The response of benthic foraminifera to the K–Pg boundary biotic crisis at Elles (northwestern Tunisia)

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Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157 – 180 www.elsevier.com/locate/palaeo

The response of benthic foraminifera to the K–Pg boundary biotic crisis at Elles (northwestern Tunisia) Rodolfo Coccioni ⁎, Andrea Marsili Istituto di Geologia e Centro di Geobiologia dell'Università, Campus Scientifico, Località Crocicchia, I-61029 Urbino, Italy Received 16 January 2006; accepted 14 February 2007

Abstract The high-resolution quantitative study of benthic foraminifera from the Elles section (NW Tunisia) that contains one of the most complete Cretaceous–Paleogene (K–Pg) boundary transition and spans about 357 kyr provides detailed data on the palaeoenvironmental turnover across the K–Pg boundary. Benthic foraminifera indicate outer neritic-uppermost bathyal depths without perceivable bathymetrical changes throughout. Uppermost Maastrichtian assemblages are well preserved and highly diversified, indicating stable environment and mesotrophic to weakly eutrophic conditions during the latest Cretaceous. Benthic foraminifera underwent a major faunal turnover in coincidence with the K–Pg boundary, where a dramatic and sudden decrease in the percentage of both infaunal morphogroups and buliminids, as well as in diversity, heterogeneity, and genus and species richness of the assemblages, are recorded indicating overall oligotrophic conditions. Benthic foraminifera do not show significant extinction at the end of the Cretaceous, with only about 3% of the species clearly becoming extinct together with the temporary disappearance of some taxa. A stepped pattern of faunal recovery and restructuring is recognizable during the lowermost Danian reflecting the gradual restabilization of the environmental conditions after the K–Pg boundary event. The nature and the abundance of food supply to the sea floor conditioned the faunal turnover in the earliest Paleogene which reflects not only a sudden collapse of the food web due to the extinction of calcareous primary producers, but also a major, rapid change in composition and abundance of food supply just after the K–Pg boundary. Short-term blooms of some opportunistic species within the G. cretacea Zone and the lowermost part of the Ps. pseudobulloides Zone would reflect instability in the benthic assemblages that might be related to the transfer to the sea floor of food supply not easily used by the benthos through short-term, large blooms or changes in abundance of opportunistic, various phytoplankton groups. The major environmental instability at the sea floor that just follows the K–Pg boundary event may have been thus related to changes in the phytoplankton composition and abundance and would have taken place over a period of about 25 kyr. Benthic foraminiferal assemblages appear to stabilize in the lowermost part of Zone Ps. pseudobulloides (∼65 kyr after the K–Pg boundary event). The sea floor ecosystem, at least at outer neritic-uppermost bathyal depths, may have recovered over a considerably shorter period than commonly suggested, even if the food delivery to the sea floor had not fully recovered the pre-K–Pg levels as indicated by the lower percentages of infaunal morphogroups and buliminids. This would be also in agreement with the rapid recovery of terrestrial ecosystems following the biotic crisis at the K–Pg boundary. The drastic change of benthic foraminiferal assemblages coincident with the K–Pg boundary at Elles and their staggered reorganization during the lowermost Paleogene are largely compatible with the catastrophic effects of a huge asteroid impact on Earth at the K–Pg boundary that severely destabilized the oceanic phytoplankton-based food web. © 2007 Elsevier B.V. All rights reserved. Keywords: Benthic foraminifera; K–Pg boundary; Palaeoecology; Palaeoenvironment; Palaeoproductivity; Tunisia

⁎ Corresponding author. Tel.: +39 0722 304237. E-mail address: [email protected] (R. Coccioni). 0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2007.02.046

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1. Introduction Benthic foraminifera are an important source of information about environmental conditions at the sea floor, such as ocean productivity and oxygenation (e.g., Van der Zwaan et al., 1999). In addition to being excellent palaeobathymetric markers, the abundance of some depth-related species, as well as the upper depth-limits of others, allow us to infer possible changes in palaeodepth (e.g., Van Morkhoven et al., 1986). Benthic foraminifera thus constitute an important tool for reconstructing palaeoenvironmental changes at the Cretaceous–Tertiary (K–Pg) boundary. In the last years, a growing number of papers focusing on benthic foraminifera at the K–Pg boundary clearly showed that this group, in contrast to planktonic foraminifera and calcareous nannoplankton, did not suffer major extinction, but only temporary faunal restructuring of different extent followed by at least partial recovery as

observed in different regions and settings (e,g., Keller, 1988; Thomas, 1990a,b; Keller, 1992; Kaiho, 1992; Widmark and Malmgren, 1992a; Coccioni et al., 1993; Kuhnt and Kaminski, 1993; Coccioni and Galeotti, 1994; Speijer, 1994; Speijer and Van der Zwaan, 1996; Peryt et al., 1997; D'Hondt et al., 1998; Kouwenhoven, 2000; Alegret et al., 2001, 2002a,b,c; Peryt et al., 2002; Alegret et al., 2003; Culver, 2003; Alegret et al., 2004a,b; Peryt et al., 2004; Alegret and Thomas, 2004, 2005; Molina et al., 2005). The temporary, drastic changes in community structure coincident with the K–Pg boundary, followed by a gradual, staggered pattern of recovery across the early Danian (see also Culver, 2003, for a review) have been interpreted as resulting from the collapse of the pelagic food web and a subsequent drop in food supply to the benthos (e.g., Thomas, 1990a,b; Kuhnt and Kaminski, 1993; Alegret et al., 2001, 2002a,b,c, 2003; Culver, 2003). However, there appear to be considerable

Fig. 1. Palaeogeographic sketch of Tunisia at K−Pg time with location of the main K−Pg boundary sections indicated by diamonds and their palaeodepth (modified after Galeotti and Coccioni, 2002).

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regional differences in the effect of the K–Pg event on the flux of flood to the sea floor (e.g., Culver, 2003; Alegret and Thomas, 2005). In order to expand the existing database and to provide available information that may help elucidating the nature, causes, and way of the benthic foraminiferal turnover as well as the changes in oceanic enviroments across the K–Pg boundary, a high-resolution quantitative analysis of uppermost Maastrichtian and lowermost Danian benthic foraminiferal assemblages has been carried out at Elles (northwestern Tunisia) (Fig. 1), one of the best exposed and most complete K–Pg boundary sections. This detailed study, following previous investigations (Said, 1978; Venturati, 2000; Zaghbib-Turki et al., 2001), provides palaeobathymetric information on

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the uppermost Cretaceous and lowermost Paleogene sediments, documents and describes the benthic foraminiferal turnover across the K–Pg transition, and infers palaeoenvironmental changes and their duration. 2. Location and stratigraphy The Elles section (Karoui-Yaakoub, 1999) is located in the Tunisian Central Atlas (to the north of the Kasserine Island), 75 km southeast of the K–Pg Global Boundary Stratotype Section and Point (GSSP) at El Kef (Fig. 1). The section occurs in on the right side of the valley cut by the Karma river, near the hamlet of Elles, where sediments spanning from Campanian to lower Eocene (Abiod, El Haria and Metlaoui Formations: see

Fig. 2. Stratigraphy and relative abundances of the calcareous benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). Planktonic foraminiferal (PF) Zones after Keller et al. (1995), Pardo et al. (1996), Arz and Molina (2002), and Arenillas et al. (2004). Calcareous nannofossil (CN) Zones after Martini (1971). Estimated time span follows Arenillas et al. (2004) and Gradstein et al. (2004). G.c. = Guembelitria cretacea; Pv. = Parvulorugoglobigerina; Ps. = Parasubbotina.

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Bensalem, 2002) are widely exposed (Karoui-Yaakoub et al., 2002). The K–Pg boundary transition, occurring within the El Haria Formation, is exposed in numerous outcrops and can be traced over hundred of metres along the slopes of the valley. The Elles section contains one of the most complete K–Pg boundary transition in Tunisia. If compared to the K–Pg GSSP and El Kef II sections, the Elles section displays a better exposure of the K–Pg boundary transition even if with a similar stratigraphic record (Zaghbib-Turki et al., 2000, Karoui-Yaakoub et al., 2002). For these reasons the section studied has been proposed as parastratotype or even as new stratotype of the K–Pg boundary (Zaghbib-Turki et al., 2000, 2001; Karoui-Yaakoub et al., 2002).

The Elles section mostly consists of marly and clayey sediments (CaCO3 content between 30% and 60%) interrupted at the K–Pg boundary by a dark, ∼50-cmthick CaCO3-depleted interval (b10%), the so-called boundary clay layer (Adatte et al., 1998; Stinnesbeck et al., 1998). The K–Pg boundary is located at the base of the boundary clay layer where a 3–4 mm-thick rusty red layer, rich in Fe-oxides, and embedded between two gypsum-jarosite layers of late diagenetic origin occurs. This layer also contains cosmic markers such as an anomalous concentration in Ir, Ni-rich spinels, and altered microtektites (Robin et al., 1998; Zaghbib-Turki et al., 2000). The palaeogeographic setting of the Elles section is similar to that of the El Kef section, both localities

Fig. 3. Stratigraphy and relative abundances of the calcareous benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). Planktonic foraminiferal (PF) Zones after Keller et al. (1995), Pardo et al. (1996), Arz and Molina (2002), and Arenillas et al. (2004). Calcareous nannofossil (CN) Zones after Martini (1971). Estimated time span follows Arenillas et al. (2004) and Gradstein et al. (2004). G.c. = Guembelitria cretacea; Pv. = Parvulorugoglobigerina; Ps. = Parasubbotina.

