Novel Heterococcolithophores, Holococcolithophores and Life Cycle Combinations from the Families Syracosphaeraceae and Papposphaeraceae and the Genus Florisphaera
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J. Micropalaeontology, 40, 75–99, 2021 https://doi.org/10.5194/jm-40-75-2021 © Author(s) 2021. This work is distributed under the Creative Commons Attribution 4.0 License. Novel heterococcolithophores, holococcolithophores and life cycle combinations from the families Syracosphaeraceae and Papposphaeraceae and the genus Florisphaera Sabine Keuter1,2, Jeremy R. Young3, Gil Koplovitz1, Adriana Zingone4, and Miguel J. Frada1,2 1The Interuniversity Institute for Marine Sciences in Eilat, POB 469, 88103 Eilat, Israel 2Dept. of Ecology, Evolution and Behavior – Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, 91904 Jerusalem, Israel 3Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK 4Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy Correspondence: Miguel J. Frada ([email protected]) and Jeremy R. Young ([email protected]) Received: 14 April 2021 – Revised: 18 June 2021 – Accepted: 22 June 2021 – Published: 18 August 2021 Abstract. Coccolithophores are a diverse group of calcifying phytoplankton, which are responsible for a large part of the modern oceanic carbonate production. Here, we describe novel or poorly known coccolithophores and novel life cycle combination coccospheres detected in samples collected either in the Gulf of Aqaba in the northern Red Sea or in the Gulf of Naples in the western Mediterranean. These include Syracosphaera win- teri, for which detached coccoliths have previously been recorded but both a formal description and taxonomic affiliation were lacking, and five undescribed sets of combination cells linking HET and HOL forms for S. pul- chra, S. mediterranea, S. azureaplaneta, S. lamina and S. orbicula. We also propose the replacement name S. kareniae for the fossil species Deutschlandia gaarderae. We describe a new species of the genus Ophiaster, O. macrospinus, displaying a unique morphological and ecological distribution as well as putative combination cells of two variants of the deep-dwelling Florisphaera profunda, which provide new insights on the affilia- tion of this genus within the Calcihaptophycideae. Additionally, in the family Papposphaeraceae we detected a new species, Pappomonas vexillata, and combination cells of Picarola margalefi and of a species resembling Papposphaera arctica. Finally, we detected three novel, unpaired holococcolithophore forms (Calyptrosphaera lluisae, Calicasphaera bipora and one form designated as Holococcolithophore A). Overall, this set of novel ob- servations and ensuing discussions provide further insights into the diversity, evolution and life cycle complexity of coccolithophores in the oceans. 1 Introduction tyre, 1979; Poulton et al., 2017). Additionally, due to calci- fication, coccolithophores influence seawater alkalinity and Coccolithophores (class Prymnesiophyceae, subclass Calci- act as ballast in faecal pellets of zooplankton and in marine haptophycidae) are calcifying protists that characteristically aggregates, thus enhancing the export of biogenic matter to produce an exoskeleton (the coccosphere) made of multi- the deep ocean and sediments (e.g., Milliman, 1993; Poulton ple calcium carbonate scales called coccoliths (Young et al., et al., 2007; Ziveri et al., 2007; Broecker and Clark, 2009). 1999). Coccolithophores are a major component of phyto- Long-term deposition of coccoliths in marine sediments has plankton communities in the oceans and significant contrib- created a remarkably successive fossil record across both the utors to marine primary productivity (e.g., Okada and McIn- Mesozoic and Cenozoic that is widely used in biostratigra- Published by Copernicus Publications on behalf of The Micropalaeontological Society. 76 S. Keuter et al.: Novel heterococcolithophores, holococcolithophores and life cycle combinations phy and paleoceanography (e.g., Bown et al., 2004). Coc- Study sites colithophores also intracellularly produce a high amount of dimethylsulfoniopropionate (DMSP) that is the precursor of The Gulf of Aqaba (GoA) is a deep terminal basin connected the volatile gas dimethylsulfide (DMS), which can act as con- at its southern end to the northern Red Sea. Over spring– ∼ ◦ densation nuclei that increase cloud albedo and thus impact summer the water column is warm (up to 28 C), markedly climate (Charlson et al., 1987; Franklin et al., 2010). stratified and nutrient-limited (considered co-limited for ni- A core attribute of coccolithophores is their life cycle. trogen and phosphorus; Mackey et al., 2009). Cyanobacte- Most species can appear as either of two morphologically ria largely dominate such conditions. However, surface cool- distinct life stages that have different