Benthic extinction in the Tasman Sea

We reconstructed environmental parameters using a wide range of proxies at Deep Sea Drilling Project (DSDP) Site 593 over the period ∼0.75–1 Ma, covering the benthic extinction (Fig. 1). Site 593 is situated in 1,063 m of water on the Challenger Plateau of the Tasman Sea (SW Pacific Ocean, Supplementary Fig. 1), lying to the north of the modern Subtropical Front, which is a complex zone delineated by large gradients in SST and salinity16. SSTs in the Tasman Sea are considered to be sensitive to glacial–interglacial displacement of the Subtropical Front7,17. Site 593 is bathed by Antarctic Intermediate Water, which is broadly characterized by low salinity (34.3–34.5 PSU), low temperatures (3.5–10 °C) and high dissolved oxygen (200–250 μmoles kg−1; refs 18, 19).

Figure 1: Reconstructed environmental proxies for Tasman Sea DSDP Site 593. (a) Global benthic foraminifera δ18O composite52 showing colder glacial (positive) and interglacial cycles. (b) Sea-surface temperature reconstructed from alkenones. (c) Small Gephyrocapsa as a % of total nannofossil assemblage. (d) Concentration of chlorin pigments used here as a proxy for photosynthetic material related to primary productivity24. (e) Bottom-water temperature reconstructed from benthic foraminiferal U. peregrina Mg/Ca ratios. (f) Bottom-water Δ[CO 3 2−] reconstructed from benthic foraminiferal C. wuellerstorfi B/Ca ratios. (g–j) Abundance per g and number of species of benthic foraminifera from the extinction group. Note that none of the environmental proxies (d–f) follows abundance of the foraminiferal extinction group (g–j). The vertical yellow bar indicates the interval over which the foraminiferal extinction occurs, and the vertical dashed line indicates where small Gephyrocapsa dominates the assemblage. Full size image

Previous low-resolution (∼22 kyr) benthic foraminiferal data from Site 593 (ref. 5) indicated that the extinction occurred between 0.8 and 0.9 Ma. Our higher-resolution (∼3.5 kyr) results indicate the extinction group declined in the Tasman Sea, irrespective of size fraction, throughout the study interval with an initial overall reduction in abundance at ∼0.95 Ma, and a major decline towards very low abundance at ∼0.83 Ma (Fig. 1g). Our data are consistent with other studies that conclude that the architecture of the extinction is captured in all size fractions7, and suggest that it was not associated with an early shortening of the life cycle, which might be apparent with an increased proportion of small specimens. Sites below ∼1 km water depth typically have the highest extinction group diversity7, and species richness at Site 593 is relatively low at ∼10–12 species per ∼10-cc sample (Fig. 1h). Site 593 is dominated by Strictocostella scharbergana and Siphonodosaria lepidula, which decline abruptly at 0.85 and 0.8 Ma, respectively (Fig. 1i,j). Different species are dominant in extinction assemblages in the Pacific, Atlantic and Mediterranean, although they are morphologically (and thus possibly ecologically) related and also became extinct during the MPT7.

Bottom-water temperature and corrosiveness

Decreased intermediate/deep-water temperature is a hypothesized cause of the extinction6, possibly due to increased oxygenation and its impact on an inferred microbial food source6,10,14. Bottom-water temperature at intermediate-depth Site 593, reconstructed from Mg/Ca of infaunal Uvigerina peregrina (see Methods), ranges from ∼3 to 8 °C (modern temperature is 4.5 °C), with warmer interglacials (Fig. 1e). Seawater absolute magnesium (17 Ma residence time) and calcium (1 Ma residence time) concentrations would have been slightly different during the Mid Pleistocene20, thus having an impact on the accuracy of the temperature estimates based on modern calibration (possibly by up to ∼1 °C), although the overall trends will be unchanged. There is no apparent correlation between bottom-water temperature and faunal abundances during the pre-extinction period before ∼0.83 Ma (Fig. 2a), nor any secular change over the extinction itself, and we conclude that the benthic extinction at Site 593 was not caused by temperature changes. Increased bottom-water corrosiveness is another physical property that has been proposed to have an impact on benthic foraminifera21,22. The living position of the extinction group is unknown, but has been inferred as infaunal7,9,11. If this were the case, pore water [CO 3 2−] might be more relevant regarding the extinction, although pore waters have lower [CO 3 2−] and changes in bottom-water [CO 3 2−] would have influenced pore water values (in addition to other factors such as organic carbon flux and sedimentation rate). Bottom-water Δ[CO 3 2−] at Site 593, reconstructed from B/Ca of epifaunal Cibicidoides wuellerstorfi (see Methods), shows relatively low values ranging from 10 to 25 μmol kg−1, with highest values recorded during cooler glacials and some potential negative outliers before 0.9 Ma (Fig. 1f). Similar to Mg/Ca, the absolute B/Ca of seawater would have been slightly different from modern values, thus potentially having an impact on the absolute values of our calculated Δ[CO 3 2−] even though the overall trends should be considered accurate23. Since all the values are oversaturated with respect to in situ [CO 3 2−] (that is, all have positive Δ[CO 3 2−] values), and the extinction group abundance does not co-vary with Δ[CO 3 2−] during the pre-extinction interval (Fig. 2b), we conclude that the extinction group was tolerant to values in this range and could not have become globally extinct because of increased bottom-water corrosiveness.