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situated on the continental shelf. Elles section is located in a slightly more proximal position than El Kef section with a generally higher terrigenous influx (Adatte et al., 2002) (Fig. 1). According to Adatte et al. (2002), Elles and El Kef sections have comparable sediment records: a sedimentation rate of 4 cm/1000 yr (at least for the Maastrichtian) was in fact calculated, based on biostratigraphic correlation with Deep Sea Drilling Project Site 525 and palaeomagnetic data from the same site (Li and Keller, 1998). The stratigraphic interval studied extends from 6 m below to 6 m above the K–Pg boundary, covering the uppermost Mastrichtian.Lowermost Danian. From a biostratigraphic point of view, at Elles the range of Plummerita hantkeninoides spans the last 7 m of the

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Maastrichtian (Karoui-Yaakoub et al., 2002; Keller et al., 2002). Parvularugoglobigerina longiapertura, Parvularugoglobigerina eugubina, and Parasubbotina pseudobulloides have their first occurrences (FOs), respectively, at 20–25 cm, 40–45 cm, and 2 m above the K–Pg boundary (Figs. 2–9). The last occurrence of Pv. eugubina at 6 m above the K–Pg boundary is nearly coincident with the FOs of Parasubbotina varianta, Subbotina triloculinoides, and Praemurica inconstans. Therefore, the stratigraphic interval studied comprises most of the Plummerita hantkeninoides (CF1) Zone of Pardo et al. (1996) and the P0 and P1a Zones of Keller et al. (1995), that is the Guembelitria cretacea and the Parvularugoglobigerina eugubina Zones, and the lowermost part of the Parasubbotina pseudobulloides Zone

Fig. 4. Stratigraphy and relative abundances of the calcareous benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). Planktonic foraminiferal (PF) Zones after Keller et al. (1995), Pardo et al. (1996), Arz and Molina (2002), and Arenillas et al. (2004). Calcareous nannofossil (CN) Zones after Martini (1971). Estimated time span follows Arenillas et al. (2004) and Gradstein et al. (2004). G.c. = Guembelitria cretacea; Pv. = Parvulorugoglobigerina; Ps. = Parasubbotina.

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Fig. 5. Stratigraphy and relative abundances of the calcareous benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). Planktonic foraminiferal (PF) Zones after Keller et al. (1995), Pardo et al. (1996), Arz and Molina (2002), and Arenillas et al. (2004). Calcareous nannofossil (CN) Zones after Martini (1971). Estimated time span follows Arenillas et al. (2004) and Gradstein et al. (2004). G.c. = Guembelitria cretacea; Pv. = Parvulorugoglobigerina; Ps. = Parasubbotina.

of Arz and Molina (2002) and Arenillas et al. (2004) (Figs. 2–9). The FO of Ps. pseudobulloides marks the P1a(1)/P1a(2) zonal boundary of Keller et al. (1995). The occurrence of a short hiatus or a condensed interval, spanning from Zone P1b to the lower part of SubZone P1c(2), appears rather reasonable and well fits with similar findings from the Tunisian sections (see also Keller, 1988; MacLeod and Keller, 1991; KarouiYaakoub et al., 2002). According to the most recent estimates (Mukhopadhyay et al., 2001; Arenillas et al., 2004; Berggren and Pearson, 2005; Arenillas et al., 2006) of the duration of planktonic foraminiferal Zones and subZones from the K–Pg boundary transition, the stratigraphic interval studied would span the last 257 kyr of the Cretaceous and the first 100 kyr of the Paleogene.

The deposition of the 3–4 mm thick ejecta layer occurred over an instantaneous geological time period. The FOs of P. longiapertura, Pv. eugubina, and Ps. pseudobulloides are placed at 6 kyr, 20 kyr, and 60 kyr, respectively (Figs. 2–9). 3. Materials and methods A total of 34 samples was collected and analysed from the section studied with sampling interval increasing near the K–Pg boundary (Figs. 2–9 and Supplementary Table). In the uppermost Maastrichtian samples were spaced at 1 m from −6 m to −1 m and at 10 cm from −60 cm to −10 cm, respectively. A total of 7 samples (−10/−5 cm, −5/−2 cm, −2/0, 0/+0.4 cm,

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Fig. 6. Stratigraphy and relative abundances of the agglutinated benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). See Fig. 2 for explanation.

+0.4/+1 cm, +1/+5 cm, +5/+10 cm) was collected from the interval spanning 10 cm below and 10 cm above the K–Pg boundary. Samples from the lowermost Danian were spaced at 10 cm from +10 cm to +60 m, at 50 cm from +1 m to +5 m, and at 1 m from +5 m to +6 m, respectively (Figs. 2–9). Samples were gently crushed and disaggregated with diluted hydrogen peroxide or with Desogen, then washed through a 32 μm sieve and dried at 50 °C. A representative split of the ≥63 μm fraction, containing at least 300 specimens, was used for quantitative studies and species richness calculations. Benthic foraminifera are abundant and well preserved in the studied material except for the first two samples overlying the barren thin rusty red layer at the base of the boundary clay layer, where specimens are scarce and poorly preserved. All specimens were picked, identified,

counted and mounted on microslides for a permanent record. The classification at the generic level largely follows Loeblich and Tappan (1988) and at the specific level largely follows the taxonomy of Tjalsma and Lohmann (1983), Keller (1988), Widmark and Malmgren (1992a,b), Bolli et al. (1994), Speijer (1994), Speijer and Van der Zwaan (1996), Widmark (1997), Widmark and Speijer (1997a,b), Alegret and Thomas (2001), and Kaminski and Gradstein (2005). A complete list of the recognised taxa is reported in Appendix A. A total of twenty-seven agglutinated and fifty-five calcareous-hyaline genera and at least fifty-two agglutinated and one hundred-five calcareous-hyaline species was identified. The relative abundance of the recognised species is shown in Figs. 2–7 and Supplementary Table. Benthic foraminifera are commonly used as bathymetric

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Fig. 7. Stratigraphy and relative abundances of the agglutinated benthic foraminifera across the K−Pg boundary transition at Elles (Tunisia). See Fig. 2 for explanation.

indicators because their depth distribution in the oceans is controlled by a series of depth-related parameters (e.g., Nyong and Olsson, 1984; Van Morkhoven et al., 1986; Culver, 2003). The comparison between fossil and recent assemblages, the occurrence and abundance of depthrelated species, and their upper-depth limits (e.g., Van Morkhoven et al., 1986; Alegret and Thomas, 2001; Alegret et al., 2003) thus allowed us to infer the palaeobathymetry of the uppermost Cretaceous and lowermost Paleogene sediments at Elles. Palaeodepth assignment was carried out following the bathymetric subdivision provided by Van Morkhoven et al. (1986) and Berggren and Miller (1989): neritic = 0–200 m, upper bathyal = 200–600 m, middle bathyal = 600–1000 m, lower bathyal = 1000–2000 m, and abyssal N 2000 m. The distribution of bathymetric indicator species has been assessed mainly following Sliter (1968), Sliter and Baker

(1972), Berggren and Aubert (1975), Aubert and Berggren (1976), Douglas (1979), Nyong and Olsson (1984), Olsson and Nyong (1984), Van Morkhoven et al. (1986), Keller (1988), Berggren and Miller (1989), Kaiho (1992), Speijer (1994), Speijer and Van der Zwaan (1996), Widmark and Speijer (1997a,b), Li et al. (1999), Widmark (2000), and Alegret et al. (2003) (Table 1). In order to infer probable microhabitat preferences and environmental parameters, such as the nutrient supply to the sea floor or sea-water oxygenation (e.g., Bernhard, 1986; Jorissen et al., 1995), all taxa were allocated to infaunal and epifaunal morphogroups following Corliss (1985), Jones and Charnock (1985), Corliss and Chen (1988), Nagy et al. (1995), and Van den Akker et al. (2000) (Fig. 8 and Table 2). In general, benthic foraminifera with plano-convex, biconvex and rounded trochospiral, and tubular and coiled-flattened

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Fig. 8. Stratigraphy and relative abundances of benthic foraminiferal morphogroups across the K−Pg boundary transition at Elles (Tunisia). See also Table 1. See Fig. 2 for explanation.

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Fig. 9. Genus and species richness, percentages of benthic foraminifera with calcareous and agglutinated tests, relative abundances of infaunal and epifaunal morphogroups, Fisher-α diversity and Shannon-Weaver H(s) heterogeneity indexes, percentages of buliminids, BFOI, and coiling ratio of Cibicidoides pseudoacutus together with summary diagram of morphotypic assemblages, survival and recovery patterns, main faunal events, environmental conditions (S = stable, U = unstable, RS = relatively stable), and trophic conditions (O = oligotrophic, M = mesotrophic, E = eutrophic) across the K−Pg transition at Elles (Tunisia). See Fig. 2 for explanation.

