induced by climatic perturbation indi¡erent parts of the Tethys may be of the samenature, but of di¡erent magnitude.

6.3. Globotruncanids

In the larger (s 150 Wm) size fraction, majorbiotic changes took place between the upperCF4^3 and the upper CF2 Zones when many glo-botruncanids decreased in relative abundance(Gansserina gansseri, G. wiedenmayeri, G. arca,G. orientalis, G. mariei, and G. havanensis,Fig. 6). This decrease demonstrates that the upperMaastrichtian decline of globotruncanids was ex-pressed not only by decreased species richness,but also by decreased population abundance. Asimilar decrease in globorotaliids was observedin the Negev sections, Israel (Abramovich et al.,1998). However, because globorotaliid are largespecies and generally few to rare, this decrease isnot evident when counting only the smaller (s 63Wm) size fraction (Fig. 5), and hence Li and Keller(1998b) who analyzed only the smaller size frac-tion, failed to note it.

Globotruncanids are usually regarded as inter-mediate to deep dwellers and geographically lim-ited to the Tethyan tropical^subtropical belt dur-ing the Cretaceous. All globotruncanid specieswere extinct before or at the K^T boundary.The limited distribution of globotruncanids andtheir characteristic complex morphologies illus-trate both their speci¢c requirements for stableundisturbed environmental conditions (mainlywell strati¢ed watermass with constant food sup-ply, and stable temperatures) and their specializedlife strategy as many modern analogous forms oftoday’s tropics indicate (Caron and Homewood,1983; Leckie, 1989; Keller et al., 1995; Keller,1996). Therefore, their decline during the lateMaastrichtian at Elles demonstrates biotic stress

induced by instability in the Tethyan tropic beltenvironment preceding the K^T boundary (Fig. 4).

7. Late Maastrichtian paleoenvironment in Tunisia

The biotic response to climatic perturbations isre£ected by relative abundance changes in speciespopulations, species census data and species rich-ness patterns (both cumulative and non-cumula-tive). At Elles all of these parameters show signi¢-cant variations during the late Maastrichtian anda progressively accelerating decrease in speciesrichness during the last 300 kyr of the Maastrich-tian. In addition, biotic stress is indicated by thedecline in relative abundances of dominant spe-cies, sporadic blooms of opportunistic species,and abundance £uctuations in populations oflong-ranging species. Interpreting these recordsin terms of speci¢c climate changes, such aswarm and cool events, variations in temperaturegradients and watermass strati¢cation, remains achallenge. In Tunisian sections, this task is furthercomplicated by oxygen isotope records of fora-minifera that are often compromised by diage-netic alteration and therefore allow no tempera-ture interpretations (e.g. El Kef, Keller andLindinger, l989).

To date, the most detailed and least diageneti-cally compromised stable isotope paleotempera-ture record for the late Maastrichtian is from mid-dle latitude DSDP Site 525A. This recordindicates that relatively cool temperatures pre-vailed during the ¢rst 3 Myr of the late Maas-trichtian (CF4^3 interval) with intermediate watertemperatures about 6^7‡C cooler than in the earlyMaastrichtian and surface temperatures cool butvariable (Li and Keller, l998a,c). This long-termcooling trend continued throughout the CF4^3interval and reached minimum temperatures inthe upper part of CF3 coincident with a hiatusat El Kef at 65.5 Ma (Li and Keller, 1998c). At

Fig. 6. Relative abundances of planktonic foraminifera in the larger (s 150 Wm) size fraction at Elles. Note that biserial taxa arestill dominant in this size fraction, but rugoglobigerinids are also common. Globotruncanids (mainly tropical complex morpholo-gies) are signi¢cantly more common than in the smaller size fraction, but decrease signi¢cantly near the top of CF3^4 and CF2.

