Climate sensitivity across marine domains of life: limits to evolutionary adaptation shape species interactions, supplementary material

Organisms in all domains, Archaea, Bacteria, and Eukarya will respond to climate change with differential vulnerabilities resulting in shifts in species distribution, coexistence, and interactions. The identification of unifying principles of organism functioning across all domains would facilitate a cause and effect understanding of such changes and their implications for ecosystem shifts. For example, the functional specialization of all organisms in limited temperature ranges leads us to ask for unifying functional reasons. Organisms also specialize in either anoxic or various oxygen ranges, with animals and plants depending on high oxygen levels. Here, we identify thermal ranges, heat limits of growth, and critically low (hypoxic) oxygen concentrations as proxies of tolerance in a meta-analysis of data available for marine organisms, with special reference to domain-specific limits. For an explanation of the patterns and differences observed, we define and quantify a proxy for organismic complexity across species from all domains. Rising complexity causes heat (and hypoxia) tolerances to decrease from Archaea to Bacteria to uni- and then multicellular Eukarya. Within and across domains, taxon-specific tolerance limits likely reflect ultimate evolutionary limits of its species to acclimatization and adaptation. We hypothesize that rising taxon-specific complexities in structure and function constrain organisms to narrower environmental ranges. Low complexity as in Archaea and some Bacteria provide life options in extreme environments. In the warmest oceans, temperature maxima reach and will surpass the permanent limits to the existence of multicellular animals, plants and unicellular phytoplankter. Smaller, less complex unicellular Eukarya, Bacteria, and Archaea will thus benefit and predominate even more in a future, warmer, and hypoxic ocean.

Polar membrane lipids and elemental composition of Thermococcus kodakarensis cells according to growth stage and phosphorus supply

We observed significant changes in the elemental and intact polar lipid (IPL) composition of the archaeon Thermococcus kodakarensis (KOD1) in response to growth stage and phosphorus supply. Reducing the amount of organic supplements and phosphate in growth media resulted in significant decreases in cell size and cellular quotas of carbon (C), nitrogen (N), and phosphorus (P), which coincided with significant increases in cellular IPL quota and IPLs comprising multiple P atoms and hexose moieties. Relatively more cellular P was stored as IPLs in P-limited cells (2-8%) compared to control cells (<0.8%). We also identified a specific IPL biomarker containing a phosphatidyl-N-acetylhexoseamine headgroup that was relatively enriched during rapid cell division. These observations serve as empirical evidence of IPL adaptations in Archaea that will help to interpret the distribution of these biomarkers in natural systems. The reported cell quotas of C, N, and P represent the first such data for a specific archaeon and suggest that thermophiles are C-rich compared to the cell carbon-to-volume relationship reported for planktonic bacteria.

Lake Baikal amphipods under climate change: Thermal constraints and ecological consequences, links to supplementary material

Lake Baikal, the world's most voluminous freshwater lake, has experienced unprecedented warming during the last decades. A uniquely diverse amphipod fauna inhabits the littoral zone and can serve as a model system to identify the role of thermal tolerance under climate change. This study aimed to identify sublethal thermal constraints in two of the most abundant endemic Baikal amphipods, Eulimnogammarus verrucosus and Eulimnogammarus cyaneus, and Gammarus lacustris, a ubiquitous gammarid of the Holarctic. As the latter is only found in some shallow isolated bays of the lake, we further addressed the question whether rising temperatures could promote the widespread invasion of this non-endemic species into the littoral zone. Animals were exposed to gradual temperature increases (4 week, 0.8 °C/d; 24 h, 1 °C/h) starting from the reported annual mean temperature of the Baikal littoral (6 °C). Within the framework of oxygen- and capacity-limited thermal tolerance (OCLTT), we used a nonlinear regression approach to determine the points at which the changing temperature-dependence of relevant physiological processes indicates the onset of limitation. Limitations in ventilation representing the first limits of thermal tolerance (pejus (= "getting worse") temperatures (Tp)) were recorded at 10.6 (95% confidence interval; 9.5, 11.7), 19.1 (17.9, 20.2), and 21.1 (19.8, 22.4) °C in E. verrucosus, E. cyaneus, and G. lacustris, respectively. Field observations revealed that E. verrucosus retreated from the upper littoral to deeper and cooler waters once its Tp was surpassed, identifying Tp as the ecological thermal boundary. Constraints in oxygen consumption at higher than critical temperatures (Tc) led to an exponential increase in mortality in all species. Exposure to short-term warming resulted in higher threshold values, consistent with a time dependence of thermal tolerance. In conclusion, species-specific limits to oxygen supply capacity are likely key in the onset of constraining (beyond pejus) and then life-threatening (beyond critical) conditions. Ecological consequences of these limits are mediated through behavioral plasticity in E. verrucosus. However, similar upper thermal limits in E. cyaneus (endemic, Baikal) and G. lacustris (ubiquitous, Holarctic) indicate that the potential invader G. lacustris would not necessarily benefit from rising temperatures. Secondary effects of increasing temperatures remain to be investigated.

