The document discusses how phytoplankton play a key role in the biological carbon pump by transferring carbon from the atmosphere to the oceans. It explains that rising CO2 levels and climate change may impact phytoplankton physiology, community structure, and size, which could influence the efficiency of the biological carbon pump and the ocean's ability to absorb carbon long-term. The review aims to explore how predicted temperature increases and changes to the carbonate system could affect phytoplankton traits in order to understand implications for the biological carbon pump and future carbon sequestration in the oceans.
impactos del cambio climatico en ecosistemas costerosXin San
Anthropogenically induced global climate change has profound implications for marine
ecosystems and the economic and social systems that depend upon them. The
relationship between temperature and individual performance is reasonably well
understood, and much climate-related research has focused on potential shifts in
distribution and abundance driven directly by temperature. However, recent work has
revealed that both abiotic changes and biological responses in the ocean will be
substantially more complex. For example, changes in ocean chemistry may be more
important than changes in temperature for the performance and survival of many
organisms. Ocean circulation, which drives larval transport, will also change, with
important consequences for population dynamics. Furthermore, climatic impacts on one
or a few leverage species may result in sweeping community-level changes. Finally,
synergistic effects between climate and other anthropogenic variables, particularly fishing
pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve
living marine systems in the face of climate change will require improvements to the
existing predictive framework. Key directions for future research include identifying key
demographic transitions that influence population dynamics, predicting changes in the
community-level impacts of ecologically dominant species, incorporating populations
ability to evolve (adapt), and understanding the scales over which climate will change and
living systems will respond.
Biogeochemical cycle, any of the natural pathways by which essential elements of living matter are circulated. The term biogeochemical is a contraction that refers to the consideration of the biological, geological, and chemical aspects of each cycle.
impactos del cambio climatico en ecosistemas costerosXin San
Anthropogenically induced global climate change has profound implications for marine
ecosystems and the economic and social systems that depend upon them. The
relationship between temperature and individual performance is reasonably well
understood, and much climate-related research has focused on potential shifts in
distribution and abundance driven directly by temperature. However, recent work has
revealed that both abiotic changes and biological responses in the ocean will be
substantially more complex. For example, changes in ocean chemistry may be more
important than changes in temperature for the performance and survival of many
organisms. Ocean circulation, which drives larval transport, will also change, with
important consequences for population dynamics. Furthermore, climatic impacts on one
or a few leverage species may result in sweeping community-level changes. Finally,
synergistic effects between climate and other anthropogenic variables, particularly fishing
pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve
living marine systems in the face of climate change will require improvements to the
existing predictive framework. Key directions for future research include identifying key
demographic transitions that influence population dynamics, predicting changes in the
community-level impacts of ecologically dominant species, incorporating populations
ability to evolve (adapt), and understanding the scales over which climate will change and
living systems will respond.
Biogeochemical cycle, any of the natural pathways by which essential elements of living matter are circulated. The term biogeochemical is a contraction that refers to the consideration of the biological, geological, and chemical aspects of each cycle.
Planetary Boundaries: Exploring the Safe Operating Space for Humanity. Slides are all about summary of Johan Rockström et al., which basically talks about the nine planetary boundaries defined by author globally and explains about the control variables, thresholds, and where we as a Human stand right now with respect to both social boundaries and planetary boundaries.
CLIMATE change affects the components of water cycle such as evaporation, precipitation and evapotranspiration and thus results in large-scale alteration in water present in glaciers, rivers, lakes, oceans, etc. The effects of cli-mate change on subsurface water relates to the changes in its recharge and discharge rates plus changes in quantity and quality of water in aquifers. Climate change refers to the long-term changes in the components of climate such as temperature, precipitation, evapotranspiration, etc. The major cause of climate change is the rising level of greenhouse gases (GHGs) in the atmosphere such as CO2, CH4, N2O, water vapour, ozone and chlorofluorocarbon. These GHGs absorb 95% of the longwave back radiations emitted from the surface, thus making the Earth warmer. Except CO2, the effects of other GHGs are minor because of their low concentration and also because of low residence times (e.g. water vapour and methane). The rise in CO2 level causing global warming was first proposed by Svante Arrhenius, a Swedish scientist in 1896 and now it is a widely accepted fact that the concentration of CO2 is the primary regulator of temperature on the Earth and leads to global warming.
Dr. Francis Chan's 2012-2014 Oregon Sea Grant-supported project, "Understanding, Forecasting and Communicating the Linkages Between Hypoxia and Ocean Acidification in Oregon's Coastal Ocean"
Water Cycle Lesson PowerPoint, Hydrological Cycle, Biogeochemical Cycles Lessonwww.sciencepowerpoint.com
This PowerPoint was one very small part of my Ecology Interactions Unit from the website http://sciencepowerpoint.com/index.html .This unit includes a 3 part 2000+ Slide PowerPoint loaded with activities, project ideas, critical class notes (red slides), review opportunities, challenge questions with answers, 3 PowerPoint review games (125 slides each) and much more. A bundled homework package and detailed unit notes chronologically follow the PowerPoint slideshow.
Areas of Focus within The Ecology Interactions Unit: Levels of Biological Organization (Ecology), Parts of the Biosphere, Habitat, Ecological Niche, Types of Competition, Competitive Exclusion Theory, Animal Interactions, Food Webs, Predator Prey Relationships, Camouflage, Population Sampling, Abundance, Relative Abundance, Diversity, Mimicry, Batesian Mimicry, Mullerian Mimicry, Symbiosis, Parasitism, Mutualism, Commensalism, Plant and Animal Interactions, Coevolution, Animal Strategies to Eat Plants, Plant Defense Mechanisms, Exotic Species, Impacts of Invasive Exotic Species. If you have any questions please feel free to contact me. Thank you again and best wishes.
Sincerely,
Ryan Murphy M.Ed
www.sciencepowerpoint@gmail.com
Planetary Boundaries: Exploring the Safe Operating Space for Humanity. Slides are all about summary of Johan Rockström et al., which basically talks about the nine planetary boundaries defined by author globally and explains about the control variables, thresholds, and where we as a Human stand right now with respect to both social boundaries and planetary boundaries.
CLIMATE change affects the components of water cycle such as evaporation, precipitation and evapotranspiration and thus results in large-scale alteration in water present in glaciers, rivers, lakes, oceans, etc. The effects of cli-mate change on subsurface water relates to the changes in its recharge and discharge rates plus changes in quantity and quality of water in aquifers. Climate change refers to the long-term changes in the components of climate such as temperature, precipitation, evapotranspiration, etc. The major cause of climate change is the rising level of greenhouse gases (GHGs) in the atmosphere such as CO2, CH4, N2O, water vapour, ozone and chlorofluorocarbon. These GHGs absorb 95% of the longwave back radiations emitted from the surface, thus making the Earth warmer. Except CO2, the effects of other GHGs are minor because of their low concentration and also because of low residence times (e.g. water vapour and methane). The rise in CO2 level causing global warming was first proposed by Svante Arrhenius, a Swedish scientist in 1896 and now it is a widely accepted fact that the concentration of CO2 is the primary regulator of temperature on the Earth and leads to global warming.
Dr. Francis Chan's 2012-2014 Oregon Sea Grant-supported project, "Understanding, Forecasting and Communicating the Linkages Between Hypoxia and Ocean Acidification in Oregon's Coastal Ocean"
Water Cycle Lesson PowerPoint, Hydrological Cycle, Biogeochemical Cycles Lessonwww.sciencepowerpoint.com
This PowerPoint was one very small part of my Ecology Interactions Unit from the website http://sciencepowerpoint.com/index.html .This unit includes a 3 part 2000+ Slide PowerPoint loaded with activities, project ideas, critical class notes (red slides), review opportunities, challenge questions with answers, 3 PowerPoint review games (125 slides each) and much more. A bundled homework package and detailed unit notes chronologically follow the PowerPoint slideshow.
Areas of Focus within The Ecology Interactions Unit: Levels of Biological Organization (Ecology), Parts of the Biosphere, Habitat, Ecological Niche, Types of Competition, Competitive Exclusion Theory, Animal Interactions, Food Webs, Predator Prey Relationships, Camouflage, Population Sampling, Abundance, Relative Abundance, Diversity, Mimicry, Batesian Mimicry, Mullerian Mimicry, Symbiosis, Parasitism, Mutualism, Commensalism, Plant and Animal Interactions, Coevolution, Animal Strategies to Eat Plants, Plant Defense Mechanisms, Exotic Species, Impacts of Invasive Exotic Species. If you have any questions please feel free to contact me. Thank you again and best wishes.
Sincerely,
Ryan Murphy M.Ed
www.sciencepowerpoint@gmail.com
Effect of Global Warming on Soil Organic CarbonAmruta Raut
Currently surface Temperature are rising by about 0.2 °C (0.36 °F) per decade so how it will affect soil organic carbon level and what are the different strategies to sequester carbon explain in detail
This study aimed to understand the behavior of the carbonate system in the Cananéia-Iguape Estuarine-Lagoon Complex
(CIELC) to evaluate its potential as a source or sink for atmospheric CO2. This estuarine-lagoon complex is one of the most
extensive in Brazil, more than 100 km long and covers protected and sparsely inhabited regions of the state of São Paulo. This
system presents, in its southern portion, most preserved areas, and evident anthropogenic impact in the northern portion,
where an artificial canal was created in the second half of the 19th century, with the aim of shortening the navigation path link
the river to the estuarine system offering a passage to the sea, resulting in several modifications, both from a hydrodynamic
and biogeochemical mechanisms. Sampling of salinity (S), temperature (T), total alkalinity (TA), pH, dissolved oxygen (DO),
and nutrients (P and Si) were performed along the CIELC in the winter of 2012 and in the summer of 2013. S, TA, pH and
nutrients were used to support the understanding the behavior of the species in the carbonate system (CO2
, HCO3
-
, CO3
2-)
and related variables were used to calculating the partial pressure of CO2
(pCO2
). The data showed the difference in salinity
and carbonate members distinguished the northern and southern areas, the influence of the marine waters entrance by the
bars, and the predominance of the system as a source of CO2
, even in the most preserved area. However, the difference in this
behavior is most evident under anthropogenic pression offering risk of extreme changes in direction to the southern sector,
now observed until the intermediate point of the system. The recommendation is an urgency in monitoring this region to
minimizes futures environmental changes, as acidification and the increase as a source of CO2
Required Resources
Required Text
1. Environmental Science: Earth as a Living Planet
a. Chapter 3: Dollars and the Environmental Sense: Economics of Environmental Issues
b. Chapter 21: Air Pollution
Multimedia
1. Annenberg Learner. (n.d.). Carbon lab [Interactive lab]. In The Habitable Planet. Retrieved from http://learner.org/courses/envsci/interactives/carbon/
2. dennettracerocks3d. (2013, June 12). Carbon tax and cap and trade [Video clip]. Retrieved from http://www.youtube.com/watch?v=RmRNCEur1ks
· Transcript
Recommended Resource
Article
1. U.S. Environmental Protection Agency. (2012). Cap and trade. Retrieved from http://www.epa.gov/captrade/
CrITICAl THINkING IssUe
Should Carbon dioxide Be Regulated Along with other Major Air Pollutants?
The six common pollutants, sometimes called the criteria pol- lutants, are ozone, particulate matter, lead, nitrogen dioxide, carbon monoxide, and sulfur dioxide. These pollutants have a long history with the EPA, and major efforts have been made to reduce them in the lower atmosphere over the United States. This effort has been largely successful—all of them have been significantly reduced since 1990.
In 2009, the EPA suggested that we add carbon dioxide to this list. Two years earlier, the U.S. Supreme Court had or- dered the EPA to make a scientific review of carbon dioxide as an air pollutant that could possibly endanger public health and welfare. Following that review, the EPA announced that greenhouse gases pose a threat to public health and welfare. This proclamation makes it possible that greenhouse gases, especially carbon dioxide, will be regulated by the Clean Air Act, which regulates most other serious air pollutants.
