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1. Phytoplankton are key players in the global carbon cycle, contributing about half of global primary productivity. Within the phytoplankton, functional groups (characterized by distinct traits) have impacts on other major biogeochemical cycles, such as nitrogen, phosphorus and silica. Changes in phytoplankton community structure, resulting from the unique environmental sensitivities of these groups, may significantly alter elemental cycling from local to global scales. 2. We review key traits that distinguish major phytoplankton functional groups, how they affect bio-geochemistry and how the links between community structure and biogeochemical cycles are modelled. 3. Finally, we explore how global environmental change will affect phytoplankton communities, from the traits of individual species to the relative abundance of functional groups, and how that, in turn, may alter biogeochemical cycles. 4. Synthesis. We can increase our mechanistic understanding of the links between the community structure of primary producers and biogeochemistry by focusing on traits determining functional group responses to the environment (response traits) and their biogeochemical functions (effect traits). Identifying trade-offs including allometric and phylogenetic constraints among traits will help parameterize predictive biogeochemical models, enhancing our ability to anticipate the consequences of global change.
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SPECIAL FEATURE ESSAY REVIEW
WHETHER IN LIFE OR IN DEATH: FRESH PERSPECTIVES ON HOW PLANTS AFFECT
BIOGEOCHEMICAL CYCLING
Global biogeochemical impacts of phytoplankton: a
trait-based perspective
Elena Litchman
1,2
*, Paula de Tezanos Pinto
3
, Kyle F. Edwards
4
, Christopher A.
Klausmeier
1,5
, Colin T. Kremer
6,7
and Mridul K. Thomas
8
1
Kellogg Biological Station, Michigan State University, 3700 E Gull Lake Dr., Hickory Corners, MI 49060, USA;
2
Department of Integrative Biology, Michigan State University, 288 Farm Lane, East Lansing, MI 48824, USA;
3
Departamento de Ecolog
ıa, Gen
etica y Evoluci
on, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos
Aires, IEGEBA (CONICET-UBA), C1428EHA, Buenos Aires, Argentina;
4
Department of Oceanography, University of
Hawaii at Manoa, 1000 Pope Road, Honolulu, HI 96822, USA;
5
Department of Plant Biology, Michigan State
University, 612 Wilson Road, East Lansing, MI 48824, USA;
6
Department of Ecology and Evolutionary Biology, Yale
University, P.O. Box 208106, New Haven, CT 06520-8106, USA;
7
Atmospheric and Oceanic Sciences Program,
Princeton University, 300 Forrestal Road, Sayre Hall, Princeton, NJ 08544, USA; and
8
Department of Aquatic Ecology,
Eawag: Swiss Federal Institute of Aquatic Science and Technology,
Uberlandstrasse 133, 8600 D
ubendorf,
Switzerland
Summary
1. Phytoplankton are key players in the global carbon cycle, contributing about half of global pri-
mary productivity. Within the phytoplankton, functional groups (characterized by distinct traits) have
impacts on other major biogeochemical cycles, such as nitrogen, phosphorus and silica. Changes in
phytoplankton community structure, resulting from the unique environmental sensitivities of these
groups, may signicantly alter elemental cycling from local to global scales.
2. We review key traits that distinguish major phytoplankton functional groups, how they affect bio-
geochemistry and how the links between community structure and biogeochemical cycles are modelled.
3. Finally, we explore how global environmental change will affect phytoplankton communities,
from the traits of individual species to the relative abundance of functional groups, and how that, in
turn, may alter biogeochemical cycles.
4. Synthesis. We can increase our mechanistic understanding of the links between the community
structure of primary producers and biogeochemistry by focusing on traits determining functional
group responses to the environment (response traits) and their biogeochemical functions (effect
traits). Identifying trade-offs including allometric and phylogenetic constraints among traits will help
parameterize predictive biogeochemical models, enhancing our ability to anticipate the consequences
of global change.
Key-words: aquatic plant ecology, biogeochemical cycles, cell size, functional groups, global
change, phytoplankton community structure, trade-offs
Introduction
Understanding the links between the structure of primary pro-
ducer communities and biogeochemistry is an important
research frontier bridging community and ecosystem ecology.
Such research is especially important as rapid, human-driven
changes in our environment affect primary producer commu-
nities and, ultimately, global biogeochemical cycles. Phyto-
plankton are major aquatic primary producers, responsible for
about half of global primary productivity each year (Field
et al. 1998). They are key contributors to biogeochemical
cycles, both at present and over the long history of our planet,
*Correspondence author: E-mail: litchman@msu.edu
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society
Journal of Ecology 2015, 103, 13841396 doi: 10.1111/1365-2745.12438
and are the subject of extensive experimental, observational
and theoretical attention. Fully appreciating the role of phyto-
plankton in elemental cycling requires characterizing their
diversity that encompasses two domains of life and several
distinct functional groups. These groups differ in how the
environment inuences their growth, in the elements and
their ratios that the groups consume and excrete, and, there-
fore, in their effects on biogeochemistry. We argue that estab-
lishing effective, mechanistic links between community and
ecosystem ecology requires characterizing the traits that dene
these groups and their environmental sensitivities. Ultimately,
this kind of trait-based approach can provide critical insights
into the biogeochemical function of aquatic and terrestrial
communities, both now and in our increasingly human-
impacted world. In this review, we describe major phyto-
plankton groups (including their history, traits and involve-
ment in biogeochemical cycling), how these groups have
been incorporated in biogeochemical models, and discuss
how they may be affected by global change.
What are the advantages of trait-based approaches? Traits
capture aspects of physiology, morphology and life history
that inuence tness and competitive success. Resource utili-
zation traits connect species abundances and growth with the
chemical compounds that are most limiting for metabolic pro-
cesses, thereby linking ecological processes (species and
community dynamics) with biogeochemical processes through
species performance. For example, the rate at which a cell
can take up phosphorus is an important determinant of its
competitive ability in environments where phosphorus limits
growth. Integrated over the community, these uptake rates
feed back to inuence external phosphorus concentrations. In
other cases, the link between biogeochemistry and ecological
success is less direct, and it may be useful to distinguish
between traits that affect biogeochemical cycles (effect traits)
and the traits that determine how abundances of these groups
would respond to changing conditions (response traits)
(Lavorel & Garnier 2002). Many phytoplankton traits are
both response and effect traits, but many are only one or the
other. For example, the optimal temperature for growth is a
purely response trait (because temperature affects growth but
not vice versa), and carbon export efciency is an effect trait
that is not tightly linked to a particular response trait. Under-
standing how response and effect traits are related will allow
us to understand the links between the community structure
of primary producers and biogeochemistry in a mechanistic
way.
Many groups of primary producers differ both in their
response and effect traits and, consequently, may have differ-
ent impacts on biogeochemical cycling. For example, free liv-
ing or symbiotic nitrogen-xers can x atmospheric nitrogen
(N) and do not require other forms of N. Thus, their N
response traits are distinct from those of non-N-xers. While
non-xers consume available N, N-xers can signicantly
increase N concentration in the environment (soil or water),
thus having contrasting N effect traits as well. The N xation
response and effect traits are tightly linked, which is true for
other resource acquisition traits.
Different traits are often not independent but connected by
trade-offs, and these trade-offs determine how community
structure and coexistence change under different conditions,
with concomitant changes in biogeochemical processes. N-x-
ers are often thought to have high phosphorus requirements
compared to other groups and thus exhibit a trade-off between
N and P competitive abilities (Lenton & Klausmeier 2007).
This trade-off can lead to coexistence of N-xers and non-x-
ers and can explain shifts in community composition with
changing N: P ratios. Similar trade-offs between N xation
and competitive abilities for light or iron may also be impor-
tant (Agawin et al. 2007; de Tezanos Pinto & Litchman
2010; Ward et al. 2013). Whether N-xers occur under par-
ticular conditions has many biogeochemical consequences,
because it determines how much newnitrogen is being
added to the ocean, because it affects the stoichiometry of
organic matter exported to the deep ocean and because xed
N can be released into the environment and consumed by
other primary producers and other microbes.
