Cambios en los foraminíferos a través del límite Paleoceno/Eoceno en el corte de Zumaya, España: registro batial de una extinción en masa gradual

Lamia Zili ^{1 *}, Dalila Zaghbib–Turki ¹, Laia Alegret ², Ignacio Arenillas ², and Eustoquio Molina ²

¹ Département de Géologie, Faculté des Sciences de Tunis, Université Tunis–El Manar, 2090, Tunisia.^* lamia_2b@yahoo.fr

² Departamento de Ciencias de la Tierra, Universidad de Zaragoza, 50009 Zaragoza, Spain.

ABSTRACT

An integrated study of benthic and planktonic foraminiferal assemblages across the Paleocene/Eocene boundary at the Zumaya section (Spain) has been carried out in order to analyse the short period that is commonly known as the Initial Eocene Thermal Maximum, and its impact on the foraminiferal assemblages. Benthic foraminiferal assemblages from uppermost Paleocene and lowermost Eocene sediments at the Zumaya section contain abundant representatives of the calcareous Velasco–type fauna and of the agglutinated flysch–type fauna, indicating a lower bathyal depth of deposition. The onset of the carbon isotope excursion, which marks the Paleocene/Eocene boundary, is recorded at the base of a 40–cm thick grey marly interval (unit U2), and it coincides with the beginning of a Benthic Foraminiferal Gradual Extinction. The pattern of extinction is adjusted more to a gradual and rapid episode rather than to a catastrophic sudden event as was proposed initially. The Paleocene/Eocene benthic foraminiferal extinction is followed by an acme of acarininids (among planktonic foraminifers) and of agglutinated benthic foraminifers, referred here as Agglutinated–Acarinina peak, which is interpreted as the result of global warming, carbonate corrosivity and environmental stress during the Initial Eocene Thermal Maximum. The occurrence of a dissolution interval above the extinction event, where agglutinated benthic foraminifers are abundant and calcareous foraminifers are scarce to absent, is compatible with the global rise of the lysocline and Calcite Compensation Depth in the lower Eocene, due to the increase in partial pressure of oceanic CO₂ and therefore, in the deep ocean water corrosiveness.

Key words: Acarinina, benthic foraminifers, gradual mass extinction, warming, late Paleocene, early Eocene, Zumaya section, Spain.

RESUMEN

Se realiza un estudio integrado de las asociaciones de foraminíferos bentónicos y planctónicos del límite Paleoceno/Eoceno en el corte de Zumaya (España) para analizar el corto periodo denominado máximo termal del Eoceno inicial, y su impacto en las asociaciones de foraminíferos. Las asociaciones de pequeños foraminíferos bentónicos de los sedimentos del Paleoceno terminal y del Eoceno inicial en Zumaya contienen abundantes representantes de la fauna calcárea de tipo Velasco y de la fauna aglutinada de tipo flysch, características de una profundidad de depósito batial inferior. El inicio del cambio isotópico, que marca el límite Paleoceno/Eoceno, está registrado en la base de un intervalo de margas grises (unidad U2) de 40 cm de potencia, y coincide con el comienzo de una Extinción Gradual de Foraminíferos Bentónicos. El patrón de extinción se ajusta más a un episodio gradual y rápido que a un evento súbito catastrófico como fue propuesto inicialmente. La extinción de los foraminíferos bentónicos del Paleoceno/Eoceno es seguida por una abundancia de acarinínidos (entre los foraminíferos planctónicos) y de foraminíferos bentónicos aglutinados, referida en este trabajo como pico de Aglutinados–Acarinina, el cual es interpretado como el resultado del calentamiento global, corrosividad de carbonatos y desestabilización medioambiental durante el máximo térmico del Eoceno inicial. La presencia de un intervalo de disolución tras el evento de extinción, donde abundan los foraminíferos bentónicos aglutinados y los foraminíferos calcáreos son escasos o ausentes, es compatible con una subida global de la lisoclina y del nivel de compesanción de la calcita en el Eoceno inferior debido al aumento de la presión parcial del CO₂ oceánico y, por tanto, de la corrosividad del las aguas profundas oceánicas.