The EPA’s conclusion that greenhouse gases harm or en- danger public health and welfare is based primarily on the role these gases play in climate change. The analysis states that the impacts include, but are not limited to, increased drought that will impact agricultural productivity; more intense rainfall, leading to a greater flood hazard; and increased frequency of heat waves that affect human health. The EPA’s proposal pro- gram to regulate carbon dioxide as an air pollutant has been upheld by court decisions
The next step in adding carbon dioxide and other green- house gasses, such as methane, to the list of pollutants regulated by the EPA was a series of public hearings and feedback from a variety of people and agencies. Some people oppose listing carbon dioxide as an air pollutant because, first of all, it is a nutrient and stimulates plant growth; and, second, it does not
directly affect human health in most cases (the exception being carbon dioxide emitted by volcanic eruption and other volcanic activity, which can be extremely toxic).
The EPA in late September of 2013 announced the initial steps to reduce carbon pollution under President Obama’s Cli- mate Action Plan. The objective will be standards for new coal burning power plants. Conversations are st ...
Soil carbon sequestration resulting from biosolids application, Silvana Torri
Como citar este trabajo
Torri S.I., Corrêa R.S., Renella G. 2014. Soil carbon sequestration resulting from biosolids application, Applied and Environmental Soil Science (ISSN: 1687-7667), Volume 2014 (2014), Article ID 821768, 9 pages. doi:10.1155/2014/821768.
Modelling climate change impacts on nutrients and primary production in coast...Marco Pesce
There is high confidence that the anthropogenic increase of atmospheric greenhouse gases (GHGs) is causing modifications in the Earth's climate. Coastal waterbodies such as estuaries, bays and lagoons are among those most affected by the ongoing changes in climate. Being located at the land-sea interface, such waterbodies are subjected to the combined changes in the physical-chemical processes of atmosphere, upstream land and coastal waters. Particularly, climate change is expected to alter phytoplankton communities by changing their environmental drivers (especially climate-related), thus exacerbating the symptoms of eutrophication events, such as hypoxia, harmful algal blooms (HAB) and loss of habitat. A better understanding of the links between climate related drivers and phytoplankton is therefore necessary for projecting climate change impacts on aquatic ecosystems. Here we present the case study of the Zero river basin in Italy, one of the main contributors of freshwater and nutrient to the salt-marsh Palude di Cona, a coastal water body belonging to the lagoon of Venice. To project the impacts of climate change on freshwater inputs, nutrient loadings and their effects on the phytoplankton community of the receiving waterbody, we formulated and applied an integrated modelling approach made of: climate simulations derived by coupling a General Circulation Model (GCM) and a Regional Climate Model (RCM) under alternative emission scenarios, the hydrological model Soil and Water Assessment Tool (SWAT) and the ecological model AQUATOX. Climate projections point out an increase of precipitations in the winter period and a decrease in the summer months, while temperature shows a significant increase over the whole year. Water discharge and nutrient loads simulated by SWAT show a tendency to increase (decrease) in the winter (summer) period. AQUATOX projects changes in the concentration of nutrients in the salt-marsh Palude di Cona, and variations in the biomass and species of the phytoplankton community.
Microbes in climate change
Biogeochemical cycle
Effects of climate on various geological regions
Terrestrial polar regions
Ocean
Fresh water
Agriculture
Soil
Key messages
Maintaining ocean ecosystems and services depends
in large part on the negotiation process
toward a global climate agreement under the
UNFCCC. In this regard, four key messages emerge
from our analysis. First, the ocean strongly influences
the climate system and provides important
services to humans. Second, impacts on key
marine and coastal organisms, ecosystems, and
services from anthropogenic CO2 emissions are
already detectable, and several will face high risk
of impacts well before 2100, even with the stringent
CO2 emissions scenario (RCP2.6). These impacts
are occurring across all latitudes and have
become a global concern that spans the traditional
north/south divide. Third, the analysis shows
that immediate and substantial reduction of CO2
emissions is required in order to prevent the massive
and effectively irreversible impacts on ocean
ecosystems and their services that are projected
with emissions scenarios more severe than RCP2.6.
Limiting emissions to below this level is necessary
to meet UNFCCC's stated objectives. Management
options that overlook CO2, such as solar
radiation management and control of methane
emission, will only minimize impacts of ocean
warming and not those of ocean acidification.
Fourth, as CO2 increases, the protection, adaptation,
and repair options for the ocean become
fewer and less effective.
Given the contrasting futures we have outlined
here, the ocean provides further compelling arguments
for rapid and rigorous CO2 emission
reduction and eventual reduction of atmospheric
CO2 content. As a result, any new global climate
agreement that does not minimize the impacts
on the ocean will be incomplete and inadequate.
Miriam Kastner: Her findings on METHANE HYDRATES in Ocean Acidification Summ...www.thiiink.com
Atmospheric carbon dioxide (CO2) levels are rising as a result of human activities, such as fossil fuel burning, and are increasing the acidity of seawater. This process is known as ocean acidi cation. Historically, the ocean has absorbed approximately 30% of all CO2 released into the atmosphere
by humans since the start of the industrial revolution, resulting in a 26% increase in the acidity of the ocean1.
Ocean acidi cation causes ecosystems and marine biodiversity to change. It has the potential to affect food security and it limits the capacity of the ocean to absorb CO2 from human emissions. The economic impact of ocean acidi cation could be substantial.
Reducing CO2 emissions is the only way to minimise long-term, large-scale risks.
Climate change is one of the primary factors contributing to the loss of biodiversity worldwide. The purpose of this review paper was to give serious thought about the present and future impacts of climate change on biodiversity, even though we are not aware of its synergistic effects on biological populations. In order to fully understand the biota's reactions to these climatic
changes, we also concentrated on how these changes impact their phenology and physiology. This review article's subjects are
covered in a non-random order to make it easier for readers to understand the connections between biodiversity and climate
change. We also discussed about how 1.1°C of global warming brought about by human activity has altered the Earth's climate
in ways never seen before and negatively impacted human health. We covered how to safeguard our biota by implementing practical conservation strategies at the end of this review article in order to reduce the effects of climate change on it. We hope that one day, because research on climate change and biodiversity protection is interdisciplinary and spans many different scientific areas, we will be able to address all these concerns and preserve our biota from their terrible consequences.
Professional air quality monitoring systems provide immediate, on-site data for analysis, compliance, and decision-making.
Monitor common gases, weather parameters, particulates.
Richard's entangled aventures in wonderlandRichard Gill
Since the loophole-free Bell experiments of 2020 and the Nobel prizes in physics of 2022, critics of Bell's work have retreated to the fortress of super-determinism. Now, super-determinism is a derogatory word - it just means "determinism". Palmer, Hance and Hossenfelder argue that quantum mechanics and determinism are not incompatible, using a sophisticated mathematical construction based on a subtle thinning of allowed states and measurements in quantum mechanics, such that what is left appears to make Bell's argument fail, without altering the empirical predictions of quantum mechanics. I think however that it is a smoke screen, and the slogan "lost in math" comes to my mind. I will discuss some other recent disproofs of Bell's theorem using the language of causality based on causal graphs. Causal thinking is also central to law and justice. I will mention surprising connections to my work on serial killer nurse cases, in particular the Dutch case of Lucia de Berk and the current UK case of Lucy Letby.
Seminar of U.V. Spectroscopy by SAMIR PANDASAMIR PANDA
Spectroscopy is a branch of science dealing the study of interaction of electromagnetic radiation with matter.
Ultraviolet-visible spectroscopy refers to absorption spectroscopy or reflect spectroscopy in the UV-VIS spectral region.
Ultraviolet-visible spectroscopy is an analytical method that can measure the amount of light received by the analyte.
What is greenhouse gasses and how many gasses are there to affect the Earth.moosaasad1975
What are greenhouse gasses how they affect the earth and its environment what is the future of the environment and earth how the weather and the climate effects.
This presentation explores a brief idea about the structural and functional attributes of nucleotides, the structure and function of genetic materials along with the impact of UV rays and pH upon them.
(May 29th, 2024) Advancements in Intravital Microscopy- Insights for Preclini...Scintica Instrumentation
Intravital microscopy (IVM) is a powerful tool utilized to study cellular behavior over time and space in vivo. Much of our understanding of cell biology has been accomplished using various in vitro and ex vivo methods; however, these studies do not necessarily reflect the natural dynamics of biological processes. Unlike traditional cell culture or fixed tissue imaging, IVM allows for the ultra-fast high-resolution imaging of cellular processes over time and space and were studied in its natural environment. Real-time visualization of biological processes in the context of an intact organism helps maintain physiological relevance and provide insights into the progression of disease, response to treatments or developmental processes.
In this webinar we give an overview of advanced applications of the IVM system in preclinical research. IVIM technology is a provider of all-in-one intravital microscopy systems and solutions optimized for in vivo imaging of live animal models at sub-micron resolution. The system’s unique features and user-friendly software enables researchers to probe fast dynamic biological processes such as immune cell tracking, cell-cell interaction as well as vascularization and tumor metastasis with exceptional detail. This webinar will also give an overview of IVM being utilized in drug development, offering a view into the intricate interaction between drugs/nanoparticles and tissues in vivo and allows for the evaluation of therapeutic intervention in a variety of tissues and organs. This interdisciplinary collaboration continues to drive the advancements of novel therapeutic strategies.
THE IMPORTANCE OF MARTIAN ATMOSPHERE SAMPLE RETURN.Sérgio Sacani
The return of a sample of near-surface atmosphere from Mars would facilitate answers to several first-order science questions surrounding the formation and evolution of the planet. One of the important aspects of terrestrial planet formation in general is the role that primary atmospheres played in influencing the chemistry and structure of the planets and their antecedents. Studies of the martian atmosphere can be used to investigate the role of a primary atmosphere in its history. Atmosphere samples would also inform our understanding of the near-surface chemistry of the planet, and ultimately the prospects for life. High-precision isotopic analyses of constituent gases are needed to address these questions, requiring that the analyses are made on returned samples rather than in situ.
Nutraceutical market, scope and growth: Herbal drug technologyLokesh Patil
As consumer awareness of health and wellness rises, the nutraceutical market—which includes goods like functional meals, drinks, and dietary supplements that provide health advantages beyond basic nutrition—is growing significantly. As healthcare expenses rise, the population ages, and people want natural and preventative health solutions more and more, this industry is increasing quickly. Further driving market expansion are product formulation innovations and the use of cutting-edge technology for customized nutrition. With its worldwide reach, the nutraceutical industry is expected to keep growing and provide significant chances for research and investment in a number of categories, including vitamins, minerals, probiotics, and herbal supplements.
Earliest Galaxies in the JADES Origins Field: Luminosity Function and Cosmic ...Sérgio Sacani
We characterize the earliest galaxy population in the JADES Origins Field (JOF), the deepest
imaging field observed with JWST. We make use of the ancillary Hubble optical images (5 filters
spanning 0.4−0.9µm) and novel JWST images with 14 filters spanning 0.8−5µm, including 7 mediumband filters, and reaching total exposure times of up to 46 hours per filter. We combine all our data
at > 2.3µm to construct an ultradeep image, reaching as deep as ≈ 31.4 AB mag in the stack and
30.3-31.0 AB mag (5σ, r = 0.1” circular aperture) in individual filters. We measure photometric
redshifts and use robust selection criteria to identify a sample of eight galaxy candidates at redshifts
z = 11.5 − 15. These objects show compact half-light radii of R1/2 ∼ 50 − 200pc, stellar masses of
M⋆ ∼ 107−108M⊙, and star-formation rates of SFR ∼ 0.1−1 M⊙ yr−1
. Our search finds no candidates
at 15 < z < 20, placing upper limits at these redshifts. We develop a forward modeling approach to
infer the properties of the evolving luminosity function without binning in redshift or luminosity that
marginalizes over the photometric redshift uncertainty of our candidate galaxies and incorporates the
impact of non-detections. We find a z = 12 luminosity function in good agreement with prior results,
and that the luminosity function normalization and UV luminosity density decline by a factor of ∼ 2.5
from z = 12 to z = 14. We discuss the possible implications of our results in the context of theoretical
models for evolution of the dark matter halo mass function.
Earliest Galaxies in the JADES Origins Field: Luminosity Function and Cosmic ...
Sustainability 10-00869
1. 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; kmackey@uci.edu
* Correspondence: basusamarpita@gmail.com
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
2. Sustainability 2018, 10, 869 2 of 18
the euphotic zone to the ocean interior and subsequently to the underlying sediments [6,7]. Thus,
the biological pump takes carbon out of contact with the atmosphere for several thousand years or
longer and maintains atmospheric CO2 at significantly lower levels than would be the case if it did not
exist [8]. An ocean without a biological pump, which transfers roughly 11 Gt C yr−1 into the ocean’s
interior, would result in atmospheric CO2 levels ~400 ppm higher than present day [9,10].
