Global and Planetary Change 204 (2021) 103549 Contents lists available at ScienceDirect Global and Planetary Change journal homepage: www.elsevier.com/locate/gloplacha Planktic foraminiferal changes in the western Mediterranean Anthropocene Sven Pallacks a, *, Patrizia Ziveri a, b, Belen Martrat c, P. Graham Mortyn a, d, Michael Grelaud a, Ralf Schiebel e, Alessandro Incarbona f, Jordi Garcia-Orellana a, g, Griselda Anglada-Ortiz a a Institute of Environmental Science and Technology (ICTA), Autonomous University of Barcelona (UAB), Bellaterra, Barcelona, Spain b Catalan Institution for Research and Advanced Studies, Barcelona, Spain c Department of Environmental Chemistry, Spanish Council for Scientific Research (CSIC), Institute of Environmental Assessment and Water Research (IDAEA), Barcelona, Spain d Department of Geography, Autonomous University of Barcelona, Bellaterra, Barcelona, Spain e Department of Climate Geochemistry, Max Planck Institute for Chemistry, Mainz, Germany f Department of Earth and Marine Sciences, University of Palermo, Palermo, Italy g Department of Physics, Autonomous University of Barcelona, Bellaterra, Barcelona, Spain A R T I C L E I N F O A B S T R A C T Editor: Dr. Fabienne Marret-Davies The increase in anthropogenic induced warming over the last two centuries is impacting marine environment. Planktic foraminifera are a globally distributed calcifying marine zooplankton responding sensitively to changes Keywords: in sea surface temperatures and interacting with the food web structure. Here, we study two high resolution Western Mediterranean Sea multicore records from two western Mediterranean Sea regions (Alboran and Balearic basins), areas highly Last 1500 years affected by both natural climate change and anthropogenic warming. Cores cover the time interval from the Planktic foraminifera Medieval Climate Anomaly to present. Reconstructed sea surface temperatures are in good agreement with other Natural variability Anthropogenic warming results, tracing temperature changes through the Common Era (CE) and show a clear warming emergence at Marine surface production about 1850 CE. Both cores show opposite abundance fluctuations of planktic foraminiferal species (Globigerina bulloides, Globorotalia inflata and Globorotalia truncatulinoides), a common group of marine calcifying zooplankton. The relative abundance changes of Globorotalia truncatulinoides plus Globorotalia inflata describe the intensity of deep winter mixing in the Balearic basin. In the Alboran Sea, Globigerina bulloides and Globorotalia inflata instead respond to local upwelling dynamics. In the pre-industrial era, changes in planktic foraminiferal productivity and species composition can be explained mainly by the natural variability of the North Atlantic Oscillation, and, to a lesser extent, by the Atlantic Multidecadal Oscillation. In the industrial era, starting from about 1800 CE, this variability is affected by anthropogenic surface warming, leading to enhanced vertical stratification of the upper water column, and resulting in a decrease of surface productivity at both sites. We found that natural planktic foraminiferal population dynamics in the western Mediterranean is already altered by enhanced anthropogenic impact in the industrial era, suggesting that in this region natural cycles are being overprinted by human influences. 1. Introduction stratification (Behrenfeld et al., 2006; Li et al., 2020). In a world sub­ jected to high anthropogenic pressure and affected by a continuous in­ Mankind’s influence on the climate has grown over the last two crease in atmospheric CO2 since the Industrial Revolution, knowledge centuries, with exponential enrichment of greenhouse gases in the at­ about the impacts of rising sea surface temperatures (SST) on changes in mosphere (Abram et al., 2016; Crutzen, 2002). As observed by marine productivity plays an important role in understanding biological comparing data retrieved from instrumental measurements and ice core and environmental changes in the ocean. records (Bauska et al., 2015; Friedli et al., 1986; Tans and Keeling, The Mediterranean Basin, as a climate change hotspot (Giorgi, 2020), the unprecedented increase of atmospheric CO2 accelerated 2006), is particularly affected by environmental changes. The western during the 20th century, warming surface oceans (Gleckler et al., 2012) Mediterranean is under the influence of large scale atmospheric patterns and depleting marine surface production through enhanced vertical like the North Atlantic Oscillation (NAO), since fluctuations of the * Corresponding author. E-mail address: sven.pallacks@uab.cat (S. Pallacks). https://doi.org/10.1016/j.gloplacha.2021.103549 Received 21 January 2021; Received in revised form 22 May 2021; Accepted 15 June 2021 Available online 24 June 2021 0921-8181/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 atmospheric pressure gradient between the Icelandic Low and the availability are supposed to be the main factors controlling foraminiferal Azores High are associated with changes in climatic and oceanographic distribution, abundance and diversity in the Mediterranean Sea conditions (Hurrell, 1995; Tsimplis et al., 2013; Ulbrich et al., 2012), (Bárcena et al., 2004; Giamali et al., 2020; Pujol and Grazzini, 1995; altering marine ecosystems (Drinkwater et al., 2003). The Atlantic Rigual-Hernández et al., 2012; Zarkogiannis et al., 2020), whereas dif­ Multidecadal Oscillation (AMO) is closely linked to SST variations in the ferences in the seawater carbonate chemistry between the eastern and western Mediterranean Sea (Marullo et al., 2011). NAO and AMO varies western basin play a minor role (Mallo et al., 2017). Post-industrial age on multidecadal to centennial time scales (Mann et al., 2009; Olsen changes in planktic foraminiferal assemblages in oceans are subtle, et al., 2012; Trouet et al., 2009) with positive phases prevailing during limited to ~ 600 km latitudinal shift compared to pre-industrial com­ the Medieval Climate Anomaly (MCA), a warm period which begins in munities (Field et al., 2006; Jonkers et al., 2019; Schiebel et al., 2018). the western Mediterranean at roughly 800 CE. With the onset of the In the Mediterranean Sea, no evidence of anthropogenic influence on Little Ice Age (LIA), a subsequent, cold period lasting from around 1300 planktic foraminiferal assemblages has been documented. Even over the CE to 1800 CE, negative NAO phases became predominant (Gray et al., latest climate anomalies (e.g. MCA, LIA), the planktic foraminiferal 2004; Lüning et al., 2019; Moreno et al., 2012; J. Wang et al., 2017). The response appears weak, with small percentage changes in selected spe­ first part of the 20th century was characterized by low pressure gradi­ cies and/or in the ratio between taxa that indicate different local hy­ ents, whereas from the 1970s on, positive NAO phases were stronger and drographic conditions (Incarbona et al., 2019; Lirer et al., 2014; occurred more frequently (Hurrell, 2020). The high NAO index by the Margaritelli et al., 2018; Vallefuoco et al., 2012). end of the 20th century appears unprecedented during the last 130 years The main objectives of this study are to determine how natural (Osborn, 2004), but is not unusual in the context of the past centuries climate change, in particular large scale atmospheric oscillations like the (Hernández et al., 2020). The close relation between NAO, AMO, and NAO and AMO, have driven planktic foraminiferal assemblage dynamics SST in the pre-industrial Mediterranean (Lüning et al., 2019) was during the Common Era at two strategically ideal locations in the superimposed by anthropogenic induced warming during the second western Mediterranean to study high-frequency changes in water mass half of the 20th century (Macías et al., 2013). Since 1880 CE, the annual dynamics and marine surface productivity, and to assess if the signal of mean air temperature has warmed more abruptly in the Mediterranean natural variability in planktic foraminiferal composition is super­ region compared to the global average (Cramer et al., 2018), acceler­ imposed by accelerated anthropogenic SST warming, starting with the ating the increase of SSTs in the Mediterranean at a rate of 0.35 ◦ C per onset of the Industrial Revolution. For this reason, we investigate the decade (Shaltout and Omstedt, 2014). Direct (changes in reproduc­ planktic foraminiferal accumulation rate records in two high resolution ibility, behavior, fitness and survival of marine organisms) and indirect multicores collected in the Alboran Sea and the Balearic Sea spanning (changes in biotic interactions or hydrography, e.g. displacement and approximately the last 1.2 and 1.7 ky. We also report abundances of intensity of marine currents, sea surface stratification) effects of ocean selected taxa in the > 150 μm fraction, to test the impact of large-scale warming resulting in biogeographical shifts of species, mainly towards atmospheric oscillations like the NAO and AMO during the Common the northwest, causing a tropicalization and homogenization of the Era. The planktic foraminiferal palaeoecological reconstruction is car­ Mediterranean biota, and altering biodiversity and ecosystem func­ ried out along with data on alkenone-derived SST, organic biomarkers, tioning (Bianchi, 2007; Lejeusne et al., 2010; Philippart et al., 2011). and coccolithophore (calcifying