Sedimentological and benthic foraminiferal data pertaining to ODP Holes 208-1262A and 208-1263C

Eocene Thermal Maximum 2 (ETM2) occurred ~1.8 Myr after the Paleocene Eocene Thermal Maximum (PETM) and, like the PETM, was characterized by a negative carbon isotope excursion coupled with warming. We combined benthic foraminiferal and sedimentological records for Southeast Atlantic Sites 1263 (1500 m paleodepth) and 1262 (3600 m paleodepth) to show that benthic foraminiferal diversity and accumulation rates declined more precipitously and severely at the shallower site during peak ETM2. The sites are in close proximity, so differences in surface productivity cannot have caused this differential effect. Instead, on the basis of an analysis of climate modelling experiments, we infer that changes in ocean circulation pattern across ETM2 may have resulted in more pronounced warming at intermediate depths (Site 1263). The effects of more pronounced warming include increased metabolic rates, leading to a decrease in effective food supply and increased deoxygenation, thus potentially explaining the more severe benthic impacts at Site 1263. In response to more severe benthic disturbance, bioturbation may have decreased at Site 1263 as compared to Site 1262, hence differentially affecting the bulk carbonate record. We use a sediment-enabled Earth system model to test whether a reduction in bioturbation and/or the likely reduced carbonate saturation of more poorly ventilated waters can explain the more extreme excursion in bulk d13C and sharper transition in wt% CaCO3 at Site 1263. We find that both enhanced acidification and reduced bioturbation during peak ELMO conditions are needed to account for the observed features. Our combined ecological and modelling analysis illustrates the potential role of ocean circulation changes in amplifying local environmental changes and driving temporary, but drastic, loss of benthic biodiversity and abundance.

Tomographic measurements of O. umbonatus and N. truempyi during the PETM and ETM-2 at ODP Sites 208-1262 and 208-1263

Predicting the impact of ongoing anthropogenic CO2 emissions on calcifying marine organisms is complex, owing to the synergy between direct changes (acidification) and indirect changes through climate change (e.g., warming, changes in ocean circulation, and deoxygenation). Laboratory experiments, particularly on longer-lived organisms, tend to be too short to reveal the potential of organisms to acclimatize, adapt, or evolve and usually do not incorporate multiple stressors. We studied two examples of rapid carbon release in the geological record, Eocene Thermal Maximum 2 (~53.2 Ma) and the Paleocene Eocene Thermal Maximum (PETM, ~55.5 Ma), the best analogs over the last 65 Ma for future ocean acidification related to high atmospheric CO2 levels. We use benthic foraminifers, which suffered severe extinction during the PETM, as a model group. Using synchrotron radiation X-ray tomographic microscopy, we reconstruct the calcification response of survivor species and find, contrary to expectations, that calcification significantly increased during the PETM. In contrast, there was no significant response to the smaller Eocene Thermal Maximum 2, which was associated with a minor change in diversity only. These observations suggest that there is a response threshold for extinction and calcification response, while highlighting the utility of the geological record in helping constrain the sensitivity of biotic response to environmental change.

Haemolymph inorganic ion composition, physiology and behaviour dependent on temperature and magnesium in adult Paralomis granulosa (Decapoda, Anomura, Lithodidae)