Understanding the response of the biological carbon pump to global change is required to
accurately predict future atmospheric CO2 concentrations [11]. Oceans are projected to undergo
significant changes due to the rising atmospheric CO2 levels. The dissolution of anthropogenic CO2
in the ocean and the subsequent formation of carbonic acid has already resulted in a 30% increase in
[H+] concentration in seawater (resulting in a decrease of 0.1 pH unit and will continue to lower pH
by an additional 0.2–0.3 pH units by the end of the century. This decline in ocean pH is referred to as
ocean acidification [12]. At the same time, warming will increase the mean surface temperatures by
an average of 3 ◦C, leading to longer periods of stratification with fewer deep mixing events [13,14].
Increased stratification is expected to lead to nutrient limitation and an increase in average irradiance
in the euphotic layer, where phytoplankton grow [5,15] (Figure 1). Phytoplankton are a highly diverse
group of microscopic photosynthesizing microalgae and cyanobacteria which act as a link to couple
atmospheric and oceanic processes [16]. They contribute nearly 50% to the total primary production of
Earth by fixing about 50 Gt carbon per annum [1].
Sustainability 2017, 9, x FOR PEER REVIEW 2 of 17
transfers both organic and inorganic carbon fixed by primary producers (phytoplankton) in the
euphotic zone to the ocean interior and subsequently to the underlying sediments [6,7]. Thus, the
biological pump takes carbon out of contact with the atmosphere for several thousand years or longer
and maintains atmospheric CO2 at significantly lower levels than would be the case if it did not exist
[8]. An ocean without a biological pump, which transfers roughly 11 Gt C yr−1 into the ocean’s interior,
would result in atmospheric CO2 levels ~400 ppm higher than present day [9,10].
Understanding the response of the biological carbon pump to global change is required to
accurately predict future atmospheric CO2 concentrations [11]. Oceans are projected to undergo
significant changes due to the rising atmospheric CO2 levels. The dissolution of anthropogenic CO2
in the ocean and the subsequent formation of carbonic acid has already resulted in a 30% increase in
[H+] concentration in seawater (resulting in a decrease of 0.1 pH unit and will continue to lower pH
by an additional 0.2–0.3 pH units by the end of the century. This decline in ocean pH is referred to as
ocean acidification [12]. At the same time, warming will increase the mean surface temperatures by
an average of 3 °C, leading to longer periods of stratification with fewer deep mixing events [13,14].
Increased stratification is expected to lead to nutrient limitation and an increase in average irradiance
in the euphotic layer, where phytoplankton grow [5,15] (Figure 1). Phytoplankton are a highly diverse
group of microscopic photosynthesizing microalgae and cyanobacteria which act as a link to couple
atmospheric and oceanic processes [16]. They contribute nearly 50% to the total primary production
of Earth by fixing about 50 Gt carbon per annum [1].
Figure 1. Global change effects on the surface ocean: By the year 2100, pH of the ocean will decline to
7.8 due to increased uptake of atmospheric CO2. Concomitantly, increased thermal stratification will
trap phytoplankton in the surface ocean, resulting in increased light exposure and lower nutrient
availability to the cells (adapted from ref. [4]).
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 [16].
Ocean acidification can potentially affect phytoplankton community composition and lead to
physiological and evolutionary changes in their constituent species [17]. The eco-physiological
characteristics of the species in the phytoplankton community regulate the quality (elemental and
biochemical composition) and quantity of primary production that is eventually transferred up the
food web and exported to the deep ocean and sediment via the biological pump. Despite its critical
importance, the role of phytoplankton community structure in modulating the biological pump is
poorly understood and is often a neglected component in carbon-climate research [18]. Thus, an
increased understanding of how phytoplankton community size structure will respond to ocean
acidification and global change is required to gain insight into the biological pump and the ability of
the ocean to serve as a long-term sink for atmospheric CO2. In this review article, we first provide
background on the biological carbon pump and then review studies aimed at understanding how
Figure 1. Global change effects on the surface ocean: By the year 2100, pH of the ocean will decline
to 7.8 due to increased uptake of atmospheric CO2. Concomitantly, increased thermal stratification
will trap phytoplankton in the surface ocean, resulting in increased light exposure and lower nutrient
availability to the cells (adapted from ref. [4]).
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 [16].
Ocean acidification can potentially affect phytoplankton community composition and lead to
physiological and evolutionary changes in their constituent species [17]. The eco-physiological
characteristics of the species in the phytoplankton community regulate the quality (elemental and
biochemical composition) and quantity of primary production that is eventually transferred up the
food web and exported to the deep ocean and sediment via the biological pump. Despite its critical
importance, the role of phytoplankton community structure in modulating the biological pump
is poorly understood and is often a neglected component in carbon-climate research [18]. Thus,
an increased understanding of how phytoplankton community size structure will respond to ocean
acidification and global change is required to gain insight into the biological pump and the ability of
the ocean to serve as a long-term sink for atmospheric CO2. In this review article, we first provide
background on the biological carbon pump and then review studies aimed at understanding how
global changes in temperature, the carbonate system, light intensity and nutrients affect phytoplankton
3. Sustainability 2018, 10, 869 3 of 18
physiology and community composition, in an attempt to understand the ability of the biological
pump to sequester carbon in the future ocean.
2. Components of the Biological Carbon Pump: Role of Marine Phytoplankton
The biological carbon pump is one of the chief determinants of the vertical distribution of carbon
in the oceans and therefore of the surface partial pressure of CO2 governing air-sea CO2 exchange [19].
It comprises phytoplankton cells, their consumers and the bacteria that assimilate their waste and
plays a central role in the global carbon cycle by delivering carbon from the atmosphere to the deep
sea, where it is concentrated and sequestered for centuries [7]. Photosynthesis by phytoplankton
lowers the partial pressure of CO2 in the upper ocean, thereby facilitating the absorption of CO2
from the atmosphere by generating a steeper CO2 gradient [20]. It also results in the formation of
particulate organic carbon (POC) in the euphotic layer of the epipelagic zone (0–200 m depth). The POC
is processed by microbes, zooplankton and their consumers into fecal pellets, organic aggregates
(“marine snow”) and other forms, which are thereafter exported to the mesopelagic (200–1000 m depth)
and bathypelagic zones by sinking and vertical migration by zooplankton and fish (Figure 2) [21].
Although primary production includes both dissolved and particulate organic carbon (DOC and
POC respectively), only POC leads to efficient carbon export to the ocean interior, whereas the DOC
fraction in surface waters is mostly recycled by bacteria [22]. However, a more biologically resistant
DOC fraction produced in the euphotic zone (accounting for 15–20% of net community productivity),
is not immediately mineralized by microbes and accumulates in the ocean surface as biologically-semi
labile DOC [23]. This semi-labile DOC undergoes net export to the deep ocean, thus constituting
a dynamic part of the biological carbon pump [24]. The efficiency of DOC production and export
varies across oceanographic regions, being more prominent in the oligotrophic subtropical oceans [25].
Because the overall efficiency of the biological carbon pump is mostly controlled by the export of
POC [22], we focus on this fraction of the organic carbon pool in this review.
Sustainability 2017, 9, x FOR PEER REVIEW 3 of 17
global changes in temperature, the carbonate system, light intensity and nutrients affect
phytoplankton physiology and community composition, in an attempt to understand the ability of
the biological pump to sequester carbon in the future ocean.
2. Components of the Biological Carbon Pump: Role of Marine Phytoplankton
The biological carbon pump is one of the chief determinants of the vertical distribution of carbon
in the oceans and therefore of the surface partial pressure of CO2 governing air-sea CO2 exchange
[19]. It comprises phytoplankton cells, their consumers and the bacteria that assimilate their waste
and plays a central role in the global carbon cycle by delivering carbon from the atmosphere to the
deep sea, where it is concentrated and sequestered for centuries [7]. Photosynthesis by phytoplankton
lowers the partial pressure of CO2 in the upper ocean, thereby facilitating the absorption of CO2 from
the atmosphere by generating a steeper CO2 gradient [20]. It also results in the formation of
particulate organic carbon (POC) in the euphotic layer of the epipelagic zone (0–200 m depth). The
POC is processed by microbes, zooplankton and their consumers into fecal pellets, organic aggregates
(“marine snow”) and other forms, which are thereafter exported to the mesopelagic (200–1000 m
depth) and bathypelagic zones by sinking and vertical migration by zooplankton and fish (Figure 2)
[21]. Although primary production includes both dissolved and particulate organic carbon (DOC and
POC respectively), only POC leads to efficient carbon export to the ocean interior, whereas the DOC
fraction in surface waters is mostly recycled by bacteria [22]. However, a more biologically resistant
DOC fraction produced in the euphotic zone (accounting for 15–20% of net community productivity),
is not immediately mineralized by microbes and accumulates in the ocean surface as biologically-
semi labile DOC [23]. This semi-labile DOC undergoes net export to the deep ocean, thus constituting
a dynamic part of the biological carbon pump [24]. The efficiency of DOC production and export
varies across oceanographic regions, being more prominent in the oligotrophic subtropical oceans
[25]. Because the overall efficiency of the biological carbon pump is mostly controlled by the export
of POC [22], we focus on this fraction of the organic carbon pool in this review.
Figure 2. Schematic of the biological carbon pump: Phytoplankton fix CO2 in the euphotic zone using
solar energy and produce particulate organic carbon (POC). POC formed in the euphotic zone is
processed by microbes, zooplankton and their consumers into organic aggregates (marine snow),
which is thereafter exported to the mesopelagic (200–1000 m depth) and bathypelagic zones by
sinking and vertical migration by zooplankton and fish. Export flux is defined as the sedimentation
out of the surface layer (at approximately 100 m depth) and sequestration flux is the sedimentation
out of the mesopelagic zone (at approximately 1000 m depth). A portion of the POC is respired back
to CO2 in the oceanic water column at depth, mostly by heterotrophic microbes and zooplankton, thus
maintaining a vertical gradient in concentration of dissolved inorganic carbon (DIC). This deep-ocean
DIC returns to the atmosphere on millennial timescales through thermohaline circulation. Between
1% and 40% of the primary production is exported out of the euphotic zone, which attenuates
exponentially towards the base of the mesopelagic zone and only about 1% of the surface production
reaches the sea floor (adapted from ref. [11,21]).
Figure 2. Schematic of the biological carbon pump: Phytoplankton fix CO2 in the euphotic zone
using solar energy and produce particulate organic carbon (POC). POC formed in the euphotic zone
is processed by microbes, zooplankton and their consumers into organic aggregates (marine snow),
which is thereafter exported to the mesopelagic (200–1000 m depth) and bathypelagic zones by sinking
and vertical migration by zooplankton and fish. Export flux is defined as the sedimentation out of the
surface layer (at approximately 100 m depth) and sequestration flux is the sedimentation out of the
mesopelagic zone (at approximately 1000 m depth). A portion of the POC is respired back to CO2 in the
oceanic water column at depth, mostly by heterotrophic microbes and zooplankton, thus maintaining a
vertical gradient in concentration of dissolved inorganic carbon (DIC). This deep-ocean DIC returns to
the atmosphere on millennial timescales through thermohaline circulation. Between 1% and 40% of
the primary production is exported out of the euphotic zone, which attenuates exponentially towards
the base of the mesopelagic zone and only about 1% of the surface production reaches the sea floor
(adapted from ref. [11,21]).
4. Sustainability 2018, 10, 869 4 of 18
Passow and Carlson [11] defined sedimentation out of the surface layer (at approximately 100 m
depth) as the “export flux” and that out of the mesopelagic zone (at approximately 1000 m depth) as
the “sequestration flux” (Figure 2). Once carbon is transported below the mesopelagic zone, it remains
in the deep sea for 100 years or longer, hence the term “sequestration” flux. According to the modelling
results of Buesseler and Boyd [26], between 1% and 40% of the primary production is exported out
of the euphotic zone, which attenuates exponentially towards the base of the mesopelagic zone and
only about 1% of the surface production reaches the sea floor [27]. The export efficiency of particulate
organic carbon shows regional variability. For instance, in the North Atlantic, over 40% of net primary
production is exported out of the euphotic zone as compared to only 10% in the South Pacific [26],
and this is driven in part by the composition of the phytoplankton community including cell size and
composition (see below). Exported organic carbon is remineralized, that is, respired back to CO2 in the
oceanic water column at depth, mainly by heterotrophic microbes and zooplankton (Figure 2). Thus,
the biological carbon pump maintains a vertical gradient in the concentration of dissolved inorganic
carbon (DIC), with higher values at increased ocean depth [28]. This deep-ocean DIC returns to the
atmosphere on millennial timescales through thermohaline circulation [29].