phytoplankton) assemblage that pro­ Enhanced stratification as a consequence of sea surface warming is vide evidence of a simultaneous modification in water column dynamics predicted to lower the primary production rate in the western basin, and in the planktic ecosystem network. Especially significant are Uk’37 causing biomass loss in the entire Mediterranean Sea (Coma et al., 2009; estimates that capture a pronounced post-industrial SST rise in both the Macías et al., 2015). Particularly calcifying organisms seem to be Balearic and the Alboran seas, which is in line with instrumental affected by climate-induced warming (Beaugrand et al., 2013). measurements. The northwestern and southwestern Mediterranean regions are ideal locations to study impacts of natural versus anthropogenic climate 2. Study area change on surface ocean properties, since deep water formation in the Gulf of Lion is strongly connected to NAO variability (Josey et al., 2011; 2.1. Oceanographic settings Vignudelli et al., 1999), driving surface productivity in the Alboran Sea (Macías et al., 2008; Macías et al., 2016; Macías et al., 2007). The see- The semi-enclosed Mediterranean Sea is separated by the Sicily Strait saw pattern between high productive phases linked to strong deep sill into the western and eastern Mediterranean basins. It is character­ water formation and vice versa is described in several Holocene marine ized by an anti-estuarine thermohaline circulation with eastward surface sediment records (Ausín et al., 2015; Bazzicalupo et al., 2020; Cacho and westward subsurface flow, due to net buoyancy loss from west to et al., 2000; Cisneros et al., 2019; Nieto-Moreno et al., 2015; Schirr­ east as a consequence of changes in evaporation, precipitation and macher et al., 2019), while anthropogenic warming has affected both runoff (Millot, 1999; Rohling et al., 2009; Schroeder et al., 2012; study regions, as reported through instrumental data and paleoenvir­ Schroeder et al., 2008). The Mediterranean Sea features large eastward onmental archives (Nieto-Moreno et al., 2013; Sicre et al., 2016). surface gradients in physical and chemical characteristics with Planktic foraminifera are single-celled marine eukaryotes producing increasing salinity, SST, and alkalinity, and decreasing surface nutrient calcite and yield an excellent marine sedimentary record. The sensitivity concentrations and dissolved inorganic carbon (Schneider et al., 2007; of planktic foraminifera to changing physical and chemical conditions Shaltout and Omstedt, 2014; Stambler, 2014; Tanhua et al., 2013). and their good preservation in marine sediments makes them good The two study sites, as shown in Fig. 1, are under the influence of tracers of changing environmental conditions, regardless of whether large-scale atmospheric phenomena. The differences of atmospheric sea alterations are caused by natural or anthropogenic drivers. Planktic level pressure between the Icelandic Low and the Azores High, known as foraminifera are under the influence of several surface seawater prop­ the NAO, is influencing the climate and oceanographic conditions of the erties (Bé, 1977; Bé and Tolderlund, 1971; Schiebel and Hemleben, western Mediterranean (Hurrell, 1995). Positive NAO phases charac­ 2017), although the most important factor controlling assemblage terized by a strong subtropical high-pressure cell and a deeper Icelandic composition and diversity is SST (Jentzen et al., 2018; Morey et al., Low generate strong westerly winds, crossing the Atlantic on a more 2005; Rutherford et al., 1999). On a regional and seasonal scale, quality northerly track and result in warm and dry conditions over the Medi­ of food plays a crucial role for the distribution of surface to subsurface terranean Sea with reduced storm activity and below average precipi­ dwelling species (Schiebel et al., 2001), indicated by the close relation tation rates. A weak pressure gradient between the Azores High and the between marine primary production and flux rates of planktic forami­ Icelandic Low (negative NAO phase) causes a more southeasterly niferal tests (Kucera, 2007). Water column configuration and food pathway and enhanced storminess in southern Europe, which brings 2 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Fig. 1. Locations of the study areas in the western Mediterranean Sea, bathymetry, hydrography, SST, and chlorophyll-a data. (a-b) Ocean Data View (ODV) bathymetric maps (Schlitzer, 2019). Dark arrows represent surface currents and gyres. (a) Station MedSeA-S23 in the Balearic Sea. Core location indicated by a blue cross. NC: Northern Current (surface). WMDW: Western Mediterranean Deep Water formation. M: Mistral. T: Tramontana. (b) Station MedSeA-S3 in the Alboran Sea. Core location indicated by a red cross. AJ: Atlantic Jet (surface). WAG: Western Alboran Gyre. EAG: Eastern Alboran Gyre. Upwelling area (orange). References of studies close to core location cited in text. (c) Monthly sea surface temperature (SST), (d) Monthly surface chlorophyll-a concentration (e) annual mean chlorophyll-a concentration from 2003 to 2019 CE at the Balearic (blue open circles) and Alboran Sea (red crosses) core site. Linear fit for both time series indicated by blue (Balearic Sea) and red (Alboran Sea) line. Data is retrieved from AQUA-Modis, Level 3 sensor, covers the period from July 2002 to February 2020, and is centered at the exact core location, covering 16 km2. more moisture to the Mediterranean region (Ulbrich et al., 2012). NAO cascading and open-sea deep convection mainly in January to February phases vary on annual to multicentennial time scales and are recorded in due to cold air masses (Canals et al., 2006; Rohling et al., 2009). Cold, environmental archives like lake sediments, tree rings and speleothems, orographically channeled air from the northern European continent is thus allowing for reconstructing high resolution records dating back causing strong evaporation and surface water cooling and results in several thousand years (Faust et al., 2016; Olsen et al., 2012; Smith buoyancy loss in the Gulf of Lion, thus affecting deep water formation et al., 2016; Trouet et al., 2009). (Medoc, 1970; Mertens and Schott, 1998; R. O. Smith et al., 2008). The AMO is a climate cycle varying on multidecadal to -centennial Interannual variabilities between cold and dry or warm and wet air timescales, which affects SST of the North Atlantic Ocean. SST changes masses have been detected and linked to the winter state of the NAO vary with an amplitude of 0.4 ◦ C at their extremes on a 65–80 year cycle (Ausín et al., 2015; Cisneros et al., 2019; Josey et al., 2011; Vignudelli (Enfield et al., 2001; Schlesinger and Ramankutty, 1994). The AMO has et al., 1999). a strong connection to SST changes in the western Mediterranean Sea. The hydrography of the Alboran Sea is mainly characterized by two SSTs in the Mediterranean region exhibit a 70 year cyclicity, which is anticyclonic, quasi-permanent gyres, the Western Alboran Gyre (WAG) similar to the AMO variability, when looking at instrumental data and the Eastern Alboran Gyre (EAG) both spanning around 100 km in (Marullo et al., 2011). diameter (Gascard and Richez, 1985; Heburn and La Violette, 1990). Each study site shows a characteristic hydrography, influenced by Driven by the strength of the Atlantic Jet (AJ) (Bormans and Garrett, the previously described large-scale atmospheric patterns. As an end- 1989; Flexas et al., 2006), the Alboran gyre system is characterized by a member of the Mediterranean Atlantic Water (MAW) flowing through complex mesoscale variability and can vary between a one gyre (1G), the Tyrrhenian Sea, the Northern Current (NC) connects the Gulf of Lion two gyre (2G) or three gyre (3G) system (Peliz et al., 2013; Renault et al., with the study area in the Balearic Sea (Millot, 1999). Primarily in the 2012; Vargas-Yáñez et al., 2002). Variations in the Mediterranean Gulf of Lion, Western Mediterranean Deep Water (WMDW) is formed Thermohaline Circulation (MTHC) during winter months force surface through two oceanographic processes described as dense shelf water net water flux into the Mediterranean Sea through the Strait of Gibraltar 3 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 (SoG), to compensate for water masses transported to the interior during after the cruise and sliced every 0.5 cm. deep water formation. The MTHC is the main mechanism controlling velocity and direction of the AJ, whereas local wind forcing and sea level 3.2. Radiocarbon and radionuclides analysis pressure are playing a minor role (Macías et al., 2016). Upwelling in the region is controlled by winds and direction and velocity of the AJ Determination of total 210Pb activities was accomplished through the (Macías et al., 2008; Macías et al., 2007; Sarhan et al., 2000). A strong measurement of its alpha-emitter daughter nuclide 210Po, following the AJ located northwards along the Spanish coast and prevailing westerlies methodology described in Sánchez-Cabeza et al. (1998) at the Autono­ cause coastal upwelling and result in highly fertile, nutrient rich surface mous University of Barcelona. After addition of 209Po as an internal water. Weak Atlantic water inflow and presence of easterlies induces a tracer, sample aliquots of 200–300 mg were totally digested in acid southward shift of the AJ, moving the upwelling area further offshore media