High risk of extinction of benthic foraminifera in this century due to ocean acidification

Increased atmospheric CO₂ concentrations lead to decreased pH and carbonate availability in the ocean (Ocean Acidification, OA). Carbon dioxide seeps serve as ‘windows into the future’ to study the ability of marine invertebrates to acclimatise to OA. We studied benthic foraminifera in sediments from shallow volcanic CO₂ seeps in Papua New Guinea. Conditions follow a gradient from present day pH/pCO₂ to those expected past 2100. We show that foraminiferal densities and diversity declined steeply with increasing pCO_2. Foraminifera were almost absent at sites with pH < 7.9 (>700 μatm pCO₂). Symbiont-bearing species did not exhibit reduced vulnerability to extinction at <7.9 pH. Non-calcifying taxa declined less steeply along pCO₂ gradients, but were also absent in samples at pH < 7.9. Data suggest the possibility of an OA induced ecological extinction of shallow tropical benthic foraminifera by 2100; similar to extinctions observed in the geological past.

A core-top study of dissolution effect on B/Ca in Globigerinoides sacculifer from the tropical Atlantic: potential bias for paleo-reconstruction of seawater carbonate chemistry.

It has been recently shown that B/Ca in planktonic foraminiferal calcite can be used as a proxy for seawater pH. Based on the study of surface sediments (multi-cores) retrieved along a depth transect on the Sierra Leone Rise (Eastern Equatorial Atlantic), we document the decrease of B/Ca and Mg/Ca of Globigerinoides sacculifer shells with increasing water depth and dissolution. This effect of dissolution on B/Ca may potentially represent a severe bias for paleo-pH reconstructions using this species. Samples of G. sacculifer were analyzed independently at two laboratories for B/Ca and Mg/Ca. Both sets of results show a systematic decrease of B/Ca and Mg/Ca along the depth transect, with an overall loss of ∼14 µmol/mol (∼15%) for B/Ca and of ∼0.7 mmol/mol (∼21%) for Mg/Ca between the shallowest (2640 m) and the deepest (4950 m) sites. Because of this dissolution effect, surface water pH reconstructed from B/Ca of G. sacculifer decreases by ∼0.11 units between the shallowest site and the deepest site, a magnitude similar to the expected glacial/interglacial surface water pH changes.

The marine carbon system and ocean acidification during Phanerozoic time

The global CO₂-carbonic acid-carbonate system of seawater, although certainly a well-researched topic of interest in the past, has risen to the fore in recent years because of the environmental issue of ocean acidification (often simply termed OA). Despite much previous research, there remain pressing questions about how this most important chemical system of seawater operated at the various time scales of the deep time of the Phanerozoic Eon (the past 545 Ma of Earth’s history), interglacial-glacial time, and the Anthropocene (the time of strong human influence on the behaviour of the system) into the future of the planet. One difficulty in any analysis is that the behaviour of the marine carbon system is not only controlled by internal processes in the ocean, but it is intimately linked to the domains of the atmosphere, continental landscape, and marine carbonate sediments.

For the deep-time behaviour of the system, there exists a strong coupling between the states of various material reservoirs resulting in an homeostatic and self-regulating system. As a working hypothesis, the coupling produces two dominant chemostatic modes: (Mode I), a state of elevated atmospheric CO₂, warm climate, and depressed seawater Mg∕Ca and SO₄∕Ca mol ratios, pH (extended geologic periods of ocean acidification), and carbonate saturation states, and elevated Sr concentrations, with calcite and dolomite as dominant minerals found in marine carbonate sediments (Hothouses, the calcite-dolomite seas), and (Mode II), a state of depressed atmospheric CO₂, cool climate, and elevated seawater Mg∕Ca and SO₄/Ca ratios, pH, and carbonate saturation states, and low Sr concentrations, with aragonite and high magnesian calcites as dominant minerals found in marine carbonate sediments (Icehouses, the aragonite seas).