Hugh et al. [29] expressed the efficiency of the biological pump as the amount of carbon
exported from the surface layer (export production) divided by the total amount produced by
photosynthesis (overall production). Modelling studies by Buesseler and Boyd [26] revealed that
the overall transfer efficiency of the biological pump is determined by a combination of factors:
seasonality; the composition of phytoplankton species; the fragmentation of particles by zooplankton;
and the solubilization of particles by microbes. In addition, the efficiency of the biological pump is also
dependent on the aggregation and disaggregation of organic-rich aggregates and interaction between
POC aggregates and suspended “ballast” minerals [30]. Ballast minerals (silicate and carbonate
biominerals and dust) are the major constituents of particles that leave the ocean surface via sinking.
They are typically denser than seawater and most organic matter, thus, providing a large part of the
density differential needed for sinking of the particles [31]. Aggregation of particles increases vertical
flux by transforming small suspended particles into larger, rapidly-sinking ones. It plays an important
role in the sedimentation of phytodetritus from surface layer phytoplankton blooms [21]. As illustrated
by Turner [21], the vertical flux of sinking particles is mainly due to a combination of fecal pellets,
marine snow and direct sedimentation of phytoplankton blooms, which are typically composed of
diatoms, coccolithophorids, dinoflagellates and other plankton. Marine snow comprises macroscopic
organic aggregates >500 µm in size and originates from clumps of aggregated phytoplankton
(phytodetritus), discarded appendicularian houses, fecal matter and other miscellaneous detrital
particles [21]. Appendicularians secrete mucous feeding structures or “houses” to collect food particles
and discard and renew them up to 40 times a day [32]. Discarded appendicularian houses are highly
abundant (thousands per m3 in surface waters) and are microbial hotspots with high concentrations
of bacteria, ciliates, flagellates and phytoplankton. These discarded houses are therefore among the
most important sources of aggregates directly produced by zooplankton in terms of carbon cycling
potential [33].
The composition of the phytoplankton community in the euphotic zone largely determines
the quantity and quality of organic matter that sinks to depth [27]. The main functional groups of
marine phytoplankton that contribute to export production include nitrogen fixers (diazotrophic
cyanobacteria), silicifiers (diatoms) and calcifiers (coccolithophores). Each of these phytoplankton
groups differ in the size and composition of their cell walls and coverings, which influence their
sinking velocities [17]. For example, autotrophic picoplankton (0.2–2 µm in diameter)—which include
taxa such as cyanobacteria (e.g., Prochlorococcus spp. and Synechococcus spp.) and prasinophytes
(various genera of eukaryotes <2 µm)—are believed to contribute much less to carbon export from
surface layers due to their small size, slow sinking velocities (<0.5 m/day) and rapid turnover in the
microbial loop [17,34]. In contrast, larger phytoplankton cells such as diatoms (2–500 µm in diameter)
are very efficient in transporting carbon to depth by forming rapidly sinking aggregates [11]. They are
5. Sustainability 2018, 10, 869 5 of 18
unique among phytoplankton, because they require Si in the form of silicic acid (Si(OH)4) for growth
and production of their frustules, which are made of biogenic silica (bSiO2) and act as ballast [17,35].
According to the reports of Miklasz and Denny [36], the sinking velocities of diatoms can range from
0.4 to 35 m/day [17,35,36]. Analogously, coccolithophores are covered with calcium carbonate plates
called ‘coccoliths,’ which are central to aggregation and ballasting, producing sinking velocities of
nearly 5 m/day [11,17]. Although it has been assumed that picophytoplankton, characterizing vast
oligotrophic areas of the ocean [27], do not contribute substantially to the particulate organic carbon
(POC) flux, Richardson and Jackson [34] suggested that all phytoplankton, including picoplankton
cells, contribute equally to POC export. They proposed alternative pathways for picoplankton carbon
cycling, which rely on aggregation as a mechanism for both direct sinking (the export of picoplankton as
POC) and mesozooplankton- or large filter feeder-mediated sinking of picoplankton-based production.
The biological pump is hypothesized to have played a significant role in atmospheric CO2
fluctuations during past glacial-interglacial periods and also responds to contemporary variations
in climate. However, it is not yet clear how the biological pump will respond to future global
changes in climate [21]. For such predictions to be reasonable, it is important to first decipher the
response of phytoplankton, one of the key components of the biological pump to future changes
in atmospheric CO2. Due to their phylogenetic diversity, different phytoplankton taxa will likely
respond to climate change in different ways [17]. For instance, a decrease in the abundance of diatom
is expected due to increased stratification in the future ocean [37]. Diatoms are highly efficient
in transporting carbon to depths by forming large, rapidly sinking aggregates and their reduced
numbers could in turn lead to decreased carbon export [11]. Also, decreased ocean pH due to ocean
acidification may thwart the ability of coccolithophores to generate calcareous plates, potentially
affecting the biological pump [17]; however, it appears that some species are more sensitive than
others [38]. Thus, future changes in the relative abundance of these or other phytoplankton taxa could
have a marked impact on total ocean productivity, subsequently affecting ocean biogeochemistry
and carbon storage. In a recent study, Jensen et al. [39] used species distribution modelling (SDM)
to predict the future global distribution of two phytoplankton species important to the biological
pump: the diatom Chaetoceros diadema and the coccolithophore Emiliania huxleyi. They employed
environmental data described in the Intergovernmental Panel on Climate Change’s Representative
Concentration Pathways scenario 8.5 (RCP 8.5), which predicts radiative forcing in the year 2100
relative to pre-industrial values. Their modelling results predicted that the total ocean area covered
by C. diadema and E. huxleyi would decline by 8% and 16%, respectively, under the examined climate
scenario. Furthermore, they suggested that the predicted changes in the range and distribution of these
two phytoplankton species under future ocean conditions, if realized, might result in their reduced
contribution to carbon sequestration via the biological pump.
Because phytoplankton growth depends on temperature and is also affected by competition for
light and nutrients, all of which change as atmospheric CO2 levels rise, predicting the response of
phytoplankton community structure to climate change is rather complicated [40]. In the next section,
we review literature to explore the effect of these concomitant changes on various parameters such as
phytoplankton species and elemental composition and cell size which play important role in regulating
the biological carbon pump.
3. Phytoplankton Responses to Global Change: Influence of Cell Size, Species and Elemental
Composition of Phytoplankton on the Biological Carbon Pump
Understanding the response of phytoplankton, the key mediators of the biological pump,
to changing environmental conditions is a prerequisite to predict future atmospheric concentrations of
CO2. Temperature, irradiance and nutrient concentrations, along with CO2 are the chief environmental
factors that influence the physiology and stoichiometry of phytoplankton [41]. The stoichiometry or
elemental composition of phytoplankton is of utmost importance to secondary producers such as
copepods, fish and shrimp, because it determines the nutritional quality and influences energy
6. Sustainability 2018, 10, 869 6 of 18
flow through the marine food chains [5]. Climate change may greatly restructure phytoplankton
communities leading to cascading consequences for marine food webs, thereby altering the amount of
carbon transported to the ocean interior [42].
Figure 3 gives an overview of the various environmental factors that together affect phytoplankton
productivity. All of these factors are expected to undergo significant changes in the future ocean due to
global change [4]. Global warming simulations predict oceanic temperature increase; dramatic changes
in oceanic stratification, circulation and changes in cloud cover and sea ice, resulting in an increased
light supply to the ocean surface. Also, reduced nutrient supply is predicted to co-occur with ocean
acidification and warming, due to increased stratification of the water column and reduced mixing of
nutrients from the deep water to the surface (Figure 1) [13].
3.1. pCO2
The Earth’s oceans are a major sink for anthropogenic CO2 and oceanic partial pressure of CO2
(pCO2) rises at nearly the same rate as atmospheric pCO2, thereby inducing changes in the seawater
carbonate system [11]. If CO2 emissions keep rising at current rates, it is predicted that the seawater
pCO2 would increase from the present value of ~400 to 800–1000 ppm by the year 2100 [43].
3.1.1. Ocean Carbonate System
Once dissolved, CO2 reacts with seawater to form carbonic acid (H2CO3). Oceans, however, store
CO2 as dissolved inorganic carbon (DIC), which remains as dissolved CO2 and H2CO3 (1%) and the
rest remains in the form of HCO3
− (~90%) and CO3
2− (~9%).Carbonic acid [H2CO3] is a weak acid
which dissociates into hydrogen ions [H+] and bicarbonate ions [HCO3
−]. The additional hydrogen
ions form bicarbonate ions by combining with carbonate ions [CO3
2−] [44]:
[CO2] + [H2O] → [H2CO3]
[H2CO3] → [H+
] + [HCO3
−
]
[H+
] + [CO3
2−
] → [HCO3
−
]
CO2 addition to seawater thus increases HCO3
−, which brings about a decline in the ocean pH
by increasing H+ concentration [44]. Such changes in carbonate chemistry are referred to as ocean
acidification, which has already led to a nearly 30% increase in seawater H+ [45] and is expected to
result in a mean pH drop from 8.2 to 7.8 by the year 2100 [43].
Sustainability 2017, 9, x FOR PEER REVIEW 6 of 17
phytoplankton communities leading to cascading consequences for marine food webs, thereby
altering the amount of carbon transported to the ocean interior [42].
Figure 3 gives an overview of the various environmental factors that together affect
phytoplankton productivity. All of these factors are expected to undergo significant changes in the
future ocean due to global change [4]. Global warming simulations predict oceanic temperature
increase; dramatic changes in oceanic stratification, circulation and changes in cloud cover and sea
ice, resulting in an increased light supply to the ocean surface. Also, reduced nutrient supply is
predicted to co-occur with ocean acidification and warming, due to increased stratification of the
water column and reduced mixing of nutrients from the deep water to the surface (Figure 1) [13].
3.1. pCO2
The Earth’s oceans are a major sink for anthropogenic CO2 and oceanic partial pressure of CO2
(pCO2) rises at nearly the same rate as atmospheric pCO2, thereby inducing changes in the seawater
carbonate system [11]. If CO2 emissions keep rising at current rates, it is predicted that the seawater
pCO2 would increase from the present value of ~400 to 800–1000 ppm by the year 2100 [43].
3.1.1. Ocean Carbonate System
Once dissolved, CO2 reacts with seawater to form carbonic acid (H2CO3). Oceans, however, store
CO2 as dissolved inorganic carbon (DIC), which remains as dissolved CO2 and H2CO3 (1%) and the
rest remains in the form of HCO3- (~90%) and CO32− (~9%).Carbonic acid [H2CO3] is a weak acid which
dissociates into hydrogen ions [H+] and bicarbonate ions [HCO3-]. The additional hydrogen ions form
bicarbonate ions by combining with carbonate ions [CO32−] [44]:
[CO2] + [H2O] → [H2CO3]
[H2CO3] → [H+] + [HCO3−]
[H+] + [CO32−] → [HCO3−]
CO2 addition to seawater thus increases HCO3−, which brings about a decline in the ocean pH
by increasing H+ concentration [44]. Such changes in carbonate chemistry are referred to as ocean
acidification, which has already led to a nearly 30% increase in seawater H+ [45] and is expected to
result in a mean pH drop from 8.2 to 7.8 by the year 2100 [43].
Figure 3. Overview of the various environmental factors that affect phytoplankton productivity
(adapted from ref. [46]).
3.1.2. Role of Phytoplankton CCM
Increased CO2 availability may benefit phytoplankton species, or they may be harmed by the
pH decrease depending on the species, other environmental conditions or other stressors [46]. Most
Figure 3. Overview of the various environmental factors that affect phytoplankton productivity
(adapted from ref. [46]).
7. Sustainability 2018, 10, 869 7 of 18
3.1.2. Role of Phytoplankton CCM
Increased CO2 availability may benefit phytoplankton species, or they may be harmed by
the pH decrease depending on the species, other environmental conditions or other stressors [46].