by using an analytical microwave oven and Po isotopes plated on and generating less fertile surface water conditions in the northwestern silver discs in HCl 1N at 70 ◦ C while stirring for 8 h. Po emissions were Alboran region (Fig. 1b). subsequently counted using α-spectrometers equipped with low- background silicon surface barrier (SSB) detectors (EG&G Ortec) for 2.2. SST and surface productivity at the two study sites 4x105 seconds. The concentrations of excess 210Pb used to obtain the age models were determined as the difference between total 210Pb and the Satellite-derived data from 2003 to 2019 (AQUA-Modis, Level 3) uniform 210Pb at depth. Maximum mean sediment accumulation rates shows with 18.8 ◦ C (Balearic Sea) and 18.9 ◦ C (Alboran Sea) an almost and therefore the age-depth model over the last decades/century was equal mean annual SST at both study sites, whereas higher mean annual estimated using the Constant Flux : Constant Sedimentation (CF:CS) chlorophyll-a concentrations of 0.44 mg m− 3 at the Alboran core station, model (Krishnaswamy et al., 1971; Robbins, 1978). compared to 0.33 mg m− 3 in the Balearic Sea site, confirm the Alboran Radiocarbon dating (14C) was performed on the lower part of cores Sea to be a high productivity area (NASA Goddard Space Flight Center, MedSeA-S3-c1 and MedSeA-S23-c1. Planktic foraminifera (Globorotalia Ocean Ecology Laboratory, Ocean Biology Processing Group, 2020). The inflata) isolated from the 250 – 315 μm fraction from two different Balearic Sea is characterized by lower productivity levels compared to depths (MedSeA-S3-c1: 15–16 cm, 30–31 cm and MedSeA-S23-c1: the Alboran Sea, but is still one of the high productivity regions in the 19.0–19.5cm, 39.0–39.5 cm) were used for radiocarbon dating. Anal­ Mediterranean Sea (Colella et al., 2003; Stambler, 2014). As shown in ysis was performed by using accelerator mass spectrometry (AMS) at the Fig. 1c, seasonal SST variations in the Balearic Sea (August: 26.0 ◦ C; NOSAMS facility at Woods Hole Oceanographic Institution (Volkman February: 13.2 ◦ C) have a higher amplitude compared to the Alboran et al., 1995). Taking the marine radiocarbon reservoir effect into ac­ Sea (August: 23.7 ◦ C; February: 15.2 ◦ C). In the Balearic Sea, SSTs are count, with an offset of 400 years (Siani et al., 2000), radiocarbon ages mainly controlled by warm summer and cold winter airflow, coming were calibrated to calendar ages by using Marine13 calibration curve from the European continent, whereas cold Atlantic water inflow in­ (Reimer et al., 2013) where ages were reported with a 2σ uncertainty. fluences SST at the Alboran study site. The age-depth models of the sediment records were obtained by With highest productivity in March (0.64 mg m− 3) and lowest values combining the surficial age models obtained from the 210Pb activity- in August (0.12 mg m− 3), primary production is driven by the annual depth profiles with the ages obtained using the 14C technique from cycle of the thermal structure of the water column in the northwestern planktic foraminifera from sections 15.5 cm to 30.5 cm (MedSeA-S3-c1) Mediterranean. High summer SSTs cause a strong stratification of the and 19.25 cm to 39.25 cm (MedSeA-S23-c1) (Appleby and Oldfield, water column, impeding vertical advection of nutrients to the surface 1992; Bradley, 2015). causing oligotrophic conditions. Cold katabatic winds during winter The age-depth models for the entire sediment cores in the Alboran enhance deep mixing and surface nutrient supply, which leads to high and the Balearic Seas were calculated considering both 14C dates and the primary production by late winter to early spring, amplified by higher ages from the 20th century reported by the 210Pb age model (up to 5.5 cm solar radiation. Interannual variabilities between cold and dry or warm core depth of MedSeA-S3-c1, up to 11.5 cm core depth of MedSeA-S23- and wet air masses influencing the deep water formation in the Gulf of c1 and MedSeA-S23-c3) and using Bayesian statistics applied by the R- Lion through buoyancy loss, have been detected and linked to the winter code package “rbacon” (Blaauw and Christen, 2011) shown in Figs. S1, state of the NAO (Cisneros et al., 2019; Josey et al., 2011; Vignudelli S3 and S4. et al., 1999). At the Alboran core station, highest chlorophyll-a con­ centrations occur in March (0.66 mg m− 3) and lowest ones in August 3.3. Biomarkers (0.22 mg m− 3). High primary productivity levels are the consequence of fresh nutrient rich upwelled water at the northern Alboran Sea (Bárcena Alkenones (heptatriaconta-8E,15E,22E-trie2-one and heptatriac and Abrantes, 1998; Bárcena et al., 2004; Garcia-Gorriz and Carr, 2001), onta-15E,22E-die2-one) of core MedSeA-S3-c1 and MedSeA-S23-c3 the local occurrence of which is highly dependent on the hydrography of were extracted from sediments, purified using organic solvents and the WAG system. quantified with a Varian gas chromatograph Model 450 equipped with a septum programmable injector, flame ionization detector and a CPSIL-5 3. Material and methods CB column (coated with 100% dimethyl siloxane; film thickness of 0.12 μm; L(m ) * ID(mm) * OD(mm): 50 * 0.32 * 0.45). Hydrogen was the 3.1. Material carrier gas (2.5 mL min− 1). Concentrations were determined using n- hexatriacontane (CH3(CH2)34CH3) as an internal standard. Absolute The study is based on high resolution multicore records (MedSeA-S3- concentration errors were below 10% (resolution between the alkenones c1; MedSeA-S23-c1; MedSeA-S23-c3), collected at two sites of the from 1.5 to 1.7). Reproducibility tests showed that uncertainty in the western Mediterranean Sea with a MC400-Multicorer system during the Uk’37 determinations was lower than 0.015 (ca. 0.5 ◦ C) (Cacho et al., MedSeA cruise (Mediterranean Sea Acidification in a changing climate) 1999; Martrat et al., 2004; Martrat et al., 2014; this study), confirming on 2 May to 2 June 2013 onboard the R/V Àngeles Alvariño. Core the precision of this paleothermometry tool (Eglinton et al., 2001). SST MedSeA-S3-c1 was retrieved in the Alboran basin (Lat. 36.0746◦ N, reconstructions are based on the global calibration of Conte et al. Long. 04.11040◦ W) at a water depth of 1137 m, with a core length of 33 (2006), estimating the standard error on surface sediments at 1.1 ◦ C. cm. Cores MedSeA-S23-c1 and MedSeA-S23-c3 were recovered at a water depth of 1156 m in the Balearic basin offshore Barcelona (Lat. 41.1121◦ N, Long. 2.38200◦ E) with core lengths of 43 cm. MedSeA-S23- c3 was sliced onboard every cm, whereas MedSeA-S23-c1 was processed 4 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 3.4. Planktic foraminifera core MedSeA-S3-c1, and at depth 19.25 cm (1481 yr CE, 2σ cal 1442 – 1529 yr CE) and 39.25 cm (1050 yr CE, 2σ cal 992 – 1140 yr CE) of core 3.4.1. Taxonomic concepts MedSeA-S23-c1, through Bayesian modelling approach, an age depth Analysis of planktic foraminiferal tests was performed on cores model was calculated. The mean sedimentation rate (SR) is 33.5 cm MedSeA-S3-c1 and MedSeA-S23-c1. The five morphospecies Globiger­ kyr− 1 (MedSeA-S3-c1), 50.6 cm kyr− 1 (MedSeA-S23-c1), and 53.8 cm inoides ruber (d’Orbigny 1839), Globigerina bulloides (d’Orbigny 1826), kyr− 1 (MedSeA-S23-c3) (Table S1). Globorotalia inflata (d’Orbigny 1839), Globorotalia truncatulinoides (d’Orbigny 1839), and Orbulina universa (d’Orbigny 1839) were iso­ 4.2. Absolute changes in reconstructed SST lated. Classification of the different foraminiferal species was carried out by visual identification using a binocular stereo microscope (magnifi­ Data on SST and alkenone concentration of both records is summa­ cation 10× - 20×) and a bifurcated illuminator. Taxonomic identifica­ rized in Fig. 2 and Data Set S4 & S5 (Supplementary Information). In the tion of the target species was based on Schiebel and Hemleben (2017). Balearic Sea record, SST ranged between 16.0 ◦ C to 18.0 ◦ C, with slightly The white (G. ruberWHITE) and pink (G. ruberPINK) varieties were higher SST during the MCA (17.0 ◦ C; 895 – 1135 CE) than during the LIA collected separately. A distinction between the two morphotypes of (16.8 ◦ C; 1135–1755 CE). An SST drop to ~16.2 ◦ C is detected between G. ruberWHITE, G. ruber sensu lato (G. ruberSL) and G. ruber sensu stricto 1135 CE and 1195 CE, and to 16.0 ◦ C around 1851 CE. The 20th century (G. ruberSS) was made, based on differences in test morphology (Kon­ is marked by an SST increase of almost 2 ◦ C. SST recorded in the Alboran takiotis et al., 2017; Numberger et al., 2009; L. Wang, 2000) Sea is ranging between 18.8 ◦ C and 17.3 ◦ C. Differences between MCA (18.4 ◦ C; 378 – 1046 CE) and LIA (17.7 ◦ C; 1103 – 1762 CE) are more 3.4.2. Analyzed size fraction pronounced than in the Balearic Sea. Two minimums of SST are detected Bulk sediment mass was obtained after drying samples at 60 ◦ C for at the end of the 13th century (17.3 ◦ C) and at the end of the 1960s CE approximately 24 hours. Samples were washed over a 63 μm screen (17.4 ◦ C). An SST warming is detected from the 1970s of up to 18.6 ◦ C. using distilled Elix water. The size fraction larger than 63 μm was oven dried at 60 ◦ C for 1 - 2 hours. Samples were dry sieved and divided by a 4.3. Planktic foraminiferal species abundances Riffle Splitter at the chosen size fractions, 150–250, 250–315 and > 315 μm. Results are presented and discussed for > 150 μm size fraction. More Even though