Seawater carbonate chemistry, cell numbers and growth rate during experiments with dinoflagellates, 2007

The effects of dissolved inorganic carbon (DIC) on the growth of 3 red-tide dinoflagellates (Ceratium lineatum, Heterocapsa triquetra and Prorocentrum minimum) were studied at pH 8.0 and at higher pH levels, depending upon the pH tolerance of the individual species. The higher pH levels chosen for experiments were 8.55 for C. lineatum and 9.2 for the other 2 species. At pH 8.0, which approximates the pH found in the open sea, the maximum growth in all species was maintained until the total DIC concentration was reduced below ~0.4 and 0.2 mM for C. lineatum and the other 2 species, respectively. Growth compensation points (concentration of inorganic carbon needed for maintenance of cells) were reached at ~0.18 and 0.05 mM DIC for C. lineatum and the other 2 species, respectively. At higher pH levels, maximum growth rates were lower compared to growth at pH 8, even at very high DIC concentrations, indicating a direct pH effect on growth. Moreover, the concentration of bio-available inorganic carbon (CO2 + HCO3-) required for maintenance as well as the half-saturation constants were increased considerably at high pH compared to pH 8.0. Experiments with pH-drift were carried out at initial concentrations of 2.4 and 1.2 mM DIC to test whether pH or DIC was the main limiting factor at a natural range of DIC. Independent of the initial DIC concentrations, growth rates were similar in both incubations until pH had increased considerably. The results of this study demonstrated that growth of the 3 species was mainly limited by pH, while inorganic carbon limitation played a minor role only at very high pH levels and low initial DIC concentrations.

Seawater carbonate chemistry, growth rate and light sensitivity of marine diatom Chaetoceros muelleri (strain CSIRO CS-176) during experiments, 2011

This study investigated the impact of photon flux and elevated CO2 concentrations on growth and photosynthetic electron transport on the marine diatom Chaetoceros muelleri and looked for evidence for the presence of a CO2-concentrating mechanism (CCM). pH drift experiments clearly showed that C. muelleri has the capacity to use bicarbonate to acquire inorganic carbon through one or multiple CCMs. The final pH achieved in unbuffered cultures was not changed by light intensity, even under very low photon flux, implying a low energy demand of bicarbonate use via a CCM. In short-term pH drift experiments, only treatment with the carbonic anhydrase inhibitor ethoxyzolamide (EZ) slowed down the rise in pH considerably. EZ was also the only inhibitor that altered the final pH attained, although marginally. In growth experiments, CO2 availability was manipulated by changing the pH in closed flasks at a fixed dissolved inorganic carbon (DIC) concentration. Low-light-treated samples showed lower growth rates in elevated CO2conditions. No CO2 effect was recorded under high light exposure. The maximal photosynthetic capacity, however, increased with CO2 concentration in saturating, but not in subsaturating, light intensities. Growth and photosynthetic capacity therefore responded in opposite ways to increasing CO2 availability. The capacity to photoacclimate to high and low photon flux appeared not to be affected by CO2treatments. However, photoacclimation was restricted to growth photon fluxes between 30 and 300 µmol photons m-2 s-1. The light saturation points for photosynthetic electron transport and for growth coincided at 100 µmol photons m-2 s-1. Below 100 µmol photons m-2 s-1 the light saturation point for photosynthesis was higher than the growth photon flux (i.e. photosynthesis was not light saturated under growth conditions), whereas at higher growth photon flux, photosynthesis was saturated below growth light levels.

