Benthic foraminiferal assemblage turnover during intensification of the Northern Hemisphere glaciation in the Piacenzian Punta Piccola section (Southern Italy)

Palaeogeography, Palaeoclimatology, Palaeoecology 333–334 (2012) 59–74

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Benthic foraminiferal assemblage turnover during intensification of the Northern Hemisphere glaciation in the Piacenzian Punta Piccola section (Southern Italy) Franca Sgarrella a,⁎, Valentino Di Donato a, Rodolfo Sprovieri b a b

Università degli Studi di Napoli “Federico II”, Dipartimento di Scienze della Terra, Largo S. Marcellino 10, 80138, Napoli, Italy Università di Palermo, Dipartimento di Geologia e Geodesia, via Archirafi 22, 90123, Palermo, Italy

a r t i c l e

i n f o

Article history: Received 23 June 2011 Received in revised form 29 February 2012 Accepted 10 March 2012 Available online 21 March 2012 Keywords: Benthic foraminifera Palaeoecology Sapropelites Piacenzian

a b s t r a c t We present the results of a high-resolution analysis of the benthic foraminiferal assemblages at the Punta Piccola section (Stratotype for the Piacenzian Stage), which spans the gradual climate transition of the intensification of the Northern Hemisphere glaciation (3.6–2.6 Ma). This study highlighted a major benthic foraminiferal fauna turnover, which started at about 3.05 Ma with LO of Cibicidoides italicus, registered the gradual decline of Stilostomella spp. and culminated at about 2.7–2.75 Ma, when the dominant Siphonina reticulata was replaced by Cibicidoides pachyderma, costate Bulimine, spinose Bulimine, spinose Uvigerine and the Bolivina dilatata group. Four compositional zones, identified by constrained cluster analysis, are indicative of palaeoenvironmental changes and document the transition from stable and mainly oligotrophic conditions to unstable, mesotrophic and more fluctuating bottom conditions. Two intervals of deposition of sapropelite clusters coded as O and A, investigated using both benthic and planktic assemblages, reveal that anoxia conditions were never reached. Planktic foraminifera in the sapropelite layers of cluster O indicate deep mixing and benthic foraminifera suggest an increase in export productivity to the sea floor. By contrast, planktic foraminifera in the uppermost sapropelite layers of cluster A indicate oligotrophic surface water conditions, stratification and more eutrophic subsurface water conditions, without deep mixing. The benthic foraminifera indicate hypoxic and eutrophic bottom conditions, and evidence the first episode of down-slope transport, which testifies to a strengthening of runoff and stratification of superficial waters, but not true stagnation. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The most recent benthic foraminiferal fauna turnover occurred during the middle Pleistocene when elongate, cylindrical cosmopolitan deep-sea species with complex apertural shapes disappeared (Hayward, 2002). This group gradually declined in abundance from the Late Pliocene, during the period of intensification of Northern Hemisphere Glaciation (NHG) (Zachos et al., 2001; Thomas, 2007). Several studies show pulsed declines especially during glacial periods, with partial interglacial recoveries (Hayward, 2002; Hayward et al., 2006; Hayward et al., 2007; O'Neill et al., 2007; Thomas, 2007). More recently, Hayward et al. (2009) documented this event in two pulses during the Late Pliocene (3.1–2.7 Ma) and the late Early Pleistocene also in the Mediterranean area. Turnover of benthic foraminiferal assemblages in the Mediterranean Sea, related to cooling conditions during the upper Pliocene, has been recorded by Van der Zwaan (1983) and Sprovieri (1986). Verhallen (1991) described changes in the foraminiferal benthic

⁎ Corresponding author. E-mail address: [email protected] (F. Sgarrella). 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2012.03.009

assemblages during the latest Piacenzian–early Pleistocene in land sections of southern Italy (Calabria), characterized by three sapropelite clusters informally coded as A, B and C (Verhallen, 1987). The author highlighted the strong role of oxygen, suggesting an increase in oxygen deficiency from the Late Pliocene onward, which lay at the origin of repeated sterilisation of the bottom. The benthic foraminiferal assemblages of these sapropelite groups showed a rhythmic pattern of opportunistic, stress-tolerant species and ‘in equilibrium’, stress non-tolerant species. To investigate the Piacenzian segment of this benthic foraminiferal turnover in the central part of the Mediterranean Sea, we studied the Punta Piccola section (Fig. 1), which is the unit stratotype for the Piacenzian Stage, covering the time interval between about 3.6 and 2.58 Ma (Lourens et al., 1996). Benthic foraminifera at this locality were previously investigated quantitatively by Brolsma (1978) using low-resolution sampling. In this paper we propose a detailed quantitative study of the benthic foraminifera through the same section as that of Sprovieri et al. (2006), in order to reconstruct the local palaeoecological evolution of the bottom waters. This section spans the gradual climate transition of intensification of the Northern Hemisphere glaciation (NHG) (Mudelsee and Raymo, 2005). The Pliocene climate optimum (from

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about 3.25 to 3.205 Ma) and short term glaciations M2–MG2 and MIS110 are included in our section. The lithostratigraphy of the section was reconstructed in detail on the basis of lithology, isotope and planktonic foraminifera distribution and abundance fluctuation (Lourens et al., 1996; Sprovieri et al., 2006). Sprovieri et al. (2006) provided a high-resolution analysis of planktic assemblages in the Punta Piccola section and demonstrated the astronomical control over the quantitative fluctuation of the planktic foraminifera Globigerinoides group. This group is essentially sensitive to hydrographic changes in the surface waters more or less directly induced by insolation forcing. 2. The Punta Piccola section The well-known Punta Piccola section, a stratigraphic segment of the Rossello composite (Hilgen, 1991b), outcrops some 10 km west of Agrigento (Fig. 1) along the road from Porto Empedocle to the Rossello beach. It is the main reference for the Piacenzian Stage, of which it represents the unit stratotype. Along the total thickness of 54.30 m the Trubi Formation is present in its lower 14 m and the marly Monte Narbone formation (with discrete laminated levels) is present in the remaining upper part. The oxygen isotope data and the sequence of the lithological cycles were described by Hilgen (1991b), who also provided the astro-chronology of the middle part of the “sapropel layers” of the section. The Punta Piccola section is referable to MPl4a– MPl5a (middle part) of the planktic foraminifera biostratigraphy (Sprovieri, 1993). The section has been extensively studied (Hilgen, 1987; de Visser et al., 1989; Hilgen and Langereis, 1989; Zachariasse et al., 1989; Langereis and Hilgen, 1991; Van Os et al., 1994). It is

Fig. 1. Location of Punta Piccola section.