the time interval under investigation is comparably than 300 specimens were identified in the > 150 μm size fraction in all short, assuming little changes in climatological and oceanographic samples. conditions, some species reveal large abundance variations and trends at The standard > 150 μm analysis for planktic foraminifera analysis in both study sites, beyond the 95% confidence level errors related with the oceans is a legacy of the CLIMAP project (CLIMAP Project Members counting (Fig. 3, Data Set S1 & S2). et al., 1984), mainly aimed at reconstructing SST variations in the In the Balearic Sea record, G. bulloides is the dominant target species oceans over glacial-interglacial cycles and benefits from a huge modern (5.4–26.2%, on average 17.6%) followed by G. truncatulinoides reference database (Schmidt et al., 2004). This fraction is commonly (2.3–12.7%, on average 6.7%), G. inflata (1.6–10.8%, on average 4.6%) used by Mediterranean specialists even if some species would be un­ and G. ruberWHITE (0.2–8.6%, on average 3.6%). The Alboran Sea record derrepresented, among others Turborotalita quinqueloba, an important reveals G. bulloides (28.0–57.4%, on average 38.2%) and G. inflata proxy for surface productivity during glacials (Capotondi et al., 2004; Di (17.6–44.9%, on average 27.5%) as the two dominant species, followed Donato et al., 2015; Sprovieri et al., 2003). The number of total planktic by G. ruberWHITE (4.8–11.5%, on average 7.9%). In both Balearic and foraminiferal shells and their total accumulation rate was evaluated on Alboran records, the morphospecies G. ruberSL (0.1–8.0% and 3.6–9.1%, the > 150 μm size fraction. on average 3.2% and 5.9%, respectively), which occurs mainly as “platys” and elongate morphotypes, dominates over G. ruberSS (0–2.1% 3.5. Coccolithophore sedimentary record and 0.6–3.7%, on average 0.4% and 2.0%, respectively). Other selected species are less abundant on average (< 2%). Noteworthy, G. bulloides, Analysis of relative abundance of calcareous nannoplankton assem­ G. inflata and G. truncatulinoides show abundance fluctuations of oppo­ blages (coccolithophores) was done on core MedSeA-S3-c1. Following site signs at their core locations over some time intervals, but also be­ standard procedures in Bown and Young (1998) smear slides of each tween study sites (Fig. 3). Due to their low relative abundances, sample (<63 μm) were prepared and analyzed by a polarized micro­ variations in G. ruberSS, G. ruberPINK and O. universa are not statistically scope (x 1000 magnification). Considering around 20 taxonomic units, significant. Only the morphospecies G. ruberSL displays significant at least 500 specimens were counted and identified by taxonomic con­ abundance changes in both records at the Balearic Sea site during the cepts of extant coccolithophores (Young et al., 2003). Common Era. To display modern planktic foraminiferal productivity during the last 4. Results 30 years, the annual mean test accumulation rates for core top samples representing the time period between 1980 to 2013 CE were calculated, 4.1. Age model showing higher rates in the Alboran (30.1 ind. cm− 2 yr− 1) than in the Balearic (22.5 ind. cm− 2 yr− 1) record. In both cores, the gradual increase Concentrations of 210Pbtot and 210Pbxs with depth in the sediment of test accumulation rates occurs within radionuclide dating. The rates records are shown in Figs. S1, S3 and S4. 210Pbtot activity of the 3 of test flux per gram of sediment and the standardized test accumulation analyzed cores is decreasing from the surface, reaching a constant rates show accelerated declines during the 20th century at both study average value (210Pbsup) of ~31 ± 2 Bq kg− 1 at ~12.5 cm depth areas. (MedSeA-S3-c1), ~35 ± 3 Bq kg− 1 at ~20.5 cm depth (MedSeA-S23-c1) and ~33 ± 2 Bq kg− 1 at ~18.5cm depth (MedSeA-S23-c3). Applying the 4.4. Calcareous nannoplankton species composition CF:CS model the maximum mean mass accumulation rate (MAR) is 0.047 ± 0.002 g cm− 2 yr− 1 (MedSeA-S3-c1), 0.105 ± 0.008 g cm− 2 yr− 1 Calcareous nannofossils are well preserved, indicating absence of (MedSeA-S23-c1), and 0.110 ± 0.004 g cm− 2 yr− 1 (MedSeA-S23-c3). significant dissolution phenomena. The entire assemblage of counted Combining the calculated 210Pb ages for the upper core parts (first 5.5 and identified species is available in Data Set S3 (Supplementary In­ cm and 11.5 cm for cores MedSeA-S3-c1 and MedSeA-S23-c1, respec­ formation). Taxa do not show any significant abundance variation tively) with calibrated 14C ages at depth 15.5 cm (1297 yr CE, 2σ cal throughout the record, except for Emiliania huxleyi, Gephyrocapsa oce­ 1257 – 1337 yr CE) and 30.5 cm (433 yr CE, 2σ cal 358 – 534 yr CE) of anica and Florisphaera profunda since the 20th century (Fig. 2). Most 5 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Fig. 2. Downcore variations of SST, surface production of calcareous organisms and relative abundances of calcareous nanno­ plankton taxa during the Common Era in the Alboran (red) and Balearic cores (blue). (a) Alkenone (Uk’37) derived SSTs. (b) Alkenone concentration of total C37. (c-d) Test accu­ mulation rates and test concentrations per gram sediment in Balearic and Alboran cores. (e-g) Red symbols show percentage values of calcareous nannoplankton species, with 95% confidence interval of the counts indicated by the error bars. Red lines show 3- pt running average of calcareous nanno­ plankton species data. Duration of the Dark Age (DA), Medieval Climate Anomaly (MCA), Little Ice Age (LIA) and Industrial Era (IE) is based on estimates by Nieto- Moreno et al. (2011). strikingly, relative abundances of G. oceanica triple over the past 100 5. Discussion years in the Alboran core and E. huxleyi and F. profunda show a continuous and gradual decrease. 5.1. Age model Age depth-models calculated for both study sites are in good agree­ ment with results from other studies obtained nearby (Cisneros et al., 6 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Fig. 3. Downcore variations of relative planktic foraminiferal species abundances (a-g) during the Common Era in the Alboran (red) and Balearic cores (blue). Symbols show percentage values of planktic foraminiferal species with 95% confidence interval of the counts indicated by the error bars. Solid lines indicate 3-pt running average of >150 μm size fraction of planktic foraminiferal species. Duration of the Dark Age (DA), Medieval Climate Anomaly (MCA), Little Ice Age (LIA) and Industrial Era (IE) is based on estimates by Nieto-Moreno et al. (2011). 7 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 2016; Frigola et al., 2007; Masqué et al., 2003; Moreno et al., 2012; Puig measuring 14C and 210Pb activity, like differences in reservoir ages in et al., 2015), further discussed in the Supplementary Information (Text seawater (Alves et al., 2018; Ascough et al., 2005; Philippsen, 2013; S2). There is a rapid change in sedimentation rate from the upper (oldest Siani et al., 2000; Struglia et al., 2004), carbonate tests (Barker et al., 210 Pb date; MedSeA-S3-c1: 1925 ±4 yr CE at 5.5 cm core depth; 2007; Waelbroeck et al., 2001) or vertical lead diffusion and mixing MedSeA-S23-c1: 1922 − 8 +7 yr CE at 11.5 cm; MedSeA-S23-c3: 1926 (Mekik, 2014; Nittrouer et al., 1984), which is further discussed in ±7 yr CE at 11.5 cm) to the lower core section (youngest 14C date; Supplementary Information (Text S2). MedSeA-S3-c1: 1297 − 45 +40 yr CE at 15.50 cm core depth; MedSeA- The poor detection of changing sedimentation rates due to sediment S23-c1: 1481 − 39 +48 yr CE at 19.25 cm), which we attribute to consolidation behavior and the uncertainties occurring when combining 210 changes in sediment consolidation. Due to higher overburden, deeper Pb and 14C dating techniques, are both influencing parameters which parts of the core experience a higher consolidation leading to lower are dependent on sedimentation rate. As a result, test accumulation rates sedimentation rates, whereas unconsolidated top core sediments have a seem to be overestimated in the upper (dataset based on 210Pb dating) very high sedimentation rate. Due to the lack of a high-resolution age and underestimated in the lower core part (dataset based on 14C dating), control, sedimentation rate changes because of poor consolidation are causing an anomalous increase at the beginning of the 20th century detected by abrupt changes in our age models. Rapid changes in sedi­ (Fig. 2). Through standardization of both datasets, setting variation on mentation rates between core parts based on high resolution 210Pb dates the same scale, not the amplitude of varying test accumulation rates, but and low resolution 14C dating are also reported in other studies (Cisneros the slope between the two datasets becomes comparable. Despite the et al., 2016; Margaritelli et al., 2020a). By increasing the numbers of 14C above mentioned difficulties when combining age models derived from 210 datings below the unconsolidated core part, the distortion would be Pb and 14C dating results, to obtain high resolution age control, we partly removed, as can be seen in the study of Sicre et al. (2016). Abrupt reconstructed a robust age-depth model, supported by changing pa­ changes in sedimentation rates may be influenced by uncertainties when rameters independent from sedimentation rate, like relative abundance Fig. 4. SST records from the Balearic