Using past interglacial temperature maxima to explore transgressions in modern Maldivian coral and Amphistegina bleaching thresholds

Study site and target foraminiferal species

The Maldivian archipelago is a partially drowned carbonate platform within the central, equatorial Indian Ocean. It consists of two rows of north–south orientated atolls, which encompass an Inner Sea. The lowermost neritic carbonate unit sits upon volcanic bedrock and has been dated back to the Eocene¹⁹ with continuous drift deposition, within the Inner Sea, starting ~ 12.9 Ma at the establishment of the modern South Asian Monsoon (SAM)^35,36. This seasonally reversing, major climatic system has an impact on both the regional precipitation patterns as well as physiochemical oceanographic properties (Fig. 1). The summer southwest SAM brings warm, wet conditions to the Indian subcontinent, as well as higher saline surface waters from the Arabian Sea into the Maldives region. In comparison, the winter northeast SAM results in cool, dry continental conditions and transports lower salinity water from the Bay of Bengal into the central, equatorial Indian Ocean. As a result, the Maldives seasonal salinity depth profiles can vary significantly, yet due to its tropical location the seasonal sea water temperatures are relatively stable.

Three symbiont-bearing foraminiferal species are used in this study: Amphistegina lessonii, Globigerinoides ruber (white) and Trilobatus sacculifer (with sac-like final chamber):

Amphistegina lessonii is a larger benthic, symbiont-bearing (diatoms) foraminiferal species. It has a shallow depth range (0–50 m)^37,38,39 and is globally abundant in tropical coral reef, benthic foraminiferal shoal and general carbonate shelf settings⁴⁰. Similarly to corals, amphisteginids have been shown to bleach under high temperatures/high irradiance levels with the new development of the Amphistegina Bleaching Index (ABI) as an indicator of photo-inhibitory stress in coral reef settings^41,42. From ~ 30 °C this species starts showing signs of thermal stress, with bleaching and mortality reported for temperatures > 31 °C^11,12.

Globigerinoides ruber (w) hosts dinoflagellate endosymbionts and is the most common planktonic foraminiferal species in tropical-subtropical waters¹³ state that while G. ruber (w) is generally considered one of the shallowest-dwelling species, its depth distribution does vary in relation to regional ecological conditions. It has a particular relation to the nutricline depth in less turbid, oligotrophic conditions⁴³ which has been confirmed for the Maldives²⁸. It is omnivorous, however in comparison to other omnivorous, symbiont-bearing species, it has demonstrated an elevated adaptation for consuming phytoplankton protein over zooplankton protein¹³. From culture experiments, it has a broad temperature (14–31 °C) and salinity (22–49 PSU) tolerance, and has been reported as the most tolerant species to low sea surface salinity (SSS)¹³. This species occurs year-round and has a fortnightly reproduction¹³.

Trilobatus sacculifer is a planktonic foraminiferal species abundant in tropical-subtropical surface waters and as such is extensively used in paleo-reconstructions. It hosts dinoflagellate endosymbionts yet is omnivorous, feeding predominantly on calanoid copepods¹³. It is a euryhaline species, with a broad salinity (24–47 PSU) and temperature (14–32 °C) tolerance. Similarly to G. ruber (w), this species occurs year-round and has a monthly reproduction on a synodic lunar cycle¹³. While a shallow dwelling species, it is generally reported to live slightly deeper in the water column, in comparison to G. ruber (w)^28,30,44.

Sampling

All planktonic foraminiferal specimens (G. ruber (w) and T. sacculifer (w/s)) for the geochemical analysis (δ¹⁸O_c and Mg/Ca) originate from the International Ocean Discovery Program (IODP) Expedition 359, Site U1467 (4° 51.0274′ N, 73° 17.0223′ E) drilled in 2015 within the Inner Sea of the Maldivian archipelago at a water depth of 487 m¹⁹. The age model for these samples was adopted from a previous study⁴⁵ which is based on the correlation of their long-term (0–1800 kyr) Site 359-U1467 C. mabahethi and G. ruber (w) δ¹⁸O_c records to the stacked reference curve of⁴⁶. Recent surface sediment samples (mudline A and B: representing the sample from the sediment/water interface), as well as three samples from the peak of MIS9e (U1467C, 2H6, 0–1 cm; U1467C, 2H6, 15–16 cm; U1467C, 2H6, 18–19 cm) and MIS11c (U1467B, 3H2, 147–148 cm; U1467B, 3H3, 9–10 cm; U1467B, 3H3, 12–13 cm) were analysed^19,28 (sample locations are shown on Fig. 3). The mudline is identified as Recent, likely representing the last few hundred years, based on the presence of Rose Bengal (1 g/L) stained ostracods and benthic foraminifera. The study by⁴⁵ has verified that diagenetic influences, within this shallow, carbonate environment, are not a concern for foraminiferal geochemical compositions over the investigated time-interval (MIS1-11).