INTRODUCTION

During the last decades, much research has been focused on the Paleocene–Eocene interval transition, on the study of the rapidity and nature of the warming event that is associated to this interval, its ultimate cause, and its effects on the marine and terrestrial biota, including the mass extinction suffered by benthic foraminifers (see review by Thomas, 2007). This major extinction of benthic foraminifers is commonly known as the Benthic foraminiferal Extinction Event or BEE (Tjalsma, 1977; Schnitker, 1979; Tjalsma and Lohmann, 1983; Thomas, 1990), and its record has been traditionally placed at the Paleocene/Eocene (P/E) boundary. Benthic foraminiferal assemblages were indeed affected by a major environmental disturbance that has been related to the Initial Eocene Thermal Maximum (IETM, also known as the Paleocene Eocene Thermal Maximum, PETM) (e.g., Thomas and Shackleton, 1996; Thomas et al., 2000; Alegret et al., 2005; Zachos et al., 2005; Alegret and Ortiz, 2006). The benthic foraminiferal extinctions affected 30–50 % of the species in the deep sea (Thomas, 1990; Katz and Miller, 1991; Thomas and Shackleton, 1996; Thomas, 2007; Alegret et al., 2009a, 2009b), whereas the extinctions were less severe in marginal and epicontinental basins (Thomas, 2003; Alegret et al., 2005; Alegret and Ortiz, 2006). This benthic foraminiferal extinction occurred within a short period, with an estimated duration between ~3 and 17 kyr (Speijer et al., 1997; Schmitz et al., 1997; Kaiho et al., 2006; Alegret et al., 2009a, 2009b), shortly after a negative shift in δ¹³C values (carbon isotope excursion, CIE) in bulk carbonate in marine and continental sections (Shackleton et al., 1985; Kennett and Stott, 1991; Arenillas et al., 1999; Röhl et al., 2000; Thomas, 2003, 2007).

The most abrupt global warming event in the Cenozoic occurred in coincidence with the IETM, coeval with the BEE and the CIE (Zachos et al., 2001, 2005). Several mechanisms have been proposed in order to explain the climate and geochemical anomalies across the IETM, the most plausible hypothesis being the dissociation of methane hydrates along the continental margins, which would increase the amount of δ¹³C–depleted carbon released into the atmospheric and oceanic reservoirs (Dickens et al., 1995; 1997; Sluijs et al., 2007; Thomas, 2007). In some sections, these anomalies are associated with dark organic–rich deposits (Speijer, 1994; Bolle et al., 1999; Kaiho et al., 2006; Aubry et al., 2007), suggesting that the oxygen minimum zone occurred at the seafloor in some epicontinental basins across the P/E boundary. Oxygen depletion may have resulted from oxidation of methane in the ocean, local increased productivity or carbonate dissolution (Dickens et al., 1997; Thomas, 2003, 2007; Kaiho et al., 2006; Sluijs et al., 2007; Zeebe and Zachos, 2007), triggering disturbance in benthic foraminiferal assemblages. A severe carbonate dissolution has been documented from many parts of the oceans in coincidence with the isotopic and geochemical anomalies (Canudo and Molina, 1992a, 1992b; Dickens et al., 1997; Guernet and Molina, 1997; Arenillas and Molina, 2000; Alegret et al., 2005; Thomas, 2007), and a 2 km rise of the Calcite Compensation Depth (CCD) has been inferred for the southeastern Atlantic (Zachos et al., 2005; Thomas, 2007). Carbonate dissolution and shallowing of the CCD may also have resulted from methane oxidation in the ocean or atmosphere. However, there is no independent evidence for globally increased or decreased productivity or carbonate dissolution, nor for global anoxia or dysoxia (Thomas, 2007), and more studies are needed to understand the nature and consequences of the IETM. Isotopic and geochemical anomalies, carbonate dissolution and abrupt changes in foraminiferal assemblages linked to the IETM have been identified in Spanish sections (Molina et al., 1994, 2003; Arenillas and Molina, 1996; Lu et al., 1996; Alegret et al., 2009a, 2009b), including the Zumaya section (Basque–Cantabrian Basin), which contains one of the most complete and expanded deep–water successions across the Paleocene–Eocene transition so far reported (Coccioni et al., 1994; Canudo et al., 1995; Ortiz, 1995; Orue–Etxebarria et al., 1996; Sztràkos, 1996; Schmitz et al., 1997; Pardo et al., 1997; Molina et al., 1999; Arenillas and Molina, 2000; Alegret et al., 2009a). High resolution analyses of benthic foraminiferal assemblages carried out for the Zumaya section show that the P/E extinction affected 30 % to 55 % of abyssal and bathyal benthic foraminiferal species (Ortiz, 1995; Schmitz et al., 1997; Alegret et al., 2009a). This extinction, recorded in the middle part of the Morozovella velascoensis Biozone (Arenillas and Molina, 2000), also coincides with a negative shift in δ¹³C (Schmitz et al., 1997). In order to elucidate the benthic foraminiferal extinction pattern at the base of the IETM interval and to reconstruct the palaeoenvironmental evolution, we carried out a detailed study of benthic and planktonic foraminiferal assemblages across the Paleocene/Eocene boundary at the Zumaya section, and compared it with previous results on planktonic foraminifers.

