Planktonic foraminifers across the Bonarelli Event (OAE2, latest Cenomanian): The Italian record

Palaeogeography, Palaeoclimatology, Palaeoecology 224 (2005) 167 – 185 www.elsevier.com/locate/palaeo

Planktonic foraminifers across the Bonarelli Event (OAE2, latest Cenomanian): The Italian record Rodolfo Coccioni a,*, Valeria Luciani b a

Istituto di Geologia e Centro di Geobiologia dell’Universita` bCarlo BoQ, Campus Scientifico, Localita` Crocicchia, 61029 Urbino, Italy b Dipartimento di Scienze della Terra dell’Universita`, Corso Ercole I d’Este, 32, 44100 Ferrara, Italy Received 19 December 2003; accepted 23 March 2005

Abstract A high-resolution, quantitative study of the planktonic foraminiferal assemblages across the Bonarelli Level (OAE2, latest Cenomanian) of Italy from different areas and geological settings, has allowed the recognition of several events and biotic changes, including acmes and crises of different genera. It provides evidence of a progressive and rapid change of palaeoenvironmental conditions, reaching a climax coincident with the Bonarelli Event, and of the subsequent, gradual, although not complete, resumption of previous conditions. The observed pattern is illustrated by marked changes in the assemblages that indicate five discrete phases of environmental perturbation within the marine ecosystem. Though there are several similarities, our analyses highlight that each section has its own peculiarities, clearly indicating more or less extreme environmental conditions. D 2005 Elsevier B.V. All rights reserved. Keywords: Italy; Latest Cenomanian; Oceanic anoxic events; Black shales; Planktonic foraminifers

1. Introduction This study is part of an international research project that aims to describe and interpret the biotic and abiotic changes across the major, widespread episode of organic carbon (Corg) accumulation and preservation of the Cretaceous. The Corg-rich Bonarelli Level (BL) is the well-known sedimentary record

* Corresponding author. Tel.: +39 0722304237; fax: +39 0722304220. E-mail address: [email protected] (R. Coccioni). 0031-0182/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2005.03.039

in Italy (see Coccioni and Luciani, 2004 and references therein) of Oceanic Anoxic Event 2 (OAE2: Schlanger and Jenkyns, 1976; Jenkyns, 1980; Arthur et al., 1990), which occurs around the Cenomanian– Turonian boundary, and that records major oceanographic changes and extreme perturbations in the marine environment. Two main still debated and contrasting hypotheses have been offered to explain the deposition of Corgsediments during the OAEs. These imply (1) oceanic anoxia preventing the degradation of organic matter settling through the water column and at the sediment/ water interface (e.g., Bralower and Thierstein, 1984;

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Fig. 1. (A) Palaeogeographical map of late Cenomanian (ca. 94 Ma) proto-North-Atlantic and Tethys. Light shaded regions represent continental plates (from GEOMAR map generator, www.odsn.de/odsn/services/paleomap/paleomap.html). Dark shaded regions represent land (adapted from Dercourt et al., 1993). (B) Cretaceous peri-Adriatic palaeoenvironments (redrawn and modified from Zappaterra, 1994) showing locations of the Bottaccione (1), Valdagno (2), and Calabianca–Guidaloca (3) sections.

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Tyson, 1995) or (2) enhanced productivity in the surface-waters (Pedersen and Calvert, 1990; Weissert and Lini, 1991; among others). Beyond the controversy, it is indisputable that OAE2, even if a shortlived event, induced both major oceanographic changes in the marine environment and severe disturbance of the biosphere which, in turn, triggered the ecological stress forcing one of the largest biotic crises of the Mesozoic Era (see Hallam and Wignall, 1997). Stable oxygen-isotope data reveal that the OAE2 is related to one of the most extreme warm episodes in the past 150 Ma (e.g., Jenkyns et al., 1994; Huber et al., 1995; Clarke and Jenkyns, 1999; Norris et al., 2002). There is also evidence for a reversed greenhouse effect after the thermal maximum coinciding with OAE2 (Clarke and Jenkyns, 1999; Jenkyns, 1999). Changes in calcareous nannofossil assemblages support the interpretation of cooler surfacewaters in the late phase of OAE2 and immediately after it (Erba, 2004). The carbon-isotope curves across OAE2 record a pronounced positive excursion in marine carbonate, organic matter and terrestrial higher plant material, caused by a major perturbation of the global carbon budget generally interpreted as due to accelerated burial of organic matter during episodes of enhanced productivity (see Jenkyns, 2003 and reference therein). Unlike the early Toarcian and early Aptian Oceanic Anoxic Events, there is no preceding negative carbon-isotope excursion that might suggest dissociation of gas hydrates as a mechanism for amplifying global warmth. Supply of volcanogenic carbon dioxide from Large Igneous Provinces (Caribbean Province and Ontong Java Plateau) is indicated for the OAE2, with possible stimulation of plankton productivity by hydrothermally sourced trace metals (Sinton and Duncan, 1997; Kerr, 1998). OAE2, as well as OAE1a, is marked by a major decrease in the 87 Sr/86Sr record (Bralower et al., 1997; Jones and Jenkyns, 2001), implying that increased rates of seafloor spreading and hydrothermal activity dominated over continental weathering in governing seawater chemistry (see synthesis in Jenkyns, 2003). Based on cyclostratigraphy, the duration of OAE2 is estimated at between 100 and 900 ky (Kuhnt et al., 1997; Sageman et al., 1997; Caron et al., 1999; Prokoph et al., 2001; Scopelliti et al., 2004), following the time scale of Hardenbol et al. (1998). Planktonic

