ARTICLE https://doi.org/10.1038/s43247-023-00947-7 OPEN Anthropogenic acidification of surface waters drives decreased biogenic calcification in the Mediterranean Sea Sven Pallacks 1 ✉, Patrizia Ziveri 1,2, Ralf Schiebel3, Hubert Vonhof 3, James W. B. Rae 4, Eloise Littley 1,4, Jordi Garcia-Orellana 1,5, Gerald Langer1, Michael Grelaud 1 & Belen Martrat6 Anthropogenic carbon dioxide emissions directly or indirectly drive ocean acidification, warming and enhanced stratification. The combined effects of these processes on marine 1234567890():,; planktic calcifiers at decadal to centennial timescales are poorly understood. Here, we ana- lyze size normalized planktic foraminiferal shell weight, shell geochemistry, and supporting proxies from 3 sediment cores in the Mediterranean Sea spanning several centuries. Our results allow us to investigate the response of surface-dwelling planktic foraminifera to increases in atmospheric carbon dioxide. We find that increased anthropogenic carbon dioxide levels led to basin wide reductions in size normalized weights by modulating for- aminiferal calcification. Carbon (δ13C) and boron (δ11B) isotopic compositions also indicate the increasing influence of fossil fuel derived carbon dioxide and decreasing pH, respectively. Alkenone concentrations and test accumulation rates indicate that warming and changes in biological productivity are insufficient to offset acidification effects. We suggest that further increases in atmospheric carbon dioxide will drive ongoing reductions in marine biogenic calcification in the Mediterranean Sea. 1 Institute of Environmental Science and Technology (ICTA), Autonomous University of Barcelona (UAB), Bellaterra, Barcelona, Spain. 2 Catalan Institution for Research and Advanced Studies, Barcelona, Spain. 3 Department of Climate Geochemistry, Max Planck Institute for Chemistry, Mainz, Germany. 4 School of Earth & Environmental Sciences, University of St Andrews, St Andrews, UK. 5 Department of Physics, Autonomous University of Barcelona, Bellaterra, Barcelona, Spain. 6 Department of Environmental Chemistry, Spanish Council for Scientific Research (CSIC), Institute of Environmental Assessment and Water Research (IDAEA), Barcelona, Spain. ✉email: pallacks.s@gmail.com COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv 1 ARTICLE COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 S ince the onset of the Industrial Revolution, human-induced climate change has rapidly modified the Earth system with notable impacts on the oceans. Rapidly increasing atmo- spheric carbon dioxide (CO2) concentrations have resulted in global surface ocean pH decline of approximately 0.1 units compared to pre-Industrial levels1, impacting the calcification process of marine calcifiers2,3. Since the mid-19th century, enhanced CO2 emissions have also contributed to global ocean surface warming by 0.76 ± 0.16 K between 1904 and 20164,5. In the second half of the 20th century, anthropogenically induced warming has also intensified vertical ocean stratification6, leading to changes in nutrient cycling and depletion of surface marine productivity7. These alterations of pH, temperature, and food availability are each assumed to influence the calcification rates of critical calcifying taxa such as planktic foraminifera8,9, but their response to the combination of these factors is still unclear. The Mediterranean is a primary climate change hot-spot that shows amplified climate responses to global change10,11, making it a key region to investigate the response of marine ecosystems to human-induced changes of the chemical, physical, and biological environment. Due to its high alkalinity and the short residence times of its water bodies, the Mediterranean Sea is expected to have an exceptionally high uptake rate of anthropogenic carbon12–14. Both annual mean surface air temperature and sea surface temperature (SST) have accelerated in the Mediterranean region compared to the global average since 1880 Common Era (CE)11. The recent SST warming at a rate of 0.35 K per decade15, may result in thermally induced stratification and decreasing biological productivity16. Fig. 1 Sea surface temperature (SST) and surface pH at the 3 study Comprehensive, multi-decadal monitoring of plankton com- locations in the western Mediterranean basin. a Western Mediterranean munities started in 193117, while time series measurements of SSTs from World Ocean Atlas 2018119. b Sea surface pH based on a global seawater carbonate chemistry18 and surface ocean productivity19 gridded dataset covering the period 1982–2020120. Both maps are began only in the late 20th century. As a result, observational time produced with Ocean Data View (version: 5.6.3)121. Red pins indicate core series are too short to reasonably attribute changes in the ocean’s locations: MedSeA-S3-c1 (Alboran Sea; 3), MedSeA-S23-c1 (Balearic Sea; biological productivity to anthropogenically driven climate 23), MedSeA-S7-c2 (Strait of Sicily; 7). change20. Laboratory experiments give important clues on how calcifying plankton copes with rapid climate change, but it remains difficult to capture the complex natural environment in a anthropogenically-driven productivity changes during the IE16. laboratory setting. Paleo-reconstructions of plankton calcification Warming of western Mediterranean surface waters over the 20th and accompanying records of environmental conditions can century is shown by alkenone derived SST data and (HadISST) address these issues, providing records going back to pre- satellite time series observations (Figs. 2a, 3c). A mid-20th century industrial times which could capture the impact of changing cooling period by > 1 K in the Mediterranean from the end of the physical and chemical conditions on the marine ecosystem. 