Material and methods

The Zumaya section is located in northern Spain (43°18'00.35"N and 2°15'35.17"W), near the locality of Zumaya (Guipúzcoa province, Basque Country, western Pyrenees), on the Itzurun beach (Punta Mariantón). The access to the Zumaya section is easy by San Telmo beach (Figure 1). The Zumaya section contains one of the most complete and expanded deep–water successions across the Paleocene–Eocene transition (Molina et al., 1999). For this reason, multidisciplinary studies have been carried out across the Paleocene–Eocene transition in this section, including magnetostratigraphic, isotopic, cyclostratigraphic and micropalaeontological analyses (Canudo et al., 1995; Ortiz, 1995; Arenillas and Molina, 1996; Orue–Etxebarria et al., 1996; Kuhnt and Kaminski, 1997; Schmitz et al., 1997; Arenillas and Molina, 2000; Alegret et al., 2009a).

The total thickness of the studied section is 310 cm (Figure 2). We have distinguished five lithological units in this stratigraphical interval. The lower units (U1 and U2) were deposited during the latest Paleocene and the upper units (U3, U4 and U5) during the earliest Eocene:

– Unit U1 (50 cm) consists of decimetric–bedded grey marls–limestones and clay intercalations. It contains abundant well preserved planktonic and benthic foraminifers (Figure 2).

– Unit U2 (60 cm) consists of a massive grey calcareous bed, with a thin turbiditic bed at its base, below the benthic extinction event (Schmitz et al., 1997, 2001).

– Unit U4 (150 cm) consists of reddish brown clays. This unit is rich in gypsum crystals (especially in samples Z8, Z9, Z13, Z15), and oxidized pyrite (e.g., Z15 sample). At the base of this unit, the planktonic and benthic foraminifers are very rare (from Z9 to Z14). When they exist, the calcareous tests present differential dissolution features. Few specimens show pyritized tests (e.g., Tappanina selmensis and Nuttallides truempyi).

– U5 (~20 cm) consists of reddish to grey clays rich in gypsum crystals. Foraminiferal tests are still affected by dissolution, but less intensely than in the previous interval.

Fourteen samples weighing 200 g were collected from the Zumaya section; these were spaced at 10 cm intervals close to the P/E boundary (i.e., U3 and first half of U4) and at 50 cm to 1 m intervals below and above it. All samples were washed through three sieves (250 µm, 100 µm and 63 µm) and the obtained residues were dried. When possible, about 300 specimens of benthic foraminifers were picked up (from Z4 to Z8 and from Z15 to Z17, see data on Table 1). In sample Z4, the foraminifers were very abundant, for this reason an Otto micro–splitter was used allowing to obtain an available fraction occurring non–selective grained size and containing about 300 specimens. The total residues from the other samples (i.e., from Z9 to Z14) were used because the foraminifers there are very scarce and strongly affected by dissolution (<100 specimens per sample). Within the total dissolution interval, agglutinated tests dominate the assemblages because calcareous planktonic and benthic foraminiferal tests were completely dissolved. Calcareous–cemented, agglutinated foraminifera were also probably dissolved in this interval, which is therefore dominated by organic–cemented agglutinated foraminifera.

All counted species (Table 1) were mounted on micro–slides for a permanent record and deposited in the Invertebrate Paleontology, Paleoecology and Biostratigraphy Laboratory–Research Unit (DPS): 02/UR/10–02 at the Faculty of Sciences of Tunis. Most of the identified species were photographed under a reflected light microscope. The planktonic foraminiferal quantitative information is based on data by Arenillas and Molina (2000). The environmental deposition at the Zumaya section may be deduced from the range and tolerance depth of species composing different benthic foraminiferal assemblages (Figure 2). Based on benthic foraminiferal data, we attempted to infer the palaeobathymetry, faunal turnover and pattern of extinction. The identification of benthic foraminiferal species is mainly based on Ellis and Messina (Catalogue of Micropalaeontology, 1940 to present), Tjalsma and Lohmann (1983), Van Morkhoven et al. (1986), Alegret and Thomas (2001), Kaminski and Gradstein (2005), Ortiz (2006), and Alegret and Ortiz (2006).