PALAEO 2753 1-5-02


PALAEO 2753 1-5-02


Elles, the environmental parameters of planktonicforaminifera for the equivalent late Maastrichtianinterval (CF4^3) indicate a well-strati¢ed watercolumn characteristic of a cooler climate in whichdeeper water habitats are well populated, partic-ularly in the lower part of the CF4^3 interval.These conditions are mainly demonstrated bythe high species richness and the relative abun-dance of species with complex trochospiral shells(globotruncanids), and biserial species that inhab-it the intermediate to deeper waters (e.g. at orbelow the thermocline, Fig. 7). However, towardsthe upper part of the Zone CF4^3 interval globo-truncanids began to decline (from V30% toV20%, see Fig. 7) and species richness decreasedby 10 species, resulting in depleted intermediatewater communities (Fig. 4). This decline may re-£ect a decrease in water temperatures below theoptimal tolerance range for globotruncanid spe-cies. In general, the geographic restriction ofmost globotruncanid species to low latitudes, theirrelatively low abundance at middle latitudes, andnear absence in higher latitudes re£ects a narrowtemperature tolerance range. Alternatively, it ispossible that the onset of the subsequent warmingin CF2^1 (Li and Keller, l998a,c) began earlier inthe Tethys resulting in decreased thermal gra-dients and hence habitats for subsurface popula-tions. Stable isotope data of the eastern Tethysare still needed to evaluate which scenario ismost likely.

In middle to high southern latitudes, the long-term late Maastrichtian cooling was interruptedby a short-term warming of 3^4‡C in both surfaceand intermediate waters (e.g. Sites 690 and 525A,Barrera, 1994; Li and Keller, 1998a,c). Thiswarming began 450 kyr before the K^T boundary(base of Zone CF2), reached a maximum at 65.3Ma (base of Zone CF1) and ended 100 kyr beforethe K^T boundary (Li and Keller, 1998c). During

the last 100 kyr of the Maastrichtian temperaturesdropped rapidly, and returned to the previous lowlevel. The biotic e¡ect of this warm event on theTethyan ecosystem is well demonstrated at Elles(Fig. 7). Globotruncanids, which began to declinein the upper part of the CF4^3 interval, experi-enced another decline during the maximum warm-ing (lower to middle part of Zone CF1) whentheir combined relative abundance decreased byanother 10%, and the species richness decreasedby ca. ¢ve species. The same response was alsoobserved in the Negev sections (Abramovich etal., 1998). Heterohelix dentata (a biserial inter-mediate dweller) was also a¡ected by this event.During the warm interval the relative abundanceof this species decreased by V30%, and with thereturn to cooler temperatures the relative abun-dance increased again. The two species of the ge-nus Pseudotextularia (P. elegans, and P. deformis)also seem to respond to this climatic change.When the relative abundance of the surface dwell-er, P. deformis, decreased near the base of ZoneCF1, the relative abundance of the intermediatedweller P. elegans increased (Fig. 7). The £uctua-tion in the relative abundances of other majorspecies, such as Pseudoguembelina costulata, Ru-goglobigerina spp., Heterohelix navarroensis, andHedbergella spp., does not seem to correspond tomajor temperature changes.

It is interesting to note that some species, whichrespond in the same way to climatic changes, donot share the same habitat. Also, some speciesthat share the same habitat show opposite re-sponses to climatic changes. For example, boththe intermediate dwelling globotruncanids andthe surface dweller Pseudotextularia deformis de-clined during the maximum warming. But the in-termediate dweller Heterohelix globulosa increasedduring the warming, whereas the intermediatedweller Heterohelix dentata decreased. This dem-

Fig. 7. Summary of relative abundances of dominant planktonic foraminiferal species and genera from the two size fractions(s 150 Wm and s 63 Wm) at Elles. Abundance changes re£ect planktonic foraminiferal response to climatic instability. Shaded in-terval marks the late Maastrichtian warm event (age estimate based on biostratigraphic correlation with the warm event at Site525A, Li and Keller, 1998c). Note the species turnover within the biserial population in response to the warm event; the biserialspecies Heterohelix dentata, and Pseudotextularia deformis decreased, whereas the biserial species Heterohelix globulosa, Pseudotex-tularia elegans and Pseudotextularia costulata increased. Globotruncanids also decreased preceding and during the warm event.