considered a reference section for the orbital calibration of the lower middle Pliocene time scale (Hilgen, 1991b). The GSSP (Global Stratotype Section and Point) of the Piacenzian was defined in lithological cycle 77 (Castradori et al., 1998) and the base of the Gelasian is recorded at its top, where a reddish laminitic level can be clearly correlated to the Nicola bed of the Monte San Nicola section, GSSP of the Gelasian (Rio et al., 1998). Two clusters of sapropelites, informally coded as O (cycles 102, 103, 105, 106 and 107) and A (cycles 114–119) occur (Hilgen, 1991a; Lourens et al., 1996) in the section. Cycles 110–113 are considered composite, containing an extra cycle caused by the influence of obliquity (Hilgen, 1991b; Lourens et al., 1996). All the lithological cycles reported by Hilgen (1991b) were visually identified and their sequence was checked by comparing our biostratigraphic data with the bioevents reported by Zachariasse et al. (1989) and Hilgen (1991b). 3. Material and methods Samples of about 50 g of sediment were collected by an electric power driller with a small cylindrical core (7 cm long, with a diameter of 5 cm). Each sample was drilled at the top of the underlying one, obtaining a continuous 5 cm sampling sequence. The lowermost sample was drilled at the base of the white wall outcropping along the road (lithological cycle 77). The section was then sampled up to the base of the blackish level outcropping at the top of the slope (lithological cycle 114, A1). The uppermost part of the section was sampled along the small slope outcropping about 50 m to the east, where the basal laminated level may be correlated with lithological cycle 114. Along this small section six thicker lithological cycles outcrop, in which the sediment accumulation rate increases compared to the lower part of the section. In this part of the total sequence the samples were collected about every 15 cm. A total of 841 samples were studied by Sprovieri et al. (2006) and provided a high-resolution calcareous plankton biostratigraphy. The age model for the section is based (Sprovieri et al., 2006) on biostratigraphic events used as reference points (Fig. 2). In this study, the benthic foraminiferal assemblages were examined about every 10–15 cm and quantitative analysis was carried out on 471 samples. About 200–300 specimens of benthic foraminifera were counted from the residues greater than >125 μm. The list of key species is reported in Appendix 1. Some species, taxonomically close to one another, are similar in some aspects and show specimens which are difficult to separate in quantitative analyses. For this reason the following species are lumped together: Uvigerina mediterranea and U. peregrina, reported as costate Uvigerine; Uvigerina auberiana and U. proboscidea, reported as spinose Uvigerine; Bolivina dilatata, B. alata and B. spathulata, reported as Bolivina dilatata group; Bulimina costata and B. inflata, reported as costate Bulimine. Moreover, Bulimina aculeata and its morphological variation sensu Verhallen (1991) are reported as spinose Bulimine. The analysis of benthic foraminiferal assemblages was carried out by means of compositional data analysis (CODA) methods, under the statistical theory developed in the last few decades following the seminal work of Aitchison (1986). Our data analysis first aimed to obtain a zonation of the Punta Piccola section. This was done by means of constrained cluster analysis (CCA) (Grimm, 1987), re-adapted to CODA (Di Donato et al., 2008, 2009). CCA preserves the stratigraphic order of samples by forcing each sample or already formed clusters to be grouped with preceding or following ones. The algorithm can be simply adapted to compositional data by basing the analysis on a matrix of Aitchison distances (Aitchison, 1992) among samples, which are equal to the Euclidean distances among log-centred variables (Aitchison, 1986). This transformation requires a zero substitution procedure. Following Daunis-i-Estadella et al. (2008), zero replacement was carried out by adopting a Bayesian approach, based on a posteriori

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Fig. 2. Punta Piccola section. Magnetostratigraphy and numbering of lithologic cycles are from Hilgen (1991a, 1991b). The letter S indicates the position of sapropel layers throughout the sedimentary section. Circled numbers and letters indicate the following: 1, FO G. crassaformis (3.592 Ma); 2, LO G. puncticulata (3.563 Ma); 3, reappearance G. crassaformis (3.361 Ma); 4, FO G. bononiensis (3.323 Ma); 5 LO Sphaeroidinellopsis spp. (3.211 Ma); 6, LO D. altispira (3.175 Ma); 7, FO N. atlantica (2.854 Ma); and A, LCO D. tamalis (2.823 Ma). Correlation among lithologic record and precession and insolation curves (La041,1) from Laskar et al., 2004. From Sprovieri et al., 2006 modified.

estimation of the parameter of the multinomial distribution with Jeffreys and Uniform priori (Walley, 1996). In order to reduce the amount of zero values requiring substitution, only the most abundant species were included in the CODA, discarding species with scattered occurrences in the intervals analysed.

The benthic foraminifera of the Punta Piccola section recorded the Last Occurrence (LO) of Cibicidoides italicus. Therefore, as regards the zonation of the section, the samples located below this extinction level were considered as belonging to a distinct interval, regardless of CCA. This is because the zeros in the percentages of C. italicus can

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be considered absolute zeros (Aitchison and Kay, 2003) for the samples located above its LO. As a consequence, in the CODA approach, the distance between the samples located below and above this level can be considered as infinite. Constrained cluster analysis was coupled with relative variation biplots (RVB) (Aitchison and Greenacre, 2002), a technique based on singular value decomposition of the covariance matrix of logcentred data to investigate the relationships among the variables as well as those among variables and samples. Methods and properties for the interpretation of the results can be found in Aitchison and Greenacre (2002). Although form biplots, which are scaled in order to give a better representation of samples, were computed to obtain scores for the two first axes along the section, our analysis centred on covariance biplots, in which distances (links) between the apexes of the vectors originating from the origin, each of which represents a variable, are approximations of the standard deviation of the corresponding log-ratios. For the above-mentioned statements, RVB for the interval below the LO of C. italicus was carried out separately. For the upper interval, the row points representing the samples were symbolised within the biplot according to the zonation obtained through CCA. Finally, an RVB was also carried out separately to gain an insight into the upper interval defined by means of CCA, which includes sapropelite cluster A. 4. Results 4.1. Benthic foraminiferal distribution The relative abundance fluctuations of species or taxonomic groups, expressed as percentages, are reported in Fig. 3a,b, with the more significant species being grouped in Fig. 3a. The most important bioevent is the Last Occurrence (LO) of Cibicidoides italicus (Fig. 3a) at 19.15 m (lithological cycle 102). It is also noteworthy that spinose Bulimine italicus (Fig. 3a) is recorded only above 14 m, close to the Trubi/Monte Narbone boundary. Siphonina reticulata (Fig. 3a) is the dominant species from the base to about 35–40 m. Cibicidoides ungerianus, Planulina ariminensis (Fig. 3a), Gyroidina spp., Cibicidoides robertsonianus and Pullenia spp. (Fig. 3b) are other important taxa. In the upper part of the section Cibicidoides pachyderma (Fig. 3a) and Bulimina (Fig. 3a) and Uvigerina (Fig. 3a) species are dominant. Oridorsalis umbonatus and Melonis barleeanus (Fig. 3b) are relatively abundant from the base up to 20 m. Anomalinoides helicinus and Stilostomella spp. (Fig. 3a) decrease regularly from the base to about 35 m. By contrast, some species show an increasing trend upwards: spinose Bulimine display scattered high values from 20.85 m, but very high pulsating abundance from 40 m upwards; costate Bulimine and costate Uvigerine are abundant from about 35 m, C. pachyderma increases from about 38 m and C. ungerianus shows an increasing trend with high fluctuations from about 40 m upwards. In the topmost part of the section, from about 50 m, Hoeglundina elegans and Valvulineria complanata (Fig. 3b) increase, the latter showing peaks of very high dominance (60% and 30%). 4.2. Compositional data analysis As shown in Fig. 4, within Punta Piccola section 4 the main intervals were distinct, from BF1 to BF4.