PLANKTONIC FORAMINIFERAL BIOSTRATIGRAPHY

Planktonic foraminiferal ranges and zonations

We have mainly used the planktonic foraminiferal zonations proposed by Molina et al. (1999) and Berggren and Pearson (2005). In Figure 3, we compare the recent P/E planktonic foraminiferal zonations for middle–low latitude areas. The most used standard P/E biozones (Figure 4), based on index species are Luterbacheria pseudomenardii (synonym of Planorotalites), Morozovella velascoensis and Morozovella subbotinae zones, named P4, P5 and P6 by Berggren et al. (1995). Berggren and Pearson (2005) proposed a new alphanumeric notation for the Paleogene zones, using the prefix "P" for the Paleocene zones and "E" for the Eocene ones (Figure 3). According to their zonal definitions, Biozone P5 spans M. aequa, M. gracilis and A. berggreni subzones by Molina et al. (1999), and E1 and E2 are equivalent to A. sibaiyaensis and P. wilcoxensis subzones by Molina et al. (1999), respectively. According to Berggren and Pearson (2005), the estimated ages of the lower and upper boundaries of E1 are 55.50 and 55.35 Ma, respectively. New astronomical calibrations of the Paleocene suggest an age of 55.53 to 56.33 Ma for the P/E boundary (Westerhold et al., 2008). A radiometric calibrated age of approximately 55.8 Ma for the P/E boundary was previously proposed by Westerhold et al. (2007), suggesting that the lower and upper boundaries of E1 are, respectively, 55.8 and 55.65 Ma, and the top of the revised section is approximately 55.74 Ma in age. According to Berggren and Pearson (2005), the lower boundary of E1 coincides with the P/E boundary (55.8 Ma), although this contradicts the biostratigraphical data from the Zumaya section.

The stratigraphical distribution of planktonic foraminiferal species across the P/E boundary at the Zumaya section is based on Arenillas and Molina (2000). The P/E boundary, officially defined in coincidence with the major negative excursion in δ¹³C, was recognized near the base of the carbonate dissolution interval and the main foraminiferal extinction horizon in the middle part of the chronozone C24r and the middle part of the M. velascoensis Zone (= P5 by Berggren et al., 1995). The beginning of the δ¹³C decrease precedes the main benthic foraminiferal disturbance horizon and the carbonate dissolution interval, and it approximately coincides with the base of the A. berggreni Subzone. The δ¹³C negative shift is close to the base of the A. sibaiyaensis Subzone at the Zumaya section.

Quantitative stratigraphical distribution

The study of the quantitative stratigraphical distribution of species and genera by Arenillas and Molina (2000) showed relevant events across the P/E boundary at the Zumaya section. Their quantitative analyses indicated a major increase in low latitude acarininids coinciding with the CIE interval, similar to that recognized by Canudo and Molina (1992a) and Canudo et al. (1995). As illustrated in Figure 4, the Acarinina increase and the Morozovella decrease coincide with the δ¹³C and δ¹⁸O shifts across the P/E boundary at the Zumaya section (Figures 4 and 5), according to data by Schmitz et al. (1997) and Arenillas and Molina (2000).

The planktonic foraminiferal species richness is about 40 species per sample in the uppermost Paleocene, and assemblages suggest relatively temperate superficial waters, dominated by Atlantic currents. In the uppermost Morozovella gracilis Subzone, the relative abundance of Morozovella increases up to ~27 %, suggesting a slight increase of superficial water temperature. The lower part of the A. berggreni Subzone is characterized by rapid and gradual increase of Acarinina, reaching 39 % of the assemblages immediately below the planktonic foraminiferal dissolution intervals (Figure 5). This percentage is only surpassed by Subbotina (~50 %), whereas Morozovella decreases suddenly to ~4 % of the planktonic assemblages. The Acarinina acme spans the A. berggreni and A. sibaiyaensis subzones (Arenillas and Molina, 2000; and Figure 4) and includes species such as A. esnaensis, A. wilcoxensis, A. triplex, A. strabocella and A. apanthesma. In this stratigraphical interval, the first record of new compressed acarininids species occurs, including A. berggreni, A. sibaiyaensis, A. africana and A. quetra. Arenillas and Molina (2000) did not identify Morozovella allisoniensis at the Zumaya section. The evolution and proliferation of this species during the IETM (Kelly et al., 1995, 1998; Speijer and Wagner, 2002) seem to be restricted to tropical sea water.