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tests, are inferred to have an epifaunal mode of life, living at the sediment surface or in its uppermost layers, as seen in living faunas. Infaunal foraminifera, living in the deeper layers of the sediment, have cylindrical or flattened tapered, spherical, rounded planispiral, flattened ovoid, globular unilocular or elongate multilocular tests. Caveats in using morphotype analyses to infer microhabitats and environmental parameters have been exhaustively discussed in Jorissen (1999) and Alegret and Thomas (2004, 2005). For this reason, also following Gooday (2003), the relative abundance of morphotypes has been commonly used as an indicator of food delivery to the sea floor and only major changes in percentages of the morphogroups are here retained likely to be significant. Infaunal species dominate in assemblages associated with relatively high organic carbon fluxes (e.g., Corliss and Chen, 1988; Jorissen et al., 1992, 1995), and epifaunal ones in nutrient-poor environment (Thomas, 1990a; Gooday, 1994; Jorissen et al., 1995). The relative abundances of calcareous and agglutinated taxa and of infaunal and epifaunal morphogroups within the benthic foraminiferal assemblages were calculated (Fig. 9 and Supplementary Table). The genus and species richness (number of genera and species), the Fisher-α diversity, and the H(S) Shannon-Weaver heterogeneity indexes (Murray, 1991; Hayek and Buzas, 1996) were evaluated in order to observe possible changes in diversity across the K–Pg boundary transition Table 1 Distribution of bathymetric indicator species from the Elles section (Tunisia) based on Sliter (1968), Sliter and Baker (1972), Berggren and Aubert (1975) Aubert and Berggren (1976), Douglas (1979), Nyong and Olsson (1984), Olsson and Nyong (1984), Van Morkhoven et al. (1986), Keller (1988), Berggren and Miller (1989), Kaiho (1992), Speijer (1994), Speijer and Van der Zwaan (1996), Widmark and Speijer (1997b), Li et al. (1999), Widmark (2000), and Alegret et al. (2003) Middle neritic

Outer neritic

Outer neritic-bathyal

Alabamina wilcoxensis Bulimina midwayensis Osangularia cordieriana Valvalabamina depressa

Bolivinoides draco

Coryphostoma incrassata gigantea Loxostomum applinae

Cibicidoides pseudoacutus Coryphostoma midwayensis Coryphostoma plaitum Eouvigerina subsculptura Gaudryina pyramidata

Marssonella oxycona Oridorsalis umbonatus Pseudouvigerina plummerae Tappanina selmensis Sitella cushmani Sliteria varsoviensis Spiroplectammina spectabilis

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Table 2 Habitat preferences of calcareous (Corliss, 1985; Corliss and Chen, 1988) and agglutinated (Jones and Charnock, 1985; Nagy et al., 1995; Van den Akker et al., 2000) benthic foraminiferal morphogroups. See also Alegret et al. (2003) Epifaunal calcareous Rounded trochospiral Anomalinoides rubiginosus Plano-convex trochospiral Alabamina wilcoxensis Cibicides beaumontianus Gyroidinoides spp. Valvalabamina depressa Biconvex trochospiral/planispiral Anomalinoides spp. Cibicidoides abudurbensis Cibicidoides pseudoacutus Hemirobulina spp. Lenticulina spp. Marginulinopsis spp. Nonionella spp. Osangularia cordierana Saracenaria spp. Sliteria varsoviensis Milioline Quinqueloculina arrisi Quinqueloculina stelligera Palmate Frondicularia linearis Neoflabellina reticulata Neoflabellina rugosa Infaunal calcareous Cylindrical/elongate tapered Bulimina midwayensis Bulimina pupoides Chrysalogonium cretaceum Chrysalogonium lanceolum Dentalina spp. Dentalinoides spp. Ellipsopolymorphina spp. Eouvigerina subsculptura Laevidentalina spp. Loxostomoides applinae Neobulimina minima Nodosaria limbata Nodosaria longiscata Nodosaria spp. Pleurostomella spp. Praebulimina fang Praebulina reussi Praebulimina spp. Pseudonodosaria humilis Pseudouvigerina plummerae Pyramidulina spp. (continued on next page)

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Table 2 (continued )

Table 2 (continued )

Infaunal calcareous

Epifaunal agglutinated

Cylindrical/elongate tapered Ramulina pseudoaculeata Siphogenerinoides eleganta Siphonodosaria matanzana Siphonodosaria spp. Sitella colonensis Sitella cushmani Sitella fabilis Stainforthia farafraensis Tappanina selmensis Trifarina hannai Trifarina spp.

Flattened planispiral, trochospiral and streptospiral Ammodiscus cretaceous Ammodiscus glabratus Ammodiscus peruvianus Ammodiscus tenuissimus Ammosphaeroidina pseudopauciloculata Arenoturrispirillina sp. Glomospira serpens Glomospira spp. Glomospirella spp. Repmanina charoides Spiroloculina spp. Trochammina spp. Trochamminoides spp.

Flattened tapered Astacolus spp. Bolivinoides decoratus Bolivinoides draco Brizalina spp. Coryphostoma incassata gigantea Coryphostoma midwayensis Coryphostoma plaitum Lingulina taylorama Vaginulina spp. Vaginulinopsis spp. Sphaerical/globose Globulina lacrima Globulina spp. Guttulina spp. Lagena amphora Lagena costata Lagena sulcata Oolina spp. Praeglobobulimina quadrata Reussoolina apiculata Reussoolina spp. Rounded planispiral Pullenia malkinae Pullenia quinqueloba Flattened ovoid Fissurina spp. Palliolatella striolata Palliolatella spp. Biconvex trochospiral Oridorsalis umbonatus Epifaunal agglutinated Tubular or branching Bathysiphon spp. Hyperammina spp. Nothia spp Rhabdammina spp. Rhizammina spp.

Globular/subglobular Saccamina placenta Psammosphaera fusca Psammosphaera spp. Rounded trochospiral/streptospiral Cribrostomoides spp. Recurvoides spp. Elongate tapered Clavulinoides spp. Gaudryina aissana Gaudryina cretacea Gaudryina pyramidata Hagenowella sp. Heterostomella austiniana Marssonella oxycona Tritaxia pyramidata Rounded/flattened planispiral Haplophragmoides spp. Elongate flattened Ammomarginulina spp. Elongate flattened and tapered Spiroplectammina laevis Spiroplectammina spectabilis

(Fig. 9 and Supplementary Table). High values of H(S) indicate an even distribution of specimens over species. The percentage of buliminids was calculated (Fig. 9); a high abundance of this group has been related to high productivity and high delivery of food to the sea floor (e.g., Widmark and Speijer, 1997a; Fontanier et al., 2002; Alegret and Thomas, 2005). The benthic foraminifera oxygenation index (BFOI) was calculated according to the definition of Kaiho (1994, 1999) (Fig. 9 and Supplementary Table). The index has been evaluated as BFOI = [O/(O + D)] × 100,

R. Coccioni, A. Marsili / Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157–180 Table 3 Classification of benthic foraminiferal species into Oxic and Dysoxic groups following Kaiho (1994, 1999), Alegret et al. (2002c, 2003), and Alegret and Thomas (2004, 2005) Oxic

Dysoxic

Anomalinoides rubiginosus Anomalinoides spp. Cibicides beaumontianus Cibicidoides abudurbensis Cibicidoides pseudoacutus Osangularia cordierana Quinqueloculina harrisi Quinqueloculina stelligera Sliteria varsoviensis

Bolivinoides decoratus Bolivinoides draco Brizalina spp. Coryphostoma incrassata gigantea Coryphostoma midwayensis Coryphostoma plaitum Dentalina spp. Dentalinoides spp. Loxostomoides applinae Pleurostomella spp. Siphonodosaria matanzana

where O indicates oxic, whereas D indicates dysoxic. The allocation of the species into the O and D groups follows Kaiho (1994, 1999), Alegret et al. (2002c, 2003), and Alegret and Thomas (2004, 2005) (Table 3). According to some recent works (e.g., Jorissen et al., 1995, 1998; Den Dulk et al., 2000; Morigi et al., 2001; see also review by Gooday, 2003) we do interpret the BFOI values as reflecting food flux rather than oxygenation. The coiling ratio (number of sinistral versus dextral individuals) in the benthic foraminifer Cibicidoides pseudoacutus was calculated according to the method of Galeotti and Coccioni (2002) and Coccioni et al. (2005) (Fig. 9 and Supplementary Table). 4. Results and discussion 4.1. Palaeobathymetry Benthic foraminiferal assemblages at Elles are dominated by calcareous taxa (Fig. 9) indicative of a deposition floor well above the calcite compensation depth. The planktonic/benthic ratio is high (N90%) in all samples. The relative abundance (see Figs. 2–7 and Supplementary Table and Table 1) of the bathymetric indicator species is consistent with an outer neriticuppermost bathyal depth (∼200–300 m) of the studied section without perceivable depth fluctuations throughout. 4.2. Benthic foraminiferal turnover at the K–Pg boundary Five assemblages (I–V) and four intervals (preextinction, survival, recovery, and post-recovery) can be recognised at Elles related to changes in benthic assemblages (Fig. 9 and Supplementary Table).

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4.2.1. Assemblage I (a 6 m-thick, pre-extinction interval below the K–Pg boundary; most of the Plummerita hantkeninoides Zone; the last ∼257 kyr of the Cretaceous) Benthic foraminiferal assemblages during the latest Cretaceous are well preserved and politaxic (up to 44 genera and 66 species), with a complex trophic structure (Figs. 2–9 and Supplementary Table). Infaunal morphogroups and calcareous taxa prevail (∼68–86% and ∼81–92%, respectively). Cylindrical/elongate/flattened tapered and biconvex trochospiral morphogroups dominate both the infaunal and morphogroups, respectively. Some fluctuations in diversity, heterogeneity, BFOI and C. pseudoacutus coiling ratio are observed without any recognizable significant changes. Buliminids also fluctuate in abundance (∼10–28%) with the highest percentages just predating the K–Pg boundary (Fig. 9). Trifarina hannai, Stainforthia farafraensis, Anomalinoides spp., Sitella colonensis, Euvigerina subscultura, Sitella cushmani, Heterostomella austiniana, Gyroidinoides spp., Sitella fabilis, Brizalina spp., Coryphostoma midwayensis, C. incrassata gigantea, C. plaitum, Spiroplectammina spectabilis, Sliteria varsoviensis, Laevidentalina spp., and Gaudryina pyramidata are the most abundant taxa making ∼55–83% of the assemblages (Figs. 2–7 and Supplementary Table). The infaunal E. subsculptura and T. hannai markedly increase in abundance upwards, whereas the infaunal S. farafaensis shows an opposite trend (Figs. 2 and 5). Accordingly, Assemblage I with rich faunas characterised by high diversity and low dominance and dominated by calcareous taxa and infaunal morphogroups can be considered indicative of marine stable, mesotrophic to moderately eutrophic environments, with a fluctuating nutrient supply to the sea floor high enough to sustain both infaunal and epifaunal morphogroups and with a small supply of terrigenous sediment. Moreover, the relative abundances of infaunal morphogroups and buliminids, both indicative of high food supply, suggest an increased flux of organic matter to the sea floor at the very end of the Cretaceous (Fig. 9). Finally, many genera and species here recognised have been also observed world-wide and the taxonomic composition is similar to that recorded in other shallow, outer-platform to upper bathyal Tunisian sections, such as El Kef and Ain Settara (e.g. Keller, 1988; Speijer and Van der Zwaan, 1996; Kouwenhoven, 2000; Alegret et al. 2002c; Peryt et al., 2002, 2004; Alegret et al., 2004a). 4.2.2. Assemblage II (a 5–10 cm-thick, lower survival interval above the K–Pg boundary; lowermost part of the G. cretacea Zone; the first ∼ 6 kyr of the Paleogene) Just above the thin red layer with geochemical anomalies and barren in foraminifera which marks the