dilatata gr., A. helicinus, S. reticulata, costate Uvigerine and costate Bulimine with respect to B. albatrossi, must be considered with caution. It is also noteworthy that most taxa are located near the origin of the biplots. This implies a low standard deviation of the log-centred variables, which in turn indicates a low contribution of these taxa to the variability of the data set. A possible explanation for this poor result is that within this interval stable conditions prevail, such that the variability is mainly related to random changes, with a high singularity of taxa. Also the rounded shape of the cloud of row points does not indicate a clear trend in the data, apart from the increase in B. albatrossi recorded between 7 and 11 m, highlighted by the row points located near the apex of the corresponding vector. 4.2.2. Upper INTERVALS (above the LO of C. italicus) The taxa included in the analysis of the upper intervals are reported in Fig. 6. The variability accounted for by the first two axes of the RVB is respectively 29.22% and 13.70% of the total. The succession was divided into three main intervals: BF2, BF3 and BF4. In the RVB of Fig. 6 axis 1 opposes spinose and costate Bulimine and spinose Uvigerine with S. reticulata, A. helicinus, S. schumbergeri, Quinqueloculina spp. and arenaceous, while axis 2 opposes C. pachyderma and G. subglobosa with Stilostomella spp., Lenticulina spp., Bolivina gr. dilatata and V. complanata. The longest links, corresponding to relatively high standard deviations in the corresponding log-ratios, are those between S. reticulata and costate Bulimina column points, between S. reticulata and spinose Bulimine and between the latter and C. pachyderma. It is noteworthy that even if S. reticulata and C. pachyderma have a large log-ratio variability, as testified by the length of the corresponding link, they are not opposed along axis 1. Finally, it can be noted that several taxa, including Gyroidina spp., H. elegans, H. rodiensis, C. robertsonianus, Pullenia spp. and C. ungerianus, are located near the origin of the biplot. As noted above, this indicates a low contribution of these taxa to total variability. The RVB of the upper intervals (Fig. 6) shows the transition from a system characterised by S. reticulata (compositional zone BF2) to an oscillating state, as indicated by the dispersion of samples belonging to compositional zone BF4, between the abundance of C. pachyderma and G. subglobosa and that of costate Bulimine, spinose Bulimine, spinose Uvigerine, Bolivina dilatata gr., Stilostomella spp. and V. complanata. Fig. 7 illustrates the results of the RVB carried out for the interval BF4. The first and second axes of the biplots account respectively for 45.06% and 12.38% of total variability. Within the biplots three groups of taxa with the largest relative variation can be distinguished. The first is represented by C. pachyderma, arenaceous, S. reticulata, P. ariminensis, G. subglobosa, A. helicinus and deep miliolids, located on the positive side of axis 1. The second and third groups are both located on the negative side of axis 1, although they are located on opposite sides of axis 2. They are represented respectively by Bolivina dilatata gr. and V. complanata and by spinose Bulimine and spinose Uvigerine. Interestingly, C. pachyderma and S. reticulata, which showed the opposite relationship in long-term variations, within this portion of succession are characterised by a low log-ratio standard deviation, as indicated by the shortness of the link connecting the apex of their vectors. This means that after the strong reduction of S. reticulata detected around 40 m, these species tend to covariate. 5. Discussion 5.1. Ecological preferences of species

4.2.1. Lower INTERVAL (below the LO of C. italicus) The taxa included in the analysis of compositional zone BF1 are reported in Fig. 5. C. pachyderma and the spinose Bulimine are very rare in this interval and were not considered. The RVB provided a poor result for the analysis of this interval, the first two axes only accounting for about 25% of total variability. Hence the relationships highlighted in the biplot, especially the counterposition between Bolivina

It has been widely suggested that recent deep-sea benthic foraminifera are dependent on food availability, in terms of productivity exported to the sea floor, which is necessary to meet their energy requirements (Loubere and Fariduddin, 1999), and on oxygen bottom and pore-water content (e.g. Corliss, 1985; Gooday, 1988; Herguera and Berger, 1991; Barmawidjaja et al., 1992; Gooday, 1993; Jorissen

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Fig. 3. a and b. Distribution of the selected benthic foraminifera throughout the Punta Piccola section. Species which were rare and present in a small number of samples are not reported.

et al., 1995; Jorissen, 1999; Jorissen and Wittling, 1999; De Rijk et al., 2000; Schmiedl et al., 2000; Fontanier et al., 2002, 2003, 2006). The quality of organic matter, the timing of the input (constant or pulsed) and the penetration depth of oxygen in the sediment also affect the microhabitats of the benthic foraminifera species (Jorissen et al., 2007, and references therein). In Recent benthic ecosystems, the relationship between export productivity and oxygen bottom and pore water content is complex. However, there is a general consensus that oligotrophic and highly oxygenated environments are relatively enriched in superficially living taxa, whereas eutrophic and oxygenlimited environments are relatively dominated by deep infaunal species.

The ecological requirements of the most significant species of the Punta Piccola section are reported in Appendix 2. We also provide (Table 1) simplified ecological information as regards oxygen and food parameters of the taxa which vary greatly within the assemblages. In the compositional data analysis of intervals BF2–BF4, axis 1 opposes species characteristic of oxic bottom conditions such as S. reticulata, A. helicinus deep miliolids, and arenaceous species with those characteristic of hypoxic and eutrophic bottom conditions, such as spinose Bulimine, spinose Uvigerine and costate Bulimine. Among the oxic species, the presence of deep miliolids, which disappear when oxygen concentrations fall below critical values (Jorissen, 1999; Kuhnt et al., 2007), suggests that oxygen content is the most important parameter of axis 1.

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Fig. 4. Constrained cluster analysis and compositional zones based on benthic foraminiferal assemblages of the Punta Piccola section.

Axis 2 of the same interval also opposes species characteristic of oxic and oligotrophic bottom conditions such as C. pachyderma and G. subglobosa with those found in hypoxic and eutrophic bottom conditions such as Stilostomella spp., Lenticulina spp., Bolivina dilatata gr. and V. complanata. The compositional data analysis limited to the BF4 interval again shows the opposition between species characteristic of oxic and/or oligotrophic bottom conditions such as C. pachyderma, arenaceous, S. reticulata, P. ariminensis, G. subglobosa, A. helicinus, and deep miliolids versus species characteristic of hypoxic and eutrophic bottom conditions. This analysis grouped the oxic species, separated in the previous analysis, on the same axis; while the hypoxic–eutrophic species are again split, with B. dilatata gr. and V. complanata separated from spinose Bulimine and spinose Uvigerine. Both analyses appear to indicate a variance in the benthic ecosystem influenced, to different extents, by an interplay of fluctuations of oxygen bottom content and food flux.

As shown above, CODA did not provide reliable results for the BF1 interval. To illustrate the changes in oxygen content and food bottom supply along the section, an alternative approach was tried by separating the species in Table 1 into the following two groups: Group A, which includes species which generally prefer oxic and/or oligotrophic environments: S. reticulata, Cibicidoides spp., G. subglobosa, P. ariminensis, arenaceous, miliolids, H. elegans and A. helicinus; Group B, which includes species which are related to high food supply and are more or less tolerant of low oxygen content: spinose Bulimine, spinose Uvigerine, costate Uvigerine, costate Bulimine, Bolivina dilatata gr., Stilostomella spp., and V. complanata. Two diagrams were then constructed, based on the cumulative percentages of the taxa of Group A and Group B. They were informally termed “oxic/oligotrophic” and “hypoxic/eutrophic”, respectively, their distributions along the section being reported in Fig. 8. Moreover, to evaluate changes in species richness along the Punta Piccola section, an indicative species number, including the taxonomic

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Fig. 5. Covariance biplot of benthic foraminiferal assemblages of compositional zone BF1 of Punta Piccola section. 1) Bolivina dilatata group, 2) Anomalinoides helicinus, 3) Bolivina albatrossi, 4) costate Bulimina, 5) Cibidoides italicus, 6) Cibicidoides ungerianus, 7) Globocassidulina subglobosa, 8) Gyroidina spp., 9) Hanzawaia rodiensis, 10) Stilostomella spp, 11) Melonis barleanum, 12) Lenticulina spp., 13) Oridorsalis umbonatus, 14) Cibicidoides robertsonianus, 15) Planulina ariminensis, 16) Pullenia spp., 17) Quinqueloculina spp., 18) Sigmoilopsis schlumbergerii, 19) Siphonina reticulata, 20) Sphaeroidina bulloides, 21) costate Uvigerina, 22) spinose Uvigerina, 23) arenaceous.