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foraminifers, which are sensitive to chemical–physical parameters, provide the potential for monitoring stress conditions, via environmental-proxy taxa, and to shed light on the palaeoceanographic changes through this interval. The aim of this paper is to describe and interpret the results of a high-resolution study carried out on planktonic foraminifers across the BL, and BL equivalents, of some key sections in Italy which belong to different geographical areas and geological settings: (1) the Bottaccione section (type locality of the Umbria-Marche Basin type-area), (2) the Valdagno section (Venetian Prealps), and (3) the Calabianca–Guidaloca composite section (NW Sicily) (Fig. 1).

2. Geological and stratigraphical context 2.1. Bottaccione section The BL (Scisti ittiolitici of Bonarelli, 1891) is a prominent, ichthyolithic–bituminous–radiolaritic regional marker-bed, about 1 m thick on average, which characterizes the top of the uppermost Albianbasal Turonian Scaglia Bianca Formation of the pelagic sequence of the Umbria-Marche Basin (e.g., Arthur and Premoli Silva, 1982) within the lowermost part of the planktonic foraminiferal Whiteinella archaeocretacea Zone (Premoli Silva and Sliter, 1994, 1999) (Figs. 2 and 3). Following Coccioni and Luciani (2004), the BL is considered the whole limestonefree interval sandwiched between two distinct cherty layers of the Scaglia Bianca. The BL, which is located 5 to 6 m below the first occurrence of Helvetoglobotruncana helvetica, following Premoli Silva and Sliter (1994), is referable to the uppermost part of the Cenomanian Stage (see Bengtson, 1996). This classic, pelagic sequence of the Umbria-Marche Basin was deposited in a complex basin and swell topography along the continental margin of the Apulian Block. The dominant lithology of the Scaglia Bianca (overall carbonate content N 70%) is lithified nannofossil-planktonic foraminiferal ooze, deposited above the calcite compensation depth, at an estimated water-depth of 1500–2500 m (Arthur and Premoli Silva, 1982; Kuhnt, 1990). The Tethyan Bottaccione reference-section is 5.48 m thick (Figs. 2 and 3) and located in the type-area of

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Fig. 3. The Bonarelli Level (BL, 0.82 m thick), northern slope of the Bottaccione Valley, along the road S.S. 298. Hammer length = 33 cm.

the BL, 1 km NE of the town of Gubbio, on the northern slope of the Bottaccione Gorge, along the road S.S. 298. The 0.82-m-thick BL of the type-area is devoid of carbonate and consists of olive-green to black mudstones and black, Corg-rich, finely laminated-shales, often rich in fish remains, pyrite nodules and/or radiolaria, which alternate with radiolarian-rich layers (Arthur and Premoli Silva, 1982; Coccioni et al., 1991) (Figs. 2 and 3). The Corg content progressively increases in the lower part and generally reaches the highest values, up to 23% total weight, in the upper part of the BL (Arthur and Premoli Silva, 1982; Baudin et al., 1998). Features of the pre- and post-BL planktonic foraminiferal community have allowed the characterization of the BL of the type-area, based on the presence of two distinct critical intervals, each some decimetres

thick and lasting some tens of thousands of years (Coccioni et al., 1991; Coccioni and Luciani, 2004). These intervals are named the lower and upper critical intervals (LCI and UCI), respectively (Fig. 2). 2.2. Valdagno section The Valdagno section is 3.84 m thick, and is located in the Venetian Prealps, a few hundreds of metres S of the town of Valdagno, close to the tunnel opening along the Valdagno-Schio road (Figs. 1, 4 and 5). The Venetian Prealps belong to the Southern Alps, the structural unit of the Alpine Chain, bounded by the Periadriatic Line to the north and the Po Plain to the south. The Late Cretaceous palaeogeography of the Southern Alps consists (from E to W) of the

Fig. 2. Stratigraphy of the studied interval from the Bottaccione section plotted against radiolarian and planktonic foraminiferal % total abundances estimated according to diagrams for visual percentage estimation in sedimentary rocks given by Baccelle and Bosellini (1965), and the foraminifer genera relative abundance and genus richness (expressed as number of genera per sample). Our analysis was focused on the 313 ky before and 153 ky after the Bonarelli Event. Changes in abundance, overall size and composition of the planktonic foraminiferal assemblages are well recognizable. The planktonic foraminifers temporarily disappear within the Corg-rich Bonarelli Level where only radiolarians occur. A lower critical interval (LCI) and an upper critical interval (UCI) sandwich the Bonarelli Level (see text). From the distribution, overall size, diversity and faunal composition, four dramatic and abrupt faunal turnovers can be identified characterizing five discrete phases (see text). LCO = last common occurrence.