PALAEO 2753 1-5-02


onstrates that a given change in the environmentcan have di¡erent e¡ects on species that share thesame habitat depth zone. Consequently, speciesthat inhabit the same depth habitats do not nec-essarily have the same requirements for resources,or the same tolerance for environmental changes.For example, the intermediate dwelling heterohe-licids are considered to have a high tolerance forlow oxygen conditions (Premoli Silva and Boers-ma, l989; Keller, 1993; Barrera and Keller, 1994),but intermediate dwelling globotruncanids clearlydo not, they decrease or disappear during times ofexpanded low oxygen conditions (e.g. Almogi-La-bin et al., 1993). The small triserial Guembelitria,best known as disaster species that thrived afterthe mass extinction of tropical and subtropicalspecies at the K^T boundary, generally thrivedat times of major biotic stress associated withmajor climate transitions. In addition to the K^T boundary, two blooms of these disaster specieswere observed during the upper Maastrichtian atElles and in the eastern Tethys (Abramovich etal., l998).

8. Conclusions

Upper Maastrichtian planktonic foraminiferalassemblages at Elles reveal major faunal turnoversthat re£ect the global long-term climate coolingfollowed by rapid and extreme warming between200 and 400 kyr before the K^T boundary, and areturn to a cooler climate during the last 100 kyrof the Maastrichtian. Although there are still fewstudies that evaluate the association of speci¢cCretaceous species with particular environmentalchanges, preliminary results are encouraging andpromise that this approach will reveal much aboutthe environmental changes and biotic stresses thataccompany major climate transitions.

From the Elles study a number of preliminaryconclusions can be reached.

(1) Cumulative species richness data (totalnumber of species living), which re£ect evolution-ary trends, show a gradual decrease in diversitythrough the last 3 Myr of the Maastrichtian witha rapid decrease during the last 100 kyr of theMaastrichtian.

(2) Non-cumulative species richness data (ac-tual number of species present), which re£ect en-vironmental changes, show major broad-based£uctuations that mirror climate changes and asso-ciated variations in ocean circulation, thermalgradients and watermass strati¢cation. The Ellesrecords indicate that environmental changes wereparticularly strong during the last 500 kyr of theMaastrichtian.

(3) Non-cumulative depth ranked (surface, in-termediate, deep dwellers) species richness datareveal the particular habitat most severely a¡ectedby ongoing climate and environmental changes.At Elles, the intermediate dwellers living withinthermocline depths drove both the long-term evo-lutionary trends and the response to short-termenvironmental changes. Surface and deeper dwell-er groups remained relatively stable.

(4) Species census data (individual speciesranges) also reveal environmental £ux. At Elles,17 species (intermediate dwellers) gradually disap-peared during the upper Maastrichtian and re£ectthe increasing environmental stress during the last2 Myr of the Cretaceous.

(5) Globotruncanids are the most sensitive in-dicators of Maastrichtian climate changes. Thisgroup of thermocline dwellers (intermediate)thrived during relatively cool climates and awell-strati¢ed water column. But their tempera-ture tolerance limit is relatively low and they areprone to extinctions when temperatures are eithertoo cool or too warm.

(6) Guembelitrids are useful indicators for en-vironmental extremes and high biotic stress, par-ticularly at transitions from warm to cold climatesand vice versa. During these times, Guembelitriaspecies responded with opportunistic blooms thatre£ect the high stress and unstable planktonicpopulation structure.

Acknowledgements

We gratefully acknowledge Dr. Ben Haj Ali,Director of the Geological Survey of Tunisia, andDr. Ben Salem for their tremendous logistical andtransportation support for the field excursion andWorkshop of May l998. Fieldwork was done

PALAEO 2753 1-5-02


jointly with Thierry Adatte and Wolfgang Stin-nesbeck and we gratefully acknowledge theircollaboration and discussions. We thank thereviewers Francis Robaszynski and one anon-ymous reviewer for their helpful comments, andChaim Benjamini for discussions. This study wassupported by NSF-INT 95-04309.

References

Abramovich, S., Almogi-Labin, A., Benjamini, C., 1998. De-cline of the Maastrichtian pelagic ecosystem based onplanktic foraminiferal assemblage changes: Implicationsfor the terminal Cretaceous faunal crisis. Geology 26, 63^66.