In this review, we focus on biogeochemically relevant traits
and trade-offs to discuss what is known about the feedbacks
between phytoplankton community structure and biogeochem-
istry, with the hope that some of these ideas can also be
applied to terrestrial plants. We begin by reviewing the dis-
tinct biogeochemical signatures and impacts of the major tax-
onomic groups of phytoplankton. Next, we discuss modelling
approaches that link phytoplankton community structure and
key traits to biogeochemical cycles. Finally, we describe
major global change stressors in aquatic environments and
discuss how they can change phytoplankton communities,
selecting for groups and species with certain traits, with con-
sequences for biogeochemistry.
Major phytoplankton groups and their
biogeochemical signatures
Phytoplankton are a paraphyletic group of photoautotrophs
with a complex evolutionary history extending across
2.53.5 billion years (Olson & Blankenship 2004; Yoon et al.
2004). Despite this paraphyly, they fall into evolutionarily
distinct functional groups, including one major prokaryotic
group (the cyanobacteria) and a number of eukaryotic groups
(diatoms, green algae, coccolithophorids, dinoagellates and
others).
The evolution of oxygenic photosynthesis in cyanobacteria
was a major advance in metabolic strategy that changed the
fate of our planet forever. This major evolutionary innovation
likely happened only once and changed the atmosphere of our
planet from anoxic to oxygenic after two billion years in the
former state (Knoll 2003). Vast amounts of solar energy were
subsequently channelled into driving geochemical cycles
(Rosing et al. 2006), reducing atmospheric carbon dioxide to
a wide range of organic substances (Holm
en 1992). Signicant
quantities of molecular oxygen started to accumulate in the
atmosphere about 2.22.4 billion years ago (Catling & Zahnle
2002; Holland 2006). The timing of Earths oxygenation coin-
cided with the disappearance of large non-mass-dependent
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
Global biogeochemical impacts of phytoplankton 1385
sulphur isotope (
33
S and
36
S) fractionations (Holland 2006)
and of iron banded formations (Isley & Abbott 1999), showing
the impacts of oxygenation on other element cycles.
This process of oxygenation was largely driven by the cy-
anobacteria, which remained the dominant phytoplankton for
well over a billion years and strongly inuence elemental
cycles today. They are the only phytoplanktonic group with
members capable of atmospheric nitrogen xation (the
absence of N xation in eukaryotes is poorly understood,
Schopf 1983) that has a major impact on global nitrogen
cycle. Nitrogen xation is one of the most metabolically
expensive processes in biology (16 ATPs are hydrolysed per
N
2
xed) (Simpson & Burris 1984) and is crucial for Earths
nitrogen budget and primary productivity. The evolution of
the ability to x nitrogen is thought to be extremely ancient
(Staley & Orians 1992), possibly older than oxygenic photo-
synthesis. Several authors infer that the nitrogenase family
had already evolved in the last common ancestor of extant
organisms (Normand et al. 1992; Fani, Gallo & Lio 2000),
though another hypothesis suggests a later origin (see Ray-
mond et al. 2004). Because nitrogen xation is a process
highly sensitive to the presence of oxygen, the evolution of
oxygenic photosynthesis posed a major physiological burden
on nitrogen xation in cyanobacteria. This limitation was
overcome by xing nitrogen during the night (in the absence
of oxygen production), hence separating N xation and pho-
tosynthesis in time. Another strategy was the separation of
photosynthesis and N xation in space, by performing N xa-
tion in anaerobic specialized cells, heterocysts, during day-
light and photosynthesis in vegetative cells. There could still
be other undiscovered strategies.
Marine cyanobacteria are responsible for 2550% of
natural (i.e. not anthropogenic via the HaberBosch process)
global nitrogen xation, or approximately 4.599
10
12
mol N year
1
(Mahaffey, Michaels & Capone 2005;
Caneld, Glazer & Falkowski 2010; Zehr 2011). This spatial
extent of nitrogen xation is limited both by temperature (Sta-
al, Meysman & Stal 2003) and by the availability of iron,
which is needed for the production of the nitrogenase enzyme
(Berman-Frank et al. 2001; Kustka et al. 2003). Conse-
quently, nitrogen xation occurs most strongly in the tropical
and subtropical oceans, and in regions with high Fe: N ratios
(Monteiro, Dutkiewicz & Follows 2011; Ward et al. 2013).
The process of nitrogen xation is leaky; between 50 and
90% of xed nitrogen may be released to surrounding waters
in the form of dissolved organic nitrogen (Glibert & Bronk
1994; Mulholland & Bernhardt 2005), thereby subsidizing
non-xers. The cyanobacteria possess the highest N: P ratio
of any phytoplankton group, with an average N: P ratio of
around 22:1, relative to 13:1 in eukaryotic taxa (data com-
piled from earlier studies by Deutsch & Weber 2012). This is
considerably higher in the nitrogen-xing Trichodesmium sp.,
which may be >40:1 due to the high nitrogen requirement for
light-harvesting machinery (Letelier & Karl 1996; data com-
piled from earlier studies by Klausmeier et al. 2004).
Although nitrogen xation is a unique trait of cyanobacteria,
not all cyanobacteria x nitrogen. Among those that do not,
Prochlorococcus and Synechococcus play an important role in
the carbon cycle, because they are major components of the
photosynthetic biomass in the oligotrophic oceans (Johnson
et al. 2006).
The eukaryotic taxa originated with the engulfment of a
cyanobacterium by a heterotrophic protozoan, leading to the
formation of a symbiotic relationship between the two,
approximately 1.5 billion years ago (Yoon et al. 2004). The
endosymbiotic cyanobacterium subsequently evolved into the
contemporary chloroplast. Thereafter, this eukaryotic clade
diverged into green and red lineages that differ based on their
pigment composition (Delwiche 1999). Subsequent engulf-
ment of these green and red eukaryotes by heterotrophs led to
secondary and even tertiary endosymbioses: diatoms, for
example, are the product of an endosymbiotic event between
a heterotroph and a red alga (Archibald & Keeling 2002). As
a consequence, contemporary eukaryotic phytoplankton are
composed of two superfamilies. The green superfamily con-
tains the green algae and groups formed by the engulfment of
a green alga by a heterotroph, such as the euglenophytes. The
red superfamily contains the red algae (now largely benthic)
and groups containing red plastids, including diatoms, crypto-
phytes and coccolithophores. While both green and red super-
families primarily use chlorophyll a, the former also
possesses chlorophyll b, while the latter uses chlorophyll c
and several accessory pigments that absorb blue and green
wavelengths (Falkowski et al. 2004; Katz et al. 2004).
The eukaryotic superfamilies exhibit distinct stoichiometries
from each other and the cyanobacteria. Members of the green
superfamily possess higher C: P and N: P ratios than their
counterparts in the red superfamily as well as higher require-
ments for some micronutrients (Fe, Cu and Zn) and lower
requirements for others (Cd, Co and Mn; Quigg et al. 2003).
These differences in stoichiometry are thought to be related to
oceanic environmental conditions when these groups diversi-
ed, and have important implications for biogeographic pat-
terns in ocean N: P ratios, which they both inuence and are
inuenced by Weber & Deutsch (2010). Because functional
groups also differ in their response to other environmental
variables (characterized by their traits), environment-driven
shifts in functional group composition are likely to drive
changes in biogeochemical cycles due to shifts in the average
cell stoichiometry. We discuss a few of the major eukaryotic
groups here, but note that other less studied groups may be of
considerable biogeochemical importance, though we lack data
with which to draw broad conclusions. These include the
non-calcifying haptophytes, chrysophytes, cryptophytes, raphi-
dophytes, rhodophytes and euglenophytes, among others.