Canudo and Molina (1992a), Canudo et al. (1995) and Arenillas and Molina (2000) noticed two planktonic foraminiferal dissolution intervals (PFDI–1 and PFDI–2) across the A. berggreni and A. sibaiyaensis subzones (Figure 4). Between these two dissolution intervals, they identified a ~50 cm thick level in the lower part of the A. sibaiyaensis Subzone, corresponding to the unit U5 at the top of the revised section (Figure 5). This level contains planktonic foraminiferal assemblages with abundant Acarinina (~38 %) and Subbotina (~45 %), whereas percentages of Morozovella (~8 %) continue to be relatively low. The abundance of "large" morozovellids (including M. velascoensis, M. acuta and M. parva) seems to decrease across the A. sibaiyaensis and P. wilcoxensis subzones at the Zumaya section. The "large" morozovellids abundance decreases suddenly near the P/E boundary, from an average of ~5 % in the uppermost Paleocene to ~0.3 % across the IETM. Its abundance returns to ~2 % in the upper part of M. velascoensis Zone, but it does not reach the pre–P/E boundary values. On the contrary, the "small" morozovellid group (that includes M. subbotinae, M. aequa, M. lacerti, M. gracilis, M. marginodentata and M. edgari) increases in abundance before the IETM (Arenillas and Molina, 2000). At the Zumaya section, its pre–P/E abundance is ~14 % in average, its IETM abundance is ~6 %, and its post–IETM abundance is ~28 %. The biconvex morozovellids, e.g., M. occlusa and M. cf. albeari (=M. crosswicksensis by Arenillas and Molina, 2000), show a quantitative distribution similar to the "large" morozovellids but with slightly lower values (pre–P/E abundance of ~2 %, IETM abundance of ~0.2 %, and post–IETM abundance of ~1.5 %).

PALAEOBATHYMETRY

Among calcareous taxa, representatives of the bathyal and abyssal Velasco–type fauna (Tjalsma, 1977; Tjalsma and Lohmann, 1983; Van Morkhoven et al., 1986; Alegret et al., 2003, 2009a) are common (e.g., Nuttallides truempyi, Aragonia velascoensis, A. aragonensis, Bulimina trinitatensis, B. tuxpamensis and Stensioeina beccariiformis; Figure 2). The benthic assemblages also include abundant deep–water agglutinated taxa (Ortiz, 1995; Kaminski and Gradstein, 2005) such as Karrerulina conversa, Spiroplectammina spectabilis, Haplophragmoides spp., Trochamminopsis spp., Glomospira charoides, Reticulophragmoides jarvisi and Hyperammina dilatata (Figure 2). These agglutinated taxa represent more than 25 % of the assemblages (Figure 5A). On the basis of the benthic foraminiferal assemblages composition, we infer a lower bathyal environment of deposition for the uppermost Paleocene and lowermost Eocene at the Zumaya section, exceeding 600 m depth in agreement with Ortiz (1995) and Alegret et al. (2009a).

The detailed analysis of benthic foraminifers from the Zumaya section allow us to identify several assemblages through the uppermost Paleocene and lowermost Eocene interval:

Uppermost Paleocene assemblages

Benthic foraminifers are abundant in the uppermost Paleocene, and their assemblages are very diversified (Figure 2). Units 1 and 2 contain mixed calcareous and agglutinated species. Anomalinoides (A. welleri, A. rubiginosus), Cibicidoides pseudoperlucidus, Coryphostoma midwayensis, Nodosaria spp., Nuttallides truempyi, Dentalina spp., Lenticulina spp., Oridorsalis umbonatus and Stensioeina beccariiformis are common among calcareous taxa. Diverse assemblages of agglutinated foraminifers such as Ammodiscus glabratus, A. peruvianus, Bathysiphon spp., Nothia robusta and Spiroplectammina spectabilis are also present. The benthic foraminiferal assemblages from the two basal units (U1 and U2) are dominated by infaunal morphogroups. These assemblages composition characterized by high species richness and various morphotypes indicate a normal–oxic environment and stable mesotrophic to oligotrophic conditions (Kaminski et al., 1995; Jorissen et al., 1995) at the seafloor during the deposition of Units U1 and U2 at the latest Paleocene.

