Ocean Carbon and Biogeochemistry Studying marine biogeochemical cycles and associated ecosystems in the face of environmental change Volume 9, Number 3 Fall 2016 News A chalkier ocean? Multi-decadal increases in North Atlantic coccolithophore populations Kristen Krumhardt1 and Sara Rivero-Calle2 1Environmental Studies Program and Institute of Arctic and Alpine Research, University of Colorado Boulder, Boulder, Colorado, USA 2Department of Marine and Environmental Biology, University of Southern California, Los Angeles, California, USA Coccolithophores and the carbon cycle Increasing atmospheric CO2 concentrations are resulting in both warmer sea surface temperatures due to the greenhouse effect and increas- ingly carbon-rich surface waters. The ocean has absorbed roughly one third of anthropogenic carbon emissions (1), causing a shift in car- bon chemistry equilibrium to more acidic conditions with lower calcium carbonate saturation states (ocean MODIS PIC May 2010 acidification). Organisms that pro- duce calcium carbonate structures are 0.0 0.1 0.2 0.4 0.6 0.8 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 9.0 10.0 11.0 thought to be particularly susceptible PIC concentration (mg m−3) to these changes (2-4). Coccolithophores are the most Figure 1. Moderate Resolution Imaging Spectroradiometer (MODIS) Aqua satellite-derived abundant type of calcifying uni- particulate inorganic carbon (PIC) concentration (mg m-3) averaged for the month of May 2010 cellular micro-algae in the ocean, highlights prominent coccolithophore blooms in the North Atlantic. producing microscopic calcium carbonate plates called coccoliths (5). Low-pH conditions inorganic carbon (PIC) through calcification. Detri- have been shown to disrupt the formation of coccoliths tal coccolithophore shells form aggregates with organic (calcification; e.g., (6)). Therefore, it is generally expected material, enhancing carbon export to the deep sea (7). that a higher-CO2 ocean will cause a reduction in cal- Coccolithophores also produce dimethyl sulfide (DMS), cification rates or a decrease in the abundance of these a climatically relevant trace gas that impacts cloud forma- calcifiers. Such changes could have far-reaching conse- tion, ultimately influencing Earth’s albedo (8, 9). At the quences for marine ecosystems, as well as global carbon ecosystem level, coccolithophores compete for nutrients cycling and carbon export to the deep sea. with other phytoplankton and provide energy for the rest Coccolithophores use sunlight to synthesize both of the marine food web. Coccolithophores have a broad organic carbon through photosynthesis and particulate range of irradiance, temperature, and salinity tolerances OCB NEWS • Fall 2016 1 Science Year show that coccolithophores have the ability to modulate 1970 1980 1990 2000 2010 organic carbon production and calcification in response 20 a) coccolithophore occurence (temperate/subpolar) to variable amounts of dissolved inorganic carbon (DIC) but that low pH only affects these processes below a 10 certain threshold (14 ). Another study indicated that % occurrence 15 ) −2 coccolithophores could adapt to warming and high CO 0 2 b) coccolithophore pigments (subtropical) g m μ levels over the course of a year, maintaining their relative 10 ( particulate organic carbon (POC) and PIC production hapto 5 per cell (15). One of the limitations of all laboratory Chla 400 experiments is that only a handful of species (and strains) c) Mauna Loa CO2 record 0 380 (ppm) are studied, which is only a tiny fraction of the diversity 2 360 present in the oceans. Given the challenges of extrapo- 340 2100 ) −1 air pCO lating laboratory results to real world oceans, studying 320 2080 2060 recent trends in natural populations may lead to import- mol kg d) DIC at BATS (subtropical) μ 2040 ant insights. 2020 DIC ( 0.6 2000 The North Atlantic is both a region with rapid 0.4 e) AMO accumulation of anthropogenic CO2 (1) and an import- 0.2 0.0 ant coccolithophore habitat (Fig. 1), making this region AMO −0.2 a good starting point to search for in situ evidence of −0.4 −0.6 anthropogenic carbon effects on diverse coccolithophore 1970 1980 1990 2000 2010 populations. Two recent studies did precisely that: Rive- Year ro-Calle et al. (2015)(16 ) in the subpolar North Atlantic, Figure 2. Time-series data from 1960 to 2015 on (a) CPR coccolithophore and Krumhardt et al. (2016)(17 ) in the North Atlantic annual occurrence in the temperate/subpolar North Atlantic, (b) 140m subtropical gyre. Using independent datasets, these two depth-integrated chlorophyll a from coccolithophores (haptophytes) at studies concluded that coccolithophores in the North At- BATS in the subtropical North Atlantic (µg m-2) with a 2-year Gaussian filter lantic appear to be increasing