Fig. 7. Covariance biplot of benthic foraminiferal assemblages of compositional zone BF4 of the Punta Piccola section. 1) Anomalinoides helicinus, 2) Hoeglundina elegans, 3) Planulina ariminensis, 4) Globocassidulina subglobosa, 5) spinose Bulimina, 6) Sphaeroidina bulloides, 7) Cibicidoides pachyderma, 8) Cibicidoides ungerianus, 9) spinose Uvigerina, 10) Siphonina reticulata, 11) costate Uvigerina, 12) costate Bulimina, 13) Quinqueloculina spp., 14) Bolivina dilatata group, 15) Bolivina albatrossi, 16) Melonis barleanum, 17) Gyroidina ssp., 18) Valvulineria complanata, 19) arenaceous.

units previously listed, is reported in Fig. 8. The highest values are found between about 18 and 38 m, whereas the upper part of the section shows decreasing values.

5.2. Interpretation of results 5.2.1. Palaeodepht The dominant species are commonly distributed in the depth-range of about 600–800 m in the modern sediments (Van Morkhoven et al., 1986; Murray, 1991; Sgarrella and Moncharmont Zei, 1993), with C. robertsonianus being recorded deeper than 450 m (Van Morkhoven et al., 1986). This epibathyal environment was also suggested by Brolsma (1978), Sprovieri (1986) and Sgarrella et al. (1999) for the Trubi Formation. Since this assemblage straddles the Trubi/Monte Narbone Formations we suppose that no significant bathymetric differences are recorded between the two lithologic units. Continuous and relatively abundant distribution of C. robertsonianus throughout the section corroborates this interpretation.

5.2.2. Long-term environmental changes Cluster analysis divides the section into four intervals, which show gradual phases of the change in the structure of the benthic foraminiferal assemblages and the evolution of bottom conditions. The most important benthic foraminiferal turnover occurs from about 35 and 40 m, when dominant S. reticulata is replaced by Cibicidoides pachyderma and by species of Bulimina and Uvigerina (Fig. 3a). This interval falls in the range of 2.75 and 2.7 Ma which corresponds to the onset of major NHG (Lisiecki and Raymo, 2007).

Fig. 6. Covariance biplot of benthic foraminiferal assemblages of compositional zones BF2 to BF4 of the Punta Piccola section. The samples are symbolised according to the zonation of the succession (see Fig. 1) Bolivina dilatata group, 2) Anomalinoides helicinus, 3) Bolivina albatrossi, 4) costate Bulimina, 5) spinose Bulimina, 6) Cibicidoides pachyderma, 7) Cibicidoides ungerianus, 8) Globocassidulina subglobosa, 9) Gyroidina spp., 10) Hanzawaia rodiensis, 11) Hoeglundina elegans, 12) Stilostomella spp., 13) Melonis barleanum, 14) Lenticulina spp, 15) Oridorsalis umbonatus, 16) Cibicidoides robertsonianus, 17) Planulina ariminensis, 18) Pullenia spp., 19) Quinqueloculina spp., 20) Sigmoilopsis schlumbergerii, 21) Siphonina reticulata, 22) Sphaeroidina bulloides, 23) costate Uvigerina, 24) spinose Uvigerina, 25) Valvulineria complanata; 26) arenaceous.

5.2.2.1. BF1 compositional zone (3.63–3.05 Ma BP). S. reticulata is the dominant species together with C. ungerianus, and epifaunal P. ariminensis, A. helicinus and C. italicus (Fig. 3a,b). The strong dominance of these taxa living at the sediment–water interface suggests a food-limited, rather oligotrophic environment and oxic bottom conditions during this interval. Peaks of abundance of B. albatrossi (Fig. 3b) and Bolivina dilatata gr.(Fig. 3a) may testify to short periods of enhanced productivity.

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Table 1 Ecological preferences of dominant benthic foraminiferal species based on: Jorissen, 1987, 1988; Corliss, 1991; Loubere, 1991; Barmawidjaja et al., 1992; Sen Gupta and MachainCastillo, 1993; Gooday, 1994; Rathburn and Corliss, 1994; Mackensen et al., 1995; Schmiedl et al., 1997; De Stigter et al., 1998; Jorissen et al., 1998; Altenbach et al., 1999; Bernhard and Sen Gupta, 1999; Jorissen, 1999; Kaiho, 1999; De Rijk et al., 2000; Schmiedl et al., 2000; Morigi et al., 2001; Rasmussen et al., 2002; Fontanier et al., 2002, 2003; Gooday, 2003; Schmiedl et al., 2003; Mackensen and Licari, 2004; Licari and Mackensen, 2005; Schönfeld and Altenbach, 2005; Murray, 2006; Fontanier et al., 2006, 2008; Abu-Zied et al., 2008; Melki et al., 2009; Mojtahid et al., 2009; Melki et al., 2010. The term hypoxic is used sensu Jorissen et al. (2007). Species

Microhabitat

Food

Bottom oxygen

Anomalinoides helicinus Bigenerina nodosaria Cibicidoides pachyderma Cibicidoides italicus Globocassidulina subglobosa deep Miliolids Hoeglundina elegans Planulina ariminensis Siphonina reticulata

Epifaunal Shallow infaunal Shallow infaunal Epifaunal Infaunal Shallow infaunal Shallow infaunal Epifaunal Shallow infaunal

– Meso-eutrophic Oligo-mesotrophic – Oligotrophic Oligo-mesotrophic Oligotrophic Oligotrophic –

Oxic Oxic, tolerant hypoxic Oxic Oxic Oxic Oxic Oxic Oxic Oxic

Bolivina dilatata group costate Bulimine spinose Bulimine Lenticulina spp. Stilostomella spp. spinose Uvigerine costate Uvigerine Valvulineria complanata

Shallow to deep infaunal Shallow infaunal Intermediate to deep infaunal Shallow infaunal Possibly infaunal Shallow infaunal Shallow infaunal Shallow infaunal

Meso- to eutrophic Meso- to eutrophic Eutrophic – Eutrophic Eutrophic Meso-eutrophic Eutrophic

Hypoxic Hypoxic Hypoxic Hypoxic Hypoxic Hypoxic Oxic, tolerant hypoxic Hypoxic

5.2.2.2. BF2 compositional zone (3.05–2.77 Ma BP). On the whole, the BF2 interval is more or less similar to BF1, since S. reticulata (Fig. 3a) dominates again and this is indicative of relatively stable conditions. Nevertheless, between the BF1 and BF2 intervals, the assemblage structure gradually changed because from about 20 m epifaunal C. italicus was replaced by infaunal spinose Bulimine, which became abundant with strong pulsations (Fig. 3a), and the hypoxic/ eutrophic group shows a pulsating increase (Fig. 8). This relative frequency increase in deep infaunal taxa may be the result of an

increased organic flux (Jorissen et al., 1995). In addition, also the increase in indicative species number in the BF2 interval compared to BF1 (Fig. 8) suggests a transition to slightly mesotrophic bottom conditions where the faunal diversity is at a maximum and faunal assemblages comprise epifaunal, shallow infaunal and deep infaunal species (Schmiedl et al., 2000). 5.2.2.3. BF3–BF4 compositional zone (2.77–2.58 Ma BP). Relative variation biplots of upper interval faunal assemblages (Fig. 6) evidence

Fig. 8. Distribution of the indicative species number and the informal groups of benthic foraminifera throughout the Punta Piccola section.