Investigation of the impacts of deglaciation and anthropogenic inputs on the CO₂–H₂O–CaCO₃ system in global coastal ocean waters from the Last Glacial Maximum (LGM: the last great continental glaciation of the Pleistocene Epoch, 18,000 year BP) to the year 2100 shows that with rising sea level, atmospheric CO₂, and temperature, the carbonate system of coastal ocean water changed and will continue to change significantly. We find that 6,000 Gt of C were emitted as CO₂ to the atmosphere from the growing coastal ocean from the Last Glacial Maximum to late preindustrial time because of net heterotrophy (state of gross respiration exceeding gross photosynthesis) and net calcification processes. Shallow-water carbonate accumulation alone from the Last Glacial Maximum to late preindustrial time could account for ~24 ppmv of the ~100 ppmv rise in atmospheric CO₂, lending some support to the ‘‘coral reef hypothesis’’. In addition, the global coastal ocean is now, or soon will be, a sink of atmospheric CO₂, rather than a source. The pHT (pH values on the total proton scale) of global coastal seawater has decreased from ~8.35 to ~8.18 and the CO₃^2- ion concentration declined by ~19% from the Last Glacial Maximum to late preindustrial time. In comparison, the decrease in coastal water pHT from the year 1900 to 2000 was ~8.18 to ~8.08 and is projected to decrease further from about ~8.08 to ~7.85 between 2000 and 2100. During these 200 years, the CO₃^2- ion concentration will fall by ~ 45%. This decadal rate of decline of the CO₃^2- ion concentration in the Anthropocene is 214 times the average rate of decline for the entire Holocene!

In terms of the modern problem of ocean acidification and its effects, the “other CO₂ problem”, we emphasise that most experimental work on a variety of calcifying organisms has shown that under increased atmospheric CO₂ levels (which attempt to mimic those of the future), and hence decreased seawater CO₃^2- ion concentration and carbonate saturation state, most calcifying organisms will not calcify as rapidly as they do under present-day CO₂ levels. In addition, we conclude that dissolution of the highly reactive carbonate phases, particularly the biogenic and cementing magnesian calcite phases, on reefs will not be sufficient to alter significantly future changes in seawater pH and lead to a buffering of the CO₂-carbonic acid system in waters bathing reefs and other carbonate ecosystems on timescales of decades to centuries. Because of decreased calcification rates and increased dissolution rates in a future higher CO₂, warmer world with seas of lower pH and carbonate saturation state, the rate of accretion of carbonate structures is likely to slow and dissolution may even exceed calcification. The potential of increasing nutrient and organic carbon inputs from land, occurrences of mass bleaching events, and increasing intensity (and perhaps frequency of hurricanes and cyclones as a result of sea surface warming) will only complicate matters more. This composite of stresses will have severe consequences for the ecosystem services that reefs perform, including acting as a fishery, a barrier to storm surges, a source of carbonate sediment to maintain beaches, and an environment of aesthetic appeal to tourist and local populations. It seems obvious that increasing rates of dissolution and bioerosion owing to ocean acidification will result in a progressively increasing calcium carbonate (CaCO₃) deficit in the CaCO₃ budget for many coral reef environments. The major questions that require answers are: will this deficit occur and when and to what extent will the destructive processes exceed the constructive processes?

Calcification response to climate change in the Pliocene?

As a result of anthropogenic pCO₂ increases future oceans are growing warmer and lower in pH and oxygen, conditions that are likely to impact planktic communities. Past intervals of elevated and changing pCO₂ and temperatures can offer a glimpse into the response of marine calcifying plankton to changes in surface oceans under conditions similar to those projected for the future. Here we present new records of planktic foraminiferal and coccolith calcification from Deep Sea Drilling Project Site 607 (mid North Atlantic) and Ocean Drilling Program Site 999 (Caribbean Sea) from the Pliocene, the last time that pCO₂ was similar to today, and extending through a global cooling event into the Intensification of Northern Hemisphere Glaciation (3.3 to 2.6 million years ago). Test weights of both surface-dwelling foraminifera Globigerina bulloides and thermocline-dwelling foraminifera Globorotalia puncticulata vary, with a potential link to regional temperature variation in the North Atlantic, whereas in the tropics Globigerinoides ruber test weight remains stable. In contrast, reticulofenestrid coccoliths show a narrowing size range and a decline in the largest lith diameters over this interval. Our results suggest no major changes in plankton calcification during the high pCO₂ Pliocene or during the transition into an icehouse world.