1940s to the end of the 1980s is confirmed, as seen in other western Here, we provide radiocarbon and radionuclide-dated, high- Mediterranean paleotemperature records16,22. This cooling episode resolution marine proxy records from three locations in the wes- is followed by rapid warming over the last 20 years. Any offsets tern Mediterranean Sea (Fig. 1), covering the transition from the between instrumental and paleorecords might be due to low data pre-industrial (pre-IE) to industrial era (IE), starting from about coverage for SST calibrations in the central Mediterranean (Sup- 1800 CE. With these we investigate the basin-wide, interspecies plementary Note 1). Indeed, while the Strait of Sicily alkenone (Globigerinoides elongatus and Globigerina bulloides) response of record indicates warming just above average over the last two planktic foraminiferal calcification (represented by the measured decades, other recently published paleorecords in the Alboran and Size Normalized Weight, SNW) to warming, acidification, and Balearic Sea16 consistently show accelerated 20th century sea sur- variations in primary productivity, reconstructed using a suite of face warming (Fig. 2a), with unprecedented warming rates at paleo proxies, over the onset of the Industrial Revolution. We show present in the Mediterranean Sea23. High sea surface warming rates an unprecedented basin wide SNW decrease of 18% to 34% in the at our sites confirm a rapid, anthropogenically induced sea surface species G. elongatus, and 7% to 35% in G. bulloides over the 20th warming in the western Mediterranean. century. Enhanced uptake of anthropogenic CO2 by Mediterranean Accelerated anthropogenic climate change has altered marine surface waters as shown by decreasing planktic foraminiferal δ13C productivity in the Mediterranean Sea, as reflected by plankton (Suess Effect) and decreasing pH derived from boron isotopes community changes16. The sedimentation rate of planktic (δ11B), brings us to the conclusion that anthropogenic CO2 impairs foraminiferal tests is positively related to primary productivity24, foraminiferal calcification. while alkenone concentrations are closely related to phytoplank- ton biomass25. Both foraminiferal tests and alkenones thus serve as proxies of changes in past ocean productivity and reflect Results and discussion surface productivity levels at all three study sites (Supplementary Human induced sea surface warming and productivity changes Note 1). In the Strait of Sicily, test accumulation rates decrease in the western Mediterranean. The western Mediterranean Sea is between the 1850s and 1940s, then increase rapidly, which, a hotspot of rising SST, at a rate above the global average21, and alongside increasing C37 alkenone concentrations, indicates 2 COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 ARTICLE Fig. 2 Changes of sea surface conditions and planktic foraminiferal size normalized weight (SNW) over the Common Era at three western Mediterranean core sites (Alboran and Balearic Seas, and Strait of Sicily). a Sea surface temperature (SST) changes derived from alkenones (dark blue line) and the HadISST data set (light blue line). b Marine surface productivity represented by total test accumulation rate (purple line), alkenone concentration (grey symbols), and species composition (G. bulloides versus G. inflata) and species abundance (G. inflata + G. truncatulinoides) changes (brown line)16,122. c Suess effect displayed through δ13C (‰ VPDB) signature measured in planktic foraminiferal tests of G. elongatus (red dashed line) and G. bulloides (blue dashed line) with error bars indicating 0.1 ‰ uncertainty (1 SD level) and displayed as 3 point running average. d Surface ocean pH estimated with CO2SYS (black line- see methods) and boron isotope measurements (Orange symbols) in tests of G. elongatus (Alboran Sea) and G. ruber albus (Strait of Sicily), with vertical error bars indicating one standard deviation of uncertainty and horizontal error bars displaying age error range. e Planktic foraminiferal calcification expressed as SNW for G. elongatus (red) and G. bulloides (blue) with error bars indicating one standard deviation of uncertainty, displayed as 3 point running average. Grey shaded area in Alboran and Balearic time series represents the pre Industrial Era, prior to 1800 CE with a compressed time axis. enhanced productivity during the second half of the 20th century of the western Mediterranean Sea. While fluctuations in carbo- (Fig. 2b). Biogeochemical model results26 and historical records27, nate chemistry, productivity, and hydrography may modulate the confirm productivity increase in Mediterranean surface waters carbon isotope signal, these influences are relatively small com- during the 20th century, and suggest enhanced anthropogenic pared to the change in the isotopic composition of ambient nitrate and phosphate loads as the main driver of surface water seawater due to the input of low δ13C CO2 from fossil fuel eutrophication. In contrast, a decrease in productivity is observed burning (the Suess Effect)28–30, making δ13C a good tracer for in the Alboran and Balearic records during the second half of the natural versus anthropogenic environmental changes. 20th century (Fig. 2b). At these sites, enhanced stratification We use the two morphotypes of planktic foraminiferal species through 20th century SST increase likely explain surface Globigerinoides elongatus (syn. Globigerinoides ruber white sensu productivity losses, which are also recorded through changes in lato) and G. ruber albus (syn. G. ruber white sensu stricto) as well as planktic foraminiferal species composition16. Our results and Globigerina bulloides to evaluate environmental alterations in the previous studies thus show regionally distinctive patterns of 20th upper water column, as they are surface mixed layer dwellers31. As century productivity changes for the western Mediterranean. G. bulloides thrives in late winter/early spring and G. ruber in late spring/summer32,33, we also cover most of the seasonal change in sea surface temperature and primary productivity. Anthropogenic CO2 intrusion into western Mediterranean At all three sites analyzed here, G. elongatus and G. bulloides waters recorded by planktic foraminiferal test chemistry. The show a notable δ13C drop during the IE, against a backdrop of δ13C and δ11B signatures of planktic foraminiferal tests provide pre-industrial natural variability (Figs. 2c and 3d), which we refer