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the transition from a system characterised by S. reticulata (compositional zone BF2) to an oscillating state, as indicated by the dispersion of samples belonging to the compositional zone BF4, between the abundance of C. pachyderma and G. subglobosa and that of costate Bulimine, spinose Bulimine, spinose Uvigerine, Bolivina dilatata gr., Stilostomella spp. and V. complanata. Moreover, the indicative species number decreases during BF4 compared to BF2. It is well known that stable ecosystems favour the development of complex and highly diverse faunas, whereas in ecosystems that exhibit severe environmental fluctuations diversity is generally low (Schmiedl et al., 2003). Therefore, this change implies a transition from stable (BF2) to unstable (BF4) bottom conditions. This interpretation is supported by the replacement, among the oxic species, of S. reticulata with the opportunist C. pachyderma more able to compete in an unstable environment. Among the benthic foraminifers, S. reticulata and Stilostomella spp. are especially affected by this important change. Since these taxa are absent or poorly represented in modern sediments, we consider that their distributions in the fossil record explain the strong decreasing trend in the upper part of the section. The extinction of the Stilostomella genus was widely described. The so-called “Stilostomella Extinction” (Weinholz and Lutze, 1989) has been recorded in most parts of the world's oceans during the midPleistocene Transition (MPT) (Hayward, 2002; Hayward et al., 2006; Kawagata et al., 2006; O'Neill et al., 2007). This event affected only certain elongate, cylindrical shells, often uniserial, which show a pulsed decline through the Late Pliocene to the MPT. As reported above (Hayward et al., 2009), this group declined in abundance and diversity in two pulses in Mediterranean ODP Sites. The first occurred during the Late Pliocene (3.1–2.7 Ma) and correlates with the reduction in the Punta Piccola section. The decline of these taxa has been related to palaeoceanographic changes during a time of enhanced northern hemisphere ice formation. In particular, decreased temperature and/or increased oxygenation, and changes in food supply conditions are suggested as the principal causes.

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As regards the genus Siphonina, a sharp reduction occurred in the North Atlantic area during the middle Miocene (King, 1989). Sgarrella et al. (1999) suggested that this reduction occurred during a period of change in deep bottom water circulation, when Northern Component Water-proto NADW was established (Wright and Miller, 1996) and bottom temperatures may have decreased. Moreover, we also highlighted the fact that in the Tyrrhenian Sea (ODP 107, Site 654) a similar trend of bioevents occurred with LO of C. italicus followed by the reduction of S. reticulata (Sprovieri and Hasegawa, 1990). The decrease in S. reticulata and Stilostomella spp. in the Punta Piccola section is followed by the short term glaciation of MIS 110 (about 2.7 Ma). It therefore seems to indicate a similar response to palaeoceanographic changes triggered by decreasing temperatures. Parallel to this change we observe the strong increase in planktic Turborotalita quinqueloba from 38.73 m upward (Sprovieri et al., 2006). This species is considered indicative of cold-cool, high fertility surface waters. It is noteworthy that this abrupt increase is also reported by Lourens et al. (1996) and continues upwards during the Pleistocene. We also note that the size of fluctuations of many taxa increases along the section. This trend is particularly evident in the distribution of C. ungerianus (Fig. 3a), a species which is continuously present and abundant along the section, and has the highest fluctuations in the upper part, during the intervals of deposition of sapropelite clusters A. Also“hypoxic/eutrophic” and “oxic/oligotrophic” groups show the same trend (Fig. 8). Summarising, the benthic turnover in the Punta Piccola section occurs in the time interval of 2.7–2.75 Ma and corresponds to the climate cooling linked to the intensification of the NHG. The assemblage shows the transition from stable and mainly oligotrophic conditions versus unstable and mesotrophic bottom. Large fluctuations of “oxic/oligotrophic” and “hypoxic/eutrophic” groups (Fig. 8) in the upper part of the section are indicative of large pulses of productivity and oxygenation compared to the basal pattern.

Fig. 9. Distribution of indicative species number, hypoxic/eutrophic and oxic/oligotrophic groups, and the planktic species G. bononiensis throughout cluster O of the Punta Piccola section.

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Thomas (2007) suggested that benthic faunal turnover during the Cenozoic related to global cooling may reflect increased oxygenation or increased seasonality in food delivery to the sea floor. According to this interpretation, we suggest that in the upper part of the Punta Piccola section, more fluctuating conditions are indicative of increased seasonality, which in turn affect food flux and bottom oxygenation. Superimposed upon these long trend events, benthic assemblage structures have also registered particular changes during the two intervals of deposition of sapropelite clusters coded as O and A, which will be discussed in detail in the following section. 5.2.3. Ecosystem variability of sapropelite clusters coded as O and A Dark layers of the Punta Piccola section are considered sapropels by Hilgen (1991b), while Combourieu Nebout et al. (2004) suggested the term ‘sapropelic sediment’ as more appropriate since these levels rarely reach high organic carbon content. The first noteworthy result of the analyses of both sapropelite clusters is the continuous presence and relative abundance of benthic foraminifera in the dark layers, in the fraction > 125 μm. In the foraminiferal assemblage, Brolsma (1978) recorded peaks of Benthos/Plankton ratio in the dark levels, except in the topmost levels of sapropelite cluster O (bed G, lithological cycles 107) and of sapropelite cluster A (A5). Similarly, in the section of Monte Singa (Verhallen, 1991) the benthic foraminifers are relatively abundant through the sapropelite cluster A in the fraction > 125 μm, with a small reduction in specimen number only in level A5. Bioturbations are recorded in the brown coloured intervals of these sapropelites (Brolsma, 1978). 5.2.4. Sapropelite cluster coded as O Five sapropelites are included between about 18 and 25 m. Dark beds are often laminated and show alternation of light and dark brown coloured thin layers. These laminae are irregular and difficult to sample separately. Therefore our dark samples represent a mixture of these very small changes. The distributions of oxic/oligotrophic and hypoxic/eutrophic groups within this interval are reported in Fig. 9. Whitish marls, which are characterized by the abundance of the oxic/oligotrophic group, suggest a food-limited and well-oxygenated bottom environment. S. reticulata, A. helicinus, arenaceous, deep miliolids and C. pachyderma (Fig. 3a,b) are the dominant species. Dark layers are characterized by abundance of species included in the hypoxic/eutrophic group. Among these species costate Uvigerine (mostly U. peregrina) are dominant (Fig. 3a). The continuous presence and relative abundance of C. ungerianus and P. ariminensis indicate only relative depletion of bottom water oxygenation during sapropelitic levels. Among planktic foraminifers, very high percentages of Globorotalia bononiensis (Sprovieri et al., 2006) occur in these levels (Fig. 9). In the North Atlantic and Mediterranean this species (as G. puncticulata bononiensis) became extinct (2.44 Ma) as Northern Hemisphere glaciation intensified (Scott et al., 2007). Van Os et al. (1994) suggested that productivity was high during deposition of grey layer and sapropel of cycle 102 at Punta Piccola, based on high Ba content and on abundance of G. bononiensis (as G. puncticulata), considered similar to the deep mixing species G. inflata. However, some authors have suggested that G. bononiensis lived at higher temperatures than modern G. inflata and that it was a deep-dwelling species, which possibly lived at a shallower depth than G. inflata (Loubere and Moss, 1986; Becker et al., 2005; Scott et al., 2007). On the whole foraminiferal assemblages recovered in the dark layers testify to relatively high and continuous organic matter supply (U. peregrina) and relatively oxygenated bottom conditions (oxic species), coupled with deep mixing, as indicated by the abundance of G. bononiensis. Only in the uppermost sapropelitic level (cycle 107) does the increasing abundance of the infaunal taxa B. dilatata gr. and Stilostomella, together with the decrease in indicative species number, suggest reduction in oxygen bottom content.