Adatte, T., Keller, G., Li, L., Stinnesbeck, W., Zaghbib-Turki,D., 1998. Climate and sea level £uctuations across the K^Tboundary in Tunisia: Warm and humid conditions linked tothe Deccan volcanism? In: International Workshop on Cre-taceous^Tertiary Transition, O⁄ce National des Mines, Di-rection du Service Ge¤ologique, Tunis, l998, Abstracts, pp. 7^10.

Adatte, T., Keller, G., Stinnesbeck, W., 2002. Late Cretaceousto Early Paleocene climate and sea-level £uctuations. Pa-laeogeogr., Palaeoclimatol., Palaeoecol. (this volume).

Almogi-Labin, A., Bein, A., Sass, E., 1993. Late Cretaceousupwelling system along the southern Tethys margin (Israel):Interrelationship between productivity, bottom water envi-ronments, and organic matter preservation. Paleoceanogra-phy 8, 671^690.

Appellaniz, E., Baceta, J.I., Benrnaola-Bilbao, G., Nunez-Be-lelu, K., Orue-Etxebarria, X., Payros, A., Pujalte, V., Robin,E., Rocchia, R., 1997. Analysis of uppermost Cretaceous-lowermost Tertiary hemipelagic successions in the BasqueCountry (western Pyrenees): evidence for a sudden extinc-tion of more than half planktic foraminiferal species at theK/T boundary. Bull. Soc. Geol. France 168 (6), 783^793.

Barrera, E., 1994. Global environmental changes preceding theCretaceous^Tertiary boundary: Early^upper Maastrichtiantransition. Geology 22, 877^880.

Barrera, B., Keller, G., 1994. Productivity across the Creta-ceous/Teriary boundary in high latitudes. Geol. Soc. Am.Bull. 106, 1254^1266.

Barrera, E., Savin, S.M., Thomas, E., Jones, C.E., 1997. Evi-dence for thermohaline-circulation reversals controlled bysea-level change in the latest Cretaceous. Geology 25, 715^718.

Barrera, E., Savin, S.M., 1999. Evolution of late Campanian^Maastrichtian marine climates and oceans. In: Barrera, E.,Johnson, C.C. (Eds.), Evolution of the Cretaceous Ocean-Climate System. Geological Society of America Special Pa-per 332, Boulder, CO, pp. 245^282.

Bensalem, H., 1998. The El Haria Tunisian K/T transitionserie: Bibliographic survey. In: International Workshop onCretaceous^Tertiary Transition, O⁄ce National des Mines,

Direction du Service Ge¤ologique, Tunis, l998, Abstracts, pp.11^13.

Burollet, P.F., 1967. General geology in Tunisia. In: Martin,L. (Ed.), Guidebook to the geology history of Tunisia, Pe-troleum Exploration Society of Libya, 9th Annual FieldConference, 67 pp.

Canudo, J.I., Keller, G., Molina, E., 1991. Cretaceous/Teriaryboundary extinction pattern and faunal turnover at Agostand Caravaca, SE Spain. Mar. Micropaleontol. 17, 319^341.

Caron, M., 1985. Cretaceous planktic foraminifera. In: Bolli,H.M., Saunders, J.B., Perch-Nielsen, K. (Eds.), PlanktonStratigraphy. Cambridge University Press, Cambridge, pp.17^86.

Caron, M., Homewood, P., 1983. Evolution of early plankticforaminifers. Mar. Micropaleontol. 7, 453^462.

D’Hondt, S., Keller, G., 1991. Some patterns of planktic fo-raminiferal assemblage turnover at the Cretaceous^Tertiaryboundary. Mar. Micropaleontol. 17, 77^118.

D’Hondt, S., Arthur, M.A., 1995. Interspecies variation instable isotopic signals of Maastrichtian planktonic forami-nifera. Paleoceanography 10, 123^135.

Hemleben, C., Spindler, M., Anderson, O.R., 1989. ModernPlanktonic Foraminifera. Springer Verlag, New York.

Huber, B.T., 1992. Paleobiogeography of Campanian^Maas-trichtian foraminifera in the southern high latitudes. Pa-laeogeogr. Palaeoclimatol. Palaeoecol. 92, 325^360.

