sustainability Review Phytoplankton as Key Mediators of the Biological Carbon Pump: Their Responses to a Changing Climate Samarpita Basu * ID and Katherine R. M. Mackey Earth System Science, University of California Irvine, Irvine, CA 92697, USA; [email protected] * Correspondence: [email protected] Received: 7 January 2018; Accepted: 12 March 2018; Published: 19 March 2018 Abstract: The world’s oceans are a major sink for atmospheric carbon dioxide (CO2). The biological carbon pump plays a vital role in the net transfer of CO2 from the atmosphere to the oceans and then to the sediments, subsequently maintaining atmospheric CO2 at significantly lower levels than would be the case if it did not exist. The efficiency of the biological pump is a function of phytoplankton physiology and community structure, which are in turn governed by the physical and chemical conditions of the ocean. However, only a few studies have focused on the importance of phytoplankton community structure to the biological pump. Because global change is expected to influence carbon and nutrient availability, temperature and light (via stratification), an improved understanding of how phytoplankton community size structure will respond in the future is required to gain insight into the biological pump and the ability of the ocean to act as a long-term sink for atmospheric CO2. This review article aims to explore the potential impacts of predicted changes in global temperature and the carbonate system on phytoplankton cell size, species and elemental composition, so as to shed light on the ability of the biological pump to sequester carbon in the future ocean. Keywords: phytoplankton; biological carbon pump; climate change; CO2; marine carbon cycle 1. Introduction Marine phytoplankton perform half of all photosynthesis on Earth [1,2] and directly influence global biogeochemical cycles and the climate, yet how they will respond to future global change is unknown. Carbon dioxide (CO2) is one of the principal drivers of global change and has been identified as one of the major challenges in the 21st century [3]. CO2 generated during anthropogenic activities such as deforestation and burning of fossil fuels for energy generation rapidly dissolves in the surface ocean and lowers seawater pH, while CO2 remaining in the atmosphere increases global temperatures and leads to increased ocean thermal stratification. While CO2 concentration in the atmosphere is estimated to be about 270 ppm before the industrial revolution, it has currently increased to about 400 ppm [4] and is expected to reach 800–1000 ppm by the end of this century according to the “business as usual” CO2 emission scenario [5]. Marine ecosystems are a major sink for atmospheric CO2 and take up similar amount of CO2 as terrestrial ecosystems, currently accounting for the removal of nearly one third of anthropogenic CO2 emissions from the atmosphere [4,5]. The net transfer of CO2 from the atmosphere to the oceans and then sediments, is mainly a direct consequence of the combined effect of the solubility and the biological pump [6]. While the solubility pump serves to concentrate dissolved inorganic carbon (CO2 plus bicarbonate and carbonate ions) in the deep oceans, the biological carbon pump (a key natural process and a major component of the global carbon cycle that regulates atmospheric CO2 levels) transfers both organic and inorganic carbon fixed by primary producers (phytoplankton) in Sustainability 2018, 10, 869; doi:10.3390/su10030869 www.mdpi.com/journal/sustainability Sustainability 2018, 10, 869 2 of 18 Sustainability 2017, 9, x FOR PEER REVIEW 2 of 17 the euphotic zone to the ocean interior and subsequently to the underlying sediments [6,7]. Thus, the biologicaltransfers both pump organic takes and carbon inorganic out of carbon contact fixed with by the primary atmosphere producers for (phytoplankton) several thousand in yearsthe or longereuphotic and maintains zone to the atmospheric ocean interior CO 2andat significantlysubsequently lowerto the levelsunderlying than wouldsediments be the[6,7] case. Thus, ifit the did not existbiological [8]. An ocean pump without takes carbon a biological out of contact pump, with which the atmosphere transfers for roughly several 11 thousand Gt C yr years−1 into or longer the ocean’s and maintains atmospheric CO2 at significantly lower levels than would be the case if it did not exist interior, would result in atmospheric CO2 levels ~400 ppm higher than present day [9,10]. [8]. An ocean without a biological pump, which transfers roughly 11 Gt C yr−1 into the ocean’s interior, Understanding the response of the biological carbon pump to global change is required to would result in atmospheric CO2 levels ~400 ppm higher than present day [9,10]. accurately predict future atmospheric CO concentrations [11]. Oceans are projected to undergo Understanding the response of the biological2 carbon pump to global change is required to significant changes due to the rising atmospheric CO levels. The dissolution of anthropogenic CO accurately predict future atmospheric CO2 concentrations2 [11]. Oceans are projected to undergo 2 in thesignificant ocean and changes the subsequent due to the rising formation atmospheric of carbonic CO2 levels. acid has The already dissolution resulted of anthropogenic in a 30% increase CO2 in + [H ]in concentration the ocean and inthe seawater subsequent (resulting formation in of a carbonic decrease acid of 0.1has pHalready unit resulted and will in continue a 30% increase to lower in pH by an[H additional+] concentration 0.2–0.3 in seawater pH units (resulting by the end in a of decrease the century. of 0.1 ThispH unit decline and will in oceancontinue pH to is lower referred pH to as oceanby acidification an additional [0.212].–0.3 At pH the units same by time,the end warming of the century. will increase This decline the meanin ocean surface pH is referred temperatures to as by an averageocean acidification of 3 ◦C, leading [12]. At to the longer same periodstime, warming of stratification will increase with the fewermean surface deep mixing temperatures events by [13 ,14]. Increasedan average stratification of 3 °C, leading is expected to longer to lead periods to nutrient of stratification limitation with and fewer an deep increase mixing in averageevents [13 irradiance,14]. Increased stratification is expected to lead to nutrient limitation and an increase in average irradiance in the euphotic layer, where phytoplankton grow [5,15] (Figure1). Phytoplankton are a highly diverse in the euphotic layer, where phytoplankton grow [5,15] (Figure 1). Phytoplankton are a highly diverse group of microscopic photosynthesizing microalgae and cyanobacteria which act as a link to couple group of microscopic photosynthesizing microalgae and cyanobacteria which act as a link to couple atmosphericatmospheric and and oceanic oceanic processes processes [16 [16].] They. They contribute contribute nearlynearly 50% to to the the total total primary primary production production of Earthof by Earth fixing by fixing about about 50 Gt 50 carbon Gt carbon per per annum annum [1]. [1]. Figure 1. Global change effects on the surface ocean: By the year 2100, pH of the ocean will decline Figure 1. Global change effects on the surface ocean: By the year 2100, pH of the ocean will decline to to 7.8 due to increased uptake of atmospheric CO2. Concomitantly, increased thermal stratification 7.8 due to increased uptake of atmospheric CO2. Concomitantly, increased thermal stratification will will trap phytoplankton in the surface ocean, resulting in increased light exposure and lower nutrient trap phytoplankton in the surface ocean, resulting in increased light exposure and lower nutrient availability to the cells (adapted from ref. [4]). availability to the cells (adapted from ref. [4]). TheThe efficiency efficiency of theof the biological biological pump pump isis a function of of phytoplankton phytoplankton physiology physiology and community and community structure,structure, which which are are in in turn turn governed governed byby thethe physical and and chemical chemical conditions conditions of the of oce thean ocean [16]. [16]. OceanOcean acidification acidification can can potentially potentially affectaffect phytoplanktonphytoplankton community community composition composition and andlead leadto to physiological and evolutionary changes in their constituent species [17]. The eco-physiological physiological and evolutionary changes in their constituent species [17]. 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