ploidy levels, one being ing during winter and the presence of a weak temperature gradient across the water column (deepwater temperature is haploid and the other diploid (haplodiplontic life cycle). Typ- ◦ ically, diploid cells produce heterococcoliths that are com- ca. 20.6 C) drive a unique deep vertical mixing. Mixing en- posed of a complex radial array of interlocked calcite crys- trains nutrients to the photic layer, enabling a progressive in- tals. In contrast, in certain core groups of coccolithophores, crement in spring phytoplankton biomass, with blooms of a the haploid cells produce holococcoliths formed of assem- magnitude that is unusual for subtropical, oligotrophic seas blies of euhedral calcite crystallites. These two life cycle (e.g., Genin et al., 1995; Lindell and Post, 1995; Zarubin et phases with coccoliths are usually denominated as hetero- al., 2017). coccolithophore (HET) and holococcolithophore (HOL), re- The Gulf of Naples (GoN) is a temperate coastal embay- spectively. In other species, however, the haploid cells pro- ment adjacent to the city of Naples (Italy) that is influenced duce “nannoliths” without the features of either hetero- or both by offshore oligotrophic waters of the Tyrrhenian Sea holococcoliths, or they lack coccoliths (non-calcified), such (western Mediterranean Sea) and eutrophic coastal waters as in the family Noelaerhabdaceae that includes the genera enriched by land runoff (Carrada et al., 1980; Ribera d’Alcalà Emiliania and Gephyrocapsa, which often numerically dom- et al., 2004). The location and width of the boundary between inate coccolithophore assemblages (Billard, 1994; Houdan et offshore oligotrophic and coastal eutrophic waters are highly al., 2004; Frada et al., 2019). Little is known about the sig- dynamic and variable over seasons, entailing exchanges be- nificance of life cycle transitions and the mechanisms driv- tween the two water masses (Cianelli et al., 2017). Typically, ing them. Yet, life cycling may allow coccolithophores to re- the annual cycle is driven by temperature. From December spond and adapt to a broader range of environmental con- to March the water column is thoroughly mixed and tem- peratures can be as low as 13.2 ◦C. From mid-March a tem- ditions, with each phase performing best in different set- ◦ tings (Houdan et al., 2004; Frada et al., 2019). An impor- perature increase (up to 28.9 C in late July) drives the wa- tant source of evidence for the ability of coccolithophores ter column towards stratification. The nutrient decrease over to undergo life cycle transitions comes from observations late spring–summer is interrupted by an influx of nutrients of “combination coccospheres” (e.g., Cros et al., 2000; Tri- through municipal runoff (Ribera d’Alcalà et al., 2004). In antaphyllou et al., 2016). These forms bearing both hetero- surface waters, phytoplankton biomass, typically dominated and holococcoliths are interpreted as cells undergoing transi- by diatoms and phytoflagellates most of the year, may in- tions between haploid and diploid phases and have therefore crease from late winter and generally reaches a maximum in enabled the linking of morphologically distinct life phases, late spring, with frequent additional peaks over the summer thus advancing our understanding of coccolithophore biol- and a less conspicuous autumn bloom (Zingone et al., 2010, ogy, ecology and evolution. Noticeably, in several species 2019). the heterococcolithophore life stage can be associated with multiple distinguishable holococcolithophore morphotypes. 2 Materials and methods This has been interpreted either as evidence for intraspecific variation or cryptic speciation only perceptible in the holo- Seawater samples from the GoA were collected using coccolithophore life phase (Geisen et al., 2002). Niskin bottles through the photic layer (0–140 m) between We have recently undertaken an intensive study of coc- March 2017 and December 2018 at Station A (29.467◦ N, colithophores in the Gulf of Aqaba, in the northeastern end 34.929◦ E), an offshore 750 m deep station regularly mon- of the Red Sea, to determine their local diversity, ecology itored for oceanographic parameters by the Interuniversity and seasonal succession. During that study we encountered Institute for Marine Sciences in Eilat (IUI) (see Zarubin several undescribed morphotypes and also combination coc- et al., 2017). Samples from the GoN were collected with cospheres, allowing us to infer novel life cycle associations. Niskin bottles through the water column (0–60 m) between These taxonomic observations from the Gulf of Aqaba are June 2016 and July 2017 in the framework of the Long- supplemented by observations from a second seasonal study Term Ecological Research program conducted at the site of coccolithophores in the Gulf of Naples in the western MareChiara