sensitive tracers of anthropogenic carbon uptake and acidification to here as negative anthropogenic carbon isotope excursions COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv 3 ARTICLE COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 (nCIEs). nCIEs show most marked decreases during the latter half of the 20th century with a mean amplitude of −0.60‰ and range between −1.24‰ and −0.14‰ (Supplementary Fig. 1). We attribute these nCIEs to the increase of the surface ocean concentration of anthropogenic CO234. The measured decline of δ13C in our foraminiferal tests during the second half of the 20th century describes a more pronounced Suess Effect signal when compared with results from the Northwest Atlantic (range = −0.174‰ to −0.757‰; weighted average = −0.45‰)30. Ocean uptake of anthropogenic CO2 increases hydrogen ion (H+) concentrations and hence lowers pH35. Boron isotope ratios of tests of G. ruber albus and G. elongatus reveal a notable pH decline in the Alboran Sea of −0.14 units between 1697 and 1995 CE, which is in accordance with previous estimates over the industrial period ranging from −0.06 to −0.16 units36, and also notable ocean acidification in the Strait of Sicily, with reconstructed pH decreasing by 0.22 units from 1830 to 2007 CE. These results are largely consistent with the acidification expected from anthropogenic CO2 invasion (Supplementary Fig. 2), which we calculate by assuming equilibrium between surface waters and the atmosphere alongside modern alkalinity and observed SST change at each site (see Methods); we note that absolute pH values from δ11B are lower than recent pH levels (Fig. 2d) measured in the Mediterranean Sea37–41, a feature that is discussed in more detail in the supplements (Supplementary Note 2). Slightly enhanced acidification in the Strait of Sicily might be caused by enhanced vertical mixing during the second half of the 20th century, transporting low-pH Mediterranean intermediate waters to the surface42 as indicated through enhanced productivity and SST cooling compared to other sites (Fig. 2a, b). Measurements reveal recent pH decreases between 0.0009 yr−1 and 0.0036 pH units yr−1 in the Alboran Sea41 and between 0.0013 yr−1 and 0.0030 pH units yr−1 in the North Western Mediterranean39,40, which exceed the global average trend of 0.0017 ± 0.0002 pH units yr−1 43. The rate of pre- industrial to modern pH decline is well-reflected by our boron isotope derived values and corroborated by CO2SYS model estimates (Supplementary Fig. 2), suggesting acceleration of ocean acidification in western Mediterranean surface waters during the 20th century. Whilst the nCIEs primarily reflect uptake of isotopically light Fig. 3 Basin-wide changes of western Mediterranean sea surface CO2 in the surface ocean, falling [CO32−] and pH levels tend to conditions and planktic foraminiferal size normalized weight (SNW) over increase δ13C in foraminiferal tests44, and could thus dampen the the Common Era driven by enhanced anthropogenic CO2 emissions. Suess Effect driven nCIE signal we observe. Based on laboratory a Atmospheric CO2 concentrations derived from measured102 and and field data44–46, western Mediterranean pH and [CO32−] reconstructed103,104 records. b Stack of Mediterranean Sea Surface changes since 1900 are estimated to account for approximately Temperature (SST) anomalies (blue line) with light blue shading 0.24‰ to 0.33‰ (G. ruber) and 0.48‰ (G. bulloides) of δ13C test indicating the 68% Confidence Interval23. c Generalized additive model changes (Supplementary Table 1). Ambient water temperature (GAM) fit (purple line) of standardized SST data (purple open squares) changes have a minimal, negative effect on δ13C in foraminiferal including alkenone derived SST122 and calculated mean from HadISST for tests45,47, accounting for −0.12 ‰ in G. bulloides tests, when each location. Purple shading indicates 95% Confidence Interval. d GAM basing estimations upon SST warming rates in the western fit (dark blue line) to standardized δ13C results comprising G. elongatus Mediterranean (Supplementary Table 1). Variability in upwelling (blue triangles) and G. bulloides (blue circles) of all three stations, blue strength and biological productivity can also influence δ13C in transparent ribbon indicates 95% confidence interval. e Standardized pH calcite tests at the species scale45, as can algal or bacterial values (black symbols) estimated through CO2SYS for Alboran Sea symbionts, which change the microenvironment of planktic (diamonds), Balearic Sea (full circles) and Strait of Sicily (triangles). foraminifera near the test surface impacting their δ13C Standardized pH values derived from boron isotope measurements signal48–50. Strong pH and SST changes, differential upwelling, (orange symbols) in G. ruber albus at Strait of Sicily (circles), and in G. and productivity patterns at our three study sites are thought on elongatus at the Alboran Sea (squares). f GAM fit (dark red line) to the whole to slightly counter the Suess Effect and attenuate the standardized SNW of G. elongatus (red triangles) and G. bulloides (red full magnitude of the signal of decreasing δ13C in our planktic circles) of all three stations, red transparent ribbon indicating 95% foraminiferal tests29. confidence interval. We conclude that the input of isotopically light anthropogenic CO2 in the surface ocean has caused nCIEs during the IE in both G. bulloides and G. elongatus in the western Mediterranean Sea. 4 COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 ARTICLE At the same time, enhanced CO2 uptake by the ocean drives primary productivity and SNW for our targeted species varies acidification, as indicated by boron isotope measurements and according to interspecific and intraspecific diversity and thus model estimates, attenuating the Suess Effect signal. Sea surface different calcification responses to changing trophic conditions. warming, upwelling, and changes in marine surface production Previous studies detect weak positive/negative correlations during the 20th century have minor attenuating influences on the between chlorophyll a and SNW for