Green algae, the group that gave rise to terrestrial plants,
evolved >1 billion years ago and comprised a large propor-
tion of the phytoplankton community till the Mesozoic era,
approximately 250 million years ago. Thereafter, they
declined in abundance and diversity in the oceans, being
apparently out-competed by members of the red superfamily
groups that began to rise in prominence (Falkowski et al.
2004; Katz et al. 2004). This decline has been linked to
changes in the redox state of the oceans, with their high trace
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
1386 E. Litchman et al.
metal requirements possibly constraining their present marine
distribution and diversity (they remain abundant, diverse and
broadly distributed in freshwaters). Unlike the other groups
described here, they perform no distinctive biogeochemical
functions to our knowledge. They are thought to be excep-
tionally plastic in their biomass N: P ratio, but this is based
largely on experiments with a single freshwater species,
Scenedesmus sp. (Rhee 1978).
Coccolithophorids rst occur in the fossil record approxi-
mately 220 million years ago and rose to prominence through
the Mesozoic era and then declined in diversity as the dia-
toms diversied (Bown, Lees & Young 2004; Falkowski
et al. 2004; Katz et al. 2004). They form a major portion of
high latitude phytoplankton communities today, with massive
blooms of one major species, Emiliania huxleyi, occurring
over areas of hundreds of thousands of square kilometres
(Brown & Podest
a 1997). They play a dominant role among
the phytoplankton in the marine calcium cycle through the
formation of calcium carbonate plates (coccoliths), which are
responsible for the formation of calcium carbonate rock for-
mations across the globe. Although coccolith sinking may be
expected to lead to considerable carbon export, the extent of
the export is a function of sea oor depth and calcium com-
pensation depth. If the ocean oor is lower than the compen-
sation depth, coccoliths dissolve, returning carbon to the
water. In total, they are thought to be responsible for approxi-
mately 10% of carbon export to the deep ocean (Jin et al.
2006). At the same time, calcication reduces total alkalinity,
reducing the ability of the surface ocean to take up atmo-
spheric CO
2
(Passow and Carlson 2012). Coccolithophores
also produce dimethylsulfoniopropionate (DMSP), a precursor
to dimethyl sulphide (DMS), a cloud condensation nucleus.
Though there is a clear mechanistic link between coccolitho-
phorid growth and climate in this case, the evidence for it as
a regulator of climate is weak, though it may still play a
minor role (Charlson et al. 1987; Ayers & Cainey 2007;
Quinn & Bates 2011; Rap et al. 2013).
Diatoms are believed to have originated 160200 million
years ago and diversied strongly in the past 60 million
years, at the expense of other groups (Kooistra & Medlin
1996; Falkowski et al. 2004; Sims, Mann & Medlin 2006).
Their recent dominance may be a result of their ability to
store pulses of nutrients in a large vacuole supported by the
silica cell wall and/or protection from predation accorded by
their silica shells (Smetacek 1999; Thingstad et al. 2005;
Litchman, Klausmeier & Yoshiyama 2009). As other func-
tional groups do not use silica, the ability to compete for this
element does not contribute to their success against other
functional groups, but may contribute towards determining
which diatom species predominate. Globally, they play a
dominant role in the carbon cycle, contributing an estimated
2025% of global primary productivity (Nelson et al. 1995;
Smetacek 1999). Their relatively large cell sizes lead to a
high sinking rate which contributes to major portion of carbon
export to the deep oceans (Nelson et al. 1995). They are also
the primary phytoplankton group associated with the global
silica cycle (with silicoagellates playing a minor role). This
uptake of silica is responsible for the undersaturation of silica
in the surface oceans and leads to the burial of
6.3 910
12
mol Si year
1
through sinking (Tr
eguer & De La
Rocha 2013). They have low N: P ratios characteristic of the
red superfamily, with an average of approximately 10:1
(Sarthou et al. 2005), and are most abundant in unstable,
nutrient-rich waters with similarly low N:P ratios, typically at
high latitudes and in coastal oceans (Arrigo 2005).
Dinoagellates belong to the red superfamily and became a
major component of the phytoplankton community over
200 million years ago, but have decreased in diversity over
the past 4060 million years (Katz et al. 2004). They exhibit
exceptionally complex genomes and metabolic capabilities:
members of this motile group exhibit mixotrophy (and even
pure heterotrophy), toxin production, bioluminescence and
tertiary endosymbiosis with complex symbionts such as dia-
toms and prasinophytes (Wisecaver & Hackett 2011). Despite
belonging to the red superfamily, they also contain members
that have appropriated plastids belonging to the green lineage
(Falkowski et al. 2004). They possess among the largest phy-
toplankton cells and are typically poor competitors for nutri-
ents and slow growers under autotrophic conditions
(Litchman et al. 2007); mixotrophy allows them to persist
despite this inefciency, particularly in environments with
high nutrient and organic matter concentrations.
Biogeochemical models of phytoplankton
functional types
Biogeochemical models aim to explain how biogeochemical
cycles operate today and operated in the past, and predict
how they will respond to anthropogenic stressors such as cli-
mate change. Much of the foundational and current work
on marine ecosystem models has used a NPZ (nutrient
phytoplanktonzooplankton) structure, where phytoplankton
are modelled as a single population that consumes a single
limiting nutrient (typically representing nitrogen) and are con-
sumed by a single zooplankton population (Evans and Par-
slow 1985, Fasham et al. 1990, Franks 2002). NPZ models
are formulated and parameterized by combining laboratory
data on plankton traits, eld observations of bulk stocks and
rates, and theoretical considerations such as dynamical stabil-
ity. Although they greatly simplify biological complexity,
NPZ models are useful for theoretical exploration and have
successfully represented ecosystem patterns in many situations
(Franks 2002). More complex models have been developed to
address questions such as the role of multiple limiting nutri-
ents and their biogeochemical coupling, because iron, phos-
phorus and silicon may all limit phytoplankton growth in
addition to nitrogen (Flynn 2003, Moore et al. 2013).
It has also become clear that incorporating the functional
diversity of phytoplankton is important for modelling biogeo-
chemical cycles, because community structure varies greatly
in time and space, and different kinds of phytoplankton have
distinct effects on carbon xation and export, as well as the
cycling of N and Si among other elements (Le Qu
ere et al.
2005, Hood et al. 2006). The most common way biogeo-
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
Global biogeochemical impacts of phytoplankton 1387
metal requirements possibly constraining their present marine
distribution and diversity (they remain abundant, diverse and
broadly distributed in freshwaters). Unlike the other groups
described here, they perform no distinctive biogeochemical
functions to our knowledge. They are thought to be excep-
tionally plastic in their biomass N: P ratio, but this is based
largely on experiments with a single freshwater species,
Scenedesmus sp. (Rhee 1978).
Coccolithophorids rst occur in the fossil record approxi-
mately 220 million years ago and rose to prominence through
the Mesozoic era and then declined in diversity as the dia-
toms diversied (Bown, Lees & Young 2004; Falkowski
et al. 2004; Katz et al. 2004). They form a major portion of
high latitude phytoplankton communities today, with massive
blooms of one major species, Emiliania huxleyi, occurring
over areas of hundreds of thousands of square kilometres
(Brown & Podest
a 1997). They play a dominant role among
the phytoplankton in the marine calcium cycle through the
formation of calcium carbonate plates (coccoliths), which are
responsible for the formation of calcium carbonate rock for-
mations across the globe. Although coccolith sinking may be
expected to lead to considerable carbon export, the extent of
the export is a function of sea oor depth and calcium com-
pensation depth. If the ocean oor is lower than the compen-
sation depth, coccoliths dissolve, returning carbon to the
water. In total, they are thought to be responsible for approxi-
mately 10% of carbon export to the deep ocean (Jin et al.