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K–Pg boundary, a dramatic and sudden change in the structure of the benthic foraminiferal community occurs (Fig. 9). The genus and species richness (29–30 genera and 43–44 species), the percentage of infaunal morphogroups (∼55–63% of the assemblages), the diversity, and the heterogeneity markedly decrease, whereas the BFOI increases (Fig. 9 and Supplementary Table). Calcareous taxa slightly decrease in abundance (∼ 85%) and buliminids show lower percentages (∼14–17% of the assemblages) than those recorded just before the K–Pg boundary. Biconvex trochospiral, cylindrical/elongated/flattened tapered, and sphaerical/ globose morphogroups dominate, the latter even reaching a peak in abundance with values close to 20% (Fig. 8). The C. pseudoacutus coiling ratio shows its highest values with a dominance of left-coiled specimens of this species in the lowermost Danian (Galeotti and Coccioni, 2002; Coccioni et al., 2005) (Fig. 9). At the same time, the opportunistic disaster species Guembelitria irregularis, that can be interpreted (Abramovich and Keller, 2002; Coccioni and Luciani, 2006) as useful indicator for high environmental stress, blooms (see Coccioni and Luciani, 2006). Assemblage II contains scarce and badly preserved taxa and is clearly dominated by few species (Cibicidoides pseudoacutus, Tappanina selmensis, Gaudryina aissana, Praeglobobulimina quadrata Stainforthia farafraensis, Coryphostoma midwayensis, Anomalinoides spp., Tritaxia pyramidata, Trifarina hannai, Sitella cushmani, and Sitella fabilis) of mixed epifaunal–infaunal morphogroups with about equal abundance that make ∼74– 80% of the assemblages. Cibicidoides pseudoacutus blooms (up to 25.4% of the assemblages) as also recorded at El Kef and Ain Settara (Galeotti and Coccioni, 2002; Alegret et al., 2004a). Specimens of this species are usually large, thick-walled and multichambered, in contrast to the typical low-oxygen, r-selected morphotypes, which generally have few chambers, small tests and thin walls. In correspondence with the base of this survival interval only four species (Bolivinoides draco, Eouvigerina subsculptura, Heterostomella austinana, and Sliteria varsoviensis) become extinct, with an extinction rate of ∼3%, similarly to the low extinction rates of benthic foraminifera recorded worldwide at the K–Pg boundary. Other taxa (e.g. Oridorsalis umbonatus, Praebulimina reussi, Pyramidulina spp., Globulina spp., and all the miliolids) temporarily disappear reappearing upwards as Lazarus taxa. Assemblage II, characterised by paucity of benthic foraminifera, high dominance and low diversity, and low numbers of infaunal taxa, probably reflects an instanta-

neous severe shortage of the food supply to the sea floor due to the collapse of surface-water productivity at the K– Pg boundary (Zachos and Arthur, 1986; Thomas, 1990a,b; Widmark and Malmgren, 1992a,b; Kuhnt and Kaminski, 1993; D'Hondt et al., 1998; Widmark, 2000; Alegret et al., 2001, 2002a,b,c, 2003, 2004a,b). The drastic shortage of food resulted in the large oxidation or consumption of available organic matter before its burial in the sediment, so that limited food remained for infaunal taxa. Consequently, a highly oligotrophic environment was established and species that prefer a medium-high nutrient supply (see Speijer and Van der Zwaan, 1996) such as B. draco, H. austiniana, E. subscultura, S. varsoviensis, S. cusmani, S. fabilis, and Trifarina hannai disappeared or decreased in abundance. Under oligotrophic conditions, the epifaunal species C. pseudoacutus living at the sediment surface, bloomed together with the opportunist, infaunal species G. aissana, T. pyramidata, P. quadrata, and T. selmensis. The benthic foraminiferal faunas show no evidence of low-oxygen conditions (hypoxia) during the deposition of the dark clay layer of the lowermost Danian as observed in other settings (e.g., Coccioni et al., 1993; Coccioni and Galeotti, 1994, 1998; Kaiho, 1999; Alegret et al., 2003). The argument for low-oxygen conditions is mainly based on the occurrence of low-diversity benthic faunas just above the K–Pg boundary. These lowdiversity benthic faunas, however, resulted dominated by large, heavily calcified epifaunal species, suggesting adverse conditions rather than low-oxygen conditions. In conclusion, the decrease in both infaunal taxa and buliminids suggests a decrease in food supply to the sea floor, probably related to the catastrophic mass extinction of calcareous plankton at the K–Pg boundary and the subsequent collapse of primary productivity (e.g., Zachos et al., 1986; D'Hondt et al., 1998; Alegret et al., 2001). During this period of oligotrophic conditions, epifaunal species living close to the sediment surface were able to feed on the scarce available food, whereas infaunal taxa decreased in abundance (e.g., Jorissen et al., 1995). 4.2.3. Assemblage III (an upper survival interval from 10 cm to 50 cm above the K–Pg boundary; from middle– lower part of the G. cretacea Zone to the lowermost part of the Pv. eugubina Zone; from ∼3 kyr to ∼25 kyr after the K–Pg boundary) Diversity (9.02–11.51), heterogeneity (2.3–2.95), and genus (29–33) and species (41–49) richness show the lowest values throughout the section, whereas the BFOI (∼ 65–97%) displayes the highest value. A marked decrease in abundance of both infaunal taxa (∼29–47% of the assemblages) and buliminids (∼2–

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12% of the assemblages) clearly indicates fully oligotrophic conditions. Biconvex trochospiral/planispiral, elongate tapered, and rounded/flattened planispiral morphogroups dominate (Fig. 8). An overall increase in abundance (∼ 30–52% of the assemblages) of agglutinated taxa also characterises this interval. Assemblage III is clearly dominated by few epifaunal (C. pseudoacutus, A. tenuissimus, Anomalinoides spp., Lenticulina spp., A. wilcoxensis, A. peruvianus, and Rhabdammina spp.) and infaunal (Tappanina selmensis, T. pyramidata, Haplophragmoides ssp., G. aissana, P. quadrata, and Psammosphaera spp.) taxa that make ∼62–84% of the assemblages (Figs. 2–7 and Supplementary Table). It may be argued that this interval results dominated by epifaunal taxa not because of the palaeoecological characteristics at that time, but simply due to the fact that they correspond to the dissolution–resistant forms. However, both infaunal and epifaunal species show evidence of dissolution. In addition, in spite of the fact that epifaunal species are more susceptible to dissolution in the modern oceans, the overall peak in the abundance of epifaunal morphogroups observed in the lowermost Danian and centered at 30 cm above the K–Pg boundary, suggests that the percentage of epifaunal morphogroups may have been even greater and that dissolution was present but not overwhelming. Several species have a local last occurrence, but do not become really extinct. In addition to the highest percentage (∼40%) of C. pseudoacutus, this interval is also characterised by a marked increase in abundance (∼30–52% of the assemblages) of agglutinated taxa. Infaunal, mainly detrital/bacterial scavengers (Gaudryina, Haplophramoides, Tritaxia) and epifaunal, passive and active herbivores, detritivores, and omnivores (Ammodiscus) dominate the agglutinated assemblages. The appearance of some agglutinated genera (Ammosphaeroidina, Cribrostomoides, Glomospira, Glomospirella, Psammosphaera, Repmanina, and Saccamina), previously not observed in the underlying Maastrichtian beds, is also recorded. Several opportunistic taxa (e.g. the agglutinated Haplophragmoides spp., A. peruvianus, A. tenuissimus, G. aissana, Psammosphaera spp., Rhabdammina spp., Saccamina placenta, and Tritaxia pyramidata) have short peaks in relative abundance. In particular, the genus Haplophragmoides may be considered as an opportunistic, shallow infaunal taxon that can move vertically through the sediment depending on food levels. Moreover, it can also be regarded as tolerant of low-oxygen and low-food conditions. (Kuhnt et al., 1996; Kaminski et al., 1999). Similar Haplophragmoides acmes have been reported from palaeoenvironmental instability events for other areas (Alegret et al., 2003).