and Alboran Seas in comparison with nearby paleorecords and instrumental measurements with a focus on the Industrial Era. (a) Alkenone derived SST in Balearic core (blue circles). Paleotemperature records of other studies conducted in vicinity of the Balearic study site: light and dark green lines (Moreno et al., 2012); orange line (Sicre et al., 2016). (b) Alkenone derived SST in Alboran core (red circles). Paleotemperature records of other studies conducted in vicinity of the Alboran study site: light and dark brown (Nieto-Moreno et al., 2013). Industrial SST warming at the Balearic (c) and the Alboran (d) study site. Annual SST and standardized SST anomaly (SSTA), respectively, obtained through instrumental data: grey line (HadISST) and dark line (Kaplan v2) (Kaplan et al., 1998; Rayner et al., 2003; Reynolds and Smith, 1994). Red bands indicate SST warming phases derived from Kaplan and HadISST data. Blue and red circles, respectively, show alkenone derived SST in Balearic and Alboran core. Brown line shows atmospheric CO2 concentrations measured (Tans and Keeling, 2020) and reconstructed (Friedli et al., 1986). Filled and open diamonds represent 14C dates and 210Pb dates used as tie-points for age-depth model reconstruction, respectively, color coded by the corresponding core color (Alboran = red; Balearic = blue), including their associated 2σ errors. Duration of the Dark Age (DA), Medieval Climate Anomaly (MCA), Little Ice Age (LIA) and Industrial Era (IE) is based on estimates by (Nieto-Moreno et al., 2011). 8 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 of principal planktic foraminiferal species (see 5.3.3), and alkenone- (Abram et al., 2016). SST rise during the last two centuries is more derived SST (see 5.2), which coincide with main environmental pronounced in the Balearic (2.0 ◦ C) than in the Alboran record (0.8 ◦ C), changes recorded independently. accelerating during the 20th century with an SST increase of more than 1◦ C at both study sites. This is in good agreement with satellite-derived 5.2. SST changes over the past 1600 years mean annual warming rate of 0.026 ◦ C yr− 1 for the western Mediter­ ranean basin during that period (Skliris et al., 2012). Uk’37 SST estimates show good accordance in comparison to instru­ mental measurements (HadISST & Kaplan SST V2 data) and paleo­ 5.3. Planktic foraminifera records (Fig. 4). With values ranging between 16–18 ◦ C at the Balearic and 17–19 ◦ C at the Alboran core site, they are generally consistent with 5.3.1. Total planktic foraminiferal production other late Holocene Uk’37 SST estimates (Cacho et al., 1999; Martrat Modern mean test accumulation rates are calculated for 1980 CE to et al., 2014; Schirrmacher et al., 2019; Sicre et al., 2016), displaying 2013 CE to provide an average value for planktic foraminiferal pro­ modern annual mean temperature differences at the study regions ductivity and to make our results comparable to previous studies con­ (Fig. 1c). Lower paleotemperatures (14–16 ◦ C) estimated by Moreno ducted during the last 30 years (Bárcena et al., 2004; Mallo et al., 2017; et al. (2012) for the northwestern Mediterranean, can be explained by Pujol and Grazzini, 1995; Rigual-Hernández et al., 2012). Modern mean effects on the sedimentary alkenone signal through variability in surface test accumulation rates are higher at the Alboran (30.1 ind. cm− 2 yr− 1) production and/or differential degradation of 37:3 and 37:2 alkenones. than in the Balearic (22.5 ind. cm− 2 yr− 1) core site. Our findings are in When corrected, as done by Sicre et al. (2016) using the temperature accordance with results from sediment traps, deployed at water depths calibration of Conte et al. (2006), SSTs coincide with estimates from our between 1000 and 2000 m showing that 28.6 to 35.5 ind. cm− 2 yr− 1 in study. Alboran SST estimates are slightly lower compared to values the western Alboran Sea (Bárcena et al., 2004; Hernández-Almeida (18.5–20 ◦ C) obtained by Nieto-Moreno et al. (2013), but are still inside et al., 2011) and 8.2 to 15.0 ind. cm− 2 yr− 1 in the northwestern Medi­ the lower range for autumn and average annual SSTs in the Alboran terranean Sea (Rigual-Hernández et al., 2012), displaying different basin during the Holocene (Cacho et al., 1999; Pérez-Folgado et al., trophic conditions at the two study sites. Due to nutrient rich upwelling 2003). The core location in the Alboran Sea has a strong Atlantic in­ at the northern edge of the WAG (Fig. 1b), the Alboran Sea is one of the fluence, whereas the study area in the Balearic Sea is in close vicinity to most productive marine regions in the Mediterranean (Garcia-Gorriz the deep-water mass formation area, known for strong winter convec­ and Carr, 2001). The Balearic Sea is characterized by lower productivity, tion (Rohling et al., 2009; Skliris et al., 2012). Even though both areas even if the highly dynamic character of the region with strong frontal are influenced by different meteorological and oceanographic condi­ activity (La Violette, 1990) still makes it a more productive region in the tions, they display similar SST trends. This suggests that both study sites rather oligotrophic Mediterranean Sea (Stambler, 2014). Annual are under the influence of larger-scale processes. average chlorophyll-a values (Fig. 1e) derived from satellite images The prolonged pre-industrial cooling trend throughout the MCA and during the last decades show higher values in the Alboran than in the LIA is consistent with regional (Europe, Mediterranean Sea, and North Balearic study area and support the hypothesis of a positive correlation Atlantic Ocean) and global ocean cooling from 0 CE to 1800 CE between primary production and planktic foraminiferal standing stocks, (McGregor et al., 2015). The sedimentary records reported here are in as phytoplankton serve planktic foraminifera as a major food source phase with climatic oscillations during the past millennium describing (Hemleben et al., 1989; Schiebel and Hemleben, 2005). warmer SSTs during the MCA compared to the LIA (Lüning et al., 2019; Foraminiferal accumulation rates in the core top samples of our Mann et al., 2009). Taking into account age error uncertainties, both study were comparable to the export fluxes estimated in sediment traps records describe a ~ 1.0 ◦ C cooling during the MCA-LIA transition be­ (Bárcena et al., 2004; Rigual-Hernández et al., 2012) from the western tween 1100 to 1300 CE, synchronous with the 1257 CE eruption event Mediterranean, supporting high consistency from sinking to accumula­ (Crowley and Unterman, 2013), which is associated with the onset of the tion in the sediment bed. In addition, the high carbonate saturation LIA. The marked temperature drop below 16 ◦ C at the Balearic core site horizon throughout the water column in the Mediterranean Sea, suggest at approximately 1851 − 89 +51 yr CE could be related to the 1809 CE carbonate dissolution being unlikely (Millero et al., 1979; Schneider ‘unknown’ and the 1815 CE Tambora volcanic eruptions, as recorded in et al., 2007). northeastern Mediterranean marine records (Gogou et al., 2016), marking the terminal point for the long-term cooling trend during the 5.3.2. Planktic foraminiferal assemblage composition pre-industrial Common Era, followed by warming in the last two Planktic foraminiferal core top assemblages in the Balearic and centuries. Alboran Sea are in good agreement with recent sediment trap, plankton With increasing SSTs starting in the 19th century, and accelerated sea tow, and core top studies conducted nearby (Bárcena et al., 2004; surface warming during the 20th century, both cores display the tem­ Hernández-Almeida et al., 2011; Mallo et al., 2017; Pujol and Grazzini, perature signal, already recorded in the Balearic (Sicre et al., 2016) and 1995; Rigual-Hernández et al., 2012; Thunell, 1978). In the north­ Alboran Sea (Nieto-Moreno et al., 2013), affirming pronounced 20th western Mediterranean, G. ruberWHITE (including the two morphotypes), century warming in the western Mediterranean Sea (Lionello et al., G. ruberPINK and O. universa are part of the summer assemblage associ­ 2006; Skliris et al., 2012; Vargas-Yáñez et al., 2010). The absence of a ated with low surface productivity. Globigerina bulloides, 20th century warming signal in cores collected at the Minorca contourite G. truncatulinoides, and G. inflata are dominant from winter to spring, (Moreno et al., 2012) can be ascribed to a lack of age control over the when cold temperatures driving winter-deep mixing and causing high past 500 years and age model extrapolation in the upper core part. Fig. 4 surface chlorophyll-a concentrations, which stimulate planktic forami­ shows in detail SST reconstruction in the Balearic and Alboran Sea, niferal productivity and cause high export fluxes and high accumulation compared to instrumental annual mean data estimated at core locations rates to the seafloor sediment (Rigual-Hernández et al., 2012). In the retrieved from temperature time series average over a 5◦ × 5◦ grid from western Alboran Sea, G. bulloides is the dominant species during periods Kaplan SST V2 data and the Hadley Centre Sea Ice and Sea Surface of high productivity in spring and fall, whereas G. inflata has highest Temperature data set (HadISST) (Kaplan et al., 1998; Rayner et al., relative abundances during winter and summer, characterized by 2003; Reynolds and Smith, 