Keller, G., 1988. Extinction, survivorship and evolution ofplalnktic foraminifera across the Cretaceous/Teriary bound-ary at El Kef Tunisia. Mar. Micropaleontol. 13, 239^263.

Keller, G., 1989a. Extended period of extinctions across theCretaceous/Teriary boundary in planktonic foraminifera ofcontinental shelf section: Implications for a impact and vol-canism theories. Geol. Soc. Am. Bull. 101, 1408^1419.

Keller, G., 1989b. Extended Cretaceous/Teriary boundary ex-tinctions and delayed population change in planktonic fora-minifera from Brazos River, Texas. Paleoceanography 4,287^332.

Keller, G., Lindinger, M., 1989. Stable isotopes, TOC andCaCO3 records across the Cretaceous-Tertiary boundaryat El Kef, Tunisia. Palaeogeogr. Palaeoclimatol. Palaeoecol.73, 243^265.

Keller, G., Benjamini, C., 1991. Paleoenvironment of the east-ern Tethys in the Early Paleocene. Palaios 6, 439^464.

Keller, G., 1993. The Cretaceous/Teriary boundary transitionin the Antarctic Ocean and its glocal implications. Mar.Micropaleontol. 21, 1^45.

Keller, G., Barrera, E., Schmitz, B., Matsson, E., 1993. Grad-ual mass extinction, species survivorship, and long term en-vironmental changes across the Cretaceous-Teriary boun-dariy in high latitudes. Geol. Soc. Am. Bull. 105, 979^997.

Keller, G., Li, L., MacLeod, N., 1995. The Cretaceous/Terti-ary boundary stratotype section at El Kef, Tunisia: Howcatastrophic was the mass extinction? Palaeogeogr. Pa-laeoclimatol. Palaeoecol. 119, 221^254.

Keller, G., 1996. The K/T mass extinction in planktic foramin-ifera biotic constraints for catastrophe theories. In: Mac-Leod, N., Keller, G. (Eds.), The Cretaceous^Tertiary Mass

PALAEO 2753 1-5-02


Extinction: Biotic and Environmental Changes. W.W. Nor-ton, New York, pp. 63^100.

Keller, G., Adatte, T., Stinnesbeck, W., Stuben, D., Kramar,U., Berner, Z., Li, L., vonSalisPerch-Nielsen, K., 1997. TheCretaceous^Teriary transition on the shallow Sharan plat-form of southern Tunisia. Geobios 30, 951^975.

Keller, G., Adatte, T., Stinnesbeck, W., Stuben, D., Kramar,U., Berner, Z., Li, L., von Salis Perch-Nielsen, K., 1998. TheCretaceous-Tertiary transition on the shallow Sharan plat-form of southern Tunisia. Geobios 30 (7), 951^975.

Keller, G., Adatte, T., Stinnesbeck, W., Luciani, V., Karoui,N., Zaghbib-Turki, D., 2002. Paleoecology of the Creta-ceous-Tertiary mass extinction in planktic foraminifera. Pa-laeogeogr. Palaeoclimatol. Palaeoecol. 178, 257^259.

Leckie, R.M., 1989. A paleogeographic model for the earlyevolutionary history of planktonic foraminifera. Palaeo-geogr. Palaeoclimatol. Palaeoecol. 73, 107^138.

Li, L., Keller, G., 1998a. Maastrichtian climate productivityand faunal turnovers in planktic foraminifera in South At-lantic DSDP Sites 525A and 21. Mar. Micropaleontol. 33,55^86.

Li, L., Keller, G., 1998b. Diversi¢cation and extinction inCampanian^Maastrichtian planktic foraminifera of North-western Tunisia. Ecl. Helv. 91, 75^102.

Li, L., Keller, G., 1998c. Abrupt deep-sea warming at the endof the Cretaceous. Geology 26, 995^999.

Li, L., Keller, G., Stinnesbeck, W., 1999. The Late Campanianand Maastrichtian in northern Tunisia: palaeoenvironmen-tal inferences from lithology, macrofauna and benthic fora-minifera. Cretac. Res. 20, 231^252.