Alkenones and SST of surface sediments (Appendix)

We have analysed alkenones in 149 surface sediments from the eastern South Atlantic in order to establish a sediment-based calibration of the U37K' paleotemperature index. Our study covers the major tropical to subpolar production systems and sea-surface temperatures (SST's) between 0° and 27°C. In order to define the most suitable calibration for this region, the U37K' values were correlated to seasonal, annual, and production-weighted annual mean atlas temperatures and compared to previously published culture and core-top calibrations. The best linear correlation between U37K' and SST was obtained using annual mean SST from 0 to 10 m water depth (U37K' = 0.033 T + 0.069, r**2 = 0.981). Data scattering increased significantly using temperatures of waters deeper than 20 m, suggesting that U37K' reflects mixed-layer SST and that alkenone production at thermocline depths was not high enough to significantly bias the mixed-layer signal. Regressions based on both production-weighted and on actual annual mean atlas SST were virtually identical, indicating that regional variations in the seasonality of primary production have no discernible effect on the U37K' vs. SST relationship. Comparison with published core-top calibrations from other oceanic regions revealed a high degree of accordance. We, therefore, established a global core-top calibration using U37K' data from 370 sites between 60°S and 60°N in the Atlantic, Indian, and Pacific Oceans and annual mean atlas SST (0-29°C) from 0 m water depth. The resulting relationship (U37K' = 0.033 T + 0.044, r**2 = 958) is identical within error limits to the widely used E. huxleyi calibrations of and attesting their general applicability. The observation that core-top calibrations extending over various biogeographical coccolithophorid zones are strongly linear and in better accordance than culture calibrations suggests that U37K' is less species-dependent than is indicated by culture experiments. The results also suggest that variations in growth rate of algae and nutrient availability do not significantly affect the sedimentary record of U37K' in open ocean environments.

Seawater carbonate chemistry and growth rate during experiments with dinoflagellates, 2007

The effects of dissolved inorganic carbon (DIC) on the growth of 3 red-tide dinoflagellates (Ceratium lineatum, Heterocapsa triquetra and Prorocentrum minimum) were studied at pH 8.0 and at higher pH levels, depending upon the pH tolerance of the individual species. The higher pH levels chosen for experiments were 8.55 for C. lineatum and 9.2 for the other 2 species. At pH 8.0, which approximates the pH found in the open sea, the maximum growth in all species was maintained until the total DIC concentration was reduced below ~0.4 and 0.2 mM for C. lineatum and the other 2 species, respectively. Growth compensation points (concentration of inorganic carbon needed for maintenance of cells) were reached at ~0.18 and 0.05 mM DIC for C. lineatum and the other 2 species, respectively. At higher pH levels, maximum growth rates were lower compared to growth at pH 8, even at very high DIC concentrations, indicating a direct pH effect on growth. Moreover, the concentration of bio-available inorganic carbon (CO2 + HCO3-) required for maintenance as well as the half-saturation constants were increased considerably at high pH compared to pH 8.0. Experiments with pH-drift were carried out at initial concentrations of 2.4 and 1.2 mM DIC to test whether pH or DIC was the main limiting factor at a natural range of DIC. Independent of the initial DIC concentrations, growth rates were similar in both incubations until pH had increased considerably. The results of this study demonstrated that growth of the 3 species was mainly limited by pH, while inorganic carbon limitation played a minor role only at very high pH levels and low initial DIC concentrations.