Benthic foraminiferal gradual mass extinction (BFGE) in the earliest Eocene

The onset of the carbon isotope excursion, i.e., the Paleocene/Eocene boundary, is recorded at the base of a grey clay interval at the Zumaya section (i.e., at the base of U3; Figures 4 and 5d). A gradual pattern of Last Occurrence Data (LODs) of benthic foraminiferal species has been observed within the lower 40 cm of the clay interval (Z5–Z8 corresponding to unit U3, Figures 2 and 6):

(1) the LODs of Stensioeina beccariiformis and Astacolus barksdalei are recorded ~0–5 cm above the onset of the CIE;

(2) the LODs of species such as Allomorphina trochoides, Astacolus ovatus, Gaudryina inflata, Bulimina midwayensis, Bolivinoides delicatulus, Aragonia velascoensis, Osangularia plummerae, Cibicidoides alleni, Gaudryina pyramidata, Eponides megastoma and Hyperammina dilatata are observed ~20–25 cm above the onset of the CIE;

(3) the LODs of Anomalinoides rubiginosus, Cibicidoides hyphalus, Pullenia coryelli, Clavulinoides amorpha, Coryphostoma midwayensis, Dorothia beloides, Osangularia velascoensis, and Gyroidinoides globosus are recorded ~30–35 cm above the Paleocene/Eocene boundary;

(4) the LODs of Remesella varians, Recurvoides retroseptus, Dorothia retusa, Cibicidoides dayi and Anomalinoides acuta are observed ~40–45 cm above the onset of the CIE.

In this grey clay interval (unit U3), the gradual pattern of extinction observed just after the negative excursion of δ¹³C occurred when the environmental conditions were dramatically deteriorated (Speijer et al., 1997; Alegret et al., 2009a).

Benthic foraminiferal assemblages within the interval of total dissolution of calcareous tests

A ~50 cm–thick interval (at the base of unit U4; samples Z9 to Z13), where benthic foraminiferal tests are affected by intense carbonate dissolution, is recorded above the BFGE interval (~50 cm above the onset of the CIE). Within this dissolution interval, the different samples contain very few benthic foraminifers (8–46 specimens/sample), and quantitative analysis from these samples is not reliable. For this reason, the percentages of the species and various benthic foraminiferal indices have not been plotted in Figure 6. Only agglutinated benthic foraminifers such as Karrerulina conversa, Bathysiphon spp., Ammobaculites jarvisi and Reticulophragmoides jarvisi have been found within this interval. A similar dissolution interval has been identified in the neritic stratotype section for the P/E boundary in Dababiya Quarry (Egypt), where agglutinated benthic foraminifers may have taken advantage of a high–stress, probably strongly fluctuating environment (Alegret et al., 2005; Alegret and Ortiz, 2006). Similarly, in addition to carbonate dissolution, environmental stress may have affected the benthos during deposition of the lower half of Unit 4 at the Zumaya section.

Benthic foraminiferal assemblages above the basal dissolution interval

Within the upper half of Unit 4 (Z14–Z15) several calcareous benthic foraminiferal specimens reappear, although their tests are still affected by dissolution suggesting that carbonate dissolution was not as intense as in the lower half of Unit 4.

In sample Z14, Nuttallides truempyi and Bulimina tuxpamensis show partial dissolution, whereas agglutinated taxa (e.g., Karrerulina horrida, Glomospira charoides, Saccammina placenta) dominate the assemblages.

In sample Z15 benthic foraminifers are still affected by dissolution. The relevant assemblage is oligotaxic, containing slightly more abundant and more diversified benthic foraminiferal species than Z14 assemblage. Nuttallides truempyi is relatively more abundant among those having calcareous hyaline tests (Figure 6). This epibenthic species may have been resistant to carbonate corrosivity (Jorissen et al., 2007) and is also tolerant to oligotrophic conditions (Tjalsma and Lohmann, 1983; Nomura, 1991; Jorissen et al., 1995; Speijer et al., 1997; Alegret et al., 2001; Thomas, 2007). Other calcareous (e.g., Anomalinoides praeacuta and Cibicidoides pseudoperlucidus) and agglutinated epifaunal taxa (e.g., Glomospira charoides and Bathysiphon spp.) are recorded within this interval suggesting more favourable conditions.

Abundant Tappanina selmensis and other taxa such as Spiroplectammina spp., Bulimina tuxpamensis, Pleurostomella spp., Pullenia quinqueloba and Aragonia aragonensis are also recorded in sample Z15 (Figure 6). Tappanina selmensis is common in the post–extinction interval, like at other sites and sections worldwide (e.g., Thomas, 2007), and may indicate stressed seafloor conditions (Boltovskoy et al., 1991; Takeda and Kaiho, 2007).

