Global biogeochemical impacts of phytoplankton

13 Pages·2015·0.31 MB·English

Journal of Ecology2015, 103,1384–1396 doi: 10.1111/1365-2745.12438
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 Litchman1,2*, Paula de Tezanos Pinto3, Kyle F. Edwards4, Christopher A.
Klausmeier1,5, Colin T. Kremer6,7 and Mridul K. Thomas8
1KelloggBiological Station, MichiganState University, 3700EGull LakeDr., HickoryCorners, MI 49060,USA;
2Departmentof Integrative Biology, MichiganStateUniversity, 288 Farm Lane,East Lansing,MI 48824,USA;
3Departamento deEcolog(cid:1)ıa, Gene(cid:1)ticay Evolucio(cid:1)n, Facultad deCiencias Exactasy Naturales, Universidadde Buenos
Aires, IEGEBA (CONICET-UBA), C1428EHA, BuenosAires, Argentina; 4Departmentof Oceanography, University of
Hawaii at Manoa,1000PopeRoad, Honolulu,HI 96822,USA; 5Department of PlantBiology, MichiganState
University, 612 WilsonRoad, EastLansing, MI48824,USA; 6Department ofEcology and Evolutionary Biology, Yale
University, P.O. Box208106, NewHaven,CT 06520-8106,USA; 7Atmospheric andOceanic Sciences Program,
Princeton University, 300 ForrestalRoad,Sayre Hall, Princeton, NJ08544,USA; and 8Department of AquaticEcology,
Eawag: SwissFederalInstitute ofAquatic Science andTechnology, U€berlandstrasse133, 8600Du€bendorf,
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 significantly alter elemental cycling from local to global scales.
2. We review key traits that distinguish major phytoplankton functional groups, how they affect bio-
geochemistryandhowthelinksbetweencommunitystructureandbiogeochemicalcyclesaremodelled.
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
Such research is especially important as rapid, human-driven
Introduction
changes in our environment affect primary producer commu-
Understanding the links between the structure of primary pro- nities and, ultimately, global biogeochemical cycles. Phyto-
ducer communities and biogeochemistry is an important plankton are major aquatic primary producers, responsible for
research frontier bridging community and ecosystem ecology. about half of global primary productivity each year (Field
et al. 1998). They are key contributors to biogeochemical
*Correspondenceauthor:E-mail:[email protected] cycles,bothatpresentandoverthelonghistoryofourplanet,
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety
Globalbiogeochemical impactsof phytoplankton 1385
and are the subject of extensive experimental, observational Different traits are often not independent but connected by
and theoretical attention. Fully appreciating the role of phyto- trade-offs, and these trade-offs determine how community
plankton in elemental cycling requires characterizing their structure and coexistence change under different conditions,
diversity that encompasses two domains of life and several with concomitant changesin biogeochemical processes. N-fix-
distinct functional groups. These groups differ in how the ers are often thought to have high phosphorus requirements
environment influences their growth, in the elements and comparedtoothergroupsandthusexhibitatrade-offbetween
their ratios that the groups consume and excrete, and, there- N and P competitive abilities (Lenton & Klausmeier 2007).
fore, in their effects on biogeochemistry. We argue that estab- This trade-off can lead to coexistence of N-fixers and non-fix-
lishing effective, mechanistic links between community and ers and can explain shifts in community composition with
ecosystemecologyrequirescharacterizingthetraitsthatdefine changing N: P ratios. Similar trade-offs between N fixation
these groups and their environmental sensitivities. Ultimately, and competitive abilities for light or iron may also be impor-
this kind of trait-based approach can provide critical insights tant (Agawin et al. 2007; de Tezanos Pinto & Litchman
into the biogeochemical function of aquatic and terrestrial 2010; Ward et al. 2013). Whether N-fixers occur under par-
communities, both now and in our increasingly human- ticular conditions has many biogeochemical consequences,
impacted world. In this review, we describe major phyto- because it determines how much ‘new’ nitrogen is being
plankton groups (including their history, traits and involve- added to the ocean, because it affects the stoichiometry of
ment in biogeochemical cycling), how these groups have organic matter exported to the deep ocean and because fixed
been incorporated in biogeochemical models, and discuss N can be released into the environment and consumed by
howthey may beaffected byglobal change. otherprimary producers andother microbes.
What are the advantages of trait-based approaches? Traits In this review, we focus on biogeochemically relevant traits
capture aspects of physiology, morphology and life history and trade-offs to discuss what is known about the feedbacks
that influence fitness and competitive success. Resource utili- between phytoplankton community structure and biogeochem-
zation traits connect species abundances and growth with the istry, with the hope that some of these ideas can also be
chemical compounds that are most limiting for metabolic pro- applied to terrestrial plants. We begin by reviewing the dis-
cesses, thereby linking ecological processes (species and tinct biogeochemical signatures and impacts of the major tax-
community dynamics) with biogeochemical processes through onomic groups of phytoplankton. Next, we discuss modelling
species performance. For example, the rate at which a cell approaches