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Assemblage III records severely stressed environmental conditions. Also following Alegret et al. (2003), Peryt et al. (2004), and Alegret and Thomas (2004, 2005), the strong variability in the fauna, as well as the lowered diversity and abundance of benthic foraminifera together with the occurrence of various peaks in abundance of opportunistic, epifaunal (C. pseudoacutus, A. peruvianus, A. tenuissimus) and infaunal (Haplohragmoides spp., G. aissana, G. pyramidata, P. quadrata, Psammosphaera spp., T. selmensis) taxa during the first ∼25 kyr (lower ∼50 cm) of the Paleogene, reflects not only a collapse of the food supply (e.g. Zachos and Arthur, 1986) that would have favored epifaunal morphogroups, but also a major change in the composition and abundance of the food supply driven by blooms of such genera as Thoracosphaera, Cyclagelosphaera, Braarudosphaera or Biscutum (e.g., Thierstein, 1981; Perch-Nielsen et al., 1982; Gardin and Monechi, 1998; Gardin, 2002). Under such conditions, the infaunal taxa that bloomed took over the infaunal niche whenever other taxa could not compete. Alegret et al. (2003) suggested the dissociation of gas hydrates that would have been caused by the large slumps and massive failures of sediment occurring along the western North Atlantic margin due to a meteorite impact at Chicxulub, Yucatan Peninsula, Mexico (e.g. Norris et al., 1999, 2001; Soria et al., 2001) as the main cause of the low-oxygen conditions as well as the locally enhanced bacterial food supply to the benthos just after the K–Pg boundary (e.g. De Angelis et al., 1993). Geographic variability in the abundance, composition, and extent of the phytoplankton blooms might be a major cause of the different patterns of post K–Pg benthic foraminifera faunal composition observed at different sites after the K–Pg boundary event (e.g. Coccioni and Galeotti, 1998; Culver, 2003). The relatively lower percentages of epifaunal morphogroups (∼60% on average), if compared to those (N 80%, Peryt et al., 2002, 2004) of the Ain Settara section, may indicate less severe oligotrophic conditions in the Elles area favoring also a significant percentage of infaunal population. As recognised in other settings (e.g. Alegret et al., 2003; Alegret and Thomas, 2004, 2005), the BFOI does not suggest a drop in oxygenation just after the K–Pg boundary event. 4.2.4. Assemblage IV (a recovery interval from 0.50 m to 2.50 m above the K–Pg boundary; lowermost part of the Pv. eugubina Zone to lowermost of the Ps. pseudobulloides Zone; ∼ 25 kyr to ∼65 kyr after the K–Pg boundary) Diversity (11.94–14.62), heterogeneity (2.67–3.29), and genus (33–41) and species (47–58) richness

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significantly recover through this interval. Also infaunal (∼52–73% of the assemblages) and calcareous (∼73– 93% of the assemblages) taxa return to dominate, indicating that the major environmental instability was over (Fig. 9 and Supplementary Table). The BFOI exhibits values similar to those of the uppermost Cretaceous. The infaunal set of the assemblages and buliminids, however, shows lower percentages than in the uppermost Cretaceous, suggesting mesotrophic conditions with increasing supply of food particles and calcium carbonate for benthic organisms. Assemblage IV is made of mixed epifaunal and infaunal morphogroups dominated by T. selmensis, C. pseudoacutus, C. midwayensis, Anomalinoides spp. S. farafraensis, Brizalina spp., P. quadrata, A. wilcoxensis, O. cordierana, T. pyramidata and Oolina spp. that make up to 80% of the assemblage (Figs. 2–7 and Supplementary Table). 4.2.5. Assemblage V (a post-recovery interval from 2.5 m to 6 m above the K–Pg boundary; lower part of the Ps. pseudobulloides Zone; ∼65 kyr to ∼100 kyr after the K–Pg boundary) One hundred kyr after the K–Pg boundary event, productivity did not fully recover to pre-extinction levels, as indicated by lower percentages of infaunal morphogroups (∼40–61% of the assemblages) compared to the Maastrichtian values. Nevertheless, wellpreserved, polytaxic assemblages with complex trophic structures re-occur throughout, indicating an overall stable environment at outer neritic-uppermost bathyal depths (Fig. 9). Assemblage V is composed of mixture of epifaunal and infaunal morphogroups dominated by Anomalinoides spp., Tappanina selmensis, C. abudurbensis, Osangulatia cordierana, Loxostomoides applinae, Laevidentalina spp., C. pseudoacutus, A. wilcoxensis, Lenticulina spp., Gyroidinoides spp., and C. midwayensis making up to ∼66% of the assemblages. Miliolids reappear in the middle part of the interval (Figs. 2–7 and Supplementary Table). Moreover, the significant recover of the infaunal morphogroups, diversity (11.94–16.13), heterogeneity (3.03–3.39), and genus (36–41) and species (51–63) richness of the assemblages through the lower part of the Ps. pseudobulloides Zone suggests that the overall environmental stress on the sea floor following the K–Pg boundary event lasted not longer than ∼65 kyr. Our data indicate that the sea-floor ecosystem, at least at outer neritic-uppermost bathyal depths, may have recovered faster than commonly suggested. This would be also in agreement with the rapid recovery of terrestrial ecosystems following the biotic crisis at the K–Pg

boundary (e.g., Beerling et al., 2001; Lomax et al., 2001). 5. Conclusions The detailed quantitative analysis of the benthic foraminiferal assemblages of the outer neritic-uppermost bathyal Elles section (northwestern Tunisia) encompasses the K–Pg boundary within about 357 kyr of extinctions, species turnover, and palaeoecological changes. Uppermost Maastrichtian assemblages are highly diversified and heterogeneous, and contain a mixture of abundant infaunal and less numerous epifaunal taxa, thus indicating stable environment and mesotrophic to weakly eutrophic conditions during the latest Cretaceous. In addition, our data suggest that the food supply to the sea floor increased slightly just before the K–Pg boundary. Benthic foraminifera underwent a major faunal turnover in coincidence with the K–Pg boundary, where a dramatic and sudden decrease in the percentage of infaunal morphogroups, as well as in diversity, heterogeneity, and genus and species richness of the assemblages, are recorded together with the temporal disappearance of some taxa. Benthic foraminifera did not suffer a mass extinction, with only about 3% of the species clearly becoming extinct, similarly to the low extinction rates of benthic foraminifera worldwide. Following the drastic, overall change in benthic foraminiferal communities at the K–Pg boundary, a stepped pattern of faunal recovery and restructuring is recognizable during the lowermost Danian, that reflects the gradual restabilization of the environmental conditions after the K–Pg boundary event. Assemblages from the lowermost part of Zone G. cretacea, that would span the first ∼3 kyr of the Paleogene, are taxonomically depauperated and composed of a mixture of both epifaunal and infaunal survival taxa, the latter slightly prevailing in numbers (highly oligotrophic conditions). The second step extends up to the lowermost part of Zone Pv. eugubina (∼25 kyr after the K–Pg boundary) and is characterised by assemblages with higher percentages of agglutinated forms and dominated by epifaunal taxa (fully oligotrophic conditions). A series of peaks in the relative abundance of some opportunistic species is also recorded in this interval, possibly reflecting local, short-term input of food. No evidence of oxygen deficiency at the sea floor in the earliest Danian has been inferred from benthic foraminiferal assemblages at Elles, suggesting that only regional, and not global low-oxygen conditions followed the K–Pg boundary event. Later on, the diversity, heterogeneity,

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genus and species richness of the assemblages significantly increase and calcareous and infaunal taxa return to dominate, reflecting a gradual increase in the amount, and possibly in the diversity of the food supply (mesotrophic conditions). Finally, in the lowermost part of Zone Ps. pseudobulloides (∼65 kyr after the K–Pg boundary), assemblages with high diversity, low dominance and complex trophic structure reappear together with short and long-term Lazarus taxa. This would represent a return to pre-K–Pg conditions, with faunal recovery and restructuring, and restabilization of environmental conditions almost over and with nutrient levels fully mesotrophic. The morphotype analysis herein outlined suggests that the nature and abundance of the food supply to the sea floor conditioned the structure of the benthic foraminiferal assemblages and the faunal turnover in the earliest Paleogene. This turnover reflects not only a sudden collapse of the food web due to the calcareous primary producers extinction, but also a major, rapid change in composition (from calcareous to organicwalled phytoplankton) and abundance of food supply just after the K–Pg boundary. Short-term blooms of some opportunistic species within the G. cretacea Zone and the lowermost part of the Pv. eugubina Zone would reflect instability in the benthic assemblages possibly related to the transfer to the sea floor of food supply not easily used by the benthos through short-term, large blooms or changes in abundance of opportunistic, various phytoplankton groups. The major environmental instability at the sea floor following the K–Pg boundary event would have taken place over a period of about 25 kyr. Benthic foraminiferal assemblages appear to stabilize in the lowermost part of Zone Ps. pseudobulloides, about 40 kyr after the major environmental instability at the sea floor was over, suggesting at that time the food supply to the sea floor was more stable in quality and/or quantity. Our data indicate that the sea floor ecosystem, at least at outer neritic-uppermost bathyal depths, may have recovered over a considerably shorter period than commonly suggested, even if the food delivery to the sea floor had not fully recovered the pre-K–Pg levels as indicated by the lower percentages of infaunal morphogroups and buliminids. This would also be in agreement with the rapid recovery of terrestrial ecosystems following the biotic crisis at the K–Pg boundary. The drastic change of benthic foraminiferal assemblages at Elles coincident with the K–Pg boundary and the stepped recovery during the lowermost Paleogene are largely compatible with a geologically instantaneous, widespread, and catastrophic event, such as the impact of a huge asteroid

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on Earth at the K–Pg boundary, that severely destabilized the oceanic phytoplankton-based food web. Acknowledgements We thank Valeria Luciani and Nicoletta Mancin for their helpful reviews and comments. This is publication no. 11 of the Centro di Geobiologia of the Urbino University. Appendix A. List of benthic foraminiferal species identified in the Upper Cretaceous and lower Paleogene at Elles with author attributions and dates Sixty-eight taxa were identified at the specific or generic level in the uppermost Cretaceous and lowermost Paleogene sediments from the Elles section. For the determinations at the generic level, we largely followed the taxonomy established by Loeblich and Tappan (1988). In most cases, species concepts are those employed by Alegret and Thomas (2001). Taxa are listed below alphabetically. Alabamina wilcoxensis Toulmin, 1941 Ammodiscus cretaceous = Operculina cretacea Reuss, 1845 Ammodiscus glabratus Cushman and Jarvis, 1928 Ammodiscus peruvianus Berry, 1928 Ammodiscus tenuissimus Grzybowski, 1898 Ammosphaeroidina pseudopauciloculata = Cystamminella pseudopauciloculata Myatlyuk, 1966 Anomalinoides rubiginosus = Anomalina rubiginosa Cushman, 1926 Bolivinoides decoratus = Bolivina decorata Jones, 1886 Bolivinoides draco Marsson, 1878 Bulimina midwayensis = Bulimina arkadelphiana var. midwayensis Cushman and Parker, 1936 Bulimina pupoides d'Orbigny, 1846 Chrysalogonium cretaceum Cushman and Church, 1929 Chrysalogonium lanceolum Cushman and Jarvis, 1934 Cibicides beaumontianus = Truncatulina beaumontiana d'Orbigny, 1840 Cibicidoides abudurbensis Nakkady, 1950 Cibicidoides pseudoacutus = Anomalina pseudoacuta Nakkady, 1950 Coryphostoma incrassata gigantea = Bolivina incrassata forma gigantea Wicher, 1949 Coryphostoma midwayensis Cushman, 1936 Coryphostoma plaitum = Bolivina plaitum Carsey, 1926