Assemblages from Unit 5 are strongly dominated by Nuttallides truempyi, pointing to oligotrophic conditions at the seafloor. Other common species are Bulimina tuxpamensis, Aragonia aragonensis and Tappanina selmensis among calcareous taxa, and Reticulophragmoides jarvisi, Spiroplectammina, G. charoides, Bathysiphon, Ammodiscus, and Saccammina placenta among agglutinated taxa.

DISCUSSION

The benthic foraminiferal assemblages from upper Paleocene and lower Eocene sediments at the Zumaya section contain abundant representatives of the Velasco–type fauna and the agglutinated flysch–type fauna, and indicate a lower bathyal depth of deposition, in agreement with Ortiz (1995). The benthic and planktonic foraminiferal assemblages show major disturbance and turnover across the Paleocene–Eocene transition at the Zumaya section. The upper Paleocene (upper part of the M. gracilis Subzone) is characterized by diversified assemblages of planktonic foraminifers, which are dominated by subbotinids and "large" morozovellids. These planktonic foraminiferal assemblages indicate relatively temperate surface waters, dominated by Atlantic currents. The benthic foraminiferal assemblages are diverse, and they contain mixed calcareous and agglutinated species of the Velasco–type fauna. These assemblages suggest normal conditions and environmental stability in surface waters as well as at the seafloor. The benthic foraminiferal assemblages during the upper Paleocene are highly diversified and indicate oxygenated and mesotrophic to oligotrophic conditions at the seafloor. Moreover, the occurrence of abundant species with calcareous tests indicates deposition above the CCD.

The IETM is marked, at the Zumaya section, by a red clayey bed in which the CIE is recorded (Schmitz et al., 1997). A several per mille negative excursion in marine and terrestrial δ¹³C values (which is recorded at sites and sections worldwide, as in Zumaya), is related to a rapid input of isotopically light carbon into the ocean–atmosphere system. Several hypotheses have been proposed to account for this input, being the massive dissociation of marine methane hydrates (Dickens et al., 1995) the most widely accepted one. Dissociation of marine methane hydrates has been related to changes in ocean circulation, continental slope failure in the North Atlantic Ocean, sea–level drop, impact of an extraterrestrial body, volcanism, or to a combination of these factors (see references in Thomas, 2007; Moore and Kurtz, 2008). The ultimate causes of the CIE and of the global warming recorded across the IETM are beyond the scope of this paper. However, analysis of benthic and planktonic foraminiferal turnover may throw light on the environmental consequences of the IETM.

It is broadly accepted that the foraminiferal turnover at the Zumaya section, especially the quantitative acme of the planktonic foraminifers Acarinina spp. and the severe benthic foraminiferal extinction, was likely caused by the palaeoenvironmental changes related to the IETM (Canudo et al., 1995; Schmitz et al., 2001; Alegret et al., 2009b). According to these data, the IETM begins at the base of the A. berggreni Subzone. The Acarinina species proliferating across the IETM (A. esnaensis, A. wilcoxensis, A. triplex, A. strabocella and A. apanthesma) are common in warm waters of the Tethys, suggesting that the Acarinina excursion in the Tethyan region was also related to increased global temperatures (Molina et al., 1999). However, other tropical–subtropical groups such as "large" and biconvex morozovellids suddenly decreased in abundance (Arenillas and Molina, 2000), suggesting that the palaeoenvironmental changes during the IETM were probably more complex and other environmental factors (nutrients, water corrosivity, oxygenation, symbionts, etc.) affected the planktonic foraminiferal assemblages.

The gradual –but rapid– pattern of extinction of benthic foraminifers at the Zumaya section suggests that rapid (~10 kyr to ~17 kyr; Schmitz et al., 1997; Alegret et al., 2009a) palaeoenvironmental changes occurred at the beginning of the IETM. The onset of the mass extinctions coincides with the onset of the CIE and is close to the planktonic foraminiferal turnover, suggesting that all these events are linked. Consequently, the A. berggreni Subzone is a very significant stratigraphical interval. The BFGE is followed by a sudden increase in the relative abundance of agglutinated taxa and acarininids. We have designated the Agglutinated–Acarinina peak as the AApeak, representing the horizon where the increase in agglutinated benthic foraminifers and planktonic acarininids are first recorded (Figures 5A and 5C), although these acmes continue upward across the red clayey bed (Arenillas and Molina, 2000). This horizon seems to mark a first thermal maximum pulse across the basal part of the IETM interval, although global warming and other palaeoenvironmental changes started before (Zachos et al., 2003; Giusberti et al., 2007; Sluijs et al., 2007).