A low capacity for regulation of extracellular Mg2+ has been proposed to exclude reptant marine decapod crustaceans from temperatures below 0°C and thus to exclude them from the high Antarctic. To test this hypothesis and to elaborate the underlying mechanisms in the most cold-tolerant reptant decapod family of the sub-Antarctic, the Lithodidae, thermal tolerance was determined in the crab Paralomis granulosa (Decapoda, Anomura, Lithodidae) using an acute stepwise temperature protocol (-1°, 1°, 4°, 7°, 10°, and 13°C). Arterial and venous oxygen partial pressures (Po2) in hemolymph, heartbeat and ventilation beat frequencies, and hemolymph cation composition were measured at rest and after a forced activity (righting) trial. Scopes for heartbeat and ventilation beat frequencies and intermittent heartbeat and scaphognathite beat rates at rest were evaluated. Hemolymph [Mg2+] was experimentally reduced from 30 mmol/L to a level naturally observed in Antarctic caridean shrimps (12 mmol/L) to investigate whether the animals remain more active and tolerant to cold (-1°, 1°, and 4°C). In natural seawater, righting speed was significantly slower at -1° and 13°C, compared with acclimation temperature (4°C). Arterial and venous hemolymph Po2 increased in response to cooling even though heartbeat and ventilation beat frequencies as well as scopes decreased. At rest, ionic composition of the hemolymph was not affected by temperature. Activity induced a significant increase in hemolymph [K+] at -1° and 1°C. Reduction of hemolymph [Mg2+] did not result in an increase in activity, an increase in heartbeat and ventilation beat frequencies, or a shift in thermal tolerance to lower temperatures. In conclusion, oxygen delivery in this cold-water crustacean was not acutely limiting cold tolerance, and animals may have been constrained more by their functional capacity and motility. In contrast to earlier findings in temperate and subpolar brachyuran crabs, these constraints remained insensitive to changing Mg2+ levels.

Impact of thermal stress on evolutionary trajectories of pathogen resistance in three-spined stickleback (Gasterosteus aculeatus), supplementary material

Background: Pathogens are a major regulatory force for host populations, especially under stressful conditions. Elevated temperatures may enhance the development of pathogens, increase the number of transmission stages, and can negatively influence host susceptibility depending on host thermal tolerance. As a net result, this can lead to a higher prevalence of epidemics during summer months. These conditions also apply to marine ecosystems, where possible ecological impacts and the population-specific potential for evolutionary responses to changing environments and increasing disease prevalence are, however, less known. Therefore, we investigated the influence of thermal stress on the evolutionary trajectories of disease resistance in three marine populations of three-spined sticklebacks Gasterosteus aculeatus by combining the effects of elevated temperature and infection with a bacterial strain of Vibrio sp. using a common garden experiment. Results: We found that thermal stress had an impact on fish weight and especially on survival after infection after only short periods of thermal acclimation. Environmental stress reduced genetic differentiation (QST) between populations by releasing cryptic within-population variation. While life history traits displayed positive genetic correlations across environments with relatively weak genotype by environment interactions (GxE), environmental stress led to negative genetic correlations across environments in pathogen resistance. This reversal of genetic effects governing resistance is probably attributable to changing environment-dependent virulence mechanisms of the pathogen interacting differently with host genotypes, i.e. GPathogenxGHostxE or (GPathogenxE)x(GHostxE) interactions, rather than to pure host genetic effects, i.e. GHostxE interactions. Conclusion: To cope with climatic changes and the associated increase in pathogen virulence, host species require wide thermal tolerances and pathogen-resistant genotypes. The higher resistance we found for some families at elevated temperatures showed that there is evolutionary potential for resistance to Vibrio sp. in both thermal environments. The negative genetic correlation of pathogen resistance between thermal environments, on the other hand, indicates that adaptation to current conditions can be a weak predictor for performance in changing environments. The observed feedback on selective gradients exerted on life history traits may exacerbate this effect, as it can also modify the response to selection for other vital components of fitness.

Calcareous nannofossil during the Paleocene Eocene Thermal Maximum in sediments of Walvish Ridge

Compositions and abundances of calcareous nannofossil taxa have been determined in a ca 170 kyrs long time interval across the Paleocene/Eocene boundary at 1-cm to 10-cm resolution from two ODP Sites (1262, 1263) drilled along the flank of the Walvis Ridge in the South Atlantic. The results are compared to published data from ODP Site 690 in the Weddell Sea. The assemblages underwent rapid evolution over a 74 kyrs period, indicating stressed, unstable and/or extreme photic zone environments during the PETM hyperthermal. This rapid evolution, which created 5 distinct stratigraphic horizons, is consistent with the restricted brief occurrences of malformed and/or weakly calcified morphotypes. The production of these aberrant morphotypes is possibly caused by major global scale changes in carbon cycling in the ocean-atmosphere system, affecting also photic zone environments. No marked paleoecologically induced changes are observed in abundances of the genera Discoaster, Fasciculithus and Sphenolithus at the Walvis Ridge sites. Surprisingly, there is no significant correlation in abundance between these three genera, presumed to have had a similar paleoecological preference for warm and oligotrophic conditions.

