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Impact of Trace Metal Concentrations on Coccolithophore Growth and Morphology: Laboratory Simulations of Cretaceous Stress

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Impact of Trace Metal Concentrations on Coccolithophore Growth and Morphology: Laboratory Simulations of Cretaceous Stress Biogeosciences, 14, 3603–3613, 2017 https://doi.org/10.5194/bg-14-3603-2017 © Author(s) 2017. This work is distributed under the Creative Commons Attribution 3.0 License. Impact of trace metal concentrations on coccolithophore growth and morphology: laboratory simulations of Cretaceous stress Giulia Faucher1, Linn Hoffmann2, Lennart T. Bach3, Cinzia Bottini1, Elisabetta Erba1, and Ulf Riebesell3 1Earth Sciences Department “Ardito Desio”, Università degli Studi di Milano, Milan, Italy 2Department of Botany, University of Otago, Dunedin, New Zealand 3Biological Oceanography, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany Correspondence to: Giulia Faucher ([email protected]) Received: 12 April 2017 – Discussion started: 21 April 2017 Revised: 27 June 2017 – Accepted: 29 June 2017 – Published: 31 July 2017 Abstract. The Cretaceous ocean witnessed intervals of pro- record and the experimental results converge on a selective found perturbations such as volcanic input of large amounts response of coccolithophores to metal availability. of CO2, anoxia, eutrophication and introduction of bio- These species-specific differences must be considered be- logically relevant metals. Some of these extreme events fore morphological features of coccoliths are used to recon- were characterized by size reduction and/or morphological struct paleo-chemical conditions. changes of a few calcareous nannofossil species. The cor- respondence between intervals of high trace metal concen- trations and coccolith dwarfism suggests a negative effect of these elements on nannoplankton biocalcification pro- 1 Introduction cesses in past oceans. In order to test this hypothesis, we explored the potential effect of a mixture of trace metals Trace metal concentrations influence the productivity and on growth and morphology of four living coccolithophore species composition of marine algae communities (Bruland species, namely Emiliania huxleyi, Gephyrocapsa ocean- et al., 1991; Sunda and Huntsman, 1998). A number of trace ica, Pleurochrysis carterae and Coccolithus pelagicus. The metals are important micronutrients (e.g., zinc, iron, copper, phylogenetic history of coccolithophores shows that the se- nickel), but some of them can become toxic and inhibit ma- lected living species are linked to Mesozoic species showing rine algal productivity at elevated concentrations (Brand et dwarfism under excess metal concentrations. The trace met- al., 1986; Sunda and Huntsman, 1992). Others like lead and als tested were chosen to simulate the environmental stress mercury have no known metabolic functions and can hamper identified in the geological record and upon known trace marine phytoplankton growth already at low concentrations metal interactions with living coccolithophore algae. (Sunda, 1989; Sunda et al., 2005). Our laboratory experiments demonstrated that elevated The geological record offers the opportunity to investi- trace metal concentrations, similarly to the fossil record, af- gate past case histories marked by profound changes in the fect coccolithophore algae size and/or weight. Smaller coc- ocean, such as volcanic injection of large amounts of CO2, coliths were detected in E. huxleyi and C. pelagicus, while ocean anoxia, eutrophication and introduction of biologically coccoliths of G. oceanica showed a decrease in size only at relevant metals (e.g., Larson and Erba, 1999; Erba, 2004; the highest trace metal concentrations. P. carterae coccol- Jenkyns, 2010; Erba et al., 2015). These events can be seen ith size was unresponsive to changing trace metal concen- as “natural experiments” useful to decrypt the ecosystem re- trations. These differences among species allow discriminat- sponse to major perturbations at timescales longer than cur- ing the most- (P. carterae), intermediate- (E. huxleyi and G. rent modifications. Finding out how the changes in seawater oceanica) and least-tolerant (C. pelagicus) taxa. The fossil composition affect marine biota requires the integration of a long-term and large-scale geological perspective that has been recognized as an essential ingredient for more coherent Published by Copernicus Publications on behalf of the European Geosciences Union. 