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Eouvigerina subsculptura MacNeil and Caldwell, 1981 Frondicularia linearis Franke, 1928 Gaudryina aissana ten Dam and Sigal, 1950 Gaudryina cretacea = Verneulina cretacea Karren, 1870 Gaudryina pyramidata = Gaudryina laevigata Franke var. pyramidata Cushman, 1926 Globulina lacrima Reuss, 1845 Glomospira serpens = Ammodiscus serpens Grzybouski, 1898 Heterostomella austinana Cushman, 1946 Lagena amphora Reuss, 1862 Lagena costata = Oolina costata Egger, 1857 Lagena sulcata = Serpula solcata Walker and Jacob, 1798 Lingulina taylorama Cushman, 1938 Loxostomoides applinae = Bolivina applinae Plummer, 1927 Marssonella oxycona = Gaudryina oxycona Reuss, 1860 Neobulimina minima Tappan, 1940 Neoflabellina reticulata = Flabellina reticulata Reuss, 1851 Neoflabellina rugosa = Flabellina rugosa d'Orbigny, 1840 Nodosaria limbata d'Orbigny, 1840 Nodosaria longiscata d'Orbigny, 1846 Oridorsalis umbonatus = Rotalina umbonata Reuss, 1851 Osangularia cordieriana = Rotalina cordieriana d'Orbigny, 1840 Palliolatella striolata = Lagena marginata var. striolata Sidebottom, 1912 Praebulimina fang = Bulimina (Praebulimina?) fang de Klasz, Magnè and Rèrat, 1963 Praebulimina reussi = Bulimina reussi Morrow, 1934 Praeglobobulimina quadrata = Bulimia quadrata Plummer, 1926 Psammosphaera fusca Schulze, 1875 Pseudonodosaria humilis = Nodosaria humilis Roemer, 1841 Pseudouvigerina plummerae Cushman 1927 Pullenia malkinae Coryell and Mossman, 1942 Pullenia quinqueloba = Nonionina quinqueloba Reuss, 1851 Quinqueloculina harrisi Howe and Roberts, 1939 Quinqueloculina stelligera Schlumberger, 1893 Ramulina pseudoaculeata = Dentalina pseudoaculeata Olsson, 1960 Repmanina charoides = Trochammina squamata var. charoides Jones and Parker, 1860

Reussoolina apiculata = Oolina apiculata Reuss, 1851 Saccammina placenta = Reophax placenta Grzybowski, 1898 Siphogenerinoides eleganta Plummer, 1926 Siphonodosaria matanzana = Ellipsonodosaria? matanzana Palmer and Bermudez, 1936 Sitella colonensis = Buliminella colonensis Cushman and Hedberg, 1930 Sitella cushmani = Buliminella cushmani Sandidge 1932 Sitella fabilis = Buliminella fabilis Cushman and Parker, 1936 Sliteria varsoviensis Gawor-Biedowa, 1992 Spiroplectammina laevis Roemer, 1841 Spiroplectammina spectabilis = Spiroplecta spectabilis Grzybowski, 1898 Stainforthia farafraensis = Neobulimina farafraensis LeRoy, 1953 Tappanina selmensis = Bolivinita selmensis Cushman, 1933 Trifarina hannai = Angulogerina hannai Beck, 1943 Tritaxia pyramidata Reuss, 1863 Valvalabamina depressa = Rotalina depressa Alth, 1850 Appendix B. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j. palaeo.2007.02.046. References Abramovich, S., Keller, G., 2002. High stress late Maastrichtian paleoenvironment: inference from planktonic foraminifera in Tunisia. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 145–164. Adatte, T., Keller, G., Li, L., Stinnesbeck, W., Zaghbib-Turki, D., 1998. Climate and sea level fluctuations across the K–T boundary in Tunisia: warm and humid conditions linked to the Deccan volcanism? International Workshop on Cretaceous–Tertiary Transition. Office National des Mines, Direction du Service Géologique, Tunis, Tunisie, pp. 7–10. Abstracts. Adatte, T., Keller, G., Stinnesbeck, W., 2002. Late Cretaceous to Early Paleocene climate and sea-level fluctuations. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 165–196. Alegret, L., Thomas, E., 2001. Upper Cretaceous and lower Paleogene benthic foraminifera from northeastern Mexico. Micropaleontology 47, 269–316. Alegret, L., Thomas, E., 2004. Benthic foraminifera and environmental turnover across the Cretaceous/Paleogene boundary at Blake Nose, Western Atlantic (ODP Hole 1049C). Palaeogeography, Palaeoclimatology, Palaeoecology 208, 59–83. Alegret, L., Thomas, E., 2005. Cretaceous/Paleogene boundary bathyal paleo-environments in the central North Pacific (DSDP Site 465),

R. Coccioni, A. Marsili / Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157–180 the Northwestern Atlantic (ODP Site 1049), the Gulf of Mexico and the Tethys: the benthic foraminiferal record. Palaeogeography, Palaeoclimatology, Palaeoecology 224, 53–82. Alegret, L., Molina, E., Thomas, E., 2001. Benthic foraminifera at the Cretaceous–Tertiary boundary around the Gulf of Mexico. Geology 29, 891–894. Alegret, L., Arenillas, I., Arz, J.A., Molina, E., 2002a. Environmental changes triggered by the K/T impact event at Coxquihui (Mexico) based on foraminifera. Neues Jahrbuch für Geologie und Paläontologie. Monatshefte 5, 295–309. Alegret, L., Arenillas, I., Arz, J.A., Liesa, C., Melendez, A., Molina, E., Soria, A.R., Thomas, E., 2002b. The Cretaceous/Tertiary boundary: sedimentology and micropalaeontology at El Mulato section, NE Mexico. Terra Nova 14, 330–336. Alegret, L., Arenillas, I., Arz, J.A., Molina, E., 2002c. Eventoestratigrafia del limite Cretacico/Terziario en Ain Settara, Tunica: disminucion de la productividad y/o de la oxigenacion oceanicas? Revista Mexicana de Ciencias Geologicas 19, 121–136. Alegret, L., Molina, E., Thomas, E., 2003. Benthic foraminiferal turnover across the Cretaceous/Tertiary boundary at Agost (southeastern Spain): paleoenvironmental inferences. Marine Micropaleontology 48, 251–279. Alegret, L., Arenillas, I., Arz, J.A., Molina, E., 2004a. Foraminiferal eventstratigraphy across the Cretaceous/Paleogene boundary. Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 234, 25–50. Alegret, L., Kaminski, M.A., Molina, E., 2004b. Paleoenvironmental Recovery After the Cretaceous/Paleogene Boundary Crisis: Evidence From the Marine Bidart Section (SW France). Palaios 19, 574–586. Arenillas, I., Arz, J.A., Molina, E., 2004. A new high-resolution planktic foraminiferal zonation and subzonation for the lower Danian. Lethaia 37, 79–95. Arenillas, I., Arz, J.A., Grajales-Nishimura, J.M., Murillo-Muñetón, G., Alvarez, W., Camargo-Zanoguera, A., Molina, E., RosalesDomínguez, C., 2006. Chicxulub impact event is Cretaceous/ Paleogene boundary in age: New micropaleontological evidence. Earth and Planetary Science Letters 249, 241–257. Arz, J.A., Molina, E., 2002. Bioestratigrafia y cronoestratigrafia con foraminiferos planctonicos del Campaniense superior y Maastrichtiense de latitudes subtropicales y templadas (Espana, Francia y Tunica). Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 224, 161–195. Aubert, J., Berggren, W.A., 1976. Paleocene benthic foraminiferal. Biostratigraphy and paleoecology of Tunisia. Bulletin Centre Recherche Pau 10, 379–469. Bensalem, H., 2002. The Cretaceous–Paleogene transition in Tunisia: general overview. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 139–143. Berggren, W.A., Aubert, J., 1975. Paleocene benthonic foraminiferal biostratigraphy, paleobiogeography and paleoecology of Atlantic– Tethyan regions. Palaeogeography, Palaeoclimatology, Palaeoecology 18, 73–192. Berggren, W.A., Miller, K.G., 1989. Cenozoic bathyal and abyssal calcareous benthic foraminiferal zonation. Micropaleontology 35, 308–320. Berggren, W.A., Pearson, P.N., 2005. A revised tropical to subtropical Paleogene planktonic foraminiferal zonation. Journal of Foraminiferal Research 35, 279–298. Beerling, D.J., Lomax, B.H., Upchurch Jr., G.R., Nichols, D.J., Pillmore, C.L., Handley, L.L., Scrimgeour, C.M., 2001. Evidence for the recovery of terrestrial ecosystems ahead of marine primary production following a biotic crisis at the Cretaceous–Tertiary

