RESPONSE OF CALCAREOUS NANNOPLANKTON MORPHOLOGY TO ENVIRONMENTAL PERTURBATIONS: THE LATEST CENOMANIAN OCEANIC ANOXIC EVENT 2 AND LAB SIMULATIONS

Anthropogenic emissions of carbon dioxide into the atmosphere has indirectly driven acidification and reduced carbonate saturation of the oceans. Among calcareous plankton, coccolithophore algae are the major producers of pelagic CaCO3 in the modern ocean: they are direct contributors of the ocean biogeochemical cycles and climate system and, therefore, coccolithophore sensitivity to changes in surface water conditions is of major concern. Coccolithophores build around the cell an exoskeleton of calcite (coccosphere) that consists of single platelets called coccoliths and nannoliths. This phytoplanktonic group are affected by changes in surface water temperature, fertility, salinity, light and consequently are important instrument to A) predict the future state of the ocean, particularly its carbonate chemistry B) to reconstruct changes in past surface-water conditions. This PhD thesis is aimed to combine the geological and biological approaches, quantifying tempo and mode of coccolithophore response to specific combinations of stressing environmental conditions through investigation of a geological case history and laboratory experiments trying to simulate conditions of the past. During the Aptian Oceanic Anoxic Event 1a (OAE 1a) an extreme global perturbation of the atmosphere-ocean system was documented, with evidence of geologically rapid warming associated to ocean fertility and acidification at global scale. Erba et al. (2010) demonstrated that calcareous nannoplankton was extremely sensitive to ocean acidification during OAE 1a, allowing separation of most-, intermediate-, and least-tolerant taxa. After a major calcification failure of heavily calcified forms, ephemeral coccolith dwarfism and malformation represent the most remarkable species-specific adjustments to survive surface water acidity. The case history I focused on, is the latest Cenomanian Oceanic Anoxic Event 2 (OAE 2, ~ 94 Ma) which represents a profound perturbation of the ocean-atmosphere system caused by natural CO2 emissions related to the emplacement of the Caribbean Plateau causing climate change, ocean fertilization and acidification. The study was performed on pelagic sediments from five localities: Eastbourne (Sussex, United Kingdom), Clot de Chevalier (France), Novara di Sicilia (Sicily, Italy) and two Western Interior sections (Pueblo, Colorado and Cuba, Kansas, USA). These five sections have been chosen based on availability of integrated stratigraphy. In fact, they all have a good time control, especially C isotopic stratigraphy and biostratigraphy, that offers the opportunity to correlate data from the different localities, discriminating between local, regional and global changes. Moreover, the selected sections represent short and long-distance locations with respect to the Caribbean Plateau paleo-position. Morphometric analyses were performed on selected calcareous nannofossil taxa namely Biscutum constans, Zeugrhabdotus erectus, Discorhabdus rotatorius and Watznaueria barnesiae. During OAE 2 calcareous nannoplankton responded to variations in surface-water fertility, temperature and CO2-induced acidification with a calcification decline in the form of a general size reduction of coccoliths. Calcareous nannoplankton, also, was affected by dwarfism in a species-specific way: in all the five analyzed sections B. constans shows the amplest size fluctuations through the event. D. rotatorius shows a well express reduction in size while Z. erectus displays the minor size decrease. W. barnesiae doesn’t show significant changes in mean coccolith size or in morphology (e.g. ellipticity). Coccolith size fluctuations across OAE 2 are similar and synchronous in all the analyzed sections located at great distance in different oceans and settings. The nannofossil preservation was carefully assessed in order to avoid diagenetically altered material Accurate screening under light polarizing microscope ascertained that individual coccoliths considered for morphometry were complete, with a continuous outline and without evidence of crimping due to etching or overgrowth. At the OAE 2 onset an increase in coccolith size leads to maximum dimension around the first δ13C isotopic peak (peak A). Subsequently, B. constans, Z. erectus and D. rotatorius show a progressive decrease in the mean size, reaching the maximum reduction (dwarfism) at δ13C isotopic peak B. Smaller specimens are still present till the end of the event and only after δ13C isotopic peak C, in the upper part of the analyzed sections, a partial recovery in size is observed. High-resolution integrated stratigraphy allows to say that coccolith size fluctuations match paleoceanographic changes: • the first decrease in coccolith size is coeval with a CO2 pulse at the beginning of OAE 2; • the increase in coccolith size at δ13C isotopic peak A is well correlated with a significant CO2 drawdown and a discrete cooling episode. • the major decrease in coccolith size at δ13C isotopic peak B correlates with a strong metal peak along with a new increase in sea surface temperature. B. constans appears to be the most sensitive species to OAE 2 perturbations: the decrease in its coccolith size recorded in all the analyzed sections, is associated to some malformation (increased ellipticity). Calcareous nannofossil morphometric and morphological data obtained for the latest OAE 2 were compared with those available for the early Aptian OAE 1a data in order to derive similarities and differences. Such a comparison suggests that species-specific coccolith dwarfism was experienced during both OAE 1a and OAE 2. Such calcification change is associated to: - high pCO2 (> 900 ppm); - high temperature (ca. 35°C); - trace metal enrichment. Temperature and nutrient availability in surface waters do not seem to have been crucial for B. constans size, although warmer and more fertile