172 R. Coccioni, V. Luciani / Palaeogeography, Palaeoclimatology, Palaeoecology 224 (2005) 167–185 Fig. 4. Stratigraphy of the studied interval from the Valdagno section plotted against the radiolarian and planktonic foraminiferal % total abundances, planktonic foraminiferal genus richness, main events and assemblage composition.

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Fig. 5. The Bonarelli Level equivalent (Ble, 2.35 m thick) in the Valdagno section, close to the tunnel opening along the Valdagno-Schio road (Venetian Prealps).

carbonate Friuli Platform, and two continental margin basins, the Belluno and Lombardian Basins, separated by an intervening chain of seamounts known as the Trento Plateau. The Trento Plateau (Trento–Vicenza– Verona provinces) is characterized by thinner successions, compared with the adjacent basins, of pelagic deposits, comprising calcareous pelagic and hemipelagic oozes mostly consisting of calcareous nannofossils, alternated with varicoloured marlstones of the Scaglia Variegata Formation and pinkish micrites and marlstones of the Scaglia Rossa. Though palaeobathymetry of these formations is not precisely defined, it is generally referred to upper-middle bathyal (some hundred metres) depth (e.g., Winterer and Bosellini, 1981; Channel et al., 1992). Similarly to the BL of the type-area, the 2.35-mthick BL equivalent at Valdagno is sandwiched between limestone beds and mainly consists of greenish-grey to black mudstones and shales, alternated with radiolarian-rich layers (Figs. 4 and 5). However, the BL equivalent, remarkably, contains an appreciable amount of CaCO3. The Valdagno section does not contain recognizable, platform-derived fossil organisms.

2.3. Calabianca–Guidaloca composite section The Calabianca–Guidaloca composite section is 3.68 m thick, located in NW Sicily, and is represented by two distinct segments, located along the coast a few kilometres NW of the town of Castellammare del Golfo (Figs. 1, 6, 7 and 8). The two segments allow analysis of a more complete stratigraphical interval across the BL equivalent in this region. The composite section belongs to the Scaglia Formation, which is part of a stratigraphical succession composed of Mesozoic-Tertiary carbonate, carbonate-siliceous and terrigenous deposits related to the Trapanese Domain (see Abate et al., 1991, and references therein). The lithological features of the segments studied are quite similar to those of the BL from the type-area but the BL equivalent, remarkably, contains an appreciable amount of CaCO3. A detailed palaeobathymetric assessment is not yet available, however main features suggest a middle bathyal setting. As in BL of the type-area, the 1.37-m-thick BL equivalent of NW Sicily is sandwiched between limestone beds, and mainly consists of greenish-grey to black mudstones and shales, alternating with radiolarian-rich layers (Figs. 6, 7 and 8).

174 R. Coccioni, V. Luciani / Palaeogeography, Palaeoclimatology, Palaeoecology 224 (2005) 167–185 Fig. 6. Stratigraphy of the studied interval from the Calabianca–Guidaloca composite section plotted against the radiolarian and planktonic foraminiferal % total abundances, planktonic foraminiferal genus richness, main events and assemblage composition. LCO = last common occurrence.

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Fig. 7. The Bonarelli Level equivalent (Ble, 1.37 m thick) at Calabianca, along the coast, 5 km NW of the town of Castellammare del Golfo (NW Sicily). The studied segment is 2.81 m thick.

Fig. 8. The uppermost part (0.51 m thick) of the Bonarelli Level equivalent (Ble) at Guidaloca, along the coast, 3 km NW of the town of Castellammare del Golfo (NW Sicily).

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3. Materials and methods In addition to the already studied Bottaccione samples (87 samples), a total of 120 samples from the Valdagno (40 samples), Calabianca (57 samples) and Guidaloca (23 samples) sections were investigated (Figs. 2, 4 and 6). All the samples were analysed in thin section. Samples were taken at 10 cm intervals in general, and at 1–2 cm across the BL. For each sample a large number of thin sections were obtained and investigated. The high number of tests observed has allowed an adequate identification of species. Planktonic foraminifers and radiolarian percent abundances were evaluated, using the diagrams for the visual percentage estimations in sedimentary rocks given by Baccelle and Bosellini (1965). Drawing the diagrams these authors have considered the real grain shapes, conveniently standardized and the psychological effects due to chromatic differences between the grains and the matrix. Quantitative analysis of planktonic foraminiferal genera was performed; at least 300 specimens were counted per sample. The high-frequency sampling adopted in the present analysis allowed accurate location the main ecological events occurring just before and after the Bonarelli Event and recognition of the main changes in the assemblage compositions. From this, paleoenvironmental determinations were made based on changes in planktonic foraminiferal assemblages. The biostratigraphy follows the standard low-latitude Cretaceous planktonic foraminiferal biozonation of Caron (1985), Sliter (1989, 1992), and Robaszynski and Caron (1995).