177

boundary. Journal of the Geological Society of London 158, 737–740. Bernhard, J.M., 1986. Characteristic assemblages and morphologies of benthic foraminifera from anoxic, organic-rich deposits: Jurassic through Holocene. Journal of Foraminiferal Research 16, 207–215. Bolli, H.M., Beckmann, J.-P., Saunders, J.B., 1994. Benthic foraminiferal biostratigraphy of the south Caribbean region. Cambridge University Press. 408 pp. Coccioni, R., Galeotti, S., 1994. K–T boundary extinction: geologically instantaneous or gradual event? Evidence from deep-sea benthic foraminifera. Geology 22, 779–782. Coccioni, R., Galeotti, S., 1998. What happened to small benthic foraminifera at the Cretaceous/Tertiary boundary? Bulletin de la Société Géologique de France 169, 271–279. Coccioni, R., Luciani, V., 2006. Guembelitria irregularis Bloom at the K–T Boundary: Morphological abnormalities induced by impactrelated extreme environmental stress? In: Cockell, C., Koeberl, C., Gilmour, I. (Eds.), Biological Processes Associated with Impact Events. Impact Studies Springer, pp. 179–196. Coccioni, R., Fabbrucci, L., Galeotti, S., 1993. Terminal Cretaceous deep-water benthic foraminiferal decimation, survivorship and recovery at Caravaca (SE Spain). Paleopelagos 3, 3–24. Coccioni, R., Bruni, R., Marsili, A., 2005. Changes in coiling direction of benthic foraminifera as proxy for paleotemperature estimates? A case study of Cibicidoides pseudoacutus (Nakkady) from the K–T boundary transition. Abstract volume, 16, Giornate di Paleontologia 2005, Urbino (Italia). Corliss, B.H., 1985. Microhabitats of benthic foraminifera within deep-sea sediments. Nature 314, 435–438. Corliss, B.H., Chen, C., 1988. Morphotype patterns of Norwegian Sea deep-sea benthic foraminifera and ecological implications. Geology 16, 716–719. Culver, S.J., 2003. Benthic foraminifera across the Cretaceous– Tertiary (K–T) boundary: a review. Marine Micropaleontology 47, 177–226. De Angelis, M.A., Lilley, M.D., Olson, E.J., Baross, J.A., 1993. Methane oxidation in deep-sea hydrothermal plumes of the Endeavour Segment of the Juan de Fuca Ridge. Deep-Sea Research. Part 1. Oceanographic Research Papers 40, 1169–1186. Den Dulk, M., Reichart, G.J., van Heyst, S., Zachariasse, W.J., van der Zwaan, G.J., 2000. Benthic foraminifera as proxies of organic matter flux and bottom water oxygenation? A case history from the northern Arabian Sea. Palaeogeography, Palaeoclimatology, Palaeoecology 161, 337–359. D'Hondt, S., Donaghay, P., Zachos, J.C., Luttenberg, D., Lindinger, M., 1998. Organic carbon fluxes and ecological recovery from the Cretaceous–Tertiary mass extinction. Science 282, 276–279. Douglas, R.G., 1979. Benthic foraminiferal ecology and paleoecology: a review of concepts and methods. Society of Econimic Paleontologists and Nineralogists. Short Course, vol. 6, pp. 21–53. Fontanier, C., Jorissen, F.J., Licari, L., Alexandre, A., Anschutz, P., Carbonel, P., 2002. Live benthic foraminiferal faunas from the Bay of Biscay: faunal density, composition and microhabitats. DeepSea Research. Part 1. Oceanographic Research Papers 49, 751–785. Galeotti, S., Coccioni, R., 2002. Changes in coiling direction of Cibicidoides pseudoacutus (Nakkady) across the Cretaceous– Tertiary boundary of Tunisia: palaeoecological and biostratigraphic implications. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 197–210.

178

R. Coccioni, A. Marsili / Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157–180

Gardin, S., 2002. Late Maastrichtian to early Danian calcareous nannofossils at Elles (Northwest Tunisia). A tale of one million years across the K–T boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 211–231. Gardin, S., Monechi, S., 1998. Paleoecological change in middle to low-latitude calcareous nannoplankton at the Cretaceous/Tertiary boundary. Bulletin de la Société Géologique de France 169, 709–723. Gooday, A.J., 1994. The biology of deep-sea foraminifera: a review of some advances and their applications in paleoceanography. Palaios 9, 14–31. Gooday, A.J., 2003. Benthic foraminifera (Protista) as tools in deepwater palaeoceanography: environmental influences on faunal characteristics. Advances in Biology 46, 1–90. Gradstein, F.M., Ogg, J.G., Smith, A.G., 2004. A Geologic Time Scale. Cambridge University Press. 589 pp. Hayek, L.C., Buzas, M.A., 1996. Surveying Natural Populations. Columbia University Press, New York. 448 pp. Jones, R.W., Charnock, M.A., 1985. “Morphogroups” of agglutinating foraminifera, their life positions and feeding habits and potential applicability in (paleo)ecological studies. Revue de Paléobiologie 4, 311–320. Jorissen, F.J., 1999. Benthic foraminiferal microhabitats below the sediment–water interface. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer Academic Publishers, pp. 161–179. Jorissen, F.J., Barmawidjaja, D.M., Puskaric, S., Van der Swaan, G.J., 1992. Vertical distribution of benthic foraminifera in the northern Adriatic Sea: the relation with the organic flux. Marine Micropaleontology 19, 131–146. Jorissen, F.J., Stigter, H.C., Widmark, J.G.V., 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology 26, 3–15. Jorissen, F.J., Wittling, I., Peypouquet, J.P., Rabouille, C., Rlexans, J.C., 1998. Live benthic foraminiferal faunas off Cape Blanc, NWAfrica: community structure and microhabitats. Deep-Sea Research. Part 1. Oceanographic Research Papers 45, 2157–2188. Kaiho, K., 1992. A low extinction rate of intermediate-water benthic foraminifera at the Cretaceous/Tertiary boundary. Marine Micropaleontology 18, 229–259. Kaiho, K., 1994. Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen level in the modern ocean. Geology 22, 719–722. Kaiho, K., 1999. Effect of organic carbon flux and dissolved oxygen on the benthic foraminiferal oxygen index (BFOI). Marine Micropaleontology 37, 67–76. Kaminski, M.A., Gradstein, F.M., 2005. Atlas of Paleogene Cosmopolitan deep-water Agglutinated Foraminifera. Grzybowski Foundation Special Publication, vol. 10. 547 + vii pp. Kaminski, M.A., Kuhnt, W., Moullade, M., 1999. The evolution and paleobiogeography of abyssal agglutinated foraminifera since the Early Cretaceous: A tale of four faunas. Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 212, 401–439. Karoui-Yaakoub, N., 1999. Le Paléocène en Tunisie septentrionale et centro-orientale: Systématique, Biostratigraphie des foraminifères et environnements de dépôt. Thèse de Doctorat. Université Tunis II, 357 pp. Karoui-Yaakoub, N., Zaghbib-Turki, D., Keller, G., 2002. The Cretaceous–Tertiary (K–T) mass extinction in planktic foraminifera at Elles I and El Melah, Tunisia. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 233–255. Keller, G., 1988. Extinction, survivorship and evolution of planktic foraminifera across the Cretaceous/Tertiary boundary at El Kef Tunisia. Marine Micropaleontology 13, 239–263.

Keller, G., 1992. Paleoecologic response of Tethyan benthic foraminifera to the Cretaceous –Tertiary boundary transition. In: Takayanagi, Y., Saito, T. (Eds.), Studies in Benthic Foraminifera. Tokai University Press, Tokyo, pp. 77–91. Keller, G., Li, L., MacLeod, N., 1995. The Cretaceous/Tertiary boundary stratotype section at El Kef, Tunisia: how catastrophic was the mass extinction? Palaeogeography, Palaeoclimatology, Palaeoecology 119, 221–254. Keller, G., Adatte, T., Stinnesbeck, W., Luciani, V., Karoui, N., Zaghbib-Turki, D., 2002. Paleobiogeography of the Cretaceous/ Tertiary mass extinction in planktic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 178, 257–298. Kouwenhoven, T.J., 2000. Survival under stress: benthic foraminiferal patterns and Cenozoic biotic crises. Geologica Ultraiectina 186 (206 pp.). Kuhnt, W., Kaminski, M.A., 1993. Changes in the community structure of deep water agglutinated foraminifers across the K/T boundary in the Basque Basin (Northern Spain). Revista Espanola de Micropaleontologìa 25, 57–92. Kuhnt, W., Moullade, M., Kaminski, M.A., 1996. Ecological structuring and evolution of deep sea agglutinated foraminifera: a review. Revue de Micropaléontologie 39, 271–281. Li, L., Keller, G., 1998. Global warming at the end of the Cretaceous. Geology 26, 995–998. Li, L., Keller, G., Stinnesbeck, W., 1999. The Late Campanian and Maastrichtian in northwest Tunisia: paleoenvironmental inferences from lithology, macrofauna and benthic foraminifera. Cretaceous Research 20, 231–252. Loeblich, A.R., Tappan, H., 1988. Foraminifera genera and their classification. Van Nostrand Reinhold Co., New York, pp. 1–970. Lomax, B., Beerling, D.J., Upchurch, G.R., Otto-Bliesner, B., 2001. Rapid (10-yr) recovery of terrestrial productivity in a simulation study of the terminal Cretaceous impact. Earth and Planetary Science Letters 192, 137–144. MacLeod, N., Keller, G., 1991. How complete are Cretaceous/Tertiary boundary sections? A chronostratigraphic estimate based on graphic correlation. Geological Society of American Bulletin 103, 1439–1457. Martini, E., 1971. Standard Tertiary and Quaternary calcareous nannoplankton zonation. In: Farinacci, A. (Ed.), Proceedings of the 2nd Planktonic Conference, Rome, 1970. Edizioni Technoscienza, vol. 2, pp. 739–785. Molina, E., Alegrat, L., Arenillas, I., Arz, J.A., 2005. The Cretaceous/ Paleogene boundary at the Agost section revisited: paleoenvironmental reconstruction and mass extinction pattern. Journal of Iberian Geology 31, 135–148. Morigi, C., Jorissen, F.J., Gervais, A., Guichard, S., Borsetti, A.M., 2001. Benthic foraminiferal faunas in surface sediments off NW Africa.: relationship with organic flux to the sea floor. Journal of Foraminiferal Research 31, 350–368. Mukhopadhyay, S., Farley, K.A., Montanari, A., 2001. A short duration of the Cretaceous–Tertiary Boundary Event; evidence from extraterrestrial 3He. Sciences 291, 1952–1955. Murray, J.W., 1991. Ecology and Palaeoecology of Benthic Foraminifera. Elsevier, Amsterdam. 397 pp. Nagy, J., Gradstein, F.M., Kaminski, M.A., Holbourn, A.E., 1995. Foraminiferal morphogroups, paleoenvironments and new taxa from Jurassic to Cretaceous strata of Thakkola, Nepal. In: Kaminski, M.A., Geroch, S., Gasinski, M.A. (Eds.), Proceedings of the fourth international workshop on agglutinated foraminifera. Grzybowski Foundation Special Pubblication, vol. 3, pp. 181–209.