oceans preconditioned the environmental perturbation. Available data, instead, suggest that ocean chemistry related to the amount of CO2 concentrations, played a central role in coccolith secretion by B. constans with a repetitive reduction in size during OAE 1a and OAE 2. Massive submarine volcanism of Ontong Java Plateau during OAE 1a and the Caribbean Plateau during OAE 2 triggered a disruption in the oceanic carbonate system: excess CO2 arguably induced ocean acidification associated that was detrimental to some marine calcifiers, with temporary failure of a few taxa and production of dwarf and malformed coccoliths in B. constans. Hydrothermal plumes during construction of large submarine plateaus introduced biolimiting metals that fertilized the global ocean. However, submarine hydrothermalism might have also pumped in some toxic metals that might have disturbed the functioning of some intolerant coccolithophorid species, thus affecting their biocalcification. Species-specific coccolith dwarfism seems to be the response of nannoplankton to ocean acidification during OAE 1a and OAE 2, and this resulted in a reduction in total calcification under high pCO2. Evidence of dwarfism and production of malformed coccoliths possibly represents species-specific adjustment to survive lower pH. Therefore, there is possibly a causal link between intervals of major submarine volcanism and changes in nannoplankton composition, abundance and biocalcification through OAE 1a and OAE 2. The second part of this thesis focuses on laboratory experiments of coccolithophores performed at the GEOMAR Helmholtz Centre for Ocean Research Kiel (Kiel, Germany). Only preliminary results are here presented. The starting point was the idea that changes in some environmental factors directly affect the physiology of coccolithophorid algae, thereby directly causing a change in coccolith mean size and weight. Environmental factors known to modify coccolith size and/or weight are salinity (Green et al., 1998; Bollmann and Herrle, 2007; Fielding et al., 2009), temperature (Watabe and Wilbur, 1966), nutrient availability (Batvik et al., 1997; Paasche, 1998), growth stage (Young and Westbroek, 1991), seasonality (Triantaphyllou et al., 2010) and carbonate chemistry (Riebesell et al., 2000, Iglesias-Rodriguez et al., 2008; Halloran et al., 2008; Beaufort et al., 2011; Bach et a., 2012). In this thesis I consider the potential role of some of these environmental factors - specifically salinity, carbonate chemistry, light intensities, trace metal enrichment and nutrient depleted conditions) as triggers of changes in coccolith size and/or weight. Five species were investigated (Emiliania huxleyi, Gephyrocapsa oceanica, Pleurochrysis carterae, Coccolithus pelagicus ssp. braarudii) in five different experiments. Similarly to fossils data, a species-specific response to the different treatments has been observed. E. huxleyi evidences an increase in the coccosphere diameter associated to an increase in coccolith volume under nutrient-starved conditions and specifically with low phosphate content. On the other hand, major decrease in coccolith volume has been observed for E. huxleyi only with the highest CO2 concentration (3000 ppm). However, with increased trace metal contents, a reduction in coccolith volume has been detected, too. G. oceanica appears to be very sensitive to carbonate chemistry variations and future more specific analyses should be done to figure out which parameter(s) of the carbonate system drive morphological modifications (e.g. carbon dioxide, bicarbonate, carbonate ion, protons). P. carterae instead shows very erratic patterns to the tested parameters. Furthermore, among experiments, different replicates resulted in different response suggesting unclear sensitivity to specific environmental conditions. Finally, Coccolithus pelagicus ssp. braarudii calcification appears to be beneficial under low-nutrient conditions and, specifically, in the phosphate-limited treatment. On the contrary, increased CO2 concentration appears to impart a negative feedback to coccolith volume, with an evident decrease hand in hand with increasing CO2 content. As mentioned above, further analyses are planned in the near future and particularly SEM investigation of coccolith morphology and morphometry to quantify changes in coccolith size and malformation. The results of my thesis emphasize that changes in environmental factors do affect coccolithophore growth: salinity, carbonate chemistry, nutrient content and trace metal can significantly impact coccolith calcification in present and past oceans. The OAE 2 paleoenvironmental perturbation indicates that there is a causal link between intervals of abnormal submarine volcanism and changes in nannoplankton biocalcification through OAE 2. Comparison with data available for OAE 1a and OAE 1d indicate that analogous causes (construction of large igneous provinces) have induced similar response at different times in the Cretaceous. Finally, the geological record indicates that at wide spatial scale calcareous nannoplankton can adapt to high pCO2, but past changes occurred over tens of thousands of years, giving time for life to adjust or even take advantage. Laboratory experiments on modern coccolithophore species (evolutionary-linked to Cretaceous taxa) remain the only means to assess if and which role environmental parameters have on quantity, type and amount of coccolith secretion. Although conscious of the very different time scales of processes and resolution, the double biological and geological approach to coccolithophore calcification is aimed at integrating the daily-decadal datasets with medium to long-term (thousands to millions of years in duration) data. This has the potential for achieving an improved understanding of coccolith biomineralization mechanisms and providing some guidance as to the response of biota to abrupt massive CO2 releases and how and at what rate pre-perturbation conditions are eventually restored.