Impacts of global warming on Permo-Triassic terrestrial ecosystems

Geologists and palaeontologists have expressed mixed views about the effects of the end-Permian mass extinction on continental habitats and on terrestrial life. Current work suggests that the effects on land were substantial, with massive erosion following the stripping of vegetation, associated with long-term aridification and short-term bursts of warming and acid rain. Wildfires at the Permo-Triassic boundary contributed to the removal of forests and the prolonged absence of forests from the Earth’s surface for up to 10 Myr. These physical crises on land impinged on the oceans, suggesting tight interlocking of terrestrial and marine crises. Levels of extinction on land may well have been as high as in the sea, and this is certainly the case for tetrapods. The mass extinction seems to have been less profound for plants and insects, but it is hard at present to disentangle issues of data quality from reductions in abundance and diversity. Several killing agents have been proposed, and of these tetrapods may have succumbed primarily to acid rain, mass wasting, and aridification. Plants may have been more affected by the sudden effects of heating and wildfires, and the crisis for insects has yet to be explored.

Palaeontology: plankton in a greenhouse world

The Palaeocene–Eocene Thermal Maximum was marked by global warming and ocean acidification. Fossil and experimental analyses show that different species of marine calcifying algae responded very differently to the environmental upheavals.

Response of pteropod and related faunas to climate change and ocean acidification

Recent concern over the effects of ocean acidification upon calcifying organisms in the modern ocean has highlighted the aragonitic shelled thecosomatous pteropods as being at a high risk. Laboratory studies have shown that increased pCO2, leading to decreased pH and low carbonate concentrations, has a negative impact on the ability of pteropods to calcify and maintain their shells. This study presents the micropalaeontological analysis of marine cores from the Caribbean Sea, Mediterranean Sea and Indian Ocean. Pteropods, heteropods and planktic foraminifera were picked from samples to provide palaeoenvironmental data for each core. Determination of pteropod calcification was made using the Limacina Dissolution Index (LDX) and the average shell size of Limacina inflata specimens. Pteropod calcification indices were compared to global ice volume and Vostok atmospheric CO2 concentrations to determine any associations between climate and calcification. Results show that changes in surface ocean carbonate concentrations throughout the Late Pleistocene did affect the calcification of thecosomatous pteropods. These effects can be detected in shells from marine sediments that are located well above the aragonite lysocline and have not undergone post-depositional dissolution. The results of this study confirm the findings of laboratory studies, showing a decrease in calcification during interglacial periods, when surface ocean carbonate concentrations were lower. During glacial periods, calcification was enhanced due to the increased availability of carbonate. This trend was found in all sediments studied, indicating that the response of pteropods to past climate change is of global significance. These results demonstrate that pteropods have been negatively affected by oceanic pH levels relatively higher and changing at a lesser rate than those predicted for the 21st Century. Results also establish the use of pteropods and heteropods in reconstructing surface ocean conditions. The LDX is a fast and appropriate way of determining variations in surface water carbonate saturation. Abundances of key species were also found to constrain palaeotemperatures better than planktic foraminifera, a use which could be further developed.