Thermal reaction norms of growth in Atlantic and Pacific silverside fishes

How organisms may adapt to rising global temperatures is uncertain, but concepts can emerge from studying adaptive physiological trait variations across existing spatial climate gradients. Many ectotherms, particularly fish, have evolved increasing genetic growth capacities with latitude (i.e. countergradient variation (CnGV) in growth), which are thought to be an adaptation primarily to strong gradients in seasonality. In contrast, evolutionary responses to gradients in mean temperature are often assumed to involve an alternative mode, 'thermal adaptation'. We measured thermal growth reaction norms in Pacific silverside populations (Atherinops affinis) occurring across a weak latitudinal temperature gradient with invariant seasonality along the North American Pacific coast. Instead of thermal adaptation, we found novel evidence for CnGV in growth, suggesting that CnGV is a ubiquitous mode of reaction-norm evolution in ectotherms even in response to weak spatial and, by inference, temporal climate gradients. A novel, large-scale comparison between ecologically equivalent Pacific versus Atlantic silversides (Menidia menidia) revealed how closely growth CnGV patterns reflect their respective climate gradients. While steep growth reaction norms and increasing growth plasticity with latitude in M. menidia mimicked the strong, highly seasonal Atlantic coastal gradient, shallow reaction norms and much smaller, latitude-independent growth plasticity in A. affinis resembled the weak Pacific latitudinal temperature gradient.

Seawater carbonate chemistry, thickness and carbonate elemental composition of the test of juvenile sea urchins in a laboratory experiment

Ocean surface CO2 levels are increasing in line with rising atmospheric CO2 and could exceed 900 µatm by year 2100, with extremes above 2000 µatm in some coastal habitats. The imminent increase in ocean pCO2 is predicted to have negative consequences for marine fishes, including reduced aerobic performance, but variability among species could be expected. Understanding interspecific responses to ocean acidification is important for predicting the consequences of ocean acidification on communities and ecosystems. In the present study, the effects of exposure to near-future seawater CO2 (860 µatm) on resting (M O2rest) and maximum (M O2max) oxygen consumption rates were determined for three tropical coral reef fish species interlinked through predator-prey relationships: juvenile Pomacentrus moluccensis and Pomacentrus amboinensis, and one of their predators: adult Pseudochromis fuscus. Contrary to predictions, one of the prey species, P. amboinensis, displayed a 28-39% increase in M O2max after both an acute and four-day exposure to near-future CO2 seawater, while maintaining M O2rest. By contrast, the same treatment had no significant effects on M O2rest or M O2max of the other two species. However, acute exposure of P. amboinensis to 1400 and 2400 µatm CO2 resulted in M O2max returning to control values. Overall, the findings suggest that: (1) the metabolic costs of living in a near-future CO2 seawater environment were insignificant for the species examined at rest; (2) the M O2max response of tropical reef species to near-future CO2 seawater can be dependent on the severity of external hypercapnia; and (3) near-future ocean pCO2 may not be detrimental to aerobic scope of all fish species and it may even augment aerobic scope of some species. The present results also highlight that close phylogenetic relatedness and living in the same environment, does not necessarily imply similar physiological responses to near-future CO2.

Effects of feeding and light intensity on the response of the coral Porites rus to ocean acidification

Recently, it has been suggested that there are conditions under which some coral species appear to be resistant to the effects of ocean acidification. To test if such resistance can be explained by environmental factors such as light and food availability, the present study investigated the effect of 3 feeding regimes crossed with 2 light levels on the response of the coral Porites rus to 2 levels of pCO2 at 28 °C. After 1, 2, and 3 weeks of incubation under experimental conditions, none of the factors-including pCO2-significantly affected area-normalized calcification and biomass-normalized calcification. Biomass also was unaffected during the first 2 weeks, but after 3 weeks, corals that were fed had more biomass per unit area than starved corals. These results suggest that P. rus is resistant to short-term exposure to high pCO2, regardless of food availability and light intensity. P. rus might therefore represent a model system for exploring the genetic basis of tolerance to OA.