4. Results 4.1. Bottaccione section Planktonic foraminifers abundance, and genus and species richness are higher below the LCI, remarkably declining within the critical intervals that are characterized by near-absence of large forms. Planktonic foraminifers are present in all samples except for 563 and BL1–BL41: their total abundance fluctuates from 0 to 30% (Fig. 2). The microfauna of the surveyed interval includes radiolarians, which display higher abundance (up to 50%) within, and just below and above, the BL.

In the Bottaccione section, the estimated sediment accumulation rate in the Cenomanian was about 1 cm/ ky following the time scale of Hardenbol et al. (1998). Accordingly, our analyses encompass the 313 ky preceding the onset of the Bonarelli Event and the 153 ky following its termination. The most important events in this section are summarised on the right of Fig. 2. From the distribution, overall size, species richness and faunal composition, four dramatic and abrupt foraminiferal turnovers, which delineate five discrete phases, can be identified. Phase I (258–203 ky prior to the onset of OAE2) is characterized by high planktonic foraminiferal abundance and diversity. Heterohelix is the most abundant genus, displaying an average 42% abundance. Hedbergella shows an almost consistently high abundance (average 40%), with some fluctuations towards the end part of the phase. The top of Phase I is characterized by the declipseT of larger forms that involve most of the specimens greater than 150 Am. Phase II (the 55 ky preceding the deposition of the BL) is characterized by low species diversity and several foraminiferal changes and events. This phase coincides with the LCI and a general reduction in size. A marked drop in overall abundance occurs, together with a decrease in genus and species richness (Fig. 2). Hedbergellids (principally Hedbergella planispira) markedly increase in abundance (up to 83.4%: hedbergellid acme) and dominate the assemblages together with schackoinids (Hedbergella– Schackoina shift), which peak (51%: schackoinid acme) close to the middle part of the phase, whereas heterohelicids undergo a consistent decline in abundance (heterohelicid crisis) from 14% to 0.5% with an average of 5.2%. At the base of the phase rotaliporids decrease markedly in abundance (rotaliporid crisis). Rotalipora deeckei is the first rotaliporid to disappear (Fig. 2). Moreover, Rotalipora cushmani and R. greenhornensis undergo a marked reduction in size (maximum diameter 230 Am and 300 Am, respectively) before their concurrent disappearance, which took place 15 ky before the onset of the Bonarelli Event. It is here appropriate to bear in mind that the LO of R. cushmani is dated at 93.90 F 0.2 Ma by Hardenbol et al. (1998). Other recognizable bioevents are the dicarinellid and globigerinelloidid acmes, and the disappearance of G. bentonensis.

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At the end of this phase, all planktonic foraminifers temporarily disappear. Phase III coincides with BL deposition and is characterized by radiolarian proliferation and absence of planktonic foraminifers. Occasional small hedbergellids occur as silicified ghosts (see also Premoli Silva et al., 1999; Coccioni and Luciani, 2004). Phase IV (the 35 ky following deposition of the BL) almost mirrors Phase II, except for the absence of rotaliporids, and is characterized by the proliferation of hedbergellids and schackoinids which constitute, respectively, 68.6% and 18% of the total assemblage. This phase coincides with the UCI. At the onset of this phase, planktonic foraminifers reappear. However, overall abundance is low (1–5%). Globigerinelloidids are fairly abundant (average 9%). As in Phase I, schackoinids increase when heterohelicids decrease in abundance. In Phase V (estimated duration 118 ky), the planktonic foraminiferal abundance and diversity return to values comparable to those of Phase I. This phase almost mirrors Phase I, except for the absence of rotaliporids (Fig. 2). Hedbergellids still dominate the assemblage (average 55%). Schackoinids markedly decrease in abundance while heterohelicids return to constitute an important part of the population (average 31%). The declipseT of large forms ends just above the base of the phase V and is followed by the increase in number of dicarinellids, praeglobotruncanids, and whiteinellids. 4.2. Valdagno section Planktonic foraminifers are present in all samples except for 5–12, 14–27, 29–31, and 33 (Fig. 4). Total abundance fluctuates from 0 to 30%. Hedbergellids dominate the assemblages below and above the BL equivalent. Radiolarians display higher abundance (up to 50%) within the BL. For the Valdagno section, the sediment accumulation rate cannot be evaluated due to the absence of useful stratigraphical data. The most important events recognized are summarised on the right of Fig. 4. As in the Bottaccione section, five discrete phases are recognizable on the basis of changes in planktonic foraminiferal distribution, overall size, diversity and faunal composition.