Water temperature measured in Independence Bay, Pisco, Peru

Independencia Bay can be considered as one of the most productive invertebratc fishing grounds worldwide. One of the most important exploited species is the scallop (Argopecten purpuratus) with strong catching fluctuations related to El Nino and La Nina events and to inadequate Management strategies. During strong warming periods annual landings reach up to 50000 t in an area of about 150 km**2 and during cold years they remain around 500 to 1000 t. This study analyses the changes in scallop landings at Independencia Bay observed during the last two decades and discusses the main factors affecting the scallop proliferations during the EI Nino events. In this way data on landings, sea surface temperature and those related to growth, reproduction, predation, mean density and oxygen concentration from published and unpublished Papers are used. The relationship between annual catches and average water temperature over the preceding reproductive period of the scallop over the past 20 year's period, showed that scallop production is affected positively only with strong EI Nino such as those of 1983 and 1998. Our review showed that the scallop stock proliferation can be traced to the combined effect of (1) an increase in reproductive output through an acceleration of gonad maturation and a higher spawning frequency; (2) a shortening of the larval period and an increase in larval survival; (3) an increase in the individual growth performance; (4) an increase in the juvenile and adult survival through reduction of predator biomass; (5) an increase in carrying capacity of the scallop banks due to elevated oxygen levels.

Biostratigraphy of sediment core CRP-3 from the Ross Sea, Antarctica

Early Oligocene siliceous microfossils were recovered in the upper c. 193 m of the CRP-3 drillcore. Although abundance and preservation are highly variable through this section, approximately 130 siliceous microfossil taxa were identified, including diatoms, silicoflagellates, ebridians, chrysophycean cysts, and endoskeletal dinoflagellates. Well-preserved and abundant assemblages characterize samples in the upper c. 70 m and indicate deposition in a coastal setting with water depths between 50 and 200 m. Abundance fluctuations over narrow intervals in the upper c. 70 mbsf are interpreted to reflect environmental changes that were either conducive or deleterious to growth and preservation of siliceous microfossils. Only poorly-preserved (dissolved, replaced, and/or fragmented) siliceous microfossils are present from c. 70 to 193 mbsf. Diatom biostratigraphy indicates that the CRP-3 section down to c. 193 mbsf is early Oligocene in age. The lack of significant changes in composition of the siliceous microfossil assemblage suggests that no major hiatuses are present in this interval. The first occurrence (FO) of Cavitatus jouseanus at 48.44 mbsf marks the base of the Cavitatus jouseanus Zone. This datum is inferred to be near the base of Subchron C12n at c. 30.9 Ma. The FO of Rhizosolenia antarctica at 68.60 mbsf marks the base of the Rhizosolenia antarctica Zone. The FO of this taxon is correlated in deep-sea sections to Chron C13 (33.1 to 33.6 Ma). However, the lower range of R. antarctica is interpreted as incomplete in the CRP-3 drillcore, as it is truncated at an underlying interval of poor preservation: therefore, an age of c. 33.1 to 30.9 Ma is inferred for interval between c. 70 and 50 mbsf. The absence of Hemiaulus caracteristicus from diatom-bearing interval of CRP-3 further indicates an age younger than c. 33 Ma (Subchron C13n) for strata above c. 193 mbsf. Siliceous microfossil assemblages in CRP-3 are significantly different from the late Eocene assemblages reported CIROS-1 drillcore. The absence of H. caracteristicus, Stephanopyxis splendidus, and Pterotheca danica, and the ebridians Ebriopsis crenulata, Parebriopsis fallax, and Pseudoammodochium dictyoides in CRP-3 indicates that the upper 200 m of the CRP-3 drillcore is equivalent to part of the stratigraphic interval missing within the unconformity at c. 366 mbsf in CIROS-1.