Li, L., Keller, G., Adatte, T., Stinnesbeck, W., 2000. LateCretaceous sea level changes in Tunisia: A multi-disciplinaryapproach. J. Geol. Soc. London 2, 447^458.

Luciani, V., 1997. Planktonic foraminiferal turnover across theCretaceous^Teriary boundary in the Vajont valley (SouthernAlps, northern Italy). Cretac. Res. 18, 799^821.

Masters, B.A., 1984. Comparision of planktonic foraminifersatthe Cretaceous-Teriary boundary from the El Haria shale(Tunisia) and the Esna shale (Egypt). Proceedings of the7th Exploration Seminar, March, 1984, Cairo, Egypt. Egyp-tian General Petroleum Corporation, Cairo, pp. 310^324.

Molina, E., Arenillas, I., Arz, J.A., 1998. Mass extinction inplanktic foraminifera at the Cretaceous^Tertiary boundaryin subtropical and temperate latitudes. Bull. Soc. Geol.France 169, 351^372.

Nederbragt, A., 1991. Late Cretaceous biostratigraphy and

development of Heterohelicidae (planktic foraminifera). Mi-cropaleontology 37, 329^372.

Olsson, R.K., Liu, C., 1993. Controversies on the placement ofthe Cretaceous^Paleogene boundary and the K/T mass ex-tinction of planktonic foraminifera. Palaios 8, 127^139.

Pardo, A., Ortiz, N., Keller, G., 1996. Latest Maastrichtianforaminiferal turnover and its environmental implicationsat Agost, Spain. In: MacLeod, N., Keller, G. (Eds.), Creta-ceous^Tertiary Boundary Mass Extinction: Biotic and En-vironmental Changes. W.W. Norton, New York, pp. 139^172.

Premoli Silva, I., Boersma, A., 1989. Atlantic Paleogene plank-tonic foraminiferal bioprovincial indices. Mar. Micropaleon-tol. 14, 357^371.

Robaszynski, F., Caron, M., Gonzales Donoso, J.M., Won-ders, A.A.H., 1984. Atlas of Late Cretaceous Globotrunca-nids. Rev. Micropale¤ontol. 26, 145^305.

Robaszynski, F., Caron, M., 1995. Foraminife'res planctoni-ques du Cre¤tace: Commentaire de la zonation Europe-Me¤d-iterrane¤. Bull. Soc. Geol. France 166, 681^692.

Salaj, J., 1980. Microbiostratigraphie du Cre¤tace¤ et du Pale¤o-ge'ne de la Tunisie septentrionale et orientale (Hypostrato-types tunisiens). Institut Geologique de Dionyz Stu¤ra, Bra-tislava.

Schmitz, B., Keller, G., Stenvall, O., 1992. Stable isotope andforaminiferal changes across the Creatceous-Teriary bound-ary at Stevns Klint, Denmark: Arguments for long termoceanic instability before and after bolide impact event. Pa-laeogeogr. Palaeoclimatol. Palaeoecol. 96, 233^260.

Signor, P., Lipps, J., 1982. Sampling bias, gradual extinctionpatterns and catastrophes in the fossil record. In: Sliver,L.T., Schultz, P.H. (Eds.), Geological Implications of Im-pacts of Large Asteroids and Comets on the Earth. Geo-logical Society of America, Special Paper 190, Boulder, CO,pp. 291^296.

Smit, J., 1982. Extinction and evolution of planktic forami-nifera after a major impact at the Cretaceous/Tertiaryboundary. Earth Planet. Sci. Lett. 74, 155^170.

Smit, J., 1990. Meteorite impact, extinctions and the Creta-ceous/Tertiary boundary. Geol. Mijnb. 69, 187^204.

Smith, C.C., Pessagno, E.A., Jr., 1973. Planktonic foraminiferaand stratigraphy of Corsicana Formation (Maastrichtian),north-central Texas. Contribution from the Cushman Foun-dation for Foraminiferal Research, Special Publication 12,5^66.

PALAEO 2753 1-5-02


Documents

High stress late Maastrichtian paleoenvironment: inference