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Phase I (samples 1–4a) is characterized by high planktonic foraminiferal abundance and diversity. Hedbergella shows an almost consistently very high relative abundance (average 68.5%). Heterohelix is quite rare (average 3.8%). Remarkably, the LOs of R. cushmani, R. greenhornensis, R. deeckei and G. bentonensis are recognizable at the same stratigraphic level at the top of the phase (Fig. 4). Phase II (sample 4b) coincides with the LCI and a general reduction in size. A marked drop in overall abundance occurs together with a decrease in genus richness. Hedbergellids (principally H. planispira) dominate the assemblages (85%: hedbergellid acme). The assemblage contains also Globigerinelloides ultramicrus (10%) and schackoinids (5%). At the end of this phase, all planktonic foraminifers temporarily disappear. Phase III (sample 5–33) coincides with BL deposition and is characterized by radiolarian proliferation. Only scattered and dwarfed planktonic foraminifers occur, in samples 13, 28 and 32. Phase IV (samples 34–36) coincides with the UCI and records the continuous return of planktonic foraminifers, almost all small-sized forms. This phase is characterized by the abundance of hedbergellids, which constitute up to 73.3% of the total assemblages. Globigerinelloidids and schackoinids are fairly abundant in the basal part (up to 16.3% and 10.2%, respectively). Phase V (samples 37–39) records the return of planktonic foraminiferal abundance and diversity to values comparable to those of Phase I. Hedbergellid abundance decreases (average 38.6%), whereas whiteinellids and dicarinellids increase considerably (average 32.7% and 18.3%, respectively). 4.3. Calabianca–Guidaloca composite section Planktonic foraminifers are present in all samples except for most of those within the BL equivalent (Fig. 6). Samples 19C, 50aC, 51C, 52C, 3G, 4G, 57C contain rare planktonic foraminifers. Total abundance fluctuates from 0 to 15%. Radiolarians display high abundance (up to 40%) within the BL. It is not possible to evaluate the sediment accumulation rate for this composite section due to the absence of useful stratigraphical data. The most important events recognized are summarised on the right of Fig. 6.

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As for the Bottaccione and Valdagno sections, five discrete phases can be identified, based on changes in planktonic foraminiferal distribution, overall size, diversity and faunal composition. Phase I (samples C1–C6b) is characterized by high planktonic foraminiferal abundance and diversity. Hedbergellids dominate the assemblages (up to 80%). The LOs of R. cushmani, R. greenhornensis, R. deeckei and G. bentonensis are recognizable at the same stratigraphic level at the top of the phase. Phase II (sample 6c) coincides with the LCI and a general reduction in test size. A marked drop in overall abundance occurs, together with a decrease in genus richness. At the end of this phase, all planktonic foraminifers temporarily disappear. The assemblage is composed only of hedbergellids and schackoinids, the latter peaking in abundance (schackoinid acme) (Fig. 6). Phase III (samples C7–C61, G1–G10) coincides with BL deposition and is characterized by radiolarian proliferation. Scattered dwarfed specimens of planktonic foraminifers occur at different stratigraphical levels. Assemblages are composed of schackoinids, G. ultramicrus, G. caseyi, and hedbergellids (H. planispira, H. simplex, H. delrioensis), the latter dominating. Phase IV (samples C62–C67, G11–G17) coincides with the UCI and records the continuous return of planktonic foraminifers, almost all small-sized forms of H. planispira, G. ultramicrus and schackoinids. Phase V (G18–G23) records the return of planktonic foraminiferal abundance and diversity to values comparable to those of Phase I.

5. Discussion Using primarily planktonic foraminiferal morphology and palaeobiogeographical distributions, and current ideas on their palaeoecological significance together with stable isotope data and comparison with Recent forms (mainly following Norris and Wilson, 1998; Hart, 1999; Huber et al., 1999; Premoli Silva and Sliter, 1999; Keller et al., 2001; Coccioni and Luciani, 2004), the BL population changes have been interpreted in terms of changes in the palaeoenvironments (Table 1).

This study confirms the occurrence of marked perturbations within the marine ecosystem, as previously highlighted by Coccioni and Luciani (2004). Associated with this Bonarelli Event, these perturbations display different degrees of intensity within the identified phases. A progressive and rapid change in palaeoenvironmental conditions reached a peak coincident with the Bonarelli Event, followed by a subsequent, gradual, although incomplete resumption of dnormalT conditions. Micrographs showing the microfacies characterising the different phases identified across the Bonarelli Level and equivalents are displayed in Fig. 9. Phase I is characterized by high planktonic foraminiferal abundance and diversity that implies a relatively stable environment, with different ecological niches occupied in a stratified-water column. In the type-area, relatively high percentages of hedbergellids and heterohelicids indicate a general mesotrophic– eutrophic regime and a well-developed oxygen minimum zone (OMZ). Fluctuating eutrophic conditions are testified by peaks in abundance of radiolarians. However, in the Valdagno and Calabianca–Guidaloca sections, the abundance of small-sized, and presumably low-oxygen tolerant, opportunistic heterohelicids and radiolarians is considerably lower than that recorded in the type-area. This suggests a less welldeveloped OMZ, and less eutrophic conditions, in these settings. Nevertheless, we cannot exclude the possibility that these differences may result from a different depth range of the investigated sections. In all the sections, the most dramatic changes took place during Phase II (LCI). Low diversity, dominance of surface-dwellers and schackoinids, dwarfed species, and high percentages of radiolarians, indicate increased surface productivity, an enhanced OMZ, and marked and rapid changes in ecological parameters. According to Paul and Mitchell (1994) food shortage favored species that reproduced before dying from starvation. On the other hand, following MacLeod et al. (2000), during high stress conditions the energy trade-off of planktonic organisms favored high reproduction rates over growth and hence resulted in decreased test size. Environmental instability related to marked and rapid climatic changes are generally expected to have a profound effect on unicellular plankton, which are known to be extremely sensitive to changes in the physical and chemical properties of