Most phytoplankton species possess an active uptake mechanism for inorganic carbon, utilizing CO2
and/or bicarbonate. Also, different species of phytoplankton have different requirements for inorganic
carbon due to variation in CO2 concentrating mechanisms (CCMs) in their cells [47]. CCMs increase
the concentration of CO2, surrounding the carboxylating enzyme Rubisco [43]. In the presence of
a CCM, the cell may remain carbon saturated, even when ambient CO2 levels are low. Thus, it is
difficult to predict the changes in photosynthetic rates of cells, which might increase (due to increased
availability of the substrate and/or less energy expenditure needed to operate the CCM), decrease
(due to adverse effects of low pH), or remain the same under ocean acidification scenario [46]. The shift
in CO2:HCO3
− ratio may benefit species able to utilize only CO2 by diffusive uptake. Such species
are far more likely to exhibit stimulation of growth and photosynthesis at increased oceanic pCO2,
as compared to species using HCO3
−, or taking up CO2 actively via a CCM [47]. Increased CO2
availability could potentially alter phytoplankton community composition by favoring taxa having
less efficient CCMs [43]. Ambient CO2 levels can be quite variable in marine ecosystems even in the
short-to mid-term [48]. Specific details of CCMs vary significantly among phytoplankton species.
Certain diatom species such as Skeletonema costatum possess the ability to form intense blooms due
to their capacity to overcome C limitation at high population densities using an efficient CCM [45].
An efficient CCM has also been observed in some marine bloom forming dinoflagellates such as
Prorocentrum minimum, Heterocapsa triquetra and Ceratium lineatum. [49]. Bloom dynamics are an
important aspect of phytoplankton ecology and toxin production by harmful algal blooms can affect
ecosystem services by altering food web dynamics [45]. Future elevated CO2 concentration can hinder
the population densities of such a bloom forming phytoplankton species.
3.1.3. Influence of Phytoplankton Cell Size
Cell size is a determining factor as to whether (and how) phytoplankton ultimately respond to
changes in pCO2 [50]. This is important because phytoplankton community composition strongly
determines the build-up of organic matter and its potential export to deeper layers. For instance, large
cells (e.g., diatoms) account for a large proportion of export production as compared to small cells (nano-
and pico-plankton), which are particularly important in regions with limited nutrient availability [51].
Taucher et al. [52], in their experiments with two marine diatoms, showed that the effect of CO2 was
more prominent for the large, chain-forming diatom—Dactyliosolen fragilissimus—than for the small
unicellular diatom, Thalassiosira weissflogii. Small cells have a larger surface area per unit volume than
large cells and therefore can support relatively more transporters on the cell surface that facilitates
diffusive uptake of CO2. In contrast, larger cells have lower surface-to-volume ratios and rely more
heavily on a CCM than on diffusive CO2 uptake [52]. In a study to quantify the effect of pCO2 on the
growth rate and elemental composition of five diatom species of varying diameters, Wu et al. [50]
showed that the largest CO2 growth enhancement occurred in the largest diatom species, with only
minor changes in the growth rate of small and medium sized diatom species. Thus, larger diatoms
may be more likely to be stimulated by future increases in pCO2. These findings are consistent with
the reports of Tortell et al. [53], who found a shift in phytoplankton community from small pennate
diatoms (Pseudo-nitzschia subcurvata) to large chain forming centric diatoms (Chaetoceros spp.) under
enhanced CO2. Because larger biomineralized phytoplankton are associated with increased and
more efficient carbon export rates [54], increased population size of larger diatoms may improve the
efficiency of the biological pump, due to increased carbon export to the deep ocean.
8. Sustainability 2018, 10, 869 8 of 18
3.1.4. Effect of Ocean Acidification on Coccolithophores
Among phytoplankton, coccolithophores with skeletal calcium carbonate structures are predicted
to be most strongly affected due to shift in carbonate chemistry [55]. They are primarily responsible for
creating and maintaining the ocean’s vertical gradient in seawater alkalinity. Upper ocean alkalinity
is directly affected by air/sea CO2 exchange, which is in turn modified by the formation of calcite
skeletons in the surface layer and their subsequent sinking to depth. Continued acidification of
surface seawater due to increased atmospheric CO2 levels changes the chemical conditions for biogenic
calcification, although the outcome for different coccolithophore species is difficult to predict [38,56,57].
For example, certain species and strains show dissolution of coccolith structure in response to
acidification while others appear more resistant to it [38,58]. Moreover, most strains calcify less
under higher CO2 conditions, consistent with observations from the fossil record that suggest more
heavily calcified cells were favored during times with reduced CO2 levels such as glacial maxima [59].
An overall reduction in pelagic calcification could lower the ratio of calcium carbonate to organic
carbon in the vertical flux of biogenic material (rain ratio). This, in turn, affects the air/sea CO2
exchange, resulting in an increase in the CO2 storage capacity of the upper ocean, constituting a
negative feedback to rising atmospheric CO2 [56].
3.2. Temperature
The mean global surface temperature across the planet has risen by 0.74 ◦C over the last century,
with accelerated rates of warming occurring in the last 50 years (0.13 ◦C per decade) [47]. Oceans absorb
more than 90% of the extra heat energy from climate warming, raising the temperature of the ocean,
particularly at high latitudes [16]. Ocean warming can affect biota directly, such as by affecting the
rates of biological processes, or indirectly, such as by increasing stratification, which in turn affects
nutrient supply and light availability to organisms in the mixed layers [47].
3.2.1. Influence of Ocean Warming on Phytoplankton Community Composition
Temperature affects phytoplankton physiology by controlling metabolic rates, such as the rate
and efficiency of enzymatic reactions. Elevated temperature can increase enzymatic turnover rates
(until a maximum rate is reached) through increased activity of thermally sensitive enzymes. However,
while higher temperatures can increase phytoplankton metabolism, each species has a temperature
maxima beyond which a sharp decline in metabolic efficiency occurs [16]. Thus, the response to ocean
warming is highly species-specific in phytoplankton [52]. Because the temperature range for optimal
growth is very narrow in some phytoplankton species, the predicted 2–3 ◦C rise in temperature [14]
might affect growth and metabolic activities in phytoplankton and thereby push poorly adapted
species beyond their optima. This could result in a shift in phytoplankton community composition in
addition to shifts in the latitudinal distribution of the given species [47]. Such changes in community
composition will likely affect the biological pump. However, it is worth mentioning that interspecific
competition is a key determinant of the relative abundance of a particular species. Thus, a species
may be most prevalent in an area where it does not grow under its optimum conditions. Additionally,
increased stratification of the ocean’s surface layer due to warming results in reduced nutrient input
from below. This might result in shifts in phytoplankton community composition, such as from
dominance by diatoms to coccolithophorids or from diatoms to cyanobacteria. Such shifts decrease
the trophic efficiency of marine food chains by reducing the export of particulate detrital food to
depth [21]. Other effects of ocean warming include a decrease in phytoplankton cell size, shifts in
phenology and alterations in phytoplankton carbon cycling [52]. Several studies predict a shift towards
smaller primary producers in a warmer ocean [55,60]. Flombaum et al. [61] assessed the present and
future global abundances of the picoplanktonic cyanobacteria, Prochlorococcus and Synechococcus, using
projections of sea surface temperature at the end of the 21st century. Their niche models suggested
an increase in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively, in the
9. Sustainability 2018, 10, 869 9 of 18
future ocean. A decline in mean cell size and numbers of larger diatoms due to ocean warming could
lead to poorer feeding conditions for copepod zooplankton, resulting in less efficient energy transfer
from primary to fish production [62].
3.2.2. Effects of Ocean Warming on Organic Matter Partitioning
As discussed in Section 2, export of particulate organic carbon (POC) is the chief determinant
of the efficiency of the biological carbon pump, while only a small percentage of dissolved organic
carbon (DOC) is sequestered in recalcitrant DOC molecules [22]. Ocean warming may reduce the
biological drawdown of dissolved inorganic carbon (DIC) in the surface layer, resulting in increased
accumulation of DOC, relative to POC, subsequently leading to reduced POC export flux through
the biological pump [21]. Using an indoor-mesocosm approach, Wohlers et al. [63], showed that
elevated temperature accelerates respiratory consumption of organic carbon relative to autotrophic
production in a natural plankton community. Thus, a temperature increase of 2–6 ◦C decreased the
biological drawdown of DIC in the surface layer by up to 31%, subsequently shifting the partitioning
of organic matter between the particulate and dissolved phase, with a greater fraction building up as
dissolved material. A similar mesocosm experiment by Kim et al. [22], also supported this observation.
Such changes in biogenic carbon flow might reduce the transfer of primary produced organic matter
to higher trophic levels, thereby weakening the biological carbon pump and providing a positive
feedback to rising atmospheric CO2 [63].
3.2.3. Effects of Ocean Warming on Phytoplankton Stoichiometry and TEP Production
Temperature is major determinant of stoichiometry in marine phytoplankton [64].
Yvon-Durocher et al. [64] used meta-analyses to demonstrate that variation in the N:P and C:P
ratios of marine algal assemblages were significantly related to the average sea-surface temperature.
They suggested that intracellular P was the primary factor that varied with temperature, because only
the N:P and C:P ratios showed temperature dependence, while the C:N ratio did not. They attributed
the observed rise in algal N:P and C:P ratios, with rising temperatures, to decline in cellular quotas of
P-rich assembly machinery (ribosomes), relative to N-rich light harvesting machinery (chloroplasts and
proteins), with increasing temperature. On the contrary, Martiny et al. [65], showed that thermal effect
leads to increased cellular quotas of nitrogen and carbon, whereas the cellular phosphorous quota
changes very little in the marine cyanobacterium, Prochlorococcus. Their results point towards other
physiological acclimation mechanisms as the principal drivers of elemental changes in Prochlorococcus.
They attributed the observed elemental changes to an increase in cell size, as the carbon and nitrogen
cell quota increased in tandem.
Ocean warming may enhance the formation of marine snow and other organic aggregates [21].
For instance, the aggregation of marine diatoms is enhanced at higher temperatures due to an
increase in the concentration of the surface-active carbohydrates—called transparent exopolymer
particles (TEP) [66]. TEP form abiotically from dissolved and colloidal exopolymer carbohydrates and
are abundant in marine ecosystems [67]. Increased TEP production at higher temperatures would
result in increased aggregation and faster sedimentation rates, thereby strengthening the biological
pump, while providing a negative feedback on increasing levels of atmospheric CO2 [21]. However,
Wohlers et al. [63] observed a decrease in particulate matter concentration with increased TEP levels
at rising temperatures, thus limiting the potential for TEP-mediated particle export. They suggested
that the extent to which enhanced TEP production could affect particle sinking under ocean warming
critically depends on the timing of TEP production along with the interplay with other biological
processes such as microbial degradation and grazing.
3.3. Irradiance
In addition to causing acidification and warming of the ocean, global climate change also affects
the penetration of light into the water column. As the euphotic layer shoals due to increased thermal
10. Sustainability 2018, 10, 869 10 of 18
stratification, phytoplankton will be concentrated closer to the surface where irradiance levels are
higher. Additionally, penetration of photosynthetically active radiation (PAR, 400–700 nm), UV-B
(280–315 nm) and UV-A (315–400 nm) radiation through surface waters would increase due to changes
in cloud cover and levels of dissolved organic matter [68]. Enhanced stratification of the ocean, due to
future changes in the climate, will intensify photodegradation of the colored part of dissolved inorganic
matter (CDOM), which controls the penetration of UV radiation into water bodies. The resultant
increase in transparency of the water column may increase the mean irradiance exposures and UV-B
effects on organisms inhabiting the surface layer [69,70].
Aquatic primary producers like marine phytoplankton dwell in the surface layers in order to
harvest sufficient solar radiation for photosynthesis [46]. Different species have different optimal
irradiances at which photosynthetic efficiency is optimal; however, photosynthetic plasticity allows
cells to grow over a broader range of light levels. These include acclimation strategies such as synthesis
or degradation of photosynthetic antennae, non-photochemical quenching, state transitions, activation
of alternative electron pathways and sinks and other processes [71–76]. The ability of cells to cope
with higher light levels depends on their irradiance optima and the acclimation strategies they employ,
both of which can vary even within a species. For example, different strains of Synechococcus fall along
a light preference continuum that ranges from low light to high light optimized [77]. Strains that are
able to cope under higher light may come to outcompete less tolerant strains under future conditions
if they are better able to avoid photoinhibition, which requires energy to repair.