Planktic foraminiferal populations and test flux in the eastern North Atlantic Ocean

Planktic foraminiferal assemblages vary in response to seasonal fluctuations of hydrographic properties, between water masses, and after periodical changes and episodic events (e.g. reproduction, storms). Distinct annual variability of the planktic foraminiferal flux is also known from sediment trap data. In this paper we discuss the short-term impacts on interannual flux rates based on data from opening-closing net hauls obtained between the ocean surface and 500 m water depth. Data were recorded during April, May, June, and August at around 47°N, 20°W (BIOTRANS) in 1988, 1989, 1990, 1992, 1993, and during May 1989 and 1992 at 57°N, 20-22°W. Species assemblages closely resemble each other when comparing the mixed layer fauna with the fauna of the upper 100 m and the upper 500 m of the water column. In addition, species assemblages >100 µm are almost indistinguishable from assemblages that are >125 µm in test size. The standing stock of planktic foraminifers at BIOTRANS can vary by more than one order of magnitude over different years; however, species assemblages may be similar when comparing corresponding seasons. Early summer assemblages (June) are distinctly different from late summer assemblages (August). Significant variations in the species composition during spring (April/May) are independent of the mixed layer depth. Spring assemblages are characterized by high numbers of Globigerinita glutinata. In particular, day-to-day variations of the number of specimens and in species composition may have the same order of magnitude as interannual variations. This appears to be independent of the reproduction cycle. Species assemblages at 47°N and 57°N are similar during spring, although surface water temperatures and salinities differ by up to 10°C and 0.7 (PSU). We suggest that the main factors controlling the planktic foraminiferal fauna are the trophic properties in the upper ocean productive layer. Planktic foraminiferal carbonate flux as calculated from assemblages reveals large seasonal variations, a quasi-annual periodicity in flux levels, and substantial differences in timing and magnitude of peak fluxes. At the BIOTRANS station, the average annual planktic foraminiferal CaCO3 fluxes at 100 and 500 m depth are estimated to be 22.4 and 10.0 g/m**2/yr, respectively.

Source data for Plos ONE publication Redefining thermal regimes to design reserves for coral reefs in the face of climate change

Reef managers cannot fight global warming through mitigation at local scale, but they can use information on thermal patterns to plan for reserve networks that maximize the probability of persistence of their reef system. Here we assess previous methods for the design of reserves for climate change and present a new approach to prioritize areas for conservation that leverages the most desirable properties of previous approaches. The new method moves the science of reserve design for climate change a step forwards by: (1) recognizing the role of seasonal acclimation in increasing the limits of environmental tolerance of corals and ameliorating the bleaching response; (2) including information from several bleaching events, which frequency is likely to increase in the future; (3) assessing relevant variability at country scales, where most management plans are carried out. We demonstrate the method in Honduras, where a reassessment of the marine spatial plan is in progress.

Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: Understanding the unique host + symbiont response

The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.

Seawater carbonate chemistry and biological processes during experiments with the spider crab Hyas araneus in Kongsfjorden, Svalbard, 2009