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Table 1 Inferred ecological-strategies of late Cenomanian planktonic foraminifers, derived mainly from latitudinal distributions and abundances, together with depth-ranking based on environmental inferences (morphology and palaeobiogeographic distribution) and stable isotopic data (mainly following Norris and Wilson, 1998; Hart, 1999; Huber et al., 1999; Premoli Silva and Sliter, 1999; Keller et al., 2001; Coccioni and Luciani, 2004, and this paper), plotted against the oceanic surface-water trophic resource continuum (see Hallock, 1987)

K-mode specialists highly oligotrophic

r/K-mode intermediate forms

oligotrophic

R. deeckei R. cushmani R. greenhornensis

primitive marginotruncanids

deep-dwellers (below thermocline) R. cushmani * R. deeckei R. greenhornensis *

mesotrophic

r-mode opportunists eutrophic

highly euthrophic

Hb. delrioensis (1) D. algeriana (1) Hb. simplex D. canaliculata (1) Hb. planispira D. hagni (1,2) Hx. moremani D. imbricata Hx. reussi (1,2) P. gibba Schackoina spp. (2) P. stephani G. bentonensis G. caseyi G. ultramicrus (1) W. archaeocretacea (1) W. aprica (1) W. aumalensis W. baltica (1) (1) W. praehelvetica W. brittonensis (1) W. inornata (1) W. paradubia (1)

intermediate-dwellers (thermocline) G. bentonensis G. caseyi G. ultramicrus Schackoina sp. Hx. moremani Hx. reussi D. algeriana D. canaliculata D. hagni * D. imbricata P. gibba P. stephani *

surface-dwellers (surface mixed-layer) Hb. delrioensis * Hb. planispira * Hb. simplex * W. aprica W. archaeocretacea * W. aumalensis W. baltica W. brittonensis W. inornata W. paradubia W. praehelvetica

R = Rotalipora, D = Dicarinella, P = Praeglobotruncana, G = Globigerinelloides, Hb = Hedbergella, Hx = Heterohelix, W = Whiteinella. (1) = upwelling form, (2) = low-oxygen-tolerant form, * = stable isotope data. Modified after Coccioni and Luciani (2004).

their surrounding water (e.g., Lipps, 1979). From all the above, the significant temperature rise across the Bonarelli Event (e.g., Jenkyns, 2003) may have

inflicted a change in the reproduction/growth strategy leading to smaller-sized specimens. Remarkably, a similar interpretation has been provided to explain

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the strong reduction in size of planktonic foraminiferal assemblages during the warm event of the latest Maastrichtian (Abramovich and Keller, 2002). On the other hand, foraminifers constitute an important fraction of marine plankton and play a signif-

icant role in the carbon cycle through the production of shell calcite. Recent studies (Spero et al., 1997; Bijma et al., 1999; Barker and Elderfield, 2002) on the effects of atmospheric CO2 on planktonic foraminifer calcification indicate that biocalcification is strongly inhib-

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ited under high pCO2. Accordingly, as an alternative interpretation for the dwarfism of planktonic foraminifers across the Bonarelli Event, we suggest that conditions of higher fertility and higher atmospheric CO2 influenced the degree of biomineralization leading to a strong reduction in test size (bbiocalcification crisisQ). The intervals corresponding to Phase II are considerably thinner in the Venetian Prealps (see also Coccioni et al., 2001) and in NW Sicily than in the type-area. It is speculated that the onset of the Bonarelli Event took place much more rapidly in these locations than in the Umbria-Marche Basin. However, the possibility that these reduced thicknesses are the result of condensation or erosion cannot be excluded. The concurrent LOs of all the rotaliporids together with G. bentonensis in the same stratigraphic level in the Valdagno and Calabianca–Guidaloca sections would support the hypothesis that the stratigraphical record might be affected by a short hiatus. Further investigations are in progress to clarify this point. The declipseT of large forms (N 150 Am) which characterizes phase II looks like a prelude to the marked foraminiferal changes culminating at the base of the BL with the temporary disappearance of all planktonic foraminifers. Phase III coincides with the BL deposition and is characterized by highly eutrophic conditions, as testified by radiolarian proliferation. We cannot exclude the possibility that dissolution may have benefited the high radiolarian abundance. If so, the dissolution would have been more effective in the UmbriaMarche Basin (probably a deeper setting) where car-