Succeeding this gradual extinctions (BFGE) interval, the base of the red clayey bed coincides with the base of a dissolution interval. This later interval contains oligotaxic benthic foraminifera assemblage composed of only agglutinated specimens. This assemblage is typical of environments with undersaturated carbonate waters, which are deposited below the CCD. Moreover, these oligotaxic assemblages may indicate stressed conditions at the sea floor.

The carbonate dissolution intervals might be the result of a progressive global rise of the lysocline and CCD, due to the increased partial pressure of CO₂, and therefore, of the deep ocean water corrosiveness (Dickens et al., 1997; Arenillas et al., 1999; Arenillas and Molina, 2000; Dickens, 2001).

The CCD may have reached the bottom waters shortly after the beginning of the IETM at Zumaya, initiating the total dissolution interval that is recorded at the base of the red clayey bed (see Arenillas and Molina, 2000). However, calcareous benthic foraminiferal tests are well preserved below the dissolution interval, and the gradual and rapid pattern of extinctions of benthic foraminifers reported here, which started well below the dissolution interval, suggests that carbonate corrosiveness was not the main cause of the benthic foraminiferal extinctions event. The beginning of the BFGE is recorded at the onset of the CIE, indicating that some kind of environmental stress, not related to carbonate dissolution, triggered the benthic foraminiferal extinctions. Severe global warming is the only major cause that may have induced the benthic foraminiferal disturbance in all oceans and at all latitudes (Thomas, 2007; Alegret et al., 2009a, 2009b).

Although there are some samples where calcareous foraminiferal tests can be found (e.g., samples Z15, Z16, Z17), the dissolution interval spans all red clayey beds in the uppermost A. berggreni and A. sibaiyaensis subzones. Across this interval, the assemblages are still dominated by agglutinated taxa, but some small–sized calcareous benthic foraminifers have been identified (e.g., Tappanina selmensis, Nuttallides truempyi and Aragonia aragonensis). This size reduction affecting the benthic foraminiferal tests was probably related to environmental stress.

Benthic foraminiferal species richness is still low towards the top of the studied interval (Figure 5B), suggesting that environmental conditions at the seafloor had not recovered in the A. sibaiyaensis Subzone. The benthic foraminiferal turnover at the Zumaya section is compatible with a rapid onset of the IETM anomalies lasting a time period <20 kyr as documented by Röhl et al. (2000). However, a return to more normal conditions occurred over longer time scales.

CONCLUSIONS

The benthic and planktonic foraminiferal turnover across the Paleocene–Eocene transition at the Zumaya section illustrates the impact of the IETM on lower bathyal foraminiferal dwellers. A gradual –but rapid– pattern of benthic foraminiferal mass extinctions (BFGE) has been identified. The base of this gradual extinctions interval coincides with the onset of CIE (i.e., with the P/E boundary). The top of this interval coincides with the base of a dissolution one. A global cause, such as warming of the oceans, must have triggered the benthic foraminiferal mass extinctions in all oceans and all latitudes.

We identified the Agglutinated–Acarinina peak (AApeak) 40 cm above the P/E boundary. This represents the horizon where the increase in agglutinated benthic foraminifers and planktonic acarininids are first recorded, although these acmes continue upward across the red clayey bed. The Acarinina species thriving across the IETM suggest a rise of tropical–subtropical taxa toward higher latitudes; thus we speculate that the AApeak might mark a first thermal maximum pulse in the basal part of the IETM interval, although global environmental changes (such as global warming) started earlier, possibly triggering the benthic foraminiferal mass extinctions.

A dissolution interval, containing oligotaxic agglutinated benthic foraminiferal assemblages, spans the A. berggreni Subzone and the A. sibaiyaensis Subzone. Carbonate dissolution might be the result of a progressive upward migration of the lysocline and CCD due to the increased partial pressure of CO₂, possibly resulting from methane oxidation in the ocean or atmosphere.

The species richness of the benthic foraminiferal assemblages is still low towards the top of the studied interval (~55.44 Ma), suggesting that environmental conditions at the seafloor had not yet entirely recovered.

ACKNOWLEDGEMENTS

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