1994). Industrial SST warming starting stratification of the water column, reduced upwelling and less produc­ around 1850 CE is well captured by both instrumental and proxy data, tive conditions (Bárcena et al., 2004; Kontakiotis et al., 2016). describing the two phase warming of the western Mediterranean (Lio­ The species composition is assumed to reflect the climatic and nello et al., 2006), and importantly the exact moment of warming oceanographic differences at both study sites. Globigerinoides ruberWHITE emergence under anthropogenic pressure in most of sites globally is a surface dwelling, symbiont bearing warm water species (Bé and 9 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Tolderlund, 1971; Schiebel et al., 2002). Although it is a shallow anthropogenic warming may lead to surface ocean productivity decline. dwelling species, it may occur at nutricline depths in less turbid oligo­ trophic waters (Pujol and Grazzini, 1995; Schiebel et al., 2004; Zarko­ 5.3.3.1. Natural variability as a driver in pre-industrial times (TSI, AMO). giannis et al., 2020). Globigerinoides ruberPINK seems to exhibit high Decreasing solar activity revealed through increasing number and in­ sensitivity to changing SST, and to prosper only at maximum SSTs tensity of solar activity minima Maunder, Spörer and Wolf (Usoskin (Mallo et al., 2017). Orbulina universa has a high tolerance to tempera­ et al., 2016), and the more frequent occurrence of volcanic eruptions has ture and salinity (Anderson et al., 1979; Bijma et al., 1990). As a sym­ led to a pronounced cooling since the MCA-LIA transition (Crowley and biont bearing species, O. universa is restricted to the euphotic zone and Unterman, 2013; McGregor et al., 2015). Decreasing SSTs in the western occurs from temperate to tropical waters (Bemis et al., 2000; Hemleben Mediterranean are closely linked to negative AMO phases during the LIA et al., 1989), while in the Mediterranean Sea it proliferates by the end of (Lüning et al., 2019), affecting water column properties mainly during summer (Pujol and Grazzini, 1995). Globorotalia inflata and summer seasons (Marullo et al., 2011; O’Reilly et al., 2017), triggering G. truncatulinoides are subsurface-dwelling species, which favor mixed changes in planktic foraminiferal assemblages (Incarbona et al., 2019). conditions and cool water temperatures (Hemleben et al., 1989; Pujol During the second phase of the LIA, relative abundances of G. ruberWHITE and Grazzini, 1995). In the Mediterranean, both species are indicators of decrease from ~8.1% to ~0.5% in the Balearic core (Fig. 3a). The eutrophic conditions with a deeply mixed winter ocean layer (Rigual- surface-dwelling species, favoring warm, stratified waters was probably Hernández et al., 2012; Rohling et al., 2004). Globorotalia inflata shows disadvantaged by decreasing SSTs and intensified vertical mixing of the an opportunistic behavior in mesotrophic conditions (Chapman, 2010; water column. As winter SSTs are quite low at present, warm times with Lončarić et al., 2007; Retailleau et al., 2011; Storz et al., 2009), and can a monthly mean of 13.2 ◦ C in February (Fig. 1e), winter months are be outnumbered by more opportunistic species such as G. bulloides in expected to be colder during the LIA, with SSTs falling below temper­ eutrophic environments. Globigerina bulloides thrives in high- ature tolerance of G. ruberWHITE (Bijma et al., 1990), affecting standing productivity regions and is an indicator of upwelling intensity, stocks of this species even in summer. The drop in G. ruberWHITE is responding to phytoplankton blooms and may outnumber species, synchronous with an abundance increase of G. inflata and which are adapted to less productive conditions (Conan et al., 2002; G. truncatulinoides (Fig. 3), two species associated with deep-winter Schiebel et al., 2004; Thiede, 1975). mixing in this region (Rigual-Hernández et al., 2012). Results are sup­ Higher percentages of warm water species G. ruberSL in the Alboran ported by former studies in the Tyrrhenian Sea with a positive response Sea might be explained by a narrower annual SST amplitude compared of deep dwelling species during minimum solar activity during the LIA to the Balearic Sea (Fig. 1e), which favors the warm water species since (Lirer et al., 2014; Margaritelli et al., 2018; Margaritelli et al., 2020b; SST is not falling below its specific temperature minimum limit of 14 ◦ C Margaritelli et al., 2016). Increasing abundances of the deep dwelling (Bijma et al., 1990). Higher relative abundances of G. truncatulinoides in species might indicate more intense vertical mixing during winter the Balearic Sea is of the same magnitude of those reported in the nearby months, delaying the spring bloom and shortening the growing season Minorca Basin (Margaritelli et al., 2018). This abundance peak increases for G. ruberWHITE. It is not clear if reduced light levels during solar ac­ in coincidence of the Maunder Minimum event of the LIA, as in a wide tivity minima have a direct negative impact on the symbiont bearing portion of the central-western Mediterranean, and is due to the devel­ species, since the species uses dinoflagellates for photosymbiosis opment of enhanced vertical mixing in winter (Margaritelli et al., (Hemleben et al., 1989). 2020b). This interpretation is compatible with enhanced atmospheric During the older part of the Alboran record, percentage values of the circulation developed in close vicinity to the Gulf of Lion and its wind warm water species G. ruberWHITE are in phase with Uk’37 SST estimates driven deep mixed conditions and/or a strong NC that may transport likely driven by variabilities in AMO (Fig. 5). As a main representative of G. truncatulinoides to our study site (Fig. 1a). High relative abundances of the summer assemblage (Bárcena et al., 2004), proliferation of G. G. bulloides, a species associated with periods of elevated primary pro­ ruberWHITE is favored by higher SST during the DA, whereas lower ductivity in the western Mediterranean Sea (Bárcena et al., 2004; temperatures throughout the MCA result in a relative abundance drop. A Hernández-Almeida et al., 2011; Rigual-Hernández et al., 2012), prevailing negative AMO during the LIA is not recorded in G. ruber demonstrate that the Balearic Sea is one of the most productive regions k’ WHITE. Instead, it increases its stock continuously in line with U 37 SST in in the Mediterranean Sea (Stambler, 2014), although satellite data the Alboran Sea. reveal that surface primary production may be even higher in the Alboran Basin (Fig. 1). 5.3.3.2. Natural variability as a driver for planktic foraminiferal popula­ Great percentage values of non-target species in the Balearic Sea tion dynamics in pre-industrial times (NAO). Changes of climatologic and (Fig. 3g) are caused by high abundances of small sized species (150-250 oceanographical conditions in the Mediterranean are closely linked to μm; Dataset S1 & S2), dominated by Neogloboquadrina incompta. Its af­ the boreal winter NAO index (Hurrell, 1995; Lionello et al., 2006; Nieto- finity to low-productive conditions with enhanced stratification of the Moreno et al., 2015; Schirrmacher et al., 2019; Tsimplis et al., 2013; surface water column (Schiebel and Hemleben, 2000) would explain the Ulbrich et al., 2012), affecting phytoplankton and zooplankton com­ abundance pattern contrasting to the deep mixing indicator species munities through changes in ocean circulation and air-sea heat fluxes G. truncatulinoides. (Drinkwater et al., 2003), including plankton calcifier (Ausín et al., 2015; Bazzicalupo et al., 2020; Mojtahid et al., 2015). Long-term vari­ 5.3.3. Planktic foraminiferal response to natural versus anthropogenic ability is displayed by planktic foraminiferal records, i.e. by ratios be­ drivers tween indicators of eutrophic (G. bulloides) and deep-mixing (G. inflata External forcing, like variations in solar activity and the cooling ef­ and G. truncatulinoides) conditions, and the NAO and AMO (Figs. 5 & 6). fect of sulphate aerosols expelled into the atmosphere after volcanic In the northwestern Mediterranean, G. inflata and G. truncatulinoides eruptions, are thought to be main mechanisms driving climate during are associated with stronger winter mixing conditions (Rigual-Hernán­ the last millennium (Crowley, 2000; McGregor et al., 2015). These dez et al., 2012). A relation between large scale atmospheric patterns drivers influence large scale atmospheric patterns like NAO and AMO and these species has been reported from the central Mediterranean Sea (IPCC, 2014), which in turn are associated with changes in climate and and is interpreted as changes in deep winter mixing (Incarbona et al., oceanographic conditions. Synchronously, anthropogenic induced 2019). The flow of cold and dry air masses from continental regions into climate change is responsible for almost half of the 20th century the western Mediterranean, which enhances heat loss and strengthens warming (Macías et al., 2013). Figs. 5 and 6 demonstrate how natural the NC circulation (Vignudelli et al., 1999), resulting in strong vertical variability controls planktic foraminiferal species composition of the mixing of water masses during WMDW formation in the Gulf of Lion western Mediterranean Sea in pre-industrial times, whereas 10 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 (caption on next page) 11 