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bonates are absent within the BL. On the other hand, local volcanism also may have contributed to the radiolarian-acme/preservation event. It must be noted that the proliferation of radiolarians within the BL suggests an upper water column not extremely depleted in oxygen content, unless it is demonstrated that radiolarians tolerate strongly dysoxic conditions. It is possible that pH was low within the BL and equivalents here studied, which contain a large amount of organic matter, and hence dissolution of carbonate cannot be totally excluded. However, major changes in assemblage composition and relative abundance of genera start below the onset of the BL within the critical interval where sediments are mostly limestones, organic matter is not preserved, and pH was presumably higher. For this reason we assume that the biotic content of the BL reflects essentially primary environmental conditions. The most remarkable difference between the BL of the type-area and the BL equivalents studied here is the occurrence, at different stratigraphic levels, of scattered, dwarfed specimens of hedbergellids, schackoinids and G. ultramicrus and G. caseyi. These findings suggest less extreme environments possibly related to occasionally less eutrophic conditions. The lack of rotaliporids and G. bentonensis within the fossiliferous layers from the BL equivalents strongly supports the assumption that the disappearance of these forms just below the BL is a true last occurrence. We are not able at the moment to establish if these last occurrences correspond to the real last appearance of the genus, which, following avail-

Fig. 9. Micrographs showing the microfacies characterising the different phases identified across the Bonarelli Level and equivalents. Changes in abundance, overall size and composition of the planktonic foraminiferal assemblages are well recognizable. (A) Micrograph of a limestone referable to the R. cushmani zone (Bottaccione section, sample 544). The rich, diversified and normal-sized assemblage is indicative of a relatively stable environment (phase I). (B) Micrograph of a limestone partly silicified (Bottaccione section, sample 562a) with rare, small-sized planktonic foraminifers (mainly hedbergellids, globigerinelloidids, and schackoinids). The features of this interval suggest a perturbed environment heralding the Bonarelli Level deposition (lower critical interval, phase II). (C and D) Micrographs of a radiolarian-rich bed (Calabianca section, sample 8) and of a laminated, radiolarian-rich black shale (Calabianca section, sample 17), respectively. Both samples are from the lower part of the Bonarelli Level equivalent. The absence of foraminifers indicates extremely perturbed environmental conditions for this group (phase III). (E and F) Micrographs of a thinly laminated black shale (Calabianca section, sample 57) and of an indurated shale (Valdagno section, sample 28) located in the upper part of the Bonarelli Level equivalent. Very rare and small-sized planktonic foraminifers (hedbergellids, globigerinelloidids, schackoinids) are present. These occurrences document less extreme environmental conditions with respect to the Bonarelli Level of the type-area (Bottaccione section) which is completely barren of planktonic foraminifers and with respect to the horizons rich in organic matter and radiolarians. (G) Micrographs of a limestone located just above the Bonarelli Level (Bottaccione section, sample 564) showing small and rare planktonic foraminifers (hedbergellids, globigerinelloidids, schackoinids). The features of this assemblage imply a perturbed environment (upper critical interval, phase IV). (H) Micrographs of a limestone showing a rich, diversified and normal-sized assemblage referable to the Whiteinella archeocretacea zone (Bottaccione section, sample 573). The features of this assemblage suggest a partial recovery of the environmental conditions after the Bonarelli Level deposition (phase V). Scale bar: 0.5 mm.

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able studies (Caron, 1985; Kuhnt et al., 1990; Premoli Silva and Sliter, 1994, 1999; Nederbragt and Fiorentino, 1999; Paul et al., 1999; Keller et al., 2001, 2004; Coccioni and Luciani, 2004; Keller and Pardo, 2004; among others), coincides with the disappearance of R. cushmani. However, according to the most reliable chemostratigraphic and planktonic foraminifer biostratigraphic record across OAE2 (e.g., Accarie et al., 1996; Nederbragt and Fiorentino, 1999; Paul et al., 1999; Hart et al., 2002; Keller et al., 2001, 2004; Keller and Pardo, 2004; Scopelliti et al., 2004; Takashima et al., 2004; Tsikos et al., 2004), the LO of R. cushmani unambiguously precedes the maximum positive carbon-isotope excursion. The sequence of these two events (i.e., LO of R. cushmani and maximum positive carbon-isotope excursion) is also recorded in the Calabianca–Guidaloca and Gubbio sections of Italy (Scopelliti et al., 2004; Tsikos et al., 2004, respectively), even if in the Calabianca–Guidaloca section all the rotaliporids disappear at the same time probably due to a short hiatus. Accordingly, the LO of R. cushmani, found in the Italian sections might correspond, even if roughly, to the real last appearance of the genus. Phase IV (UCI), almost mirroring Phase II except for the absence of rotaliporids, is characterized by the proliferation of opportunistic hedbergellids and schackoinids, indicating that the environment remained ecologically unstable. Phase IV is of similar thickness in all the areas investigated. The end of the declipseT of larger forms marks the onset of Phase V. During Phase V, planktonic foraminiferal abundance and diversity returned to values comparable to those of Phase I, showing gradual recovery of the original ecosystem. However, high numbers of the opportunist hedbergellids suggest that the environmental perturbation related to the Bonarelli Event did not end during Phase III but continued well beyond the deposition of the Corg-layers.