(Table 2) Distribution of alkenone unsaturation index UK37 of the eastern North Atlantic

This paper reports the concentrations and within-class distributions of long-chain alkenones and alkyl alkenoates in the surface waters (0-50 m) of the eastern North Atlantic, and correlates their abundance and distribution with those of source organisms and with water temperature and other environmental variables. We collected these samples of >0.8 µm particulate material from the euphotic zone along the JGOFS 20°W longitude transect, from 61°N to 24°N, during seven cruises of the UK-JGOFS Biogeochemical Ocean Flux Study (BOFS) in 1989-1991; the biogeographical range of our 53 samples extends from the cold (<10°C), nutrient-rich and highly productive subarctic waters of the Iceland Basin to the warm (>25°C) oligotrophic subtropical waters off Africa. Surface water concentrations of total alkenone and alkenoates ranged from <50 ng/l in oligotrophic waters below 40°N to 2000-4500 ng/l in high latitude E. huxleyi blooms, and were well correlated with E. huxleyi cell densities, supporting the assumption that E. huxleyi is the predominant source of these compounds in the present day North Atlantic. The within-class distribution of the C37 and C38 alkenones and C36 alkenoates varied strongly as a function of temperature, and was largely unaffected by nutrient concentration, bloom status and other surface water properties. The biosynthetic response of the source organisms to growth temperature differed between the cold (<16°C) waters above 47°N and the warmer waters to the south. In cold (<16°C) waters above 47°N, the relative amounts of alkenoates and C38 alkenones synthesized was a strong function of growth temperature, while the unsaturation ratio of the alkenones (C37 and C38) was uncorrelated with temperature. Conversely, in warm (>16°C) waters below 47°N, the relative proportions of alkenoates and alkenones synthesized remained constant with increasing temperature while the unsaturation ratios of the C37 and C38 methyl alkenones (Uk37 and Uk38Me, respectively) increased linearly. The fitted regressions of Uk37 and Uk38Me versus temperature for waters >16°C were both highly significant (r**2 > 0.96) and had identical slopes (0.057) that were 50% higher than the slope (0.034) of the temperature calibration of Uk37 reported by Prahl and Wakeham (1987; doi:10.1038/330367a0) over the same temperature range. These observations suggest either a physiological adjustment in biochemical response to growth temperature above a 16-17°C threshold and/or variation between different E. huxleyi strains and/or related species inhabiting the cold and warm water regions of the eastern North Atlantic. Using our North Atlantic data set, we have produced multivariate temperature calibrations incorporating all major features of the alkenone and alkenoate data set. Predicted temperatures using multivariate calibrations are largely unbiased, with a standard error of approximately ±1°C over the entire data range. In contrast, simpler calibration models cannot adequately incorporate regional diversity and nonlinear trends with temperature. Our results indicate that calibrations based upon single variables, such as Uk37, can be strongly biased by unknown systematic errors arising from natural variability in the biosynthetic response of the source organisms to growth temperature. Multivariate temperature calibration can be expected to give more precise estimates of Integrated Production Temperatures (IPT) in the sedimentary record over a wider range of paleoenvironmental conditions, when derived using a calibration data set incorporating a similar range of natural variability in biosynthetic response.

Body mass, flipper length, oxidative balance indices and telomere length of king penguin chicks (A. patagonicus) on Possession Island

One of the reasons for animals not to grow as fast as they potentially could is that fast growth has been shown to be associated with reduced lifespan. However, we are still lacking a clear description of the reality of growth-dependent modulation of ageing mechanisms in wild animals. Using the particular growth trajectory of small king penguin chicks naturally exhibiting higher-than-normal growth rate to compensate for the winter break, we tested whether oxidative stress and telomere shortening are related to growth trajectories. Plasma antioxidant defences, oxidative damage levels and telomere length were measured at the beginning and at the end of the post-winter growth period in three groups of chicks (small chicks, which either passed away or survived the growth period, and large chicks). Small chicks that died early during the growth period had the highest level of oxidative damage and the shortest telomere lengths prior to death. Here, we show that small chicks that grew faster did it at the detriment of body maintenance mechanisms as shown by (i) higher oxidative damage and (ii) accelerated telomere loss. Our study provides the first evidence for a mechanistic link between growth and ageing rates under natural conditions.