symbiont-barren G. δ13C signal. bulloides/symbiont bearing G. elongatus in the Atlantic Ocean8,58, while a reverse correlation is observed for those species in the Mediterranean Sea63. Evidence for a minor effect of varying Anthropogenic impacts on planktic foraminiferal calcification. productivity on the calcification response of planktic foraminifera SNW is a useful tool for understanding the differential response is given by the fact that, despite opposing productivity signals of planktic foraminifera to climate change stressors like ocean during the second half of the 20th century (Fig. 2b), we see warming, acidification, and productivity changes. SNW provides consistent SNW decreases in both species at all three stations a normalized measure of chamber wall thickness and density, (Figs. 2e; 3f). reflecting carbonate production and preservation of planktic Changes of the chemical test microenvironment due to foraminiferal tests47, and is used as a proxy for past [CO32−]9,51, photosynthetic activity also influences calcification of planktic though has also been suggested to provide a potential proxy for foraminifera48. Higher photosynthetic activity increases pH and growth rate in planktic and benthic foraminifera52,53. Although reduces CO2 concentrations near the shell, resulting in enhanced secondary influences such as physico-chemical conditions of calcification rates49. If enhanced stratification led to enhanced ambient seawater, and autecological properties can influence light availability during the 20th century, this would likely have SNW, these do not seem to prevent the application of the increased SNW of planktic foraminiferal species associated with proxy8,54. We found that SNW of G. elongatus and G. bulloides symbionts capable of performing photosynthesis, though this decreased at all three stations throughout the last 200 yr., effect is evidently masked by the dominant role of [CO32−] on unprecedented against the backdrop of our ~1500 yr. long records calcification. Diagenetic processes can bias the significance of in the Alboran and Balearic Seas (Figs. 2e; 3f). Basin-wide relative SNW as a proxy for planktic foraminiferal calcification, as SNW loss during the 20th century in G. elongatus ranges from dissolution/precipitation of carbonates on tests might be inter- 18% to 34% and in G. bulloides from 7% to 35% (Supplementary preted as reduced/enhanced mass of planktic foraminiferal shells. Fig. 3). Across all three western Mediterranean records (Fig. 1), scanning Decreasing ocean pH and [CO32−] due to enhanced CO2 electron microscope images (Supplementary Figs. 5–7) of both uptake from the atmosphere can impede the biological species G. bulloides and G. elongatus show approximately the precipitation of carbonate tests55, depending on the species- same degree of dissolution from top to bottom core depth with specific response. Commonly, G. elongatus and G. bulloides minor surface corrosion and breakup of the surface layer reduce their test calcite mass with lower [CO32−], calcite structure of the test wall67,68. Therefore, calcite saturation level saturation (Ω), and pH, shown by numerous studies based on of subsurface to bottom waters at the three core sites are assumed sediment and water samples, sediment trap time series, as well to not have significantly changed, and weight loss of settling tests as culture experiments9,51,56,57. Despite this, in the natural in the deep water column as discussed by Schiebel et al.69 may environment, it is important to consider the combined influence have been the same over the entire time interval discussed here. of the various environmental drivers on planktic foraminiferal As western Mediterranean deep and bottom waters are super- calcification, with studies using cultures, sediment traps, saturated with regard to calcite13,37,70, dissolution at the sediment plankton nets and marine sediments attributing SNW changes pore water interface is unlikely. The post-sapropel (<6 kyrs) to surface ocean carbonate chemistry, alongside temperature western Mediterranean is a mesotrophic sea with limited changes and productivity8,9,51,54,57–60. and overall decreasing biological productivity over the past 150 Sea surface warming decreases the solubility of atmospheric years16,71. Accordingly, supra-lysoclinical dissolution as well as CO2, elevating [CO32−] in surface water, while higher tempera- corrosive porewater conditions, which may infer post deposi- ture can also foster enzymatic activity, resulting in faster growth tional test weight reduction in surface seafloor sediments through rates and enhanced calcification rates61. Both effects cause an decomposing organic matter can be assumed absent72. This is in increase in planktic foraminiferal SNW, a relationship observed line with previous sediment trap and core top studies from the in our target species in a number of earlier studies8,9,51,56,58,62. western Mediterranean Sea, reporting no signs of dissolution in Sea surface warming in the western Mediterranean, as shown in fossil planktic foraminifera assemblages32,33,73. In contrast, early our records (Figs. 2a; 3c), should have enhanced SNW in both diagenetic calcite coating is reported for both species from core species over the IE if temperature were the leading influence. The top samples at certain sites in the western and central negative correlation between SST and SNW of G. elongatus and Mediterranean Sea74,75. However, no signs of diagenetic over- G. bulloides at all three study sites during the IE, is indicative of growth and secondary precipitated inorganic carbonates (e.g., an overriding effect of declining [CO32−] due to anthropogenic inorganic calcite crusts, inorganic calcite crystals, overgrown carbon input during the last 150 yr., masking any small opposing pores) are present in the tests of G. elongatus and G. bulloides effect of temperature changes. Although temperature rise may from the three core sites analyzed here (Supplementary Figs. 5–7). have somewhat dampened the decrease in SNW, our results Accordingly, due to the constant mild surface etching dissolution substantiate the dominant role of [CO32−] decline due to ocean of similar magnitude of all tests observed across all three records, acidification as the main driver of test calcite production. the relative foraminiferal SNW changes at the three core sites are Marine primary productivity in surface waters is assumed to expected to result from changes in biogenic calcification at the sea influence test calcite production and therefore SNW8,63. Test surface rather than diagenetic processes during sedimentation. calcification is energy demanding64, as greater food availability Driven by industrial carbon dioxide emissions, enhanced could allow foraminifera to allocate more energy to it. anthropogenic CO2 penetration into the western Mediterranean Chlorophyll a concentrations may serve as a proxy for marine Sea and resulting reductions in pH and [CO32−] are shown to be primary productivity and food availability, as phytoplankton is the key drivers of planktic foraminiferal SNW loss during the considered to be the basis of planktic foraminiferal 20th century (Fig. 3a–f, Supplementary Fig. 2), corroborated by alimentation65,66. However, the relationship between marine multiple regression analysis, discounting of multicollinearity COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv 5 ARTICLE COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 between the independent parameters controlling SNW changes foraminiferal target species was based on47, distinguishing between Globigerina (see methods). Reduced SNW of similar magnitude during the bulloides (d’Orbigny 1826) and the two morphotypes of Globigerinoides ruber (d’Orbigny 1839), Globigerinoides elongatus and G. ruber albus81. 20th century have been observed in the tropical Atlantic, Southern Ocean, the California Current System, and the western Size Normalized Weight. In order to obtain the calcite mass of planktic for- Mediterranean Sea, showing similar amplitudes of relative aminiferal tests, a size related measure of test wall thickness and density—the Size calcification decrease57,73,76,77. Sea surface warming, productivity Normalized Weight (SNW)—was obtained, which can be calculated by means of and solar activity changes are assumed to play only a negligible Eq. (1): role, with rising SST and solar irradiance maxima potentially slightly attenuating the impact of anthropogenic CO2 on planktic SNW ¼ C þ ððC  ð100  ð100=BÞ  AÞ=100ÞÞ ð1Þ foraminiferal SNW. Accordingly, different oceanographic settings Where C is the species average mass (μg) for each sample, A represents the average at the three selected core sites are responsible for the variability in minimum Feret diameter (μm) for each sample and B is the average minimum 20th SNW trends (Supplementary Note 3), while the effects of Feret diameter (μm) of all specimens of one species of all samples. The equation diagenetic processes biasing the planktic foraminiferal SNW (Eq. 1) includes the term to account for the relative SNW changes of the same signal can be ruled out. species. Our methodology for measuring SNW is based on the sieve-based weight (SBW) technique, however, our approach also integrates measurements of indi- vidual test sizes in SNW estimations, a parameter used for the measurement-based Conclusion weight (MBW) technique82. All specimens of a single sample are weighed together, Accelerated anthropogenically-induced surface water pH decline in while the average test size per sample is calculated by the minimum Feret diameter the western Mediterranean Sea is confirmed by boron isotopes and of each individual specimen. The SNW average standard deviation for each station (Alboran Sea: 7.0%; Balearic Sea: 8.3%; Strait of Sicily: 8.6%) is below the metho- drives decreasing SNW of planktic foraminiferal tests. Negative dological 11% error reported by Beer, Schiebel82. Narrowing down the size fraction carbon isotope excursions during the IE in tests of the planktic of analyzed tests to 250–315 µm ensured sufficient numbers of adult specimens foraminifera species G. elongatus and G. bulloides display the signal which are large enough for SNW measurements. By applying the test weight size- of the Suess Effect—the anthropogenic CO2-driven shift to lower normalization technique described above, we were able to factor out size related mass changes, mainly influenced by temperature variations. δ13C—and highlight the influence of anthropogenic emissions as SNW was determined for G. elongatus and G. bulloides. Bulk population the most important driver of foraminiferal calcite mass decline. measurements were performed on as many tests as available but not more than 10 Alkenone-derived SST and instrumental temperature records show and at least two specimens per sample per species, representing a total of 1,990 unprecedented anthropogenic sea surface warming, that potentially analyzed tests out of 224 samples included in this dataset. Selected tests were free of visible clay particles or organic matter and abnormally formed specimens were mitigates this effect slightly. This basin-wide, interspecies multi- excluded from analysis. We weighed selected specimens together by triplicate with proxy approach, covering multidecadal to centennial time scales, a Sartorius CP2P microbalance at Universitat Autònoma de Barcelona (UAB) and thus yields a much-needed high-confidence, low-variability a Mettler Toledo XP6U Ultra Micro Balance at Max Planck Institute for Chemistry assessment of the impacts of anthropogenic climate change on (MPIC) in Mainz, Germany, in environmentally controlled weighing rooms. Tests were positioned umbilical side up, photographed with a Canon EOS 650 D camera key marine species, in a critically sensitive region. device attached to a Leica Z16 AP0 at UAB and with an Olympus UC90 attached to an Olympus SZY16 stereoscope at MPIC to measure the minimum Feret diameter Methods of each individual test, using the software ImageJ 1.53k83 and Olympus Stream Material. The study is based on high resolution multicore records collected in the Essentials 2.1. After measuring mean weight and mean minimum Feret diameter central and western Mediterranean Sea with a MC400-Multicorer system during we