Rose Bengal stained A. lessonii specimens were obtained from modern surface rubble samples collected by hand, at 10 m water depth, during the 2015 International Union for Conservation of Nature (IUCN) REGENERATE cruise⁴⁷ (Supplementary Table 6). Samples were collected from the reefs of two islands, Maayafushi and Rasdhoo, both located within the central part of the Maldivian archipelago. As the foraminifera shells were stained pink, it implies they were living at the time of collection. These specimens were used for stable isotopic analysis and their reconstructed temperatures represent modern (a cumulative signal encompassing their lifespan of four to twelve months⁴⁸) conditions (Supplementary Tables 5–6). A full explanation of the Rose Bengal protein stain for foraminifera is detailed in⁴⁹.

δ¹⁸O_c stable isotopic analysis

All samples were initially washed using a 32 μm sieve to remove the finer clay and silt fractions. Subsequently, they were air dried and sieved into discrete sizes for foraminiferal picking. To ensure enough calcite for the measurements, all specimens for Individual Foraminifera Analysis (IFA) for both G. ruber (w) and T. sacculifer (w/s) (n = 632) were picked from the 355–400 μm size fraction. In addition, traditional whole-shell (pooled) measurements for G. ruber (w) (n = 24) were conducted on specimens from the 212–400 μm fraction (2–5 pooled specimens). Trilobatus sacculifer (w/s) traditional whole-shell analysis (n = 21) was measured on specimens (2 pooled specimens) from the 300–355 μm fraction. The majority of these pooled measurements are obtained from^28,45,50,51 (Supplementary Table 1). Amphistegina lessonii measurements were run on single specimens > 250 μm in size. Prior to stable isotopic analysis, all shells were briefly cleaned (1–2 s) by ultrasonication in Milli-Q water to remove any adhering particles. All stable isotopic measurements were conducted at the School of GeoSciences at the University of Edinburgh on a Thermo Electron Delta + Advantage mass spectrometer integrated with a Kiel carbonate III automated extraction line. Samples were reacted with 100% phosphoric acid (H₃PO₄) at 90 °C for 15 min, with the evolved CO₂ gas collected in a liquid nitrogen coldfinger and analysed compared to a reference gas. All samples are corrected using an internal laboratory standard and expressed as parts per mil (‰) relative to Vienna Pee Dee Belemnite (VPDB). Replicate measurements of the standards give the instrument an analytical precision (1σ) of ~ 0.05 ‰ for δ¹⁸O and δ¹³C.

Mg/Ca analysis

The Mg/Ca data is obtained from^28,45,50,51 (Supplementary Table 1). Each G. ruber (w) Mg/Ca analysis (n = 17; 212–250 μm in size) was conducted on 30 pooled specimens by inductively coupled plasma optical emission spectrometry (ICP-OES) on a Thermoscientific iCap 6300 (dual viewing) at the Institute of Geosciences of the Goethe-University of Frankfurt. All samples were initially cleaned (1–2 s) by ultrasonication in Milli-Q water and then the standard oxidative cleaning protocol of⁵² followed to prevent clay mineral contamination. The final centrifuged sample solution was diluted with an yttrium solution (1 mg/l) prior to measurement to allow for the correction of matrix effects. In addition, before each analysis five calibration solutions were measured to allow for intensity ratio calibrations. All element/Ca measurements were standardized using an internal consistency standard (ECRM 752–1, 3.761 mmol/mol Mg/Ca). Furthermore, the elements Al, Fe, and Mn were screened and blanks periodically run to monitor for further signs of contamination during the analyses.

Establishment of present and past seawater temperatures

Prior to temperature calculations, we test the IFA distributions for normality using the Shapiro‐Wilk test and the Fisher–Pearson coefficient of skewness with bootstrap confidence intervals, to define the skewness of the datasets⁵³ (Supplementary Table 3). The Recent G. ruber (w) and T. sacculifer (w/s) and MIS11c T. sacculifer are normally distributed. In the case of both MIS9e datasets and the MIS11c G. ruber population, the null hypothesis that the data are normally distributed (p ≤ 0.05) is rejected (Supplementary Table 3). Considering bioturbation within the sediment record is a possibility, we use two methods to identify and remove outliers in the IFA datasets. Firstly, the inter-quartile range (IQR) is used for each δ¹⁸O_c dataset, which defines a measurement as an outlier if it falls outside the range [Q1 − 1.5 (Q3 − Q1), Q3 + 1.5 (Q3 − Q1)], with IQR = Q3 − Q1 and Q3 and Q1 representing the third and first quartile of the dataset²⁰. But if there is considerable reworking, the IQR method would not necessarily identify reworked glacial measurements (highest δ¹⁸O_c values) within the interglacial samples. As such, the Recent IFA datasets, which are both normally distributed, are used to further set a rudimentary cut-off point for the highest δ¹⁸O_c (= lowest temperatures) value to expect during past interglacial minima periods for both G. ruber (w) and T. sacculifer (w/s) (this is discussed further in the Supplementary Materials, Supplementary Figs. 1–3).