Sea surface temperature reconstruction of ODP Site 175-1087

Successful application of the alkenone palaeothermometer, the UK'37 index, relies upon the assumption that fossil alkenone synthesisers responded to growth-temperature changes in a similar manner to the modern producers, chiefly the coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica. We compare coccolith and UK'37 data from ODP Site 1087 in the south-east Atlantic between 1500 and 500 ka, and show that evolutionary events and changes in species dominance within the coccolithophore populations had little impact on the UK'37 record. The relative abundances of the C37 and C38 alkenones also closely resembled those found in modern populations, and suggest a similar temperature sensitivity of UK'37 during the early and mid-Pleistocene to that found at present. These results support the application of the UK'37 index to reconstruct sea-surface temperatures (SSTs) throughout the Quaternary. The UK'37 record at ODP Site 1087 contains an SST signal that documents the emergence of the 100-kyr cycles that characterise the late Quaternary ice volume records. This is preceded by significant cooling at ODP Site 1087, marked by a negative shift in SSTs and a positive shift in the planktonic delta18O some 250-kyr earlier, at ca 1150-1000 ka. This results in a permanent fall in average SSTs of around 1.5 °C. The predicted increase in aridity onshore as a result of this cooling can be identified in a number of published records from southern Africa, and may have played a role in some important evolutionary events of the mid-Pleistocene.

Seawater carbonate chemistry and toxicity of Pseudo-nitzschia fraudulenta in a laboratory experiment

Anthropogenic CO2 is progressively acidifying the ocean, but the responses of harmful algal bloom species that produce toxins that can bioaccumulate remain virtually unknown. The neurotoxin domoic acid is produced by the globally-distributed diatom genus Pseudo-nitzschia. This toxin is responsible for amnesic shellfish poisoning, which can result in illness or death in humans and regularly causes mass mortalities of marine mammals and birds. Domoic acid production by Pseudo-nitzschia cells is known to be regulated by nutrient availability, but potential interactions with increasing seawater CO2 concentrations are poorly understood. Here we present experiments measuring domoic acid production by acclimatized cultures of Pseudo-nitzschia fraudulenta that demonstrate a strong synergism between projected future CO2 levels (765 ppm) and silicate-limited growth, which greatly increases cellular toxicity relative to growth under modern atmospheric (360 ppm) or pre-industrial (200 ppm) CO2 conditions. Cellular Si:C ratios decrease with increasing CO2, in a trend opposite to that seen for domoic acid production. The coastal California upwelling system where this species was isolated currently exhibits rapidly increasing levels of anthropogenic acidification, as well as widespread episodic silicate limitation of diatom growth. Our results suggest that the current ecosystem and human health impacts of toxic Pseudo-nitzschia blooms could be greatly exacerbated by future ocean acidification and 'carbon fertilization' of the coastal ocean.

Impact of elevated pCO2 on paralytic shellfish poisoning toxin content and composition in Alexandrium tamarense

Ocean acidification is considered a major threat to marine ecosystems and may particularly affect primary producers. Here we investigated the impact of elevated pCO2 on paralytic shellfish poisoning toxin (PST) content and composition in two strains of Alexandrium tamarense, Alex5 and Alex2. Experiments were carried out as dilute batch to keep carbonate chemistry unaltered over time. We observed only minor changes with respect to growth and elemental composition in response to elevated pCO2. For both strains, the cellular PST content, and in particular the associated cellular toxicity, was lower in the high CO2 treatments. In addition, Alex5 showed a shift in its PST composition from a nonsulfated analogue towards less toxic sulfated analogues with increasing pCO2. Transcriptomic analyses suggest that the ability of A. tamarense to maintain cellular homeostasis is predominantly regulated on the post-translational level rather than on the transcriptomic level. Furthermore, genes associated to secondary metabolite and amino acid metabolism in Alex5 were down-regulated in the high CO2 treatment, which may explain the lower PST content. Elevated pCO2 also induced up-regulation of a putative sulfotransferase sxtN homologue and a substantial down-regulation of several sulfatases. Such changes in sulfur metabolism may explain the shift in PST composition towards more sulfated analogues. All in all, our results indicate that elevated pCO2 will have minor consequences for growth and elemental composition, but may potentially reduce the cellular toxicity of A. tamarense.