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Fig. 5. Natural and anthropogenic forcing driving surface productivity and deep winter mixing in the western Mediterranean Sea during the Common Era expressed through planktic foraminiferal species composition and abundance changes. (a) Sulphate records in Antarctic and Greenland ice cores as a proxy for volcanic activity (Crowley and Unterman, 2013). (b) Total solar irradiance (TSI) based on 10Be and 14C data (Steinhilber et al., 2012; Steinhilber et al., 2009). Orange fillings indicate TSI periods below the mean (− 0.2 W m− 2). (c) Reconstruction of Atlantic Multidecadal Oscillation (AMO) (Mann et al., 2009), expressed as 29 point moving average (dark line). (d) Reconstruction of North Atlantic Oscillation (NAO) through tree-ring and speleothem-based records (Trouet et al., 2009) expressed as 29 point moving average (dark line), lake sediment records as a grey line (Olsen et al., 2012) and instrumental data covering 1821 CE to 2013 CE (Jones et al., 1997) expressed as 5 point moving average (orange line). Positive and negative phases for NAO and AMO indices are highlighted as red and blue areas, above and below the mean. (e) Paleotemperature reconstruction for continental Europe as orange dashed line (Ahmed et al., 2013) and alkenone derived SST for Alboran (red) and Balearic (blue) cores. (f) Paleo storm activity in the Gulf of Lion (Sabatier et al., 2012). (g) Intensity of Western Mediterranean Deep-Water formation (WMDW), recorded through de-carbonated (green) and total (dark green) grain-size fraction (Cisneros et al., 2019). (h) Added relative abundance of G. inflata + G. truncatulinoides in the Balearic Sea (blue) as a proxy for deep winter mixing and G. bulloides versus G. inflata in the Alboran Sea (dark red) as a proxy for surface productivity. Grey plus and minus symbols indicate concurrent species composition changes at both study sites, related to (de-) and increasing phases of NAO modes on multidecadal time scales (i) Standardized total planktic foraminiferal test accumulation rate at the Alboran (red) and Balearic (blue) core sites: Crosses and dashed lines show values based on sedimentation rates rest upon 14C dating. Triangles represent std. acc. rates based on sedimentation rates rest upon 210Pb dating. Solid lines represent linear fit through LIA and 20th century second half, respectively. Filled and open diamonds represent 14C dates and 210Pb dates used as tie-points for age-depth model reconstruction, respectively, color coded by the corresponding core color (Alboran = red; Balearic = blue), including their associated 2σ errors. Duration of the Dark Age (DA), Medieval Climate Anomaly (MCA), Little Ice Age (LIA) and Industrial Era (IE) is based on estimates by Nieto-Moreno et al. (2011). during winter months (Medoc, 1970; Mertens and Schott, 1998; Rohling and minus signs) in both records associated with changes in NAO modes. et al., 2009). Cold and dry northerlies and north-westerlies, better The in-phase pattern between the ratio of G. bulloides versus G. inflata in known under the names Tramontana and Mistral, in particular during a the Alboran record and the relative abundance changes of negative phase of the East Atlantic Pattern, have the potential to cause G. truncatulinoides and G. inflata in the Balearic core, is one of the most intense heat loss, affecting dense water formation (DWF) in the Gulf of striking features of the record. As illustrated in Fig. 6, productivity Lion (Josey et al., 2011). Globorotalia truncatulinoides inhabit subsurface changes in the Alboran Sea are strongly linked to DWF in the Gulf of waters most of their life span and migrate to surface waters for repro­ Lion, both related to NAO variability (Fig. 5). Stronger WMDW forma­ duction (Hemleben et al., 1989; Schiebel and Hemleben, 2005; Schiebel tion results in deficit in surface water masses in the western Mediter­ et al., 2002). Deep turbulent vertical mixing combined with a thermo­ ranean Sea, which is compensated by stronger Atlantic surface water cline breakdown during the LIA, a period characterized by more nega­ inflow through the SoG (Macías et al., 2016). This leads to higher ve­ tive NAO modes, may have caused proliferation of G. truncatulinoides locities of the AJ, flowing in a northward direction along the Iberian and G. inflata in a shallower habitat. In contrast, stronger water column Peninsula coast. Together with prevailing westerlies, this atmospheric stratification as a result of lower surface heat loss during positive NAO and hydrographic concurrence is associated with highly fertile, nutrient and AMO phases during the MCA (Moreno et al., 2012) would have rich coastal upwelling. A poor DWF with less pronounced westerlies typically caused a subsurface habitat of G. inflata and G. truncatulinoides. would weaken the AJ, streaming further southward along the northern During the first half of the LIA, relative abundances of G. ruberWHITE are African coast, resulting in further offshore upwelling characterized by changing along with deep dwelling species, which is contradictory since less fertile surface water conditions (Macías et al., 2008; Macías et al., the surface-dwelling species is a key indicator for water column strati­ 2007; Sarhan et al., 2000). Seasonal sediment trap data in the Alboran fication. As part of the summer assemblage, G. ruberWHITE might have Sea (Bárcena et al., 2004) support the relation between Atlantic water benefited by reduced surface production during LIA summer months, as inflow and planktic foraminiferal surface production. Specifically, G. reflected in test concentration and accumulation rates (Figs. 2 & 5). bulloides is associated to high surface production and G. inflata is an Intense vertical mixing during negative NAO phases might have delayed indicator for less productive conditions. We suppose that a continuous initiation of the spring bloom, shortening the growing season and strong AJ during times towards more positive NAO phases favors the decreasing phytoplankton abundance as hypothesized for regions in the occurrence of G. bulloides in the Alboran Sea as a result of high surface North Atlantic (Dickson et al., 1988; Fromentin and Planque, 1996). In primary productivity, whereas a weak AJ during periods of decreasing the northwestern Mediterranean Sea, katabatic wind bursts (Tra­ NAO modes makes the Alboran Sea more meso- to oligotrophic, thus montana, Mistral) are associated with enhanced vertical mixing and favoring G. inflata over G. bulloides. reduced surface productivity (Keerthi et al., 2021). Due to its positive The strong link between DWF in the Gulf of Lion and surface pro­ response to phytoplankton blooms in the northwestern Mediterranean ductivity in the Alboran Sea (Fig. 6) and its see-saw pattern related to (Rigual-Hernández et al., 2012), total planktic foraminiferal abun­ NAO variability was previously described in Holocene marine records dances, would decrease during years of intense winter mixing, resulting (Ausín et al., 2015; Bazzicalupo et al., 2020). There is still uncertainty as in enhanced relative stocks of G. truncatulinoides and G. inflata. to which NAO mode is associated with reinforced WMDW formation and Increasing total planktic foraminiferal stocks and low relative abun­ related surface productivity in the Alboran Sea. When looking at the dances of G. truncatulinoides and G. inflata would indicate a weakened multicenntenial variability described by G. truncatulinoides and G. inflata DWF in the northwestern Mediterranean Sea. This is further supported of the Balearic record, our data corroborate the assumption of Ausín by proxies describing the variability of paleo storm activity and deep et al. (2015) relating a negative NAO to enhanced northwesterlies and a water formation in the Northwestern Mediterranean throughout the strong WMDW formation, which is further supported by paleoenvir­ Common Era (Cisneros et al., 2019; Sabatier et al., 2012). Prevailing onmental records covering the Late Holocene (Cacho et al., 2000; negative NAO phases are associated with more intense storm activity, Schirrmacher et al., 2019). In contrast, Bazzicalupo et al. (2020) suggest bringing cold katabatic winds over the Gulf of Lion and forcing intense that throughout the Holocene positive NAO phases were associated with vertical mixing and stimulating deep water formation in the north­ strong northwesterlies which strengthen DWF and increase surface western Mediterranean Sea, explaining the enhanced abundances of productivity in the Alboran basin, which is in accordance with the G. truncatulinoides and G. inflata as a result of high vertical mixing. abundance changes on multidecadal time scales, which are in phase at At our study site in the western Alboran Sea, planktic foraminiferal both study sites (Fig. 5h). Recent hydrographic studies close to our core assemblage composition is influenced by complex small-scale hydro­ location support the hypothesis of Bazzicalupo et al. (2020) since up­ graphic conditions associated with NAO modes. On top of the multi­ welling intensity increased due to stronger westerly winds and an centennial variation between MCA and LIA as described in the previous enhanced Atlantic Water inflow (Fenoglio-Marc et al., 2013; Vargas- paragraph, selected species show a multidecadal variability (Fig. 5; plus Yáñez et al., 2008), thus enhancing productivity during the Dark Age 12 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 Fig. 6. Western Mediterranean circulation pattern and interaction with planktic fora­ miniferal community as explained in the text. (a) Enhanced northwesterly winds, deep water formation, strong Atlantic inflow inducing upwelling and increasing relative abundance of G. bulloides over G. inflata in the Alboran Sea, and G. inflata and G. truncatulinoides in the Balearic Sea. (b) Weakened northwesterly winds and deep water formation, lowering Atlantic inflow and reducing upwelling, increasing relative abundance of G. inflata over G. bulloides in the Alboran Sea, and decreasing percentages of G. inflata and G. truncatulinoides in the Balearic Sea (Figure by Jagoba Malumbres- Olarte). 