2006). At the same time, calcication reduces total alkalinity,
reducing the ability of the surface ocean to take up atmo-
spheric CO
2
(Passow and Carlson 2012). Coccolithophores
also produce dimethylsulfoniopropionate (DMSP), a precursor
to dimethyl sulphide (DMS), a cloud condensation nucleus.
Though there is a clear mechanistic link between coccolitho-
phorid growth and climate in this case, the evidence for it as
a regulator of climate is weak, though it may still play a
minor role (Charlson et al. 1987; Ayers & Cainey 2007;
Quinn & Bates 2011; Rap et al. 2013).
Diatoms are believed to have originated 160200 million
years ago and diversied strongly in the past 60 million
years, at the expense of other groups (Kooistra & Medlin
1996; Falkowski et al. 2004; Sims, Mann & Medlin 2006).
Their recent dominance may be a result of their ability to
store pulses of nutrients in a large vacuole supported by the
silica cell wall and/or protection from predation accorded by
their silica shells (Smetacek 1999; Thingstad et al. 2005;
Litchman, Klausmeier & Yoshiyama 2009). As other func-
tional groups do not use silica, the ability to compete for this
element does not contribute to their success against other
functional groups, but may contribute towards determining
which diatom species predominate. Globally, they play a
dominant role in the carbon cycle, contributing an estimated
2025% of global primary productivity (Nelson et al. 1995;
Smetacek 1999). Their relatively large cell sizes lead to a
high sinking rate which contributes to major portion of carbon
export to the deep oceans (Nelson et al. 1995). They are also
the primary phytoplankton group associated with the global
silica cycle (with silicoagellates playing a minor role). This
uptake of silica is responsible for the undersaturation of silica
in the surface oceans and leads to the burial of
6.3 910
12
mol Si year
1
through sinking (Tr
eguer & De La
Rocha 2013). They have low N: P ratios characteristic of the
red superfamily, with an average of approximately 10:1
(Sarthou et al. 2005), and are most abundant in unstable,
nutrient-rich waters with similarly low N:P ratios, typically at
high latitudes and in coastal oceans (Arrigo 2005).
Dinoagellates belong to the red superfamily and became a
major component of the phytoplankton community over
200 million years ago, but have decreased in diversity over
the past 4060 million years (Katz et al. 2004). They exhibit
exceptionally complex genomes and metabolic capabilities:
members of this motile group exhibit mixotrophy (and even
pure heterotrophy), toxin production, bioluminescence and
tertiary endosymbiosis with complex symbionts such as dia-
toms and prasinophytes (Wisecaver & Hackett 2011). Despite
belonging to the red superfamily, they also contain members
that have appropriated plastids belonging to the green lineage
(Falkowski et al. 2004). They possess among the largest phy-
toplankton cells and are typically poor competitors for nutri-
ents and slow growers under autotrophic conditions
(Litchman et al. 2007); mixotrophy allows them to persist
despite this inefciency, particularly in environments with
high nutrient and organic matter concentrations.
Biogeochemical models of phytoplankton
functional types
Biogeochemical models aim to explain how biogeochemical
cycles operate today and operated in the past, and predict
how they will respond to anthropogenic stressors such as cli-
mate change. Much of the foundational and current work
on marine ecosystem models has used a NPZ (nutrient
phytoplanktonzooplankton) structure, where phytoplankton
are modelled as a single population that consumes a single
limiting nutrient (typically representing nitrogen) and are con-
sumed by a single zooplankton population (Evans and Par-
slow 1985, Fasham et al. 1990, Franks 2002). NPZ models
are formulated and parameterized by combining laboratory
data on plankton traits, eld observations of bulk stocks and
rates, and theoretical considerations such as dynamical stabil-
ity. Although they greatly simplify biological complexity,
NPZ models are useful for theoretical exploration and have
successfully represented ecosystem patterns in many situations
(Franks 2002). More complex models have been developed to
address questions such as the role of multiple limiting nutri-
ents and their biogeochemical coupling, because iron, phos-
phorus and silicon may all limit phytoplankton growth in
addition to nitrogen (Flynn 2003, Moore et al. 2013).
It has also become clear that incorporating the functional
diversity of phytoplankton is important for modelling biogeo-
chemical cycles, because community structure varies greatly
in time and space, and different kinds of phytoplankton have
distinct effects on carbon xation and export, as well as the
cycling of N and Si among other elements (Le Qu
ere et al.
2005, Hood et al. 2006). The most common way biogeo-
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
Global biogeochemical impacts of phytoplankton 1387
nutrient limitation term, and this can cause their regional pat-
terns of growth limitation to be distinct from other phyto-
plankton types, due to variation in the supply of Si relative to
other elements (Moore et al. 2002; Aumont et al. 2003;
Blackford, Allen & Gilbert 2004). They are also thought to
contribute disproportionately to carbon export from the
euphotic zone, due to a number of potential factors: their lar-
ger size (on average), the boom-and-bust phenology of some
species, the ballastingeffect of the silica frustule and
reduced grazing rates (Smetacek 1999; Assmy et al. 2013).
Some of these effects will emerge naturally if the functional
type representing diatoms is given a higher maximum growth
rate or lower grazing rate, as described above. The increase in
export due to larger size or ballasting can be modelled with
an increased sinking rate of non-grazed and/or grazed biomass
(Moore et al. 2002; Litchman et al. 2006; Follows et al.
2007).
Coccolithophores play a distinct biogeochemical role due to
calcication and ballasting of organic matter and have a dis-
tinct (and likely varied) ecology that is still being unravelled
(Boyd et al. 2010). Their traits have been modelled in a vari-
ety of ways, although a general aim is to reproduce the fact
that they bloom under more stratied conditions than diatoms,
but are likely poorer nutrient competitors than picophyto-
plankton. Gregg & Casey (2007) give coccolithophores a
half-saturation constant for nitrogen-limited growth that is
higher than that of cyanobacteria but lower than that of dia-
toms, as well as an intermediate maximum growth rate (which
is highest for diatoms in this case) and a relatively high irra-
diance requirement. In this formulation, they essentially have
an intermediate position on a gleaneropportunist trade-off
axis (Margalef 1978; Kudela 2010; Edwards, Klausmeier &
Litchman 2013). In contrast, the PlankTOM10 model gives
coccolithophores a relatively slow maximum growth rate,
intermediate nutrient afnity traits and a minimum tempera-
ture threshold that is lower than that of the picocyanobacteria
that are the best nutrient competitors (Kwiatkowski et al.
2014, http://lgmacweb.env.uea.ac.uk/green_ocean/model/
code_description/PFT/uxes.html). An increased efciency of
carbon export for coccolithophores, due to ballasting, can be
implemented with a higher sinking rate (Moore et al. 2002;
Gregg & Casey 2007).
Diazotrophs (nitrogen-xers) are an important functional
type, due to their unique role in the nitrogen cycle. They
are thought to prosper under extreme nitrogen limitation,
while suffering a number of disadvantages described earlier.
They are often modelled as having a relatively high iron
requirement, which makes them poor competitors when iron
supply is low relative to N and P (Moore et al. 2002; Ward
et al. 2013). They are also typically given a low maximum
growth rate, which means they cannot take advantage of
variable nutrient supply (Tyrell 1999, Moore et al. 2002;
Monteiro, Dutkiewicz & Follows 2011). It may also be
important for diazotrophs to be poor P competitors (Tyrrell
1999; Lenton & Klausmeier 2007; Ward et al. 2013),
although a relatively low P stoichiometry will at least par-
tially offset this (Moore et al. 2002). In combination, these
traits will lead to diazotroph occurrence in stably stratied
regions with a low supply ratio of N: Fe and N: P (Ward
et al. 2013). Although most ocean biogeochemical models
represent diazotrophs by a single group, some models
include different diazotroph types with distinct traits, such as
lamentous Trichodesmium, unicellular N-xers and symbi-
otic N-xers living inside diatoms (e.g. Monteiro, Follows
& Dutkiewicz 2010).