Effects of UV-B Radiation
UV-B radiation can have several deleterious effects on marine primary producers: UV-B breaks
proteins and cell membranes, interferes with enzymatic reactions, impairs motility and orientation and
induces lesions in DNA (such as the formation of cyclobutane pyrimidine dimers) [46]. UV-B radiation
can also impair accessory pigments, which funnel solar energy to the reaction centers during
photosynthesis, thus inhibiting photosynthesis and growth [46,78]. However, the effects of UV
radiation on phytoplankton growth rates are species specific; thus, increased UV radiation could induce
changes in phytoplankton community structure [78]. For instance, Villafane et al. [79] investigated
the effects of solar UV radiation on the photosynthetic rates of natural assemblages of Antarctic
phytoplankton and observed an increase in diatom numbers at the expense of flagellates.
Phytoplankton employ several mechanisms to avoid damage from UV radiation. Some of these
include: active vertical migration using flagella or changes in buoyancy so as to move out of zones of
excessive irradiance [80,81]; production of photolyase enzymes to repair UV-damaged DNA [82] and
superoxide dismutase enzymes to prevent oxidative stress [83]; synthesis of UV absorbing pigments
such as scytonemin (produced by cyanobacteria to reduce the impact of UV); and production of
UV screening compounds such as mycosporine-like amino acids (MAAs) [46]. Different species of
phytoplankton have varying capacities to produce UV screening compounds and thus, enhanced
levels of UV-B radiation can potentially result in changes in species dominance within phytoplankton
communities. For instance, the bloom-forming species, Phaeocystis pouchetti, commonly present in
polar waters, produces high levels of MAAs and therefore could have a competitive advantage over
non-bloom forming phytoplankton species in the future. The dense, mucilaginous P. pouchetii blooms
could impact the consumption of this species by herbivores, subsequently affecting other trophic
levels [47]. Thus, UV-B radiation can have profound effects on trophic flow in marine ecosystems,
thereafter affecting the biological pump [78].
In contrast to a decrease in the population of phytoplankton with larger cell size due to ocean
warming, enhanced UV radiation is expected to facilitate the growth of large phytoplankton cells,
due to an increased path length for UV radiation absorption in large cells [78]. This can in turn favor
phytoplankton communities with larger cells, as observed for benthic diatoms [84]. Thus, the biological
pump, driven primarily by phytoplankton in the open ocean, is limited by the quality and quantity of
the solar spectrum reaching the ocean surface [68].
11. Sustainability 2018, 10, 869 11 of 18
3.4. Nutrients
The availability of nutrients like nitrogen, phosphorous and iron limits the productivity of marine
phytoplankton in the euphotic zone. The reduction in thickness of the upper mixed layer of oceans due
to thermal stratification decreases nutrient availability due to reduced upward transport of nutrients
from deeper layers [46].
Decreased availability of nitrogen leads to decreased chlorophyll and protein synthesis in
phytoplankton cells [85]. In addition, nitrogen limitation can affect carbon fixation because of its
potential effects on the levels of the carboxylating enzyme, Rubisco [5]. Therefore, reduced nutrient
availability may lead to a decline in primary productivity, thereby reducing the potential export flux
through the biological pump [21].
3.4.1. Influence of Phytoplankton Nutritional Quality on Higher Trophic Levels
Phytoplankton comprises the base of the marine food web providing organic matter (carbon,
nitrogen and phosphorous) to higher trophic levels. Thus, changes in nutritional quality of marine
phytoplankton (higher C:P or C:N), could lead to reduced growth rates and fecundity at higher
trophic levels, thereafter affecting the biological pump [43]. In their studies with the diatom,
Phaeodactylum tricornutum, Li et al. [5] found the highest C:N in the cells that had been cultured
under high CO2/low nitrogen conditions, which are expected to dominate the open ocean in the
near future. These synergistic effects of ocean acidification and nitrogen limitation can therefore
decrease the nutritional quality of marine phytoplankton, thus influencing secondary producers
and predators at higher levels [5]. For instance, the trophic transfer, assimilation and retention of
key nutrients contained within phytoplankton is critical for the optimal physiological functioning of
marine metazoans [43]. Large zooplankton are mainly responsible for the transfer of POC to metazoans,
through fecal pellets and vertically migrating animals. However, although zooplankton fecal pellets
are an important component of the biological carbon pump, much of the vertical flux of carbon is
attributed to marine snow and sedimenting phytoplankton blooms that sink to the benthos without
any significant contribution to pelagic food webs [21].
3.4.2. Effects on Phytoplankton Community Composition
Decreased nitrogen supply may also promote shifts in phytoplankton community composition by
making competition for nutrients more pronounced [21,47]. Phytoplankton species possessing higher
nutrient uptake efficiencies will have a competitive advantage. Diatoms, which have large cells and
high nutrient requirements, are expected to be more strongly affected by reduced nutrient levels in
the future [47]. In their simulations, Bopp et al. [37] showed that nutrient-depleted conditions in the
surface ocean favors small phytoplankton at the expense of diatoms. Similar observations were made
by Marinov et al. [40], who found a decline in diatom biomass, growth rate and abundance, with a
decrease in nitrate supply over large areas in the Indian and Atlantic Ocean. Cermeno et al. [86], in their
analysis of phytoplankton community composition in the Atlantic Ocean, found that the dominance of
coccolithophorids rises rapidly relative to diatoms as the water column stratifies. Such alterations in
phytoplankton community composition, particularly towards reduced phytoplankton cell sizes will
lower storage of sinking particulate organic matter by the ocean’s biological pump [8]. This can lead
to reduced efficiency of the biological pump in sequestering atmospheric CO2, implying a positive
feedback between climate change and the ocean carbon cycle [37]. Contrary to the above observations,
Kemp and Villareal [87] showed that diatom production and the associated export of organic carbon
might actually increase with higher thermal stratification and potentially act as a negative feedback
to climate change. Their investigation showed that some diatoms, such as the diazotroph-associated
diatom Hemiaulus hauckii, possess adaptations to stratified waters including the ability to grow in low
light conditions, vertical migrations between nutricline depths and the surface and symbioses with
nitrogen-fixing cyanobacteria. Such adaptations facilitate the maintenance of diatom seed populations
12. Sustainability 2018, 10, 869 12 of 18
that may then exploit mixing events even in oligotrophic oceanic waters. Formation of aggregates by
such diatoms promotes rapid settling, subsequently enhancing the export flux of carbon to depths.
3.4.3. Effects of Stratification on Coastal Upwelling Regions
Coastal upwelling regions such as those located along the eastern boundaries of the Pacific and
Atlantic Ocean basins, make a major contribution to the productivity of the ocean [88]. Changes in
ocean circulation and stratification are predicted to increase the flux of nitrate during upwelling events
in these regions [89]. Rykaczewski et al. [90], in their studies of the California Current Ecosystem,
attributed the increased nitrate flux to decreased ventilation of the Pacific Ocean and the associated
accumulation of nitrate in deep waters. A series of incubation experiments in coastal California showed
that increased nitrate availability relative to iron favored slower sinking single-celled diatoms over
faster sinking chain-forming diatoms [89]. Hence, changing nutrient supply ratios have the potential
to affect trophic structure and the biological carbon and silicate pumps in coastal upwelling regions by
shifting the chain forming behavior of phytoplankton.
3.4.4. Trace Metal Micronutrient Availability
The effect of climate change on the availability of trace metal micronutrients like iron is an area of
research that is rapidly expanding. The mesocosm experiments of Breitbarth et al. [91] indicated that
ocean acidification may result in increased iron bioavailability due to an enhanced fraction of dissolved
iron and elevated Fe (II) concentrations in coastal systems, fueling increased phytoplankton carbon
acquisition and export. However, it has also been proposed that ocean acidification could decrease
Fe availability by stabilizing Fe ligands, leading to lower Fe uptake rates by phytoplankton [92].
Ocean acidification is expected to affect the redox speciation of copper, yielding an enhanced Cu (I)
fraction. However, the biological implications thereof are largely unknown [93]. Iron limits productivity
in approximately 30% of the world’s oceans [94,95] and drives the evolution of phytoplankton
photosynthetic traits [96], hence factors that affect iron supply and recycling rates will directly
affect the biological pump and phytoplankton adaptation potential. The main source of iron to
the ocean is via atmospheric transport and deposition of terrigenous and anthropogenic aerosol
particles. Potential expansion of desert regions could increase the flux of aerosol iron in certain areas
of the ocean and shift the patterns of nutrient limitation. Supply of aerosol metals has been shown to
cause changes in phytoplankton community structure in numerous incubation experiments [97,98],
which in turn has the potential to alter productivity and export rates.
4. Conclusions and Future Directions
The ocean is among the largest reservoirs of carbon on Earth; hence, quantifying the efficiency of
the biological carbon pump in the face of climate change is a prerequisite to predict future atmospheric
CO2 concentrations. It is evident from literature reports that the strength of the biological pump
will likely change in the future ocean, in response to a changing climate. However, predicting the
direction of such change is difficult owing to the complexity of the problem. Numerous contrasts
arise from comparisons of different geographical areas, ecosystems, environmental conditions and
organisms. For instance, larger phytoplankton such as diatoms are likely to be stimulated under future
elevated CO2 and light levels, resulting in increased carbon export to the deep ocean. On the other
hand, ocean warming and future nutrient-depleted conditions would favor the growth of smaller
phytoplankton, such as picoplanktonic cyanobacteria, leading to reduced efficiency of the biological
pump. This makes it difficult to currently predict whether the biological pump will strengthen or
weaken in the next 100 years. Moreover, the simultaneous alterations of oceanic carbonate system,
temperature, light and nutrient availability due to global change will vary in different regions of the
ocean [21] and may have synergistic or antagonistic effects on phytoplankton. Because the efficiency
of the biological pump is a function of phytoplankton physiology and community structure, it is
important to understand how concurrent multiple stressors (including changes in temperature, light
13. Sustainability 2018, 10, 869 13 of 18
intensity, nutrients and CO2 levels) affect growth rates and competition between phytoplankton
species [45]. This further increases complexity, because the number of treatment combinations grows
exponentially with each added stressor [99]. To date, few studies have probed the combined effects of
CO2, temperature and nutrient levels on phytoplankton. Most of them have focused on nitrogen fixing
cyanobacteria because the factors that drive their abundance are already known and well characterized.
These experiments identified many interactive effects, including the unexpected finding that while
enhanced CO2 generally increases N2 fixation under nutrient replete conditions, it actually decreases
fixation when iron is limiting [100]. Future studies should evaluate multiple species and strains of
phytoplankton and incorporate multiple stressor treatments to understand the full range of potential
effects [99]. Also, the complexity of the role that the marine food web plays in the biological pump
and its high spatial and temporal variability makes global generalizations difficult [11]. Future studies
should address this issue along with the effects of interspecies activities such as competition and
predation loss on the biological carbon pump.
An additional limitation at present is that majority of the ocean acidification studies have
investigated responses in phytoplankton cells acclimated to changing environmental conditions over
time scales too short for evolution to produce major changes [45]. Using a global marine ecosystem
model, Dutkiewicz et al. [101] suggested that longer timescales of competition- and transport-mediated
adjustments are necessary for predicting the changes to the phytoplankton community structure.
In addition, experimental evolution with cultured phytoplankton is an important next step in predicting
how major phytoplankton taxa will respond to climate change [17,45]. Such studies are in turn essential
to gain insight on the biological carbon pump and the ability of the ocean to act as a long-term sink for
atmospheric CO2.
Acknowledgments: The authors thank three anonymous reviewers for their comments on the manuscript.
This work was supported by a Clare Boothe Luce endowment, an Alfred P Sloan Research Fellowship in Ocean
Sciences and the Marion Milligan Mason Award for Women in the Chemical Sciences from AAAS to KRMM.
Author Contributions: Samarpita Basu and Katherine R. M. Mackey conceived of the topic and jointly contributed
to the writing and editing of the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Baumert, H.Z.; Petzoldt, T. The role of temperature, cellular quota and nutrient concentrations for
photosynthesis, growth and light-dark acclimation in phytoplankton. Limnologica 2008, 38, 313–326.