calculated SNW for each sample using Eq. (1). the MedSeA cruise (Mediterranean Sea Acidification in a changing climate) on 2nd May to 2nd June 2013 onboard the R/V Àngeles Alvariño. Core sampling of Biomarkers. Alkenones (heptatriaconta-8E,15E,22E-trie2-one and heptatriaconta- MedSeA-S3-c1 and MedSeA-S23-c1 was previously described in ref. 16. MedSeA- 15E,22E-die2-one) of core MedSeA-S7-c2 were extracted from sediments, purified S7-c2 was retrieved in the Strait of Sicily (Lat. 37.7080° N, Long. 12.40553° E) at a using organic solvents and quantified with a Varian gas chromatograph Model 450 water depth of 263 m, with a core length of 46.5 cm, sliced every centimeter. equipped with a septum programmable injector, flame ionization detector and a CPSIL-5 CB column (coated with 100% dimethyl siloxane; film thickness of 0.12 Age Model development. Age models of cores MedSeA-S3-c1 and MedSeA-S23- μm; L(m) * ID(mm) * OD(mm): 50 * 0.32 * 0.45). Hydrogen was the carrier gas c1 were estimated through a combination of radiocarbon and radionuclide dating, (2.5 mL min−1). Concentrations were determined using n-hexatriacontane previously described in ref. 16. The age model of MedSeA-S7-c2 (Supplementary (CH3(CH2)34CH3) as an internal standard. Absolute concentration errors were Table 2; Supplementary Note 4) was estimated through radionuclide analysis, below 10% (resolution between the alkenones from 1.5 to 1.7). Reproducibility tests determining total 210Pb activity by measuring its alpha-emitter daughter nuclide showed that uncertainty in the Uk’37 determination is lower than 0.015 (ca. 0.5 °C) 210Po, following the methodology described in ref. 78. 209Po was added as an 16, this study, 84–86 confirming the precision of the paleothermometry tool87. SST internal tracer, before sample aliquots of 200–300 mg were totally digested in acid reconstructions were based on the global calibration of Conte, Sicre88, with a media by using an analytical microwave oven and Po isotopes plated on silver discs standard error on surface sediments at 1.1 °C. in HCl 1 N at 70 °C while stirring for 8 h. Po emissions were subsequently counted through α-spectrometers equipped with low background silicon surface barrier Stable isotope measurements. For chemical analysis, adult specimens were (SSB) detectors (EG&G Ortec) for 4 × 105 seconds. The difference between total selected from a narrow size range (250–315 µm) to minimize uncertainty in 210Pb and the constant 210Pb at depth describes the concentration of excess 210Pb, paleoceanographic interpretation due to vital effects, following suggestions by which was used to estimate maximum mean sediment accumulation rates and the Spero and Lea89. age-depth model by applying the Constant Flux: Constant Sedimentation (CF:CS) model79,80. The activities of 137Cs (661 keV) were determined by γ spectrometry in δ13C and δ18O. Bulk population measurements, including 5–10 specimens per a coaxial high-purity Ge detector (EG&G Ortec) calibrated with the SRM-4276 species sample (not necessarily the same specimens as used for SNW measure- solution standard supplied by the National Institute of Standards and Technology. ments), were performed on G. elongatus and G. bulloides. Sample weight was The quality of the results determined by gamma and alpha spectrometry was determined through a Mettler Toledo XP6U Ultra Micro Balance at MPIC. Selected evaluated by participation in IAEA proficiency tests and continuous analysis of tests were crushed and soaked in ultrapure water (Milli-Q), before ultrasonication certified and replicate materials. for up to 20 seconds, to remove clay contamination. Samples were analyzed on a Thermo Delta V mass spectrometer equipped with Planktic foraminifera. Samples were dried at 60 °C for approximately 24 hours to a GASBENCH preparation device. ~8–50 µg of CaCO3 sample, placed in a He- obtain dry bulk sediment mass. After washing over a 63 μm screen using distilled filled 4.5 ml exetainer vial was digested in water-free H3PO4 at a temperature of Elix water, the size fraction larger than 63 μm was oven dried at 60 °C for 70 °C. Subsequently the CO2-He gas mixture was transported to the GASBENCH 1 − 2 hours. Samples were dry sieved and divided by a riffle splitter (comparable to in Helium carrier gas. In the GASBENCH, water vapor and various gaseous an ASC Sample Microsplitter, ASC Scientific) at the chosen size fractions: 150–250 compounds were separated from the He-CO2 mixture prior to sending it to the μm, 250–315 μm, and > 315 μm. Total test accumulation rate was obtained by mass spectrometer in nine separate peaks. Isotope values of these individual peaks counting of more than 300 specimens in the >150 μm size fraction in all samples. were averaged and reported as δ13C and δ18O relative to V-PDB. A total of 20 Taxonomic analysis of planktic foraminiferal tests was performed on core replicates of two in-house CaCO3 standards were analyzed in each run of MedSeA-S7-c2 by visual identification using a binocular stereo microscope 55 samples. CaCO3 standard weights were chosen so that they span the entire range (magnification 10x–20x) and a bifurcated illuminator. Classification of of sample weights of the samples. After correction of isotope effects related to 6 COMMUNICATIONS EARTH & ENVIRONMENT | (2023)4:301 | https://doi.org/10.1038/s43247-023-00947-7 | www.nature.com/commsenv COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-023-00947-7 ARTICLE sample size the reproducibility of these standards is typically better than 0.1 ‰ The pH derived from Mg/Ca temperatures were compared to those from (1 SD) for δ18O and 0.1 ‰ (1 SD) for δ13C. temperatures determined from Hadley, Uk’37 and δ18O SST in (Supplementary Samples of 8 to 3 µg of CaCO3 were analyzed on the same equipment using a Table 4). A sample depth of 25 m was given to approximate the upper habitation cold trap technique that analyzes the entire sample in one single peak90,91. With depth of the species below the sea surface31. this setting, 30 CaCO3 standards were analyzed in each run of 30 samples. CaCO3 standard weights were chosen so that they span the entire range of sample