in abundance and, contrary (dark green) and a linear regression (dashed line), (c) global atmospheric to the prevailing paradigm, responding positively to the CO2 concentration from Mauna Loa (ppm), (d) dissolved inorganic carbon extra carbon in the upper mixed layer. (DIC) at BATS (µmol kg-1) with a 2-year Gaussian filter (darker turquoise), and (e) the Atlantic Multidecadal Oscillation (AMO) index. Evidence from long-term in situ monitoring (two independent case studies) (10, 11). Moreover, their relatively low nutrient require- Rivero-Calle et al. (2015) used data from the Continu- ments and slow growth rates offer a competitive advantage ous Plankton Recorder (CPR), a filtering device installed under projected global warming and ocean stratification on ships of opportunity, to assess changes in coccolitho- (5). This plasticity and opportunistic behavior can be phore populations from 1965 to 2010 in the subpolar critical for persistence in a changing oceanic environment. North Atlantic. This highly productive, temperate region Given the wide range of biogeochemical and ecological is dominated by large phytoplankton and characterized by processes impacted by coccolithophores, it is important to strong seasonal changes in the mixed layer depth, nutri- assess how anthropogenic changes may affect coccolitho- ent upwelling, and gas exchange that lead to intense, well phore growth and calcification. established spring phytoplankton blooms. Many laboratory studies have investigated the impact Because coccolithophore cells are smaller than the mesh of future environmental conditions on coccolithophores size used by the CPR, they cannot be accurately quanti- by decreasing pH, increasing dissolved inorganic carbon, fied in the CPR data set. Some coccolithophore cells do, and increasing temperature to mimic end-of-century however, get caught in the mesh and their occurrence projections. However, these have often yielded conflict- (i.e. probability of presence) can be calculated and serve ing results: Some show a decrease, while others show no as a proxy for coccolithophore abundance. Using re- change or even increased calcification (e.g., (6, 12, 13)). corded presence or absence of coccolithophores over this For example, laboratory simulations of contemporary multidecadal time-series, the authors showed that coc- oceanic changes (increasing CO2 and decreasing pH) colithophore occurrence in the subpolar North Atlantic OCB NEWS • Fall 2016 2 Science increased from being present in only 1% of samples to > downwelling, resulting in an oligotrophic environment. 20% over the past five decades (Fig. 2). Despite relatively low productivity, subtropical gyres cover To assess the importance of a wide range of diverse vast expanses of the global ocean and are thus important environmental drivers on changes in coccolithophore oc- on a global scale. currence, Rivero-Calle and co-authors used random forest In the North Atlantic subtropical gyre, researchers at statistical models. Specifically, they examined more than BATS have performed phytoplankton pigment analyses 20 possible biological and physical predictors, including since the late 1980s, as well as a suite of other oceano- CO2 concentrations, nutrients, sea surface temperature graphic measurements (nutrients, temperature, salinity, and the Atlantic Multidecadal Oscillation (AMO), as well etc.). This rich dataset provided insight into phyto- as possible predators and competitors. Global and local plankton dynamics occurring at BATS over the past two CO2 concentrations were shown to be the best predictors decades. Coccolithophores contain a suite of pigments of coccolithophore occurrence. The AMO, which has distinctive to haptophytes. Though there are many species been in a positive phase since the mid-1990s (Fig. 2) and is of non-calcifying haptophytes in the ocean (18), the main associated with anomalously warmer temperatures over the contributors to the haptophyte community in oligotro- North Atlantic, was also a good predictor of coccolitho- phic gyres are coccolithophores (19). Using a constant phore occurrence, but not as strong of a predictor as CO2. haptophyte pigment to chlorophyll a ratio Krumhardt et The authors hypothesize that the synergistic effects of al. (2016) quantified relative abundance of the coccolitho- increasing anthropogenic CO2, the recent positive phase of phore chlorophyll a (Chlahapto) over the BATS time-series. the AMO, and increasing global temperatures contributed A simple linear regression revealed that coccolithophore to the observed increase in coccolithophore occurrence in pigments have increased in the upper euphotic zone by the CPR samples from 1965 to 2010. 37% from 1990 to 2012 (Figure 2). On the other hand, Complementing the Rivero-Calle et al.