[CrossRef]
2. Simon, N.; Cras, A.-L.; Foulon, E.; Lemée, R. Diversity and evolution of marine phytoplankton. C. R. Biol.
2009, 332, 159–170. [CrossRef] [PubMed]
3. Lam, M.K.; Lee, K.T.; Mohamed, A.R. Current status and challenges on microalgae-based carbon capture.
Int. J. Greenh. Gas Control 2012, 10, 456–469. [CrossRef]
4. Hader, D.P.; Villafane, V.E.; Helbling, E.W. Productivity of aquatic primary producers under global climate
change. Photochem. Photobiol. Sci. 2014, 13, 1370–1392. [CrossRef] [PubMed]
5. Li, W.; Gao, K.S.; Beardall, J. Interactive effects of ocean acidification and nitrogen-limitation on the diatom
phaeodactylum tricornutum. PLoS ONE 2012, 7, e51590. [CrossRef] [PubMed]
6. Hulse, D.; Arndt, S.; Wilson, J.D.; Munhoven, G.; Ridgwell, A. Understanding the causes and consequences
of past marine carbon cycling variability through models. Earth-Sci. Rev. 2017, 171, 349–382. [CrossRef]
7. Chisholm, S.W. The iron hypothesis: Basic research meets environmental policy. Rev. Geophys. 1995, 33,
1277–1286. [CrossRef]
8. Hutchins, D.A.; Fu, F. Microorganisms and ocean global change. Nat. Microbiol. 2017, 2, 17058. [CrossRef]
[PubMed]
9. Sanders, R.; Henson, S.A.; Koski, M.; De la Rocha, C.L.; Painter, S.C.; Poulton, A.J.; Riley, J.; Salihoglu, B.;
Visser, A.; Yool, A.; et al. The biological carbon pump in the north Atlantic. Prog. Oceanogr. 2014, 129, 200–218.
[CrossRef]
14. Sustainability 2018, 10, 869 14 of 18
10. Boyd, P.W. Toward quantifying the response of the oceans’ biological pump to climate change. Front. Mar. Sci.
2015, 2. [CrossRef]
11. Passow, U.; Carlson, C.A. The biological pump in a high CO2 world. Mar. Ecol. Prog. Ser. 2012, 470, 249–271.
[CrossRef]
12. Bhadury, P. Effects of ocean acidification on marine invertebrates—A review. Indian J. Geo-Mar. Sci. 2015, 44,
454–464.
13. Sarmiento, J.L.; Slater, R.; Barber, R.; Bopp, L.; Doney, S.C.; Hirst, A.C.; Kleypas, J.; Matear, R.;
Mikolajewicz, U.; Monfray, P.; et al. Response of ocean ecosystems to climate warming. Glob. Biogeochem. Cycle
2004, 18. [CrossRef]
14. Pachauri, R.K.; Reisinger, A. Climate Change 2007 Synthesis Report Contribution of Working Groups I, II and III to
the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Intergovernmental Panel on
Climate Change (IPCC): Geneva, Switzerland, 2007.
15. Riebesell, U.; Schulz, K.G.; Bellerby, R.G.; Botros, M.; Fritsche, P.; Meyerhofer, M.; Neill, C.; Nondal, G.;
Oschlies, A.; Wohlers, J.; et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 2007,
450, 545–548. [CrossRef] [PubMed]
16. Petrou, K.; Kranz, S.A.; Trimborn, S.; Hassler, C.S.; Ameijeiras, S.B.; Sackett, O.; Ralph, P.J.; Davidson, A.T.
Southern ocean phytoplankton physiology in a changing climate. J. Plant Physiol. 2016, 203, 135–150.
[CrossRef] [PubMed]
17. Collins, S.; Rost, B.; Rynearson, T.A. Evolutionary potential of marine phytoplankton under ocean
acidification. Evolut. Appl. 2014, 7, 140–155. [CrossRef] [PubMed]
18. Finkel, Z.V.; Beardall, J.; Flynn, K.J.; Quigg, A.; Rees, T.A.V.; Raven, J.A. Phytoplankton in a changing world:
Cell size and elemental stoichiometry. J. Plankton Res. 2010, 32, 119–137. [CrossRef]
19. Bishop, J.K.B. Autonomous observations of the ocean biological carbon pump. Oceanography 2009, 22,
182–193. [CrossRef]
20. Falkowski, P.; Scholes, R.J.; Boyle, E.; Canadell, J.; Canfield, D.; Elser, J.; Gruber, N.; Hibbard, K.; Hogberg, P.;
Linder, S.; et al. The global carbon cycle: A test of our knowledge of earth as a system. Science 2000, 290,
291–296. [CrossRef] [PubMed]
21. Turner, J.T. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump.
Prog. Oceanogr. 2015, 130, 205–248. [CrossRef]
22. Kim, J.M.; Lee, K.; Shin, K.; Yang, E.J.; Engel, A.; Karl, D.M.; Kim, H.C. Shifts in biogenic carbon flow from
particulate to dissolved forms under high carbon dioxide and warm ocean conditions. Geophys. Res. Lett.
2011, 38. [CrossRef]
23. Hansell, D.A.; Carlson, C.A.; Repeta, D.J.; Schlitzer, R. Dissolved organic matter in the ocean a controversy
stimulates new insights. Oceanography 2009, 22, 202–211. [CrossRef]
24. Carlson, C.A.; Ducklow, H.W.; Michaels, A.F. Annual flux of dissolved organic-carbon from the euphotic
zone in the northwestern Sargasso Sea. Nature 1994, 371, 405–408. [CrossRef]
25. Roshan, S.; DeVries, T. Efficient dissolved organic carbon production and export in the oligotrophic ocean.
Nat. Commun. 2017, 8, 2036. [CrossRef] [PubMed]
26. Buesseler, K.O.; Boyd, P.W. Shedding light on processes that control particle export and flux attenuation in
the twilight zone of the open ocean. Limnol. Oceanogr. 2009, 54, 1210–1232. [CrossRef]
27. Herndl, G.J.; Reinthaler, T. Microbial control of the dark end of the biological pump. Nat. Geosci. 2013, 6,
718–724. [CrossRef] [PubMed]
28. Hofmann, M.; Schellnhuber, H.J. Oceanic acidification affects marine carbon pump and triggers extended
marine oxygen holes. Proc. Natl. Acad. Sci. USA 2009, 106, 3017–3022. [CrossRef] [PubMed]
29. Ducklow, H.W.; Steinberg, D.K.; Buesseler, K.O. Upper ocean carbon export and the biological pump.
Oceanography 2001, 14. [CrossRef]
30. De La Rocha, C.L.; Passow, U. Factors influencing the sinking of POC and the efficiency of the biological
carbon pump. Deep Sea Res. Part II Top. Stud. Oceanogr. 2007, 54, 639–658. [CrossRef]
31. Armstrong, R.A.; Lee, C.; Hedges, J.I.; Honjo, S.; Wakeham, S.G. A new, mechanistic model for organic
carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep Sea Res.
Part II Top. Stud. Oceanogr. 2001, 49, 219–236. [CrossRef]
32. Sato, R.; Tanaka, Y.; Ishimaru, T. Species-specific house productivity of appendicularians. Mar. Ecol. Prog. Ser.
2003, 259, 163–172. [CrossRef]
15. Sustainability 2018, 10, 869 15 of 18
33. Nishibe, Y.; Takahashi, K.; Ichikawa, T.; Hidaka, K.; Kurogi, H.; Segawa, K.; Saito, H. Degradation of
discarded appendicularian houses by oncaeid copepods. Limnol. Oceanogr. 2015, 60, 967–976. [CrossRef]
34. Richardson, T.L.; Jackson, G.A. Small phytoplankton and carbon export from the surface ocean. Science 2007,
315, 838–840. [CrossRef] [PubMed]
35. Ragueneau, O.; Schultes, S.; Bidle, K.; Claquin, P.; Moriceau, B. Si and c interactions in the world ocean:
Importance of ecological processes and implications for the role of diatoms in the biological pump.
Glob. Biogeochem. Cycle 2006, 20. [CrossRef]
36. Miklasz, K.A.; Denny, M.W. Diatom sinking speeds: Improved predictions and insight from a modified
stokes’ law. Limnol. Oceanogr. 2010, 55, 2513–2525. [CrossRef]
37. Bopp, L.; Aumont, O.; Cadule, P.; Alvain, S.; Gehlen, M. Response of diatoms distribution to global warming
and potential implications: A global model study. Geophys. Res. Lett. 2005, 32. [CrossRef]
38. Iglesias-Rodriguez, M.D.; Halloran, P.R.; Rickaby, R.E.M.; Hall, I.R.; Colmenero-Hidalgo, E.; Gittins, J.R.;
Green, D.R.H.; Tyrrell, T.; Gibbs, S.J.; von Dassow, P.; et al. Phytoplankton calcification in a high-CO2 world.
Science 2008, 320, 336–340. [CrossRef] [PubMed]
39. Jensen, L.O.; Mousing, E.A.; Richardson, K. Using species distribution modelling to predict future
distributions of phytoplankton: Case study using species important for the biological pump.
Mar. Ecol.-Evol. Perspect. 2017, 38, e12427. [CrossRef]
40. Marinov, I.; Doney, S.C.; Lima, I.D. Response of ocean phytoplankton community structure to climate change
over the 21st century: Partitioning the effects of nutrients, temperature and light. Biogeosciences 2010, 7,
3941–3959. [CrossRef]
41. Moreno, A.R.; Hagstrom, G.I.; Primeau, F.W.; Levin, S.A.; Martiny, A.C. Marine phytoplankton
stoichiometry mediates nonlinear interactions between nutrient supply, temperature, and atmospheric
CO2. Biogeosci. Discuss. 2017, 2017, 1–28. [CrossRef]
42. Irwin, A.J.; Finkel, Z.V.; Muller-Karger, F.E.; Ghinaglia, L.T. Phytoplankton adapt to changing ocean
environments. Proc. Natl. Acad. Sci. USA 2015, 112, 5762–5766. [CrossRef] [PubMed]
43. King, A.L.; Jenkins, B.D.; Wallace, J.R.; Liu, Y.; Wikfors, G.H.; Milke, L.M.; Meseck, S.L. Effects of CO2 on
growth rate, C:N:P, and fatty acid composition of seven marine phytoplankton species. Mar. Ecol. Prog. Ser.
2015, 537, 59–69. [CrossRef]
44. Das, S.; Mangwani, N. Ocean acidification and marine microorganisms: Responses and consequences.
Oceanologia 2015, 57, 349–361. [CrossRef]
45. Mackey, K.R.M.; Morris, J.J.; Morel, F.M.M.; Kranz, S.A. Response of photosynthesis to ocean acidification.
Oceanography 2015, 28, 74–91. [CrossRef]
46. Häder, D.-P.; Gao, K. Interactions of anthropogenic stress factors on marine phytoplankton. Front. Environ. Sci.
2015, 3. [CrossRef]
47. Beardall, J.; Stojkovic, S.; Larsen, S. Living in a high CO2 world: Impacts of global climate change on marine
phytoplankton. Plant Ecol. Divers. 2009, 2, 191–205. [CrossRef]
48. Mercado, J.M.; Gordillo, F.J.L. Inorganic carbon acquisition in algal communities: Are the laboratory data
relevant to the natural ecosystems? Photosynth. Res. 2011, 109, 257–267. [CrossRef] [PubMed]
49. Rost, B.; Richter, K.U.; Riebesell, U.; Hansen, P.J. Inorganic carbon acquisition in red tide dinoflagellates.
Plant Cell Environ. 2006, 29, 810–822. [CrossRef] [PubMed]
50. Wu, Y.; Campbell, D.A.; Irwin, A.J.; Suggett, D.J.; Finkel, Z.V. Ocean acidification enhances the growth rate
of larger diatoms. Limnol. Oceanogr. 2014, 59, 1027–1034. [CrossRef]
51. Gazeau, F.; Salon, A.; Pitta, P.; Tsiola, A.; Maugendre, L.; Giani, M.; Celussi, M.; Pedrotti, M.L.; Marro, S.;
Guieu, C. Limited impact of ocean acidification on phytoplankton community structure and carbon export
in an oligotrophic environment: Results from two short-term mesocosm studies in the mediterranean sea.