R. Coccioni, A. Marsili / Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157–180 Nyong, E.E., Olsson, R.K., 1984. A paleoslope model of Campanian to Lower Maastrichtian foraminifera in the North American basin and adjacent continental margin. Marine Micropaleontology 8, 437–477. Norris, R.D., Hubert, B.T., Self-Trail, J., 1999. Synchroneity of the K–T oceanic mass extinction and meteoritic impact: Blake Nose, western North Atlantic. Geology 27, 419–422. Norris, R.D., Klaus, A., Kroon, D., 2001. Mid-Eocene deep water, the late Paleocene Thermal maximum and continental slope mass wasting during the Cretaceous–Palaeogene impact. Special Publication Geological Society of London 183, 23–28. Olsson, R.K., Nyong, E.E., 1984. A paleoslope model for Campanian– Lower Maastrichtian Foraminifera of New Jersey and Delaware. Journal of Foraminiferal Research 14, 50–68. Pardo, A., Ortiz, N., Keller, G., 1996. Latest Maastrichtian and K/T boundary foraminiferal turnover and environmental changes at Agost, Spain. In: MacLeod, N., Keller, G. (Eds.), The Cretaceous/ Tertiary Boundary Mass Extinction: Biotic and Environmental Events. Norton, New York, pp. 155–176. Perch-Nielsen, K., McKenzie, J., He, Q., 1982. Biostratigraphy and isotope stratigraphy and the ‘catastrophic’ extinction of calcareous nannoplankton at the Cretaceous/Tertiary boundary. Geological Society of America Special Paper 190, 353–371. Peryt, D., Lahodynsky, R., Durakiewicz, T., 1997. Deep-water agglutinated foraminiferal changes and stable isotope profiles across the Cretaceous/Paleogene Boundary in the Rotwandgraben section, Eastern Alps (Austria). Palaeogeography, Palaeoclimatology, Palaeoecology 132, 287–307. Peryt, D., Alegret, L., Molina, E., 2002. The Cretaceous/Paleogene (K/P) boundary at Aìn Settara, Tunisia: restructuring of benthic foraminiferal assemblages. Terra Nova 14, 101–107. Peryt, D., Alegret, L., Molina, E., 2004. Agglutinated foraminifers and their response to the Cretaceous/Paleogene (K/P) boundary event at Ain Settara, Tunisia. In: Bubik, M., Kaminski, M.A. (Eds.), Proceedings of the Sixth International Workshop on Agglutinated Foraminifera. Grzybowski Foundation Special Publication, vol. 8, pp. 393–412. Robin, E., Rocchia, R., Lefevre, I., Pierrard, O., Dupuis, C., Smit, J., Zaghbib-Turki, D., Karoui, N., Matmati, M.F., 1998. The compositional variation of K/T spinel in Tunisia: Evidence for a global deluge of projectile debris. Abstracts International Workshop on Cretaceous–Tertiary Transition, May 1998, Tunis, pp. 49–50. Said, R., 1978. Etude stratigraphique et micropaléontologique du passage Crétacé–Tertiaire du synclinal d'Ellès (région SilianaSers) Tunisie Centrale. Thèse 3ieme Cycle, Université Pierre et Marie Curie, Paris IV, 275 pp. Sliter, W.V., 1968. Upper Cretaceous foraminifera from southern California and northwestern Baja California, Mexico. The University of Kansas Paleontoogical Contribution, pp. 1–141. Art. 7. Sliter, W.V., Baker, A., 1972. Cretaceous bathymetric distribution of benthic foraminifera. Journal of Foraminiferal Research 2, 167–183. Soria, A.R., Liesa-Carrera, C.L., Mata, M.P., Arz, J.A., Alegret, L., Arenillas, I., Melendez, A., 2001. Slumping and a sandbar deposit at the Cretaceous/Tertiary in the El Tecolote sector (northeastern Mexico): an impact induced sediment gravity flow. Geology 29, 231–234. Speijer, R.P., 1994. Extinction and recovery patterns in southern Tethyan benthic foraminiferal assemblages across the Cretaceous/ Paleogene boundary. Geologica Ultraiectina 124, 19–64. Speijer, R.P., Van der Zwaan, G.J., 1996. Extinction and survivorship of Southern Tethyan benthic foraminifera across the Cretaceous/

179

Paleogene boundary. In: Hart, M.B. (Ed.), Biotic Recovery from Mass Extinction Events. Special Publication Geological Society of London, London, UK, vol. 102, pp. 343–371. Stinnesbeck, W., Keller, G., Adatte, T., 1998. Lithological Characteristics of the K/T transitions in Tunisia: evidence of a tsunami event? International Workshop on Cretaceous–Tertiary Transition, Volume of Abstracts, pp. 53–54. Thierstein, H., 1981. Late Cretaceous nannoplankton and the change at the Cretaceous–Tertiary boundary. SEPM Special Publication 32, 355–394. Thomas, E., 1990a. Late Cretaceous through Neogene deep-sea benthic foraminifers (Maud Rise, Weddell Sea, Antarctica). In: Baker, P.F., Kennet, J.P. (Eds.), Proceedings ODP. Scientific Results, vol. 113, pp. 571–594. Thomas, E., 1990b. Late Cretaceous–early Eocene mass extinctions in the deep sea. In: Sharpton, V.L., Ward, P.D. (Eds.), Global Catastrophes in Earth history. Geological Society of America. Special Publication, vol. 247, pp. 481–495. Tjalsma, R.C., Lohmann, G.P., 1983. Paleocene–Eocene bathyal and abyssal benthic Foraminifera from the Atlantic Ocean. Micropaleontology Special Publication 4 (90 pp.). Van den Akker, T.J.A.H., Kaminski, M.A., Gradstein, F.M., Wood, J., 2000. Campanian to Palaeocene biostratigraphy and paleoenvironments in the Foula Sub-Basin, west of the Shetland Islands, UK. Journal of Micropaleontology 19, 23–43. Van der Zwaan, G.J., Duijnstee, J.A.P., Den Dulk, M., Ernst, S.R., Jannink, N.T., Kouwenhoven, T.J., 1999. Benthic foraminifers: proxies or problems? A review of paleoecological concepts. Earth Science Review 46, 213–236. Van Morkhoven, F.P.C.M., Berggren, W.A., Edwards, A.S., 1986. Cenozoic cosmopolitan deep-water benthic foraminifera. Bulletin des Centres de Recherches Exploration Production Elf Aquitanie, Mémoire 11 (423 pp.). Venturati, A., 2000. Paleoecologia a foraminiferi bentonici al passaggio Cretacico/Terziario nella sezione di Elles (Tunisia). Università di Urbino, Unpublished Thesis, 90 pp. Widmark, J.G.V., 1997. Deep-sea benthic foraminifera from Cretaceous–Paleogene boundary strata in the South Atlantic-taxonomy and paleoecology. Fossils & Strata 43, 1–94. Widmark, J.G.V., 2000. Biogeography of terminal Cretaceous benthic foraminifera: deep-water circulation and trophic gradients in the deep South Atlantic. Cretaceous Research 21, 367–379. Widmark, J.G.V., Malmgren, B., 1992a. Benthic foraminiferal changes across the Cretaceous–Tertiary boundary in the deep sea; DSDP sites 525, 527 and 465. Journal of Foraminiferal Research 22, 81–113. Widmark, J.G.V., Malmgren, B., 1992b. Biogeography of terminal Cretaceous deep-sea benthic foraminifera from the Atlantic and Pacific oceans. Palaeogeography, Palaeoclimatology, Palaeoecology 92, 375–405. Widmark, J.G.V., Speijer, R.P., 1997a. Benthic foraminiferal faunas and trophic regimes at the terminal Cretaceous Tethyan seafloor. Palaios 12, 354–371. Widmark, J.G.V., Speijer, R.P., 1997b. Benthic foraminiferal ecomarker species of the terminal Cretaceous (late Maastrichtian) deepsea Tethys. Marine Micropaleontology 31, 135–155. Zachos, J.C., Arthur, M.A., 1986. Paleoceanography of the Cretaceous/Tertiary event: inferences from stable isotope and other data. Paleoceanography 1, 5–26. Zachos, J.C., Arthur, M.A., Dean, W.E., 1986. Geochemical evidence for suppression of pelagic marine productivity at the Cretaceous/ Tertiary boundary. Nature 337, 61–64.

180

R. Coccioni, A. Marsili / Palaeogeography, Palaeoclimatology, Palaeoecology 255 (2007) 157–180

Zaghbib-Turki, D., Karoui-Yaakoub, N., Rocchia, R., Robin, E., Belayouni, H., 2000. Enregistrement des évènements remarquables de la limite Crétacé–Tertiaire dans la coupe d'Ellès (Tunisie). Comptes Rendus de l'Académie des Sciences, Paris, Sciences de la Terre et des Planètes 331, 141–149.

Zaghbib-Turki, D., Karoui-Yaakoub, N., Said-Benzarti, R., Rocchia, R., Robin, E., 2001. Révision de la limite Crétacé–Tertiaire de la coupe d'Ellès (Tunisie): proposition d'un nouveau parastratotype. Geobios 34 (1), 25–37.