3604 G. Faucher et al.: Impact of trace metal concentrations on coccolithophore growth predictions of how marine organisms might react to future Table 1. Trace metal concentrations in the growth medium of the environmental changes. Insights on ocean–atmosphere dy- different treatments. namics under warmer-than-present-day conditions predicted for the end of this century can be obtained by including geo- Control Low Medium High Extreme µmol L−1 logical data of past ecosystems, especially those derived from cases of extreme conditions. Well-known perturbations were FeCl3 · 6H2O 11.7 11.7 11.7 11.7 11.7 the oceanic anoxic events (OAEs) which took place during Na2 · 2H2O 11.7 11.7 11.7 11.7 11.7 CuSO · 5H O 0.04 0.04 0.04 0.04 0.04 the Mesozoic. These events were caused by intense volcan- 4 2 Na2MoO4 · 2H2O 0.03 0.03 0.03 0.03 0.03 ism that produced large igneous provinces (LIPs; Snow et al., CoCl2 · 6H2O 0.04 0.04 0.04 0.04 0.04 2005; Neal et al., 2008; Pearce et al., 2009; Erba et al., 2015) ZnSO4 · 7H2O 0.08 0.16 0.16 0.96 8.08 that released magmatic fluids delivering metals, mixed with Pb – 0.01 0.08 0.8 · warmed ambient seawater that had enough buoyancy to rise NiCl2 6H2O – 0.08 0.08 0.8 8.00 VOSO4 – 0.08 0.08 0.8 8.00 to the surface (Snow et al., 2005; Erba et al., 2015). During EDTA 11.7 11.7 11.7 11.7 11.7 the latest Cenomanian OAE 2, for example, less volatile ele- ments, such as nickel and iron (released during the formation of the Caribbean LIP), increased by 8–20 times above sea- Previous work on the response of living coccolithophores water background levels while more volatile elements like to trace metal concentrations focused on Emiliania huxleyi, lead and cadmium (derived from water–rock exchange reac- one of the most abundant species in the world ocean with tions) increased by about 4-8 times above background level a nearly global distribution (Westbroek et al., 1989; Winter (Orth et al., 1993; Snow et al., 2005). Entering the ocean et al., 2014). Experiments documented a decreasing growth environment, more and less volatile elements became bio- rate under high trace metal concentrations (Vasconcelos et logically relevant as evidenced by changes and turnover in al., 2001; Hoffmann et al., 2012; Santomauro et al., 2016). marine plankton communities (Leckie, 1985; Leckie et al., So far, no such studies have been performed on other coccol- 1998; Erba, 2004; Erba et al., 2015). ithophore species. Furthermore, to our knowledge, this is the Studies on calcareous nannofossils documented a size re- first study investigating the effect of high trace metal concen- duction of some coccolithophore species (Biscutum con- trations on coccolithophore and coccolith morphology and stans, Zeugrhabdotus erectus and Discorhabdus rotatorius) size. The trace metals tested (Zn, V, Ni, Pb) were chosen that are coeval with trace metal concentration peaks across based on peaks identified in the geological record (Snow et both the early Aptian OAE 1a and latest Cenomanian OAE al., 2005) and known trace metal interactions with living coc- 2 (Erba et al., 2015; Faucher et al., 2017). The fossil record colithophores to simulate the environmental conditions dur- shows that, although most of the Mesozoic nannoplankton ing OAEs. The main goal of this study is to understand if, taxa did not survive the mass extinction event at the end similarly to the fossil record, anomalously high quantities of the Cretaceous, reconstructed phylogenetic trees (Bown of essential and/or toxic metal induce changes in coccol- et al., 2004), based on morphological observations of coc- ith shape and size and cause coccolith dwarfism in coccol- colith (shape and ultrastructure), and molecular trees, mostly ithophore species. based on rDNA (de Vargas and Probert, 2004), indicate a link More specifically, we address the following questions: between selected Mesozoic groups and some living coccol- (i) does coccolithophore growth change in response to in- ithophores. The group to which the four species tested here creasing trace metal concentrations? (ii) Does coccolith size belong to, namely Emiliania huxleyi, Gephyrocapsa ocean- and morphology, as well as coccolithophore size, change in ica, Coccolithus pelagicus and Pleurochrysis carterae, evo- response to high and anomalous trace metal concentrations? lutionarily diverged from one another since the Late Cre- (iii) Do trace metal combinations, which mimic OAE condi- taceous, with the exception of E. huxleyi and G. ocean- tions, lead to a uniform response among species or to species- ica that are separated since 250 000 years ago (De Vargas specific responses on morphological features? (iv) Do coc- et al., 2007; Liu et al., 2010). Specifically, genera Emilia- colith morphometrical features have a potential to serve as a nia and Gephyrocapsa belong to the Cenozoic family Noe- proxy to reconstruct paleo-ocean trace metal concentrations? laerhabdaceae derived from the extinct Prinsiaceae that, in turn, branched off the Mesozoic family Biscutaceae. Indeed, coccolith dwarfism was observed in genus Biscutum during 2 Materials and methods times of high CO2 and metal concentrations in both OAE 1a and OAE 2 (Erba et al., 2010; Faucher et al., 2017). It is chal- 2.1 Culture conditions lenging to unambiguously disentangle the cause(s) of such changes in the fossil record, but evidence of a correspon- Monospecific cultures of the coccolithophores Emiliania dence between intervals of high trace metal concentrations huxleyi (strain RCC 1216), Gephyrocapsa oceanica (strain and coccolith dwarfism suggests a negative effect of these RCC 1303), Coccolithus pelagicus (strain PLY182G) and elements on nannoplankton biocalcification processes. Pleurochrysis carterae (no known strain number) were Biogeosciences, 14, 3603–3613, 2017 www.biogeosciences.net/14/3603/2017/ G. Faucher et al.: Impact of trace metal concentrations on coccolithophore growth 3605 grown as batch cultures in artificial seawater produced 400 Normal sample as described by Kester et al.
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