Estuar. Coast. Shelf Sci. 2017, 186, 72–88. [CrossRef]
52. Taucher, J.; Jones, J.; James, A.; Brzezinski, M.A.; Carlson, C.A.; Riebesell, U.; Passow, U. Combined effects of
CO2 and temperature on carbon uptake and partitioning by the marine diatoms thalassiosira weissflogii and
dactyliosolen fragilissimus. Limnol. Oceanogr. 2015, 60, 901–919. [CrossRef]
53. Tortell, P.D.; Payne, C.D.; Li, Y.; Trimborn, S.; Rost, B.; Smith, W.O.; Riesselman, C.; Dunbar, R.B.; Sedwick, P.;
DiTullio, G.R. CO2 sensitivity of southern ocean phytoplankton. Geophys. Res. Lett. 2008, 35, L04605.
[CrossRef]
16. Sustainability 2018, 10, 869 16 of 18
54. Fischer, G.; Karaka¸s, G. Sinking rates and ballast composition of particles in the Atlantic Ocean: Implications
for the organic carbon fluxes to the deep ocean. Biogeosciences 2009, 6, 85–102. [CrossRef]
55. Sommer, U.; Paul, C.; Moustaka-Gouni, M. Warming and ocean acidification effects on phytoplankton-from
species shifts to size shifts within species in a mesocosm experiment. PLoS ONE 2015, 10. [CrossRef]
[PubMed]
56. Rost, B.; Riebesell, U. Coccolithophores and the biological pump: Responses to environmental changes.
In Coccolithophores: From Molecular Processes to Global Impact; Springer: Berlin/Heidelberg, Germany, 2004;
pp. 99–125.
57. Fabry, V.J. Ocean science. Marine calcifiers in a high-CO2 ocean. Science 2008, 320, 1020–1022. [CrossRef]
[PubMed]
58. O’dea, S.A.; Gibbs, S.J.; Bown, P.R.; Young, J.R.; Poulton, A.J.; Newsam, C.; Wilson, P.A. Coccolithophore
calcification response to past ocean acidification and climate change. Nat. Commun. 2014, 5. [CrossRef]
[PubMed]
59. Beaufort, L.; Probert, I.; de Garidel-Thoron, T.; Bendif, E.M.; Ruiz-Pino, D.; Metzl, N.; Goyet, C.; Buchet, N.;
Coupel, P.; Grelaud, M.; et al. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification.
Nature 2011, 476, 80–83. [CrossRef] [PubMed]
60. Moran, X.A.G.; Lopez-Urrutia, A.; Calvo-Diaz, A.; Li, W.K.W. Increasing importance of small phytoplankton
in a warmer ocean. Glob. Chang. Biol. 2010, 16, 1137–1144. [CrossRef]
61. Flombaum, P.; Gallegos, J.L.; Gordillo, R.A.; Rincon, J.; Zabala, L.L.; Jiao, N.A.Z.; Karl, D.M.; Li, W.K.W.;
Lomas, M.W.; Veneziano, D.; et al. Present and future global distributions of the marine cyanobacteria
prochlorococcus and synechococcus. Proc. Natl. Acad. Sci. USA 2013, 110, 9824–9829. [CrossRef] [PubMed]
62. Sommer, U.; Lengfellner, K. Climate change and the timing, magnitude, and composition of the
phytoplankton spring bloom. Glob. Chang. Biol. 2008, 14, 1199–1208. [CrossRef]
63. Wohlers, J.; Engel, A.; Zollner, E.; Breithaupt, P.; Jurgens, K.; Hoppe, H.G.; Sommer, U.; Riebesell, U. Changes
in biogenic carbon flow in response to sea surface warming. Proc. Natl. Acad. Sci. USA 2009, 106, 7067–7072.
[CrossRef] [PubMed]
64. Yvon-Durocher, G.; Dossena, M.; Trimmer, M.; Woodward, G.; Allen, A.P. Temperature and the biogeography
of algal stoichiometry. Glob. Ecol. Biogeogr. 2015, 24, 562–570. [CrossRef]
65. Martiny, A.C.; Ma, L.Y.; Mouginot, C.; Chandler, J.W.; Zinser, E.R. Interactions between thermal acclimation,
growth rate, and phylogeny influence Prochlorococcus elemental stoichiometry. PLoS ONE 2016, 11. [CrossRef]
[PubMed]
66. Piontek, J.; Handel, N.; Langer, G.; Wohlers, J.; Riebesell, U.; Engel, A. Effects of rising temperature on the
formation and microbial degradation of marine diatom aggregates. Aquat. Microb. Ecol. 2009, 54, 305–318.
[CrossRef]
67. Engel, A. Direct relationship between CO2 uptake and transparent exopolymer particles production in
natural phytoplankton. J. Plankton Res. 2002, 24, 49–53. [CrossRef]
68. Beardall, J.; Sobrino, C.; Stojkovic, S. Interactions between the impacts of ultraviolet radiation, elevated
CO2, and nutrient limitation on marine primary producers. Photochem. Photobiol. Sci. 2009, 8, 1257–1265.
[CrossRef] [PubMed]
69. Zepp, R.G.; Erickson, D.J., III; Paul, N.D.; Sulzberger, B. Interactive effects of solar UV radiation and climate
change on biogeochemical cycling. Photochem. Photobiol. Sci. 2007, 6, 286–300. [CrossRef] [PubMed]
70. Caron, D.A.; Hutchins, D.A. The effects of changing climate on microzooplankton grazing and community
structure: Drivers, predictions and knowledge gaps. J. Plankton Res. 2013, 35, 235–252. [CrossRef]
71. Bibby, T.S.; Mary, I.; Nield, J.; Partensky, F.; Barber, J. Low-light-adapted Prochlorococcus species possess
specific antennae for each photosystem. Nature 2003, 424, 1051–1054. [CrossRef] [PubMed]
72. Kirilovsky, D.; Kerfeld, C.A. The orange carotenoid protein in photoprotection of photosystem II in
cyanobacteria. Biochim. Biophys. Acta 2012, 1817, 158–166. [CrossRef] [PubMed]
73. Biggins, J.; Bruce, D. Regulation of excitation-energy transfer in organisms containing phycobilins.
Photosynth. Res. 1989, 20, 1–34. [CrossRef] [PubMed]
74. Mackey, K.R.M.; Paytan, A.; Grossman, A.R.; Bailey, S. A photosynthetic strategy for coping in a high-light,
low-nutrient environment. Limnol. Oceanogr. 2008, 53, 900–913. [CrossRef]
75. Bailey, S.; Grossman, A. Photoprotection in cyanobacteria: Regulation of light harvesting. Photochem. Photobiol.
2008, 84, 1410–1420. [CrossRef] [PubMed]
17. Sustainability 2018, 10, 869 17 of 18
76. Bibby, T.S.; Nield, J.; Barber, J. Iron deficiency induces the formation of an antenna ring around trimeric
photosystem I in cyanobacteria. Nature 2001, 412, 743–745. [CrossRef] [PubMed]
77. Mackey, K.R.M.; Post, A.F.; McIlvin, M.R.; Saito, M.A. Physiological and proteomic characterization of light
adaptations in marine synechococcus. Environ. Microbiol. 2017, 19, 2348–2365. [CrossRef] [PubMed]
78. Beardall, J.; Stojkovic, S. Microalgae under global environmental change: Implications for growth and
productivity, populations and trophic flow. ScienceAsia 2006, 32, 1–10. [CrossRef]
79. Villafane, V.E.; Helbling, E.W.; HolmHansen, O.; Chalker, B.E. Acclimatization of Antarctic natural
phytoplankton assemblages when exposed to solar ultraviolet radiation. J. Plankton Res. 1995, 17, 2295–2306.
[CrossRef]
80. Overmann, J.; Pfennig, N. Bouyancy regulation and aggregate formation in Amoebobacter purpureus from
Mahoney Lake. FEMS Microbiol. Lett. 1992, 101, 67–79. [CrossRef]
81. Ma, Z.L.; Gao, K.S. Photosynthetically active and UV radiation act in an antagonistic way in regulating
buoyancy of Arthrospira (Spirulina) platensis (cyanobacterium). Environ. Exp. Bot. 2009, 66, 265–269. [CrossRef]
82. Ng, W.O.; Zentella, R.; Wang, Y.S.; Taylor, J.S.A.; Pakrasi, H.B. PhrA, the major photoreactivating factor in
the cyanobacterium Synechocystis sp. strain PCC 6803 codes for a cyclobutane-pyrimidine-dimer-specific
DNA photolyase. Arch. Microbiol. 2000, 173, 412–417. [CrossRef] [PubMed]
83. Wolfe-Simon, F.; Grzebyk, D.; Schofield, O.; Falkowski, P.G. The role and evolution of superoxide dismutases
in algae. J. Phycol. 2005, 41, 453–465. [CrossRef]
84. Bothwell, M.L.; Sherbot, D.; Roberge, A.C.; Daley, R.J. Influence of natural ultraviolet-radiation on lotic
periphytic diatom community growth, biomass accrual, and species composition: Short-term versus
long-term effects. J. Phycol. 1993, 29, 24–35. [CrossRef]
85. Hipkin, C.R.; Thomas, R.J.; Syrett, P.J. Effects of nitrogen deficiency on nitrate reductase, nitrate assimilation
and photosynthesis in unicellular marine-algae. Mar. Biol. 1983, 77, 101–105. [CrossRef]
86. Cermeno, P.; Dutkiewicz, S.; Harris, R.P.; Follows, M.; Schofield, O.; Falkowski, P.G. The role of nutricline
depth in regulating the ocean carbon cycle. Proc. Natl. Acad. Sci. USA 2008, 105, 20344–20349. [CrossRef]
[PubMed]
87. Kemp, A.E.S.; Villareal, T.A. High diatom production and export in stratified waters—A potential negative
feedback to global warming. Prog. Oceanogr. 2013, 119, 4–23. [CrossRef]
88. Capone, D.G.; Hutchins, D.A. Microbial biogeochemistry of coastal upwelling regimes in a changing ocean.
Nat. Geosci. 2013, 6, 711–717. [CrossRef]
89. Mackey, K.R.M.; Chien, C.T.; Paytan, A. Microbial and biogeochemical responses to projected future nitrate
enrichment in the California upwelling system. Front. Microbiol. 2014, 5. [CrossRef] [PubMed]
90. Rykaczewski, R.R.; Dunne, J.P. Enhanced nutrient supply to the California current ecosystem with global
warming and increased stratification in an earth system model. Geophys. Res. Lett. 2010, 37. [CrossRef]
91. Breitbarth, E.; Bellerby, R.J.; Neill, C.C.; Ardelan, M.V.; Meyerhofer, M.; Zollner, E.; Croot, P.L.; Riebesell, U.
Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences
2010, 7, 1065–1073. [CrossRef]
92. Shi, D.L.; Xu, Y.; Hopkinson, B.M.; Morel, F.M.M. Effect of ocean acidification on iron availability to marine
phytoplankton. Science 2010, 327, 676–679. [CrossRef] [PubMed]
93. Hoffmann, L.J.; Breitbarth, E.; Boyd, P.W.; Hunter, K.A. Influence of ocean warming and acidification on
trace metal biogeochemistry. Mar. Ecol. Prog. Ser. 2012, 470, 191–205. [CrossRef]
94. Moore, J.K.; Doney, S.C.; Glover, D.M.; Fung, I.Y. Iron cycling and nutrient-limitation patterns in surface
waters of the world ocean. Deep Sea Res. Part II Top. Stud. Oceanogr. 2002, 49, 463–507. [CrossRef]
95. Moore, C.M.; Mills, M.M.; Arrigo, K.R.; Berman-Frank, I.; Bopp, L.; Boyd, P.W.; Galbraith, E.D.; Geider, R.J.;
Guieu, C.; Jaccard, S.L.; et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 2013, 6,
701–710. [CrossRef]
96. Mackey, K.R.M.; Post, A.F.; McIlvin, M.R.; Cutter, G.A.; John, S.G.; Saito, M.A. Divergent responses of atlantic
coastal and oceanic synechococcus to iron limitation. Proc. Natl. Acad. Sci. USA 2015, 112, 9944–9949.
[CrossRef] [PubMed]
97. Mackey, K.R.M.; Buck, K.N.; Casey, J.R.; Cid, A.; Lomas, M.W.; Sohrin, Y.; Paytan, A. Phytoplankton
responses to atmospheric metal deposition in the coastal and open-ocean Sargasso sea. Front. Microbiol.
2012, 3. [CrossRef] [PubMed]