These results are in agreement with mineralogical and geochemical analyses performed by Daux et al. (2006) who documented that lithological cycle 107 of the Punta Piccola section was a true sapropel (pristine organic carbon 7%) and suggested a deposition under oxygen-bearing bottom water. They also highlighted that concentration of the organic carbon was lower than the coeval sapropels cored in deep settings and under anoxic conditions. We suggest that the light laminae in the dark layers possibly indicate intervals with improved bottom water oxygenation and are therefore indicative of no persistently anoxic bottom conditions. Above this interval, the planktic foraminiferal assemblages (as reported in Sprovieri et al., 2006) of the lithological cycles 110–113 are characterized by a marked reduction or absence of deepdwelling Gt. bononiensis, the high abundances of Neogloboquadrina atlantica, which is considered a subpolar cold species (Poore and Berggren, 1975), and an increase in Neogloboquadrina acostaensis. High abundances of Neogloboquadrina are generally well represented in eutrophic water and are related to DCM (Rohling and Gieskes, 1989). Therefore, the planktic assemblages of the interval between the two sapropelite clusters possibly indicate a glacial period, characterized by pycnocline shoaling as a result of sea-level lowering. 5.2.5. Sapropelite cluster coded as A Six cycles with sapropelitic layers and grey marly clays are present between 39 m and the top of the section. Hilgen (1991b) described small increases in the sedimentation rate in cycles 111–113 followed by considerable increase around the lowermost sapropelitic layer A1 (lithological cycle 114), correlated with glacial oxygen isotope stage 110. The author suggested that the glacio-eustatic sea level fall and the related lowering of the base level of erosion yielded an increase in sedimentation rate. Sapropelite cluster A corresponds to compositional zone BF4. The distributions of oxic/oligotrophic, hypoxic/eutrophic groups, indicative species number and some selected planktic species, relative to this interval, are reported in Fig. 10. The “indicative species number” of benthic foraminifera displays reductions within the uppermost three sapropelitic layers. Whitish marls are characterized by dominance of species of the oxic/oligotrophic group (C. pachyderma, P. ariminensis, arenaceous, S. reticulata, S. schlumbergerii, Quinqueloculina spp., A. helicinus, C. wuellerstorfi). H. elegans (Fig. 3a) is abundant only in the uppermost whitish marls (49–54.30 m). This species is considered possibly to have an opportunistic tendency (Abu-Zied et al., 2008). It is also noteworthy that the opportunistic C. pachyderma shows high and rapid fluctuations in abundance within each marl of cycles 114–116 (Fig. 3a). This distribution possibly indicates pulsating events of high oxygen content, at millennial scale. The dark layers (sapropelites) are dominated by species of the hypoxic/eutrophic group. Generally, the dominant assemblage of dark layers changes between different sapropelites, as reported in Table 2, and only spinose Bulimine are quite regularly abundant. Costate Bulimine are poorly represented in level A5; costate Uvigerine are poorly represented in level A2, while they are abundant in the upper part of A4, A4/5 and A5. Bolivina dilatata gr. and V. complanata are abundant only in the uppermost three levels (Fig. 3a). The latter species increases in abundance and is dominant during sapropelite A5. Globobulimina spp. occur with very low percentage values. This complex and fluctuating distribution may reflect the interplay of more than one parameter. An example is given in the sapropelite A5 (about 1 m thick), which shows the abundance of V. complanata and B. dilatata gr. in the middle part, but costate Uvigerine are dominant at the top. As reported above, B. dilatata gr. is resistant to very low oxygen conditions and V. complanata is considered an opportunistic and highly competitive species (Mojtahid et al., 2009; Goineau et al., 2011). In contrast, Uvigerina peregrina might be outcompeted by more

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Fig. 10. Distribution of indicative species number, hypoxic/eutrophic and oxic/oligotrophic groups, and selected planktic foraminifera throughout cluster A of the Punta Piccola section.

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Table 2 Dominant benthic species of the dark layer (sapropelites) of cluster A. Dark layers (sapropelites)

Dominant species

Subordinate

A5

V. complanata, B. gr. dilatata, costate Uvigerine (upper part)

C. ungerianus, spinose Uvigerine, costate Bulimine, spinose Bulimine

A4/5

Spinose Bulimine and costate Uvigerine

C. ungerianus, Bolivina gr dilatata, V. complanata

A4

C. ungerianus, spinose Spinose Bulimine, Uvigerine costate Uvigerine, B. gr. dilatata (basal part), costate Bulimine (base and top)

A3

Spinose Bulimine, costate Uvigerine (basal part)

C. ungerianus, spinose Uvigerine

A2

Spinose Bulimine, costate Bulimine (basal part)

C. ungerianus, Gyroidina spp.

A1

Costate Uvigerine and spinose Bulimine

C. ungerianus

opportunistic species (Licari and Mackensen, 2005). This suggests that high-stress bottom conditions occurred in the middle part of the deposition of sapropelite A5, followed by a gradual amelioration of the bottom environment. Therefore, together with food and oxygen parameters, the relationship between the species and their opportunistic nature are also important factors. Summarising, the benthic assemblage of whitish marls suggests a well-oxygenated and rather oligotrophic bottom environment. In contrast, the characteristic species of sapropelite levels are indicative of more eutrophic, not anoxic but only relatively poorly-oxygenated bottom conditions. A more stressed environment is recorded during deposition of the uppermost three sapropelites, with the reduction of the indicative species number of benthic foraminifera (Fig. 10). The planktic foraminifera (Sprovieri et al., 2006) of this interval are characterized by a continuous abundance of Globigerinoides ruber and Globigerina bulloides both in whitish and in dark layers. Globigerinoides quadrilobatus, Globigerinoides obliquus and N. acostaensis increase in abundance in some intervals of sapropelite layers, whereas T. quinqueloba and Globigerinita glutinata increase in the whitish layers (Fig. 10). In particular, the uppermost four dark layers of sapropelite cluster A are characterized by fluctuating increases of G. quadrilobatus (lithological cycles A3 and A 4) and of G. obliquus (lithological cycles A4/5 and A 5) together with peaks of N. acostaensis (Fig. 10). The distributions of these species of Globigerinoides are indicative of oligotrophic surface waters conditions precessionally forced, induced by summer continental runoff (Sprovieri et al., 2006), while the Neogloquadrina abundance is related to eutrophic water and intensification of the Deep Chlorophyll Maximum (DCM) layer (Rohling and Gieskes, 1989). This planktic foraminiferal assemblage suggests that the deposition of the uppermost dark layers occurred during periods of surface waters stratification and subsurface (intermediate) more eutrophic water mass conditions. Moreover, among benthic foraminifers, the high occurrence (18%) of C. lobatulus, an allochthonous species present in only one sample of the uppermost sapropelite A5, suggests an episode of down-slope transport and supports an increase in river runoff. Interestingly, Hilgen (1991b) considered as sapropels only the uppermost three or four dark layers of sapropelite cluster A. Actually, this suggestion is supported by the distribution of benthic and planktic foraminifera assemblages and the reduction in the indicative species number of benthic foraminifera within the uppermost sapropelitic layers.