Responses of phytoplankton communities to
global environmental change and implications
for biogeochemistry
The many dimensions of global change are increasingly affect-
ing marine environments and the phytoplankton communities
that inhabit them. In the following section, we briey summa-
rize the most important aspects of the ocean that are changing,
including temperature, acidity and nutrient availability. The
traits and functions of phytoplankton groups and species deter-
mine both how they are affected by global change and how
their responses in turn alter global biogeochemistry. In the
remaining text, we discuss how global change stressors inu-
ence phytoplankton across different levels of biological orga-
nization from functional groups to species.
Global change is multifaceted and includes not just CO
2
emissions and climate change, but also anthropogenic effects
that are independent of these factors. Acidication, rising tem-
peratures and changes in the supply of nutrients and light will
pose the greatest challenges for marine ecosystems and phyto-
plankton communities. Several reviews have examined these
effects in greater detail (e.g. Hoegh-Guldberg & Bruno 2010;
Boyd and Hutchins 2012, Doney et al. 2012), so our summary
is brief. World-wide, oceans act as a major sink for both the
rising levels of atmospheric CO
2
and the increased amount of
heat trapped by this CO
2
and other greenhouse gasses. Nearly
1/3 of anthropogenic CO
2
is being absorbed into the oceans,
where it interacts with water, altering seawater carbonate
chemistry and driving ocean acidication (Riebesell 2004; Do-
ney et al. 2009; Hoegh-Guldberg & Bruno 2010). Tempera-
tures have risen by ~0.6 °C over the last 100 years within the
surface layers of the ocean (Hoegh-Guldberg & Bruno 2010)
and are predicted to increase by another 13°C by the end of
the century (IPCC; Collins et al. 2013). Temperature plays an
important role in physical ocean processes, driving mixing,
vertical stratication and currents. In tropical and temperate
regions, warmer temperatures lead to stronger stratication
and shallower mixed layers, simultaneously intensifying nutri-
ent limitation and reducing light limitation (as plankton avoid
being mixed to deeper, darker regions) (Beardall, Stojkovic &
Larsen 2009). Regionally, warming may strengthen coastal
upwelling and nutrient supply and alter the depth of mixing in
polar oceans (Hoegh-Guldberg & Bruno 2010). Temperature
and pH also inuence the chemistry of seawater; changes in
both of these variables will alter the solubility and oxidation
state of trace metals such as iron in ways that are not yet fully
understood (Hoffmann et al. 2012). These changes will be sig-
nicant for marine organisms requiring these trace metals
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
Global biogeochemical impacts of phytoplankton 1389
often as catalysts for critical biochemical processes. The sup-
ply of more abundant (though no less important) nutrients
such as nitrogen and phosphate is also being altered by human
activities. This occurs most dramatically in coastal regions,
through the inux of agricultural run-off and sediments from
rivers, but also includes atmospheric deposition of dust and
combustion by-products. Ultimately, these nutrients affect
microbial communities producing areas of hypoxia, especially
in coastal regions (Diaz & Rosenberg 2008), and altering bio-
geochemical processes. Finally, climate-driven changes in
weather patterns and cloud cover, among other factors, alter
the amount of light (and especially ultraviolet radiation) reach-
ing and penetrating the ocean surface (Beardall, Stojkovic and
Larsen 2009).
Adding to the complexity of global change is the fact that
few environments will experience only one of these changing
stressors: marine organisms may simultaneously face rising
temperatures, changing nutrient levels and acidication (Halp-
ern et al. 2008). The combined effects of multiple stressors
can be non-additive and nonlinear, so global change studies
for most environments or species must consider the effects of
a suite of stressors (Crain, Kroeker & Halpern 2008; Boyd
2013; Boyd et al. 2015). Many aspects of global change also
exhibit signicant regional variability on top of underlying
global trends (Hansen et al. 2006).
As complex as global change is, understanding its effects
on phytoplankton and marine ecosystems presents an even
greater challenge, because these ecological systems, composed
of diverse and interacting species, are exceedingly complex in
their own right. We can organize this complexity by consider-
ing how global change affects phytoplankton at different eco-
logical resolutions, ranging from the collective response of the
phytoplankton as a whole to the ne-scale reactions of indi-
vidual species (Fig. 1). These categories roughly correspond
to the level of detail included in different biogeochemical
models of phytoplankton communities as discussed in bio-
geochemical models of phytoplankton functional types,
which range from as coarse as one or a few functional
groups, to dozens of species. Determining the appropriate
level of detail to resolve is a critical open research question,
which likely depends on which ecological or biogeochemical
features are of interest, and the degree of precision required.
The following discussion examines each of these categories in
turn, starting with the broadest and most simplied view.
At the coarsest scale, briey setting aside the particulars of
species or functional group identity, photoautotrophs such as
phytoplankton are united in their requirement for light, nutri-
ents and CO
2
to support their growth and productivity. If basic
requirements are either not met or dramatically exceeded (e.g.
photoinhibition or nutrient toxicity), whether through regional
variation or global change, growth and productivity are limited
(Fig. 1a). Modelling studies that include a generic phytoplank-
ton component, with parameters based on these requirements,
improve biogeochemistry models and can reproduce empirical
patterns of nutrient distributions (Kriest, Khatiwala & Oschlies
2010). They may also be able to crudely predict global
Fig. 1. The effects of global change on phytoplankton span nested levels of biological organization inuencing the function of phytoplankton,
including their contributions to biogeochemical cycles. For example, we can consider the consequences of increased nutrient limitation, at each
scale: (a) Collective. Changes in bulk properties of phytoplankton, such as their productivity, can alter energy uxes and carbon cycling. Increas-
ing stratication can reduce productivity in temperate and tropical oceans. (b) Intergroup. Functional groups within phytoplankton communities
can respond differently to shared stressors, altering their relative abundance. Diazotrophs may become more common in nitrogen-limited waters,
altering N cycling. (c) Intragroup. Turnover in the identity and abundance of particular species within a group may alter its functioning. Nutrient
limitation favours small-celled species, inuencing rates of zooplankton predation and carbon export to the deep ocean. (d) Intraspecic. Individ-
ual species may change their traits and function as a result of global change, through plasticity or rapid evolution. As with C, this could lead to
smaller cell sizes in the case of nutrient limitation.
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
1390 E. Litchman et al.
nutrient limitation term, and this can cause their regional pat-
terns of growth limitation to be distinct from other phyto-
plankton types, due to variation in the supply of Si relative to
other elements (Moore et al. 2002; Aumont et al. 2003;
Blackford, Allen & Gilbert 2004). They are also thought to
contribute disproportionately to carbon export from the
euphotic zone, due to a number of potential factors: their lar-
ger size (on average), the boom-and-bust phenology of some
species, the ballastingeffect of the silica frustule and
reduced grazing rates (Smetacek 1999; Assmy et al. 2013).
Some of these effects will emerge naturally if the functional
type representing diatoms is given a higher maximum growth
rate or lower grazing rate, as described above. The increase in
export due to larger size or ballasting can be modelled with
an increased sinking rate of non-grazed and/or grazed biomass
(Moore et al. 2002; Litchman et al. 2006; Follows et al.
2007).