6. Summary and conclusions The high-resolution, generic-level quantitative analysis of planktonic foraminiferal assemblages across the Bonarelli Event (OAE2) in three key sec-

tions, from different areas and geological settings in Italy, reveals the following. (1) The BL equivalents are relatively richer in carbonates, indicating that schackoinids, hedbergellids (H. planispira, H. simplex, H. delrioensis) and globigerinelloids (G. ultramicrus, G. caseyi) tolerated the environmental stresses associated with the Bonarelli Event. (2) Though no mass extinction occurred in planktonic foraminifers across the Bonarelli Event, the extinction of the most specialized forms, i.e., the rotaliporids, and G. bentonensis, is recorded just before its onset. These disappearances just below the BL may be considered as true last occurrences as testified by the absence of these forms within fossiliferous layers from the BL equivalents. Several lines of evidences suggest that the last occurrences of rotaliporids may correspond to the real last appearance of the genus. (3) Several events and biotic changes, including acmes and crises of different genera, can be recognized. They provide evidence both of a progressive and rapid change in palaeoenvironmental conditions, reaching a climax coincident with the Bonarelli Event, and of the subsequent, gradual, although incomplete recovery of previous conditions. (4) Planktonic foraminiferal assemblage patterns indicate five discrete phases of different degrees of environmental perturbation within the marine ecosystem which represent adaptations to changes in chemistry and fertility of the one most extreme warm episodes in the past 150 Ma. (5) The severe palaeoenvironmental perturbation associated with the Bonarelli Event led to assemblages dominated by the small-sized, opportunistic planktonic foraminifera, such as H. planispira and schackoinids and, subordinately, G. ultramicrus, G. caseyi, H. delrioensis and H. simplex, which are useful indicators of extremely stressed environments in low- to middle-latitude, open marine settings during the Cenomanian–Turonian interval. (6) During the Bonarelli Event, dwarfism is a peculiar feature. High-surface productivity coupled with low-oxygen conditions, rapid climatic changes and higher atmospheric CO2 (bbiocalcification crisisQ) may have led to the strong reduction in planktonic foraminiferal test size. (7) Though there are several similarities, our analyses show that each section has its own peculiarities. In particular, the concurrent disappearance of all the

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rotaliporids and G. bentonensis in the Calabianca– Guidaloca and Valdagno sections suggests the occurrence of a short hiatus just below the BL equivalents. (8) The observed spatial and temporal patterns of the foraminiferal assemblages from the three sections result from the interaction of global paleoceanographic perturbations with regional controlling factors such as paleobathymetry, basin physiography, and relative distance from land, carbonate platform and volcanic/hydrothermal source. The most prominent difference is the intensity of the perturbation, which is much stronger in the type-area. This is supported by the BL of the type-area being devoid of planktonic foraminifers, whereas the BL equivalents contain dwarfed planktonic foraminifers, suggesting less extreme environments possibly related to occasionally less eutrophic conditions. Remarkably, in the Valdagno and Calabianca–Guidaloca sections, the small-sized, and presumably low-oxygen tolerant, opportunist heterohelicidids and radiolarians are considerably less abundant than in the type-area. This would suggest a less well-developed OMZ, and less eutrophic conditions, in these settings. (9) The sequence of appearances and disappearances, together with the changes in relative abundances of the genera, contribute to a better understanding of the ecological strategies of Late Cenomanian planktonic foraminifers. When progressive, rapid deterioration of the environmental conditions developed, reaching the climax in coincidence of the Bonarelli Event, some species and genera responded by showing a preference for the new conditions, others by showing varying levels of tolerance or intolerance. These kinds of behaviour are reflected in the shifting patterns of species diversity, dominance, abundance, and size that extend well outside the established limits of variability. The first taxa to disappear were the more specialized ones, and the survivors were the generalists with greater tolerance to environmental stress. Similarly, the forms proliferating across the critical intervals and the first colonizers were opportunists, typically very small in size.

Acknowledgements This manuscript was improved thanks to suggestions and reviews by E.A.M. Koutsoukos, C.R.C.

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Paul, and M.A. Lamolda. We thank Luca Giusberti for helping us with the field work in the Venetian Prealps. This research was supported by MIUR COFIN 2001 to R.C. and MIUR ex 60% to R.C. and V.L. Centro di Geobiologia dell’Universita` degli Studi di Urbino contribution no. 8.

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