5.2.6. Comparison between the two sapropelite clusters In both sapropelite clusters the continuous presence and relatively abundance of benthic foraminifera indicate that the sea-floor was partially ventilated and conditions of anoxia were never reached. The dark layers are correlated with precession minima (Hilgen, 1991b), characterized by intensified rainfall and river runoff linked to an intensified African monsoon circulation. The formation of true sapropels is triggered by an increase in freshwater supply and reduced deep-water circulation or enhanced organic matter flux (e.g. Rossignol-Strick, 1983; Rohling, 1994), or a combination of the two processes. In the Punta Piccola section, vegetation and mineralogical analyses highlighted enhanced continental runoff and high temperatures in the brown layers of cycles 104–108 (Foucault and Mélières, 1995; Combourieu Nebout et al., 2004). The foraminiferal fauna suggests different mechanisms during deposition of dark layers in the two sapropelite clusters. In cluster O planktic foraminifera indicate deep mixing and benthic foraminifera suggest an increase in productivity. By contrast, in the uppermost sapropelites of cluster A planktic foraminifera indicate surface– water stratification, without deep mixing, and more eutrophic subsurface water conditions. The benthic assemblage is indicative of eutrophic and hypoxic bottom conditions, and evidences an episode of down-slope transport, which testifies to a strengthening of runoff and stratification of superficial waters, but not a true stagnation. In the uppermost dark layers of both sapropelite clusters O and A, the number of indicative species decreases, possibly due to repeated events of stressed bottom conditions which dramatically affected the benthic assemblage with disappearance of some non-tolerant taxa. As regards sapropelite cluster A, we compared our results with other sections in southern Italy where this interval is present. The benthic foraminifera relative abundance in Monte Singa, Calabria (Verhallen, 1991) are indicative of similar, not anoxic conditions, but at Monte San Nicola, Sicily (Sprovieri et al., 1986), laminites are devoid of benthic foraminifera, indicative of more dramatic bottom conditions. This implies the importance of local influence. 6. Conclusions On the whole the assemblages of the Punta Piccola section show the transition from stable and mainly oligotrophic versus unstable and mesotrophic bottom conditions. During the intensification of the Northern Hemisphere Glaciation at about 2.75–2.7 Ma, a major benthic foraminiferal turnover is recorded, characterized by: – a decline in Stilostomella spp. as part of the so-called “Stilostomella Extinction event”; – among the oxic species, replacement of the dominant S. reticulata by C. pachyderma, which also has an opportunist behaviour; – an increase in taxa indicative of hypoxic/eutrophic bottom conditions; – the increase in the size of the fluctuations of species and of “hypoxic/ eutrophic” and oxic/oligotrophic groups, considered an amplification of the response of benthic assemblages to palaeoceanographic changes related to precessional forcing. The highest amplitude occurs during the deposition of sapropelite of cluster A, after 2.7 Ma, suggesting more unstable bottom conditions compared to the interval of deposition of sapropelite of cluster O; – among the planktic foraminifera, the strong increase in cold-cool T. quinqueloba in the Punta Piccola section as well in other Mediterranean areas. The gradual decline of warmer G. bononiensis and the increase in cold N. atlantica (2.83 Ma) are also recorded. During deposition of the two sapropelite clusters the benthic foraminiferal assemblages indicate that conditions of anoxia were never reached. However, the foraminiferal fauna suggests different palaeoceanographic conditions. In the dark layers of sapropelite cluster O the strong abundance of planktic foraminifera G. bononiensis indicates

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deep mixing and the benthic foraminifera (mostly U. peregrina) suggests increase of export productivity to the sea floor. In the uppermost dark layers of sapropelite cluster A the planktic foraminifera indicate surface water stratification, more eutrophic subsurface water conditions, without deep mixing, and benthic foraminifera indicate hypoxic and eutrophic bottom conditions. An episode of down-slope transport is recorded only in the uppermost sapropelite A (A5) and testifies to a strengthening of runoff and stratification of superficial waters, but not a true stagnation. Acknowledgments We greatly appreciated the careful reviews by Thierry Corrège, Editor in chief, and anonymous referees, which allowed us to greatly improve the original manuscript. Appendix 1 Anomalinoides helicinus (Costa) = Nonionina helicina Costa, 1857 Bigenerina nodosaria d'Orbigny, 1826 Bolivina albatrossi Cushman, 1922 Bolivina alata (Seguenza) = Vulvulina alata Seguenza, 1862 Bolivina dilatata Reuss, 1850 Bolivina spathulata (Williamson)= Textularia variabilis Williamson var. spathulata Williamson, 1858 Bulimina costata d'Orbigny, 1852 Bulimina aculeata d'Orbigny, 1826 Bulimina inflata Seguenza, 1862 Cassidulina carinata Silvestri, 1896 Cassidulina crassa d' Orbigny, 1839 Cibicidoides ungerianus (d'Orbigny) = Rotalina ungeriana d'Orbigny, 1846 Cibicidoides italicus (di Napoli) = Cibicides italicus di Napoli, 1952 Cibicidoides robertsonianus (Brady) = Planorbulina (Truncatulina) robertsoniana Brady, 1881 Cibicidoides wuellerstorfi (Schwager) = Anomalina wuellerstorfi Schwager, 1866 Cylindroclavulina rudis (Costa) = Glandulina rudis Costa, 1855 Globocassidulina subglobosa (Brady)= Cassidulina subglobosa Brady, 1881 Globobulimina affinis (d'Orbigny) = Bulimina affinis d'Orbigny, 1839 Globobulimina pseudospinescens (Emiliani) = Bulimina pyrula var. pseudospinescens Emiliani, 1949 Gyroidina soldanii (d'Orbigny) = Rotalia soldanii d'Orbigny, 1826 Gyroidinoides laevigatus (d'Orbigny) = Gyroidina laevigata d'Orbigny, 1826 Gyroidinoides neosoldanii (Brotzen)= Gyroidina neosoldanii Brotzen, 1936 Hoeglundina elegans d'Orbigny = Rotalia elegans d'Orbigny, 1826 Karreriella bradyi (Cushman) = Gaudryina bradyi Cushman, 1911 Lenticulina spp Martinottiella communis (d'Orbigny)=Clavulina communis d'Orbigny, 1826 Martinottiella perparva (Cushman)= Listerella communis (d'Orbigny) var. perparva Cushman, 1936 Melonis barleeanum (Williamson)= Nonionina barleeana Willianson, 1858 Planulina ariminensis d'Orbigny, 1826 Pleurostomella alternans Schwager, 1866 Pullenia bulloides (d'Orbigny) = Nonionina bulloides d'Orbigny, 1846 Pullenia quadriloba Reuss = Pullenia compressiuscula Reuss var. quadriloba Reuss, 1867 Pullenia quinqueloba (Reuss) = Nonionina quinqueloba Reuss, 1851 Pullenia salisburyi R.E. & K.C. Stewart, 1930 Sigmoilina tenuis (Czjzek) = Quinqueloculina tenuis Czjzek, 1848

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Sigmoilopsis schlumbergeri (Silvestri) = Sigmoilina schlumbergeri Silvestri, 1904 Siphonina reticulata (Czjzek) = Rotalina reticulata Czjzek, 1848 Sphaeroidina bulloides d'Orbigny, 1826 Stilostomella spp. Uvigerina auberiana d'Orbigny, 1839 Uvigerina mediterranea Hofker, 1932 Uvigerina peregrina Cushman, 1923 Uvigerina proboscidea Schwager, 1866 Valvulineria complanata (d'Orbigny)=Rosalina complanata d'Orbigny, 1846 Vulvulina pennatula (Batsch) = Nautilus pennatula Batsch, 1791