Coccolithophores play a distinct biogeochemical role due to
calcication and ballasting of organic matter and have a dis-
tinct (and likely varied) ecology that is still being unravelled
(Boyd et al. 2010). Their traits have been modelled in a vari-
ety of ways, although a general aim is to reproduce the fact
that they bloom under more stratied conditions than diatoms,
but are likely poorer nutrient competitors than picophyto-
plankton. Gregg & Casey (2007) give coccolithophores a
half-saturation constant for nitrogen-limited growth that is
higher than that of cyanobacteria but lower than that of dia-
toms, as well as an intermediate maximum growth rate (which
is highest for diatoms in this case) and a relatively high irra-
diance requirement. In this formulation, they essentially have
an intermediate position on a gleaneropportunist trade-off
axis (Margalef 1978; Kudela 2010; Edwards, Klausmeier &
Litchman 2013). In contrast, the PlankTOM10 model gives
coccolithophores a relatively slow maximum growth rate,
intermediate nutrient afnity traits and a minimum tempera-
ture threshold that is lower than that of the picocyanobacteria
that are the best nutrient competitors (Kwiatkowski et al.
2014, http://lgmacweb.env.uea.ac.uk/green_ocean/model/
code_description/PFT/uxes.html). An increased efciency of
carbon export for coccolithophores, due to ballasting, can be
implemented with a higher sinking rate (Moore et al. 2002;
Gregg & Casey 2007).
Diazotrophs (nitrogen-xers) are an important functional
type, due to their unique role in the nitrogen cycle. They
are thought to prosper under extreme nitrogen limitation,
while suffering a number of disadvantages described earlier.
They are often modelled as having a relatively high iron
requirement, which makes them poor competitors when iron
supply is low relative to N and P (Moore et al. 2002; Ward
et al. 2013). They are also typically given a low maximum
growth rate, which means they cannot take advantage of
variable nutrient supply (Tyrell 1999, Moore et al. 2002;
Monteiro, Dutkiewicz & Follows 2011). It may also be
important for diazotrophs to be poor P competitors (Tyrrell
1999; Lenton & Klausmeier 2007; Ward et al. 2013),
although a relatively low P stoichiometry will at least par-
tially offset this (Moore et al. 2002). In combination, these
traits will lead to diazotroph occurrence in stably stratied
regions with a low supply ratio of N: Fe and N: P (Ward
et al. 2013). Although most ocean biogeochemical models
represent diazotrophs by a single group, some models
include different diazotroph types with distinct traits, such as
lamentous Trichodesmium, unicellular N-xers and symbi-
otic N-xers living inside diatoms (e.g. Monteiro, Follows
& Dutkiewicz 2010).
Responses of phytoplankton communities to
global environmental change and implications
for biogeochemistry
The many dimensions of global change are increasingly affect-
ing marine environments and the phytoplankton communities
that inhabit them. In the following section, we briey summa-
rize the most important aspects of the ocean that are changing,
including temperature, acidity and nutrient availability. The
traits and functions of phytoplankton groups and species deter-
mine both how they are affected by global change and how
their responses in turn alter global biogeochemistry. In the
remaining text, we discuss how global change stressors inu-
ence phytoplankton across different levels of biological orga-
nization from functional groups to species.
Global change is multifaceted and includes not just CO
2
emissions and climate change, but also anthropogenic effects
that are independent of these factors. Acidication, rising tem-
peratures and changes in the supply of nutrients and light will
pose the greatest challenges for marine ecosystems and phyto-
plankton communities. Several reviews have examined these
effects in greater detail (e.g. Hoegh-Guldberg & Bruno 2010;
Boyd and Hutchins 2012, Doney et al. 2012), so our summary
is brief. World-wide, oceans act as a major sink for both the
rising levels of atmospheric CO
2
and the increased amount of
heat trapped by this CO
2
and other greenhouse gasses. Nearly
1/3 of anthropogenic CO
2
is being absorbed into the oceans,
where it interacts with water, altering seawater carbonate
chemistry and driving ocean acidication (Riebesell 2004; Do-
ney et al. 2009; Hoegh-Guldberg & Bruno 2010). Tempera-
tures have risen by ~0.6 °C over the last 100 years within the
surface layers of the ocean (Hoegh-Guldberg & Bruno 2010)
and are predicted to increase by another 13°C by the end of
the century (IPCC; Collins et al. 2013). Temperature plays an
important role in physical ocean processes, driving mixing,
vertical stratication and currents. In tropical and temperate
regions, warmer temperatures lead to stronger stratication
and shallower mixed layers, simultaneously intensifying nutri-
ent limitation and reducing light limitation (as plankton avoid
being mixed to deeper, darker regions) (Beardall, Stojkovic &
Larsen 2009). Regionally, warming may strengthen coastal
upwelling and nutrient supply and alter the depth of mixing in
polar oceans (Hoegh-Guldberg & Bruno 2010). Temperature
and pH also inuence the chemistry of seawater; changes in
both of these variables will alter the solubility and oxidation
state of trace metals such as iron in ways that are not yet fully
understood (Hoffmann et al. 2012). These changes will be sig-
nicant for marine organisms requiring these trace metals
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
Global biogeochemical impacts of phytoplankton 1389
community composition alters the functional contributions of
a group, global change can affect biogeochemistry at the in-
tragroup level. Such dynamics occur in response to climate
change within an intermediate complexity Earth system
model, as the ranges of individual species expand and con-
tract based on their trait differences (including growth rates,
temperature optima, size and half-saturation constants), lead-
ing to substantial turnover in the composition of local com-
munities (Dutkiewicz, Scott & Follows 2013). Several
examples exist of between-species trait variation with the
potential to produce intragroup level biogeochemical effects,
limited seemingly only by the number of traits and environ-
mental factors studied so far. Biogeochemical rates are funda-
mentally linked to biological rates, such as growth rate.
Growth rates are strongly linked to temperature, yet individual
species often differ dramatically in their temperature depen-
dence (Thomas et al. 2012; Boyd et al. 2013). In turn, these
differences lead to predicted range shifts as oceans warm
(Thomas et al. 2012). Looking beyond temperature, different
coccolithophorid species and strains engage in calcication to
varying degrees, with important consequences for productivity
and carbon cycling. In nitrogen-xing cyanobacteria,
responses to CO
2
are diverse: elevated CO
2
stimulated growth
and N
2
xation in Trichodesmium species and Crocosphaera
watsonii, important open ocean diazotrophs (Behrenfeld et al.
2006; Beardall, Stojkovic and Larsen 2009, Hutchins et al.
2013), but inhibited these processes in coastal Nodularia
spumigena (Czerny, Barcelos e Ramos & Riebesell 2009;
Boyce, Lewis & Worm 2010). In this case, turnover in cyano-
bacteria species driven by rising CO
2
might actually support
consistent levels of function (N
2
xation) in the face of global
change. Overall, the effects of species turnover within func-
tional group will depend on which species are favoured by
the combinations of global change stressors experienced by
communities regionally and how these species contribute to
ecosystem function.
Finally, within a functional group, individual species need
not have xed traits (Fig. 1d). Even within primarily asexual
phytoplankton, species consist of multiple strains with differ-
ent traits, representing standing genetic and phenotypic varia-
tion. In addition to between-species differences in the
sensitivity of N xation rates to pCO
2
, Hutchins et al. (2013)
demonstrated signicant strain-level variation. Given this vari-
ation, increasing CO
2
concentrations may select for particular
strains, inuencing future biogeochemistry in complex ways.
The traits of species also respond to environmental changes
through physiological, behavioural and evolutionary mecha-
nisms. For example, the lipid content of several species of
Antarctic diatom (in the genus Navicula) declines with
increasing temperature, making them a poorer resource for
zooplankton (Teoh, Phang & Chu 2012). Many phytoplankton
are capable of nutrient storage and exhibit variable stoichiom-
etries through a variety of physiological mechanisms.
Changes in the stoichiometry of individual species can be of
similar magnitude to effects driven by turnover between spe-
cies (Behrenfeld et al. 2006; Finkel et al. 2009). This can
inuence their value as a food resource as mentioned
previously. In addition to physiological changes, evolutionary
responses are likely within the phytoplankton due to their
small size, huge populations and rapid generation times.