weights Statistical analysis of the samples. Reproducibility of these <8 µg standards with the cold trap General additive model. Statistical analysis has been performed using the statistical technique, after sample size correction, is typically better than 0.1 ‰ (1 SD) for software R113. General additive models (GAM) have been used in paleoenviron- δ18O and 0.1 ‰ (1 SD) for δ13C. mental time series as a superior alternative tool to conventional statistical trend estimations114. We used a GAM to better show the basin wide, interspecies specific δ11B. For boron isotope analysis, samples of G. ruber (250–315 µm) were prepared change in SNW and δ13C, and western Mediterranean SST changes. The complex, in a class 100 clean lab at the University of St Andrews STAiG laboratories. The non-linear GAM fits as a smoothed function, which allows us to identify the period two morphotypes of the species were analyzed separately. Samples were first cru- of significant SNW, δ13C and SST change based on proper accounting for model shed between two glass slides before transferring to acid cleaned centrifuge tubes in uncertainty. The general and applied mathematical form of the general additive preparation for clay removal by ultrasonication. This was followed by oxidative model can be described as: cleaning in 1% hydrogen peroxide buffered with 0.1 M NH4OH and a weak acid leach in 0.0005 M distilled HNO3 according to established protocols92,93. After yi ¼ β0 þ f ðxi Þ þ εi where εi  Nð0; σ 2 Þ ð4Þ addition of 100 µl boron-free Milli-Q, samples were dissolved by incremental 15 addition of 0.5 M distilled HNO3 (total volume of acid per sample 30–50 µl). A 5% SNW ¼ 4:081e þ 6:997 þ εi where εi  Nð0; σ Þ 2 ð5Þ cut of the dissolved sample was analyzed by ICP-MS for a suite of trace elements (Supplementary Table 3) including Mg/Ca on an Agilent 8900 following Foster94 δ 13 C ¼ 0:02111 þ 6:238 þ εi where εi  Nð0; σ 2 Þ ð6Þ and Rae, Foster93 with the addition of trace hydrofluoric acid in the wash to improve washout95. Samples were run alongside matrix-matched bracketing and SST ¼ 0:02993 þ 8:033 þ εi where εi  Nð0; σ Þ 2 ð7Þ consistency standards to monitor long-term instrument reproducibility which is SNW and δ13C values were standardized and merged, combining G. bulloides reported at 95% confidence (2 SD). Low Al/Ca in all samples confirms the absence and G. elongatus at all three stations. Standardized SST is based on alkenone of residual clays. Elevated Mn/Ca was recorded in one sample but it does not measurements and the calculated mean from HadISST dataset across the three display elevated Mg/Ca or any other anomalous trace element or isotopic signal. stations. Uncertainty in the estimated model fits were addressed through 95% After trace element analysis, a few samples with low boron concentrations, as confidence intervals, after confirming gaussian error distribution via histogram determined from B/Ca, meant it was necessary to combine adjacent dissolved plot, Q-Q plot and Kolmogorov-Smirnov test for standardized datasets of SNW (p- samples in MedSeA-S7-c2 core in order to reduce δ11B uncertainty (Supplementary value = 0.5501), δ13C (p-value = 0.1738) and SST (p-value = 0.7126). Additionally, Table 4). Boron was isolated from the sample matrix using boron-specific a GAM fit was applied115, by means of the the mgcv package (version 1.8.42). To Amberlite IRA 743 resin96,97 using a batch method. For this technique, 2 ml avoid under smoothing of the fit, the smoothing term was calculated using centrifuge tubes containing 50 µl of resin were pre-cleaned by addition and removal restricted maximum likelihood116,117. of 1 ml 0.5 M HNO3 (repeated 3 times) and 1 ml boron-free Milli-Q (repeated twice) and then pre-conditioned with 100 µl 0.1 M ammonium acetate buffer at pH Regression analysis. To quantify changes of SNW and δ13C during the 20th cen- 8.5. Before loading, the sample was first buffered to pH 5 with 0.1 M ammonium tury, linear regression analysis was applied including all available data points post acetate. After pipetting onto the resin, the tubes were agitated on a VWR mini 1900 CE. Estimations of SNW and δ13C (negative anthropogenic carbon isotope vortex and the solution pipetted off after the resin settled. Following rinses with excursions; nCIEs) change are defined by the difference between 1900 CE and 2013 boron free Milli-Q water, the concentrated sample was eluted in 500 μl 0.5 M CE, based on the regression model accounting for statistical significance (Supple- distilled HNO3 and the boron isotopic composition analyzed by MC-ICPMS with mentary Figs. 1, 2). To determine statistically significant relationships between the sample-standard bracketing against NIST 951 according to methods described explanatory variable (SNW) and the independent variables (productivity, SST, pH by93,94. Addition of Hydrofluoric acid at 0.3 M helped to improve washout and and δ13C) we performed multiple linear regression analysis for time windows prior reduce boron evaporation95. Matrix matched carbonate consistency standards were (pre-Industrial Era) and post 1800 CE (Industrial Era). Abundance changes of run alongside samples to monitor reproducibility which is ± 0.23 ‰ (2 SD). indicator species, along with changes in alkenone concentrations and planktic foraminiferal test accumulation rates (Fig. 2b) are included in the productivity pH Calculations variable. SST changes are based on the alkenone and HadISST datasets (Fig. 2a). CO2SYS. To estimate unknown variables in the seawater marine carbonate system, we The pH variability is calculated from pCO2 and total alkalinity on CO2SYS used the CO2SYS program (version 2.0)98. Through a set of given input conditions (Fig. 2d), and δ13C changes are based on carbon isotope measurements (Fig. 2c). (e.g., temperature, salinity, atm. CO2 concentration), this program can estimate the To generate evenly spaced time series, we standardized data for each station and remaining unknown variables of a two “master” carbonate system (TA, DIC, pH, parameter before combining station data for each parameter by interpolating non- pCO2). We estimated surface ocean pH