13 S. Pallacks et al. Global and Planetary Change 204 (2021) 103549 and MCA (Nieto-Moreno et al., 2013). However, according to our data, productivity models show a positive trend taking the whole productive the hypothesis of Bazzicalupo et al. (2020) may be applied to explain the layer reaching depths of 200 m into account (von Schuckmann et al., multidecadal NAO variabilities during the Common Era, whereas find­ 2020), whereas surface chlorophyll-a concentrations derived from sat­ ings of Ausín et al. (2015) are in good agreement with (paleo-) climatic ellites (Fig. 1) just represent the primary productivity of the upper sur­ and (paleo-) oceanographic processes stated above. face layer. Surface dwellers as G. bulloides (Rebotim et al., 2017) respond Additionally, the following reason may complicate a straightforward to productivity changes in the upper surface layer. This would explain relation between western Mediterranean deep-water formation, Alboran the low planktic foraminiferal summer production, despite the fact that Sea productivity and NAO variability. The main driver of WMDW for­ summer is the most productive season in the Mediterranean Sea when mation could have changed from air-sea heat exchange during the MCA considering the entire productive layer (von Schuckmann et al., 2020). and LIA to buoyancy loss due to more arid climates during IE (Cisneros Interestingly, G. ruberWHITE does not capture any warming signal at et al., 2019), explaining higher water fluxes through the Strait of the beginning of the IE, but describing an abundance drop at both study Gibraltar during positive NAO indices (Fenoglio-Marc et al., 2013). Our sites. Negative excursions of G. ruberWHITE during the same time period findings do not contradict Mid-Pleistocene records, relating NAO+ are detected at other regions in the western Mediterranean (Lirer et al., phases to enhanced Alboran upwelling intensity and primary production 2014; Margaritelli et al., 2016), suggesting a possible human overprint, (González-Lanchas et al., 2020), since they describe NAO phases with manifested in changes of nutrient cycling in coastal areas. The onset of millennial cyclicity, whereas our cores cover higher temporal resolution. the Modern Warm Period starting around 1950 CE is characterized by a Additionally, complex interannual hydrographic variability (Peliz et al., recovery of the warm water species, visible in both records. 2013) relocating the high productive upwelling zones on a small spatial Coccolithophore assemblages in the Alboran Sea core also testify a scale (Macías et al., 2008; Sarhan et al., 2000) and causing great inter­ drastic environmental change since the IE. In the modern ocean, Emi­ annual variability in the seasonal cycle of algal biomass (Bosc et al., liania huxleyi is the most common coccolithophore species, an oppor­ 2004; D’Ortenzio and Ribera d’Alcalà, 2009) makes the Alboran Sea a tunistic and r-selected taxon that rapidly responds to upper ocean challenging research site to study surface productivity changes (Bárcena nutrient supply (Young, 1994), and in the Alboran Sea the recent et al., 2004; Mallo et al., 2017). decrease in abundance suggests an overall decrease in productivity (Fig 2e). In the western Mediterranean, Gephyrocpasa oceanica is identified as 5.3.3.3. Anthropogenic warming as main driver in post-industrial times. In a tracer of Atlantic surface water inflow through the Gibraltar Strait the Balearic and Alboran seas, a decrease of planktic foraminiferal (Incarbona et al., 2008a; Knappertsbusch, 1993; Oviedo et al., 2015) and production, test accumulation rates, and a rapid changing species has indicated that the inflow of a sustained surface Atlantic water mass assemblage are indicating an unprecedented reduction of WMDW for­ has increased in recent time, as a consequence of enhanced DWF (Nieto- mation and surface primary productivity during the 20th century. This is Moreno et al. (2015), contradicting planktic foraminiferal composition the first evidence of significant changes in planktic foraminiferal as­ changes in the western Mediterranean (Fig. 5h). In the temperate semblages other than a geographical displacement of assemblages in the Northeastern Atlantic, G. oceanica has a clear affinity for oligotrophic oceans and took place before the oldest survey used by Jonkers et al. warm waters (Bollmann, 1997; Ziveri et al., 2004) as suggested by the (2019). Particularly, the drop of G. bulloides relative to G. inflata in the recent increase in abundance in our record (Fig. 2f). The opposite Alboran Sea over a period of low NAO indices during the first half of the abundance changes of E. huxleyi and G. oceanica described in our record, 20th century, reveals depleting surface primary productivity, corrobo­ can be interpreted as a response to decreased nutrient availability in the rated by decreasing alkenone concentrations recorded in the Alboran western Alboran Sea (Bárcena et al., 2004). Florisphaera profunda core at this time (Fig. 2b). In the Balearic Sea, declining abundances of abundance is used generally to infer nutricline dynamics and produc­ G. truncatulinoides and G. bulloides during the second half of the 20th tivity (Beaufort et al., 1997; Grelaud et al., 2012; Incarbona et al., century, indicating reduced vertical mixing and lower surface produc­ 2008b; Molfino and McIntyre, 1990). However, a recent review points tivity (Figs. 3 & 5h). During the same time period, SST shows unprec­ out that in the Mediterranean Sea, except for the Sicily Channel, the edented warming (Ahmed et al., 2013), as recorded in Uk’37 SST relationship with productivity levels is not clearly established estimates of both cores (discussed in 5.2) and more positive AMO phases (Hernández-Almeida et al., 2019). In particular, previous studies had (Figs. 5). These findings suggest that the western Mediterranean Sea shown that F. profunda can have different dynamics of deep production became more oligotrophic during the 20th century, as a result of (Stoll et al., 2007) and this seems the case for the slight decrease of this anthropogenically induced SST warming and vertical stratification of taxa recorded in our core in recent years (Fig. 2g). In summary, we the surface water column. Primary productivity depends on light, and interpret G. oceanica abundance increases and E. huxleyi decreases in the nutrient supply affected by stratification of the water column mostly top layer of the Alboran Sea sediment core as a reduction in surface driven by temperature (Longhurst, 1995). Higher SSTs increase near productivity, which agrees with changes in planktic foraminiferal surface stratification inhibiting vertical mixing. Consequently, less nu­ composition (Fig. 5). Remarkably, this study provides the first evidence trients are transported to the upper ocean causing less fertilized surface of a distinct ecological modification in Mediterranean coccolithophore conditions (Behrenfeld et al., 2006). Lower primary production levels assemblages since industrial anthropogenic greenhouse gas emission. favor the proliferation of G. inflata over the high productivity indicator species G. bulloides (Fig. 5h). As the decrease in primary production 6. Conclusions cascades through the food web, total planktic foraminiferal abundance declines at 1953 ± 5 in the Balearic and at 1947 ± 3 CE in the Alboran We found that during pre-industrial times, planktic foraminiferal Sea, manifested in decreases of test accumulation rates 10X and 25X assemblages were strongly related to variabilities in NAO and AMO faster than during the LIA respectively (Fig. 5i). This is in agreement influenced by changes in solar irradiation. Positive NAO modes pre­ with decreasing foraminiferal fluxes in the western Mediterranean Sea, vailed during the MCA and led to a weakened DWF in the Gulf of Lion. A when comparing plankton tow studies carried out from the late 1980s predominant negative NAO during the LIA is associated with intense, (Mallo et al., 2017; Pujol and Grazzini, 1995), and decreasing surface cool northwesterly winds, reinforcing WMDW formation. A multi­ chlorophyll-a concentrations at both study sites during the last two de­ decadal variability is overlaying multicentennial variation, reflected in cades (Fig. 1e). the species composition of both records showing lower surface pro­ These results differ from biogeochemical models and historical data ductivity in the Alboran because of reduced DWF in the Gulf of Lion suggesting an overall increase of surface primary productivity during the during times of declining NAO modes, and vice versa. 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