These responses might allow species to adapt to conditions
imposed by global change, suggesting that (over longer
time-scales) communities might recover from short-term per-
turbations. Understanding the effects of evolutionary
responses to global change is a complex process, requiring
detailed, specic knowledge of how environments will
change, how quickly phytoplankton can adapt and what
genetic constraints or trade-offs limit them. Experiments
designed to investigate these questions are becoming more
common, but much work remains to be done.
Ultimately, understanding how the effects of global change
will propagate through phytoplankton communities to inu-
ence biogeochemical cycling requires understanding the indi-
vidual and combined effects of stressors on phytoplankton
from species to functional groups. The key to obtaining this
knowledge rests on elucidating the links between environ-
ment, species traits and trade-offs, and their performance and
function.
Conclusions
Understanding the feedbacks between phytoplankton commu-
nity structure and biogeochemistry is a burgeoning area of
research. Distinct functional groups have been shaping the
biogeochemistry of our planet, from the period of oxygena-
tion ushered in by the cyanobacteria to contemporary patterns
of N xation and carbon cycling in the oceans. Understanding
the physiology and ecology of these groups is continuing. We
are still learning about new members of the phytoplankton
(Cuvelier et al. 2010), the environmental sensitivities and
traits of even the well-studied groups (Boyd et al. 2010),
approaches for efciently modelling diverse plankton commu-
nities and multiple element cycles (Stock, Dunne & John
2014), and methods for conceptually managing complex glo-
bal change (Boyd et al. 2015). These are crucial problems in
an era of global change. Quantifying the traits and trade-offs
that affect functional group composition will help connect
community responses to biogeochemical causes and effects.
A challenging empirical aspect of this approach is the num-
ber of important traits that must be gathered, especially given
trait variation between functional groups, species and popula-
tions. Which traits do we need to measure in order to predict
functional group dynamics? Predicting the outcome of compe-
tition between two populations requires knowledge of traits
relating to competition for resources (macronutrients,
micronutrients and light) and avoidance of predators, all of
which differ between groups (Litchman and Klausmeier 2008;
Boyd et al. 2010; Edwards et al. 2012, 2015). However, this
task is made easier because of several fundamental con-
straints, including both allometric and phylogenetic relation-
ships. Many traits scale strongly with cell size and
temperature, including cellular stoichiometry (Yvon-Durocher
et al. 2015). Due to the physical constraints that size and
shape place on cellsability to obtain nutrients, cell size cor-
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
1392 E. Litchman et al.
often as catalysts for critical biochemical processes. The sup-
ply of more abundant (though no less important) nutrients
such as nitrogen and phosphate is also being altered by human
activities. This occurs most dramatically in coastal regions,
through the inux of agricultural run-off and sediments from
rivers, but also includes atmospheric deposition of dust and
combustion by-products. Ultimately, these nutrients affect
microbial communities producing areas of hypoxia, especially
in coastal regions (Diaz & Rosenberg 2008), and altering bio-
geochemical processes. Finally, climate-driven changes in
weather patterns and cloud cover, among other factors, alter
the amount of light (and especially ultraviolet radiation) reach-
ing and penetrating the ocean surface (Beardall, Stojkovic and
Larsen 2009).
Adding to the complexity of global change is the fact that
few environments will experience only one of these changing
stressors: marine organisms may simultaneously face rising
temperatures, changing nutrient levels and acidication (Halp-
ern et al. 2008). The combined effects of multiple stressors
can be non-additive and nonlinear, so global change studies
for most environments or species must consider the effects of
a suite of stressors (Crain, Kroeker & Halpern 2008; Boyd
2013; Boyd et al. 2015). Many aspects of global change also
exhibit signicant regional variability on top of underlying
global trends (Hansen et al. 2006).
As complex as global change is, understanding its effects
on phytoplankton and marine ecosystems presents an even
greater challenge, because these ecological systems, composed
of diverse and interacting species, are exceedingly complex in
their own right. We can organize this complexity by consider-
ing how global change affects phytoplankton at different eco-
logical resolutions, ranging from the collective response of the
phytoplankton as a whole to the ne-scale reactions of indi-
vidual species (Fig. 1). These categories roughly correspond
to the level of detail included in different biogeochemical
models of phytoplankton communities as discussed in bio-
geochemical models of phytoplankton functional types,
which range from as coarse as one or a few functional
groups, to dozens of species. Determining the appropriate
level of detail to resolve is a critical open research question,
which likely depends on which ecological or biogeochemical
features are of interest, and the degree of precision required.
The following discussion examines each of these categories in
turn, starting with the broadest and most simplied view.
At the coarsest scale, briey setting aside the particulars of
species or functional group identity, photoautotrophs such as
phytoplankton are united in their requirement for light, nutri-
ents and CO
2
to support their growth and productivity. If basic
requirements are either not met or dramatically exceeded (e.g.
photoinhibition or nutrient toxicity), whether through regional
variation or global change, growth and productivity are limited
(Fig. 1a). Modelling studies that include a generic phytoplank-
ton component, with parameters based on these requirements,
improve biogeochemistry models and can reproduce empirical
patterns of nutrient distributions (Kriest, Khatiwala & Oschlies
2010). They may also be able to crudely predict global
Fig. 1. The effects of global change on phytoplankton span nested levels of biological organization inuencing the function of phytoplankton,
including their contributions to biogeochemical cycles. For example, we can consider the consequences of increased nutrient limitation, at each
scale: (a) Collective. Changes in bulk properties of phytoplankton, such as their productivity, can alter energy uxes and carbon cycling. Increas-
ing stratication can reduce productivity in temperate and tropical oceans. (b) Intergroup. Functional groups within phytoplankton communities
can respond differently to shared stressors, altering their relative abundance. Diazotrophs may become more common in nitrogen-limited waters,
altering N cycling. (c) Intragroup. Turnover in the identity and abundance of particular species within a group may alter its functioning. Nutrient
limitation favours small-celled species, inuencing rates of zooplankton predation and carbon export to the deep ocean. (d) Intraspecic. Individ-
ual species may change their traits and function as a result of global change, through plasticity or rapid evolution. As with C, this could lead to
smaller cell sizes in the case of nutrient limitation.
©2015 The Authors. Journal of Ecology ©2015 British Ecological Society, Journal of Ecology,103, 13841396
1390 E. Litchman et al.
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... First phytoplankton organisms (similar to actual marine cyanobacteria) appeared circa ~2.6 billion years ago, evolving through diverse global biogeochemical scenarios (Hedges et al., 2001;Falkowski et al., 2004; Yoon et al., 2004;Simon et al., 2009;Cardona, 2019) into the tens of thousands of described phytoplankton species extant in the modern ocean ( Fig. 1.1; Zeidner et al., 2003;Katz et al., 2004;De Vargas et al., 2015). This miscellanea of evolutionary histories implies plenty of distinguishing morphological (Chrétiennot-Dinet et al., 1993;Smetacek, 2001) and physiological traits (Beardall et al., 2009;Litchman et al., 2015;Worden et al., 2015;Stoecker et al., 2017). Such differences controls phytoplankton distribution and variability and their role in the biogeochemical cycles (Litchman et al., 2015;Worden et al., 2015;Acevedo-Trejos et al., 2018;Pierella Karlusich et al., 2020). ...
... This miscellanea of evolutionary histories implies plenty of distinguishing morphological (Chrétiennot-Dinet et al., 1993;Smetacek, 2001) and physiological traits (Beardall et al., 2009;Litchman et al., 2015;Worden et al., 2015;Stoecker et al., 2017). Such differences controls phytoplankton distribution and variability and their role in the biogeochemical cycles (Litchman et al., 2015;Worden et al., 2015;Acevedo-Trejos et al., 2018;Pierella Karlusich et al., 2020). ...