There are innumerable analytical techniques (e.g., traditional mass spectrometry, secondary-ion mass spectrometry, laser ablation inductively coupled plasma mass spectrometry), proxies (Mg/Ca, δ¹⁸O, clumped isotopes, TEX86, U^k’₃₇) as well as target medians (e.g., calcitic shells of foraminifera, aragonitic coral skeletons, ice, lipids, alkenones) which are used in marine paleo-temperature reconstructions. Furthermore, different methods exist in the literature to calculate temperature estimates using both planktonic foraminiferal δ¹⁸O_c and Mg/Ca measurements with innumerable species-specific δ¹⁸O-temperature and Mg/Ca-temperature equations reported^{20,23,30,54,55,56}. Moreover, due to the exponential nature of the Mg/Ca-temperature equations, if inappropriately applied, offsets in the upper temperature range are exacerbated. Additional considerations are species-specific offsets and differential geochemical compositions within the shell (e.g., high versus low Mg banding, gametogenic calcite). Trilobatus sacculifer gametogenic calcite has been reported to be significantly enriched in Mg in comparison to the rest of the shell⁵⁷. As T. sacculifer specimens selected for use in this study underwent reproduction, indicated by the presence of a sac-like final chamber⁵⁸, we can expect their Mg/Ca ratios to be biased. As such, to avoid overestimates we chose to use only G ruber (w, pooled) Mg/Ca and δ¹⁸O_c data to calculate representative δ¹⁸O_sw values for each time interval, for use with both the G. ruber (w) and T. sacculifer (w/s) δ¹⁸O_c IFA datasets. Considering both planktonic species are considered as shallow-dwellers with similar living depths and an affinity for the DCM, the utilisation of common δ¹⁸O_sw values is applicable^13,28,30.

The G. ruber Mg/Ca-temperature Eq. (1) from⁵⁵ (temperature calibration range: ~ 22–27 °C), similarly applied in the Maldivian study of²⁸, was used in this study:

The applied δ¹⁸O-temperature species-specific equations (Eqs. 2 and 3) were previously utilised in the local study by²⁸. Both the G. ruber (Eq. 2) and T. sacculifer (Eq. 3) equations are from the Indian Ocean study of⁵⁹ (temperature calibration range: ~ 20–31 °C):

Using the above equations, the range in temperature estimates are obtained as follows (Fig. 4):

1. 1.

   The mean G. ruber (w) Mg/Ca measurements are used together with Eq. (1) to calculate a temperature estimate for each time point (Supplementary Table 1). Since the Mg/Ca calcification temperatures are based on 30 pooled specimens, they are considered to reflect mean calcification temperatures.

2. 2.

   The Mg/Ca derived temperature estimates are then used together with the mean traditional (pooled) G. ruber (w) δ¹⁸O_c data and Eq. (2) to calculate representative δ¹⁸O_sw values for each time point (Supplementary Table 2). As these are calculated from pooled samples, they are considered to mirror mean δ¹⁸O_sw values for both the Recent and fossil populations.

3. 3.

   The G. ruber (w) and T. sacculifer (w/s) IFA datasets are then used, together with the relevant species-specific δ¹⁸O-temperature equations and δ¹⁸O_sw values, to calculate the spread in temperature estimates (Fig. 4, Supplementary Tables 3–4).

Trilobatus sacculifer (w/s) data from the glacial maxima of MIS12 are included in the study to illustrate the applicability of the IFA method, however, as they do not contribute to the discussion on bleaching thresholds, they are discussed further in the Supplementary Materials (Supplementary Figs. 1, 3).

Finally, the temperature estimates for the shallow-dwelling symbiont-bearing benthic A. lessonii are obtained using the genus-specific δ¹⁸O-temperature equation of⁶⁰ (Eq. 4) (Supplementary Tables 5–6).

Considering the benthic specimens were deemed living at the time of collection (Rose Bengal stained), a mean regional surface (0 m) δ¹⁸O_sw value (0.49 ‰) is used together with the δ¹⁸O_c data in the calculations (Supplementary Tables 5–6).

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