With global climate change, ocean warming and acidification occur concomitantly. In this study, we tested the hypothesis that increasing CO2 levels affect the acid-base balance and reduce the activity capacity of the Arctic spider crab Hyas araneus, especially at the limits of thermal tolerance. Crabs were acclimated to projected oceanic CO2 levels for 12 days (today: 380, towards the year 2100: 750 and 1,120 and beyond: 3,000 ?atm) and at two temperatures (1 and 4 °C). Effects of these treatments on the righting response (RR) were determined (1) at acclimation temperatures followed by (2) righting when exposed to an additional acute (15 min) heat stress at 12 °C. Prior to (resting) and after the consecutive stresses of combined righting activity and heat exposure, acid-base status and lactate contents were measured in the haemolymph. Under resting conditions, CO2 caused a decrease in haemolymph pH and an increase in oxygen partial pressure. Despite some buffering via an accumulation of bicarbonate, the extracellular acidosis remained uncompensated at 1 °C, a trend exacerbated when animals were acclimated to 4 °C. The additional combined exposure to activity and heat had only a slight effect on blood gas and acid-base status. Righting activity in all crabs incubated at 1 and 4 °C was unaffected by elevated CO2 levels or acute heat stress but was significantly reduced when both stressors acted synergistically. This impact was much stronger in the group acclimated at 1 °C where some individuals acclimated to high CO2 levels stopped responding. Lactate only accumulated in the haemolymph after combined righting and heat stress. In the group acclimated to 1 °C, lactate content was highest under normocapnia and lowest at the highest CO2 level in line with the finding that RR was largely reduced. In crabs acclimated to 4 °C, the RR was less affected by CO2 such that activity caused lactate to increase with rising CO2 levels. In line with the concept of oxygen and capacity limited thermal tolerance, all animals exposed to temperature extremes displayed a reduction in scope for performance, a trend exacerbated by increasing CO2 levels. Additionally, the differences seen between cold- and warm-acclimated H. araneus after heat stress indicate that a small shift to higher acclimation temperatures also alleviates the response to temperature extremes, indicating a shift in the thermal tolerance window which reduces susceptibility to additional CO2 exposure.

Impact of changing carbonate chemistry, temperature, and salinity on growth and test degradation of the benthic foraminifer Ammonia aomoriensis

The present study investigated the combined effects of ocean acidification, temperature, and salinity on growth and test degradation of Ammonia aomoriensis. This species is one of the dominant benthic foraminifera in near-coastal habitats of the southwestern Baltic Sea that can be particularly sensitive to changes in seawater carbonate chemistry. To assess potential responses to ocean acidification and climate change, we performed a fully crossed experiment involving three temperatures (8, 13, and 18°C), three salinities (15, 20, and 25) and four pCO2 levels (566, 1195, 2108, and 3843 µatm) for six weeks. Our results highlight a sensitive response of A. aomoriensis to undersaturated seawater with respect to calcite. The specimens continued to grow and increase their test diameter in treatments with pCO2 <1200 µatm, when Omega calc >1. Growth rates declined when pCO2 exceeded 1200 µatm (Omega calc <1). A significant reduction in test diameter and number of tests due to dissolution was observed below a critical Omega calc of 0.5. Elevated temperature (18°C) led to increased Omega calc, larger test diameter, and lower test degradation. Maximal growth was observed at 18°C. No significant relationship was observed between salinity and test growth. Lowered and undersaturated Omega calc, which results from increasing pCO2 in bottom waters, may cause a significant future decline of the population density of A. aomoriensis in its natural environment. At the same time, this effect might be partially compensated by temperature rise due to global warming.

Planktonic foraminiferal assemblages of the Paleocene-Eocene Thermal Maximum of ODP Hole 113-690B

High-resolution study of Antarctic planktonic foraminiferal assemblages (Ocean Drilling Program Site 690, Weddell Sea) shows that these microplankton underwent a stepwise series of changes during the Paleocene-Eocene thermal maximum (PETM). Initiation of this response coincides with the onset of the carbon isotope excursion (CIE) but precedes the benthic foraminiferal mass extinction. The "top-to-bottom" succession in the biotic response indicates that the surface ocean/atmosphere was affected before the deep sea. The earliest stage of the faunal response entailed a conspicuous turnover within the shallow-dwelling genus Acarinina and a succession of stratigraphic first appearances. The genus Morozovella, large (>180 µm) biserial planktonics, and A. wilcoxensis are all restricted to the lower CIE within this PETM section. Acarininid populations crashed as the ocean/climate system ameliorated during the CIE recovery, reflecting atypical surface water conditions. This transient decline in acarininids is paralleled by a marked increase in carbonate content of sediments. It is postulated that this interval of carbonate enrichment, and its unusual microfauna, reflects enhanced carbon storage within reservoirs of the global carbon cycle other than the marine carbonate system (sensu Broecker et al., 1993, doi:10.1029/93PA00423; Ravizza et al., 2001, doi:10.1029/2000PA000541).