Figure 2: Foraminiferal extinction group against other parameters for the pre-extinction interval ∼ 0.8–1 Ma. (a) Bottom-water temperature derived from foraminiferal Mg/Ca, (b) bottom-water Δ[CO 3 2−] derived from foraminiferal B/Ca, (c) chlorin P410 from bulk sediment and (d) % small Gephyrocapsa. Full size image

Carbon flux

Benthic foraminifera are influenced by several ecological factors, which include bottom-water oxygenation, bottom-water sediment heterogeneity and hydrodynamics, temperature, corrosiveness and organic carbon type and flux21,22. However, above the lysocline (below which calcite dissolution occurs), typical open-ocean benthic ecology is primarily affected by the organic carbon flux—which is related to primary productivity (quantity, type and duration) and remineralization of particulate organic carbon as it is transported to depth10. A change in organic carbon export, linked to primary productivity, has been hypothesized as an alternative cause of the extinction7,9,10. SST at Site 593 (Fig. 1b), reconstructed using the alkenone proxy UK 37 ′ (see Methods), shows significant variability over the study interval, ranging from 10 to 18 °C, with cooler temperatures during glacials after ∼0.95 Ma. Since modern SSTs in the Tasman Sea are tightly coupled to the position of the productive Subtropical Front, we anticipate that shifts to Subtropical Front position might have influenced the organic matter flux. Sedimentary chlorin (Fig. 1d) is derived from photosynthetic material and specifically from chlorophyll pigments24. At this distal oceanic location they are likely to have originated from a proximal phytoplankton source, although a terrestrial contribution cannot be discounted by this study. Chlorin concentrations are typically higher during colder glacials at 0.75, 0.82 and 0.93 Ma, possibly indicating enhanced productivity24 at times of Subtropical Front northward migration (cooler SSTs). However, despite significant variations, there is no prior correlation (Fig. 2c) nor secular change in chlorin concentration (and by extension phytoplankton carbon flux), which could account for the extinction in benthic foraminifera focused at ∼0.83 Ma (Fig. 1).

Phytoplankton food source

The extinction group therefore appears to have been relatively tolerant to variations in physical water properties and potentially overall organic carbon flux changes at Site 593 before the ∼0.83 Ma decline. Changing organic carbon source is another possible extinction mechanism7,9,10,11. The extinction group probably lived infaunally, according to their elongated morphology and lower shell δ13C than epifaunal foraminifera7,9,11, and preferred relatively high organic carbon flux at upper-abyssal to mid-bathyal depths; their global abundance reflects this distribution7. The specialized architectural function of extinction group apertures has been discussed at length11 but remains unknown, and may have helped direct pseudopodial flow for detritus feeding10,11, perhaps leaving them sensitive to a change in organic carbon supply.

Considering the strong benthic–pelagic coupling of benthic foraminifera10, we compiled published high-resolution calcareous nannoplankton assemblage records to assess the potential for a global changing source of organic carbon causing the extinction. Coccolithophores are one of the major mid-low latitude phytoplankton groups contributing to the organic carbon pump, known to undergo rapid evolution in the Pleistocene25. From published records, we identified that a significant peak in the morphological genus ‘small Gephyrocapsa’ (<3 μm) occurred in the SE Atlantic26, NW Pacific27 and SW Pacific11 centred at ∼0.8 Ma (Fig. 3b). This peak in abundance is consistent with records from the Indian Ocean25, and other nannoplankton records that do not differentiate this particular species from other small placoliths in the North Atlantic, South Atlantic and Mediterranean Sea (Supplementary Fig. 2). Although most of these sites do not have benthic foraminiferal data with which to directly compare the nannoplankton assemblages, Site MD97–2114 in the SW Pacific indicates that the benthic extinction coincided with this peak11, and other sites7 indicate that at a global scale the extinction had largely taken place by 0.8 Ma (Fig. 3c). To test the hypothesis that dominant small Gephyrocapsa could have been implicated in the benthic extinction, we paired records of nannoplankton and foraminiferal assemblage data in the Tasman Sea (Fig. 1c) and the North Atlantic (Supplementary Fig. 3). Both records show a consistently high % small Gephyrocapsa (>90%) during the extinction interval at ∼0.83 Ma. Interestingly, the first step in the extinction at ∼0.96 Ma at Site 593 (Fig. 1g) coincides with an initial increase in the % small Gephyrocapsa from ∼50 to 65% (Fig. 1c), showing the possibility that % small Gephyrocapsa was already exerting some control over extinction group abundance. From our research, the abundance of small Gephyrocapsa is the only oceanic parameter that shows a correlation with the extinction group leading up to the extinction in the Tasman Sea (Fig. 2d). To address the possible significance of this correlation, we explore the various possible environmental changes controlling the two groups and describe a new conceptual model that can account for both data sets.