Appendix 2. Ecological preferences of benthic species Among the arenaceous, Bigenerina nodosaria is the most abundant species. It is considered a meso-eutrophic species, positively related to deposition of fresh organic matter (Schmiedl et al., 2000; Fontanier et al., 2008). Bolivina species. B. alata, B. spathulata, and B. dilatata (lumped as B. dilatata gr.) are shallow to deep infaunal taxa, which commonly occur in a wide range of mesotrophic to eutrophic settings, possibly in combination with hypoxic conditions (e.g. Corliss, 1991; Barmawidjaja et al., 1992; Gooday, 1994; De Stigter et al., 1998; Jannink et al., 1998; Bernhard and Sen Gupta, 1999; De Rijk et al., 2000; Schmiedl et al., 2000; Mojtahid et al., 2009; Melki et al., 2010). B. dilatata is particularly abundant in low-oxic to suboxic environments in the Marmara Sea (Alavi, 1988). Jannink et al. (1998) reported B. dilatata as dominant in the upper part of the oxygen minimum zone of the NE Arabian Sea. Moreover, all the species of this group have been reported as taxa especially resistant to low oxygen conditions (Melki et al., 2010 and reference therein). Bolivina albatrossi is reported from sediments with high Corg content and reduced oxygen concentrations (Jorissen et al., 2009 and references therein), but it is more abundant during the last glacial than in the Holocene sediments of the late Quaternary in the Mediterranean Sea (Sgarrella, 1988; Abu-Zied et al., 2008). Since wind-induced mixing was higher in the glacials than during interglacials periods and bottom was well ventilated (Schmiedl et al., 2003; Abu-Zied et al., 2008), the relative abundance of B. albatrossi during last glacial suggests that this species tolerates only moderate oxygen reductions. Verhallen (1991) quoted B. dilatata as opportunist and B. albatrossi as intermediate between opportunist and in equilibrium species. Accordingly, we consider that B. dilatata is possibly more tolerant to oxygen reduction than B. albatrossi. Spinose Bulimine (B. aculeata) are also considered opportunistic, adaptable to changes in oxygenation, food availability and quality (Schmiedl et al., 2000). The occurrence of B. aculeata and B. marginata under anoxic conditions in the Bay of Biscay seems related to macrofaunal burrows with increased bacterial activity (Fontanier et al., 2002). C. pachyderma lives in oxic microhabitats (>2 ml/l of O2) and oligo- to mesotrophic, well ventilated conditions (Fontanier et al., 2002; Schmiedl et al., 2003; Melki et al., 2009). It is considered an opportunistic species characteristic of a varying organic supply in relatively oligotrophic or oligo-mesotrophic settings (Schmiedl et al., 2003; Abu-Zied et al., 2008; Melki et al., 2009). To support these ecological requirements, we also note that C. pachyderma was more abundant in deep sites of the eastern and western Mediterranean Sea during the last glacial compared to Holocene and Recent sediments (Sgarrella, 1988; Kuhnt et al., 2007; Abu-Zied et al., 2008; Melki et al., 2009). Actually, in the Mediterranean basin during Pliocene and Pleistocene glacial periods more saline surface waters probably increased the production of Mediterranean deep water that was cooler and more oxygenated than in interglacial periods (Hayward et al., 2009).

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G. subglobosa is reported as an infaunal species (Murray, 2006), but its ecology is problematical and often related to the size of the species. Small size specimens of G. subglobosa are associated to phytodetritus (Gooday, 1993). On the other hand, Loubere et al. (1988) investigated populations bigger than 149 μm from Site 548 of Late Pliocene northeast Atlantic and suggested that this species is adapted to a lower food supply and is unable to compete with more opportunistic species. Other records in the literature considered G. subglobosa as characteristic in oligotrophic areas with high bottom current (Jorissen, 1987, 1988; Mackensen et al., 1995; Rasmussen et al., 2002). Specimens of this species bigger than 350 μm are considered as oxic indicators (Kaiho, 1999). Small-size populations are not included in the present study. Hence in the present paper G. subglobosa is considered an oligotrophic and oxic species. H. elegans is considered an epifaunal and oligotrophic species (Morigi et al., 2001; Fontanier et al., 2002, 2006). Deep miliolids are characteristic of oligotrophic to mesotrophic and well-oxygenated environment (Jorissen, 1999; De Rijk et al., 2000; Schmiedl et al., 2000; Kuhnt et al., 2007; Morigi, 2009). P. ariminensis is an epifaunal species from elevated substrates, sospensivore, able to obtain the food supply transported by bottom currents (Lutze and Thiel, 1989; Linke and Lutze, 1993; Fontanier et al., 2008). S. reticulata is considered a shallow infaunal and oxic species, tolerant of only relatively low oxygen conditions in modern sediments (Rathburn and Corliss, 1994). Stilostomella spp. may have lived infaunally and reflect a relatively high food supply (Thomas, 2007). Among costate Uvigerina, U. peregrina is dominant. It is considered a shallow infaunal species, abundant in regions of high food supply of labile organic matter throughout the year (e.g. Sen Gupta and Machain-Castillo, 1993; Rathburn and Corliss, 1994; Mackensen et al., 1995; Altenbach et al., 1999; Fontanier et al., 2002; Gooday, 2003; Mackensen and Licari, 2004; Schönfeld and Altenbach, 2005; Murray, 2006) needing an exported labile organic flux of at least 2.5 g C/m2/yr (De Rijk et al., 2000). This species tolerates only moderate oxygen deficiency and avoids strong oxygen depletion (Schmiedl et al., 1997). Both U. peregrina and U. mediterranea can also live associated with macrofaunal burrows that create biological and chemical conditions similar to those of the topmost centimetre (Loubere et al., 1995). Spinose Uvigerine (U. auberiana and U. proboscidea) has been extensively described from organic-rich/low-oxygen environments (Loubere, 1991; Sen Gupta and Machain-Castillo, 1993; Schmiedl et al., 1997; Licari and Mackensen, 2005). V. complanata is very similar to V. bradyana, and some authors consider the latter species as a junior synonym of V. complanata (Parker, 1958). Considered a shallow infaunal species, it is reported in eutrophic environments and tolerant of low oxygen values (Fontanier et al., 2002). This species has been described in oxygen-poor sediments from the centre of the Adriatic Sea mud belt (Jorissen, 1988; Van der Zwaan and Jorissen, 1991), although Mojtahid et al. (2009) also suggested a possibly low tolerance for anoxic conditions. References Abu-Zied, R.H., Rohling, E.J., Jorissen, F.J., Fontanier, C., Casford, J.S.L., Cooke, S., 2008. Benthic foraminiferal response to changes in bottom-water oxygenation and organic carbon flux in the eastern Mediterranean during LGM to Recent times. Marine Micropaleontology 67, 46–48. Aitchison, J., 1986. The Statistical Analysis of Compositional Data. Chapman and Hall, London. (416 pp.). Aitchison, J., 1992. On criteria for measures of compositional differences. Mathematical Geology 24, 365–380. Aitchison, J., Greenacre, M., 2002. Biplots of compositional data. Applied Statistics 51, 375–392. Aitchison, J., Kay, J.W., 2003. Possible solution of some essential zero problems in compositional data analysis. CODAWORK'03. La Universitat, Girona. Alavi, S.N., 1988. Late Holocene deep-sea benthic foraminifera from the Sea of Marmara. Marine Micropaleontology 13, 213–237.

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