... Hedges et al., 2001;Falkowski et al., 2004;Yoon et al., 2004;Simon et al., 2009;Cardona, 2019). A pesar de que esta miscelánea de historias evolutivas resultó en una gran variedad de rasgos morfológicos y fisiológicos (Chrétiennot-Dinet et al., 1993;Smetacek, 2001;Beardall et al., 2009;Litchman et al., 2015;Worden et al., 2015;Stoecker et al., 2017), para la mayoría de estos organismos su principal fuente de energía proviene de la luz solar, la cual captan y usan para transformar materia inorgánica en materia orgánica, i.e. la Fotosíntesis. A pesar de que suponen menos del 1% de la biomasa autotrófica de La Tierra (~1 Gt C; Field et al., 1998;Le Quéré et al., 2005;Bar-On et al., 2018), estos organismos son los responsables de alrededor del 50% de la producción primaria global (~50 Gt C·yr-1; Falkowski, 1994;Field et al., 1998;Behrenfeld et al., 2005;McClain, 2009;Buitenhuis et al., 2013a). ...
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Phytoplankton growth mainly depends on nutrient and light availability. Highly dynamic oceanic environments are dominated by physical processes that generally alter phytoplankton dynamics by controlling the access to these resources. Mesoscale motions have been considered the most important factor modulating the distribution of biogeochemical properties at the upper levels of the ocean. Nevertheless, recent studies have highlighted the role played by smaller processes that operate below the local Rossby radius of deformation, referred to here as submesoscale. Due to the inherent complexity of sampling at such high-resolution levels, our knowledge about submesoscale-influenced phytoplankton distribution and variability is mostly constrained to theoretical and modeling studies. In addition, little is known about the fate of meso-submesoscale impacts on phytoplankton communities under climate change stressors. Ocean warming leads to enhanced stratification in the oligotrophic ocean but also to the intensification of cross-shore wind gradients and thus of the eddy kinetic energy across eastern boundary regions of the subtropical gyres. Phytoplankton thriving in a warmer, acidified ocean could then be fertilized by enhanced meso-submesoscale activity. Consequently, meso-submesoscale contribution to global net primary production could be increased. In order to contribute to understand how physical and biogeochemical factors, resolved at a resolution close to submesoscale could affect the spatiotemporal distribution and variability of pico- and nanoplankton, the main components of planktonic communities in the Canary Islands waters, we conducted two interdisciplinary surveys across a highly variable mesoscale field and a submesoscale front south of Gran Canaria island (Canary Island). We found that autotrophic and heterotrophic pico- and nanoplanktonic organisms presented a heterogeneous distribution in response to nutrient inputs caused by meso- and submesoscale processes. On the other hand, temporal variability, which is rarely studied, was found to be a significant source of error in phytoplankton variability. Finally, we have tested the response of three size classes (0.2-2, 2-20 and >20 m) of subtropical phytoplankton communities in terms of primary production, chlorophyll and cell biomass, to increasing CO2 concentrations and nutrient fertilization during an in situ mesocosm experiment in oligotrophic waters off Gran Canaria. Our results suggest that in a future acidified subtropical ocean, mesoscale and submesoscale features would drive nutrient pumping to the surface ocean favouring the development of diatoms and increasing new production in the global ocean.
... Phytoplankton are a complex group of organisms essential to the functioning of marine ecosystems. They are of basic importance in sustaining marine food webs by providing the largest part of primary productivity of the world's ocean (Uitz et al., 2010), and largely contributing to planetary processes of oxygen production, biogeochemical cycles, climate regulation, and carbon sequestration (Vallina and Simo, 2007;Litchman et al., 2015;Culhane et al., 2018;Zhang et al., 2018). Due to their prominent ecological role, phytoplankton are considered an indispensable target in continuous global monitoring programmes (Batten et al., 2019), and have traditionally been included in routine assessments of environmental agencies worldwide as descriptors of the ecological status of aquatic ecosystems (Tweddle et al., 2018;Eriksen et al., 2019). ...
... The impact of global change on seas and oceans will likely involve a profound alteration of phytoplankton communities (Van de Waal and Litchman, 2020;Henson et al., 2021), with cascading effects affecting the whole marine system, from the surface until the deep-sea environments (Nomaki et al., 2021). Trait-based perspectives to phytoplankton research will be critical to broaden our understanding of phytoplankton community assembly and dynamics under such changes and the ensuing effects on the functioning of marine ecosystems (Litchman et al., 2007;Litchman et al., 2015;Weithoff and Beisner, 2019). However, comprehensive investigations of functional aspects often require identifying organisms at the level of species and a deep knowledge of their autecology, which is still far from being adequate for phytoplankton (Litchman and Klausmeier, 2008), making these analyses overly demanding and impractical especially in reiterate assessments (Weithoff, 2003;Kruk et al., 2010). ...
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Phytoplankton assemblages are privileged descriptors of the ecological status of marine ecosystems regularly included in routine monitoring programmes. The high spatial and temporal variability of phytoplankton and the intrinsic difficulties of species identifications, however, combine in making reiterate assessments of this component of marine biota particularly demanding. Coarse levels of taxonomic resolution (e.g., genus, family) or morpho-functional categories have been proposed to reduce identification efforts or to ease the analysis of phytoplankton assemblages for monitoring purposes, although with contrasting outcomes. A major issue is that, in the absence of control for the loss of information associated to these alternative approaches, their application may lead to poor representations of genuine spatial and/or temporal patterns of assemblages in relation to natural and anthropogenic sources of variation. We provided a new approach to reduce the efforts required to analyse phytoplankton assemblages that integrate morpho-functional classification of phytoplankton with the use of null models to estimate the consequent loss of information on species-level community patterns. Null models for information loss were built by randomly grouping the original species variables into a progressively decreasing number of groups, in order to identify the minimum number of aggregate variables needed to detect community patters as at species level. Aggregate variables were then defined as morpho-functional groups, by grouping species on the basis of a combination of morpho-functional traits, including general taxonomy, cell size, shape, elongation and complexity. We applied the approach to six case studies investigating the response of phytoplankton assemblages from marine and transitional water ecosystems under different environmental settings in areas spanning the world’s ocean, including coral atolls, mangroves, estuaries, coastal lagoons and inlets. The approach allowed obtaining parsimonious sets of morpho-functional groups, which were suitable to detect changes in phytoplankton assemblage structure as at species level in all case studies. Trait-based approaches to phytoplankton research and monitoring are crucial to shed light on processes underlying phytoplankton community assembly and dynamics in the face of global change. In this perspective, our framework incorporates cost-effectiveness, instances from traditional monitoring programmes aiming at the detection of community patterns, and the current need for a deeper understanding of functional responses of phytoplankton to environmental drivers.
... Trait-based models have a rich, yet recent, history in phytoplankton ecology (Litchman and Klausmeier, 2008) and were originally developed primarily to understand patterns of niche differentiation and diversity. The potential of such models to also improve our mechanistic understanding of biogeochemical processes has also been highlighted (Litchman et al., 2015;Zakharova et al., 2019). Traits that regulate both responses and effects are an interesting target for modeling. ...
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... In addition, a portion of the organic matter can sink to the deep oceans as sinking biogenic particles or dissolved organic matter, a process named the biological carbon pump, which is responsible for export and accumulation of organic carbon from photosynthetic CO2 fixation in deep layers of the ocean down to the sediments (Figure 1 -step 6) (Ducklow et al., 2001). Besides being key actors in the carbon cycle, the phytoplankton functional groups are also actively involved in the other major biogeochemical cycles such as nitrogen, phosphorus and silica (Litchman et al., 2015). ...
Thesis
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... Phytoplankton are regarded as an integral part of the marine ecosystem, owing to their role as the primary producers of the sea and considering their profound influence on Earth's biogeochemical cycles [1]. Despite constituting less than 1% of the Earth's primary producer biomass [2], phytoplankton are responsible for approximately half of global primary production [3,4]; and in the ocean alone, are responsible for 90% of primary production [5]. ...
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