Patterns of magnesium content in Arctic bryozoan skeletons along a depth gradient

A growing body of evidence suggests that ocean acidification acting synergistically with ocean warming alters carbonate biomineralization in a variety of marine biota. Magnesium often substitutes for Ca in the calcite skeletons of marine invertebrates, increasing their solubility. The spatio-environmental distribution of Mg in marine invertebrates has seldom been studied, despite its importance for assessing vulnerabilities to ocean acidification. Because pH decreases with water depth, it is predicted that levels of Mg in calcite skeletons should also decrease to counteract dissolution. Such a pattern has been suggested by evidence from echinoderms. Data on magnesium content and depth in Arctic bryozoans (52 species, 103 individuals, 150 samples) are here used to test this prediction, aided by comparison with six conceptual models explaining all possible scenarios. Analyses were based on a uniform dataset spanning more than 200 m of coastal water depth. No significant relationship was found between depth and Mg content; indeed, the highest Mg content among the analyzed taxa (8.7 % mol MgCO₃) was recorded from the deepest settings (>200 m). Our findings contrast with previously published results from echinoderms in which Mg was found to decrease with depth. The bryozoan results suggest that ocean acidification may have less impact on the studied bryozoans than is generally assumed. In the broad context, our study exemplifies quantitative testing of spatial patterns of skeletal geochemistry for predicting the biological effects of environmental change in the oceans.

Calibration of the boron isotope proxy in the planktonic foraminifera Globigerinoides ruber for use in palaeo-CO2 reconstruction

The boron isotope-pH proxy, applied to mixed-layer planktic foraminifera, has great potential for estimating past CO₂ levels, which in turn is crucial to advance our understanding of how this greenhouse gas influences Earth’s climate. Previous culture experiments have shown that, although the boron isotopic compositions of various planktic foraminifera are pH dependent, they do not agree with the aqueous geochemical basis of the proxy. Here we outline the results of culture experiments on Globigerinoides ruber (white) across a range of pH (∼7.5–8.2) and analysed via multicollector inductively-coupled plasma mass spectrometry (MC-ICPMS), and compare these data to core-top and sediment-trap samples to derive a robust new species-specific boron isotope-pH calibration. Consistent with earlier culture studies, we show a reduced pH dependency of the boron isotopic composition of symbiont-bearing planktonic foraminifera compared to borate ion in seawater. We also present evidence for a size fraction effect in the δ¹¹B of G. ruber. Finally, we reconstruct atmospheric CO₂ concentrations over the last deglacial using our new calibration at two equatorial sites, ODP Site 999A and Site GeoB1523-1. These data provide further grounding for the application of the boron isotope-pH proxy in reconstructions of past atmospheric CO₂ levels.

Taxonomic composition and environmental distribution of post-extinction rhynchonelliform brachiopod faunas: constraints on short-term survival and the role of anoxia in the end-Permian mass extinction

Marine taxonomic losses during the end-Permian mass extinction were driven by physiological stresses from ocean warming, acidification, and anoxia that ultimately resulted from CO₂ release from Siberian Traps flood volcanism. Despite abundant proxy evidence for anoxia, its role is not well resolved because the timing and selectivity of the extinction are better explained by warming and ocean acidification. We studied the taxonomic composition and spatial and temporal distribution of brachiopod-rich post-extinction faunas, which contain short-lived Permian survivors that lived at a key time during and immediately after the peak of the extinction, to elucidate the controls on survival and the role of anoxia. Holdover brachiopods primarily belong to extinct families and orders, not to long-term survivors, and their probability of short-term survival was a function of pre-extinction metapopulation size. Although short-term survival appears to have been stochastic, likely because of intraspecific variation in tolerance within larger metapopulations, opportunistic and possibly dysaerobic-tolerant genera thrived locally. Rhynchonelliform brachiopod distribution was patchy, both environmentally and temporally. They were more abundant in shallow-water settings, consistent with an oxygenated habitable zone, and their local demise often corresponded with the local development of low-oxygen conditions. Thus, although warming and acidification may have been the primary triggers of taxonomic loss, the addition of spatially and temporally variable anoxic conditions exacerbated physiological stress and contributed to ultimate extinction of short-lived survivors. The combination of the three stresses – warming, acidification, and anoxia – which act synergistically to negatively affect respiratory physiology of marine invertebrates, may explain the severity of the end-Permian extinction and provides a sobering analogue for modern ocean acidification and anoxic dead zones.