and carbonate ion concentrations for the linear GAM fits (method see above) using generalized cross-validation (GCV) three study sites, using seawater pCO2 and total alkalinity (TA). TA was assumed method for smoothing parameter estimation to avoid over smoothing of the fit. constant over the last century, accounting for 2400 µmol/kgSW in the Alboran Sea99, Goodness of the fit for each parameter is shown through deviance explained 2478 µmol/kgSW in the Strait of Sicily13, and 2550 µmol/kgSW in the Balearic Sea100. (Supplementary Table 5). Due to high collinearity, we have removed pH from the Surface seawater pCO2 was derived from temperature, salinity and pressure depen- model including data post 1800 CE. Both parameters are highly correlated parti- dent solubility coefficient (K0) following the formulation of Weiss101 and atmospheric cularly during the Industrial Era as the δ13C signals mirrors the input of anthro- CO2 measurements from an interpolated stack including the Mauna Loa time pogenic CO2, resulting in pH decrease (see discussion). The conditions of series102 and reconstructed CO2 concentrations103,104. Time-specific K0 values were application required for the multiple linear regression analysis have been verified determined as input conditions for down core calculations using surface pressure, by using performance package (version 0.10.3). It can be assumed that there is no SST and salinity for each study location. SST was based on alkenone (Uk’37) derived problematic amount of Multicollinearity since all parameters included in the model paleo estimates at each study location16,105 and salinity was defined as the constant show a Variance Inflation Factor below ten118. Information on multiple linear mean (1950–2019 CE) of Hadley EN4 (version EN.4.2.2) subsurface salinity objective regression models and their significance values can be found in the supplementary analysis106. Constants for our CO2SYS carbonate system estimations were the dis- material (Supplementary Tables 6, 7), confirming a significant correlation between sociation constant (K1 and K2) defined by107, refitted to seawater scale by108, the independent parameters and the explanatory variable, and substantiating the effect dissociation constants KHSO4 and KB according to109, and the chlorinity relationship of ocean acidification on SNW. and boron concentration based on110. Reporting summary. Further information on research design is available in the Nature Boron isotope transformation. To calculate pH, the δ11B of G. ruber albus and G. Portfolio Reporting Summary linked to this article. elongatus was first converted to seawater δ11Bborate using the calibration of111 for the 250 − 300 µm size fraction: δ11 Bborate ¼ ðδ 11 Bforam 9:52 ± 1:51Þ=ð0:60 ± 0:08Þ ð2Þ Data availability The boric acid dissociation constant is determined by both salinity and The dataset used in this study is publicly available online for download at PANGAEA temperature and thus calculated pH can be susceptible to variations in these Data Publisher (https://doi.org/10.1594/PANGAEA.955024). assigned values. Salinity was set at modern levels (37 PSU) for the region and temperature was calculated from Mg/Ca using the species specific calibration for G. ruber from112. 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Age model, sea surface temperature and marine calcifying Correspondence and requests for materials should be addressed to Sven Pallacks. plankton changes at two sites in the western Mediterranean Sea for the Common Era., PANGAEA (2021). Peer review information Communications Earth and Environment thanks Kate Salmon and the other anonymous reviewer for their contribution to the peer review of this work. Primary Handling Editors: Clare Davis. A peer review file is available. Acknowledgements We are grateful to Manuel F. G. Weinkauf, Laura Haynes and an anonymous reviewer Reprints and permission information is available at http://www.nature.com/reprints for their helpful comments and suggestions. We thank the captain and crew of the Spanish R/V Angeles Alvarino, and the researchers as part of the MedSeA cruise for Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in supporting the sampling of this study. We also thank Marta Casado, Yolanda Gonzalez- published maps and institutional affiliations. Quinteiro and Natalia Bravo for laboratory assistance, and Joan Manuel Bruach for his work on the analysis of 210Pb. This work contributes to the ICTA-UAB “Unit of Excellence” (FPI/MDM-2015-0552- 16-2; CEX2019-000940-M) and was funded by the Open Access This article is licensed under a Creative Commons Spanish Ministry of Science and Innovation, BIOCAL Project (PID2020-113526RB-I00), Attribution 4.0 International License, which permits use, sharing, the EU-FP7 “Mediterranean Sea Acidification in a Changing Climate” project (MedSeA; adaptation, distribution and reproduction in any medium or format, as long as you give grant agreement 265103), and the Generalitat de Catalunya (MERS, 2021 SGR 00640). appropriate credit to the original author(s) and the source, provide a link to the Creative J.W.B.R. acknowledges the European Research Council under the European Union’s Commons licence, and indicate if changes were made. The images or other third party Horizon 2020 research and innovation program (grant agreement 805246) and B.M the material in this article are included in the article’s Creative Commons licence, unless Severo Ochoa grant CEX2018-000794-S and CSIC LINKA20102. G.L. acknowledges indicated otherwise in a credit line to the material. If material is not included in the funding from the Spanish Ministry of Universities through a Maria Zambrano grant. article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from Author contributions the copyright holder. To view a copy of this licence, visit http://creativecommons.org/ S.P. and P.Z. conceived of the presented idea and organized the outline. S.P., P.Z., R.S., licenses/by/4.0/. H.V., J.W.B.R., J.G.-O., B.M. developed the methodology. S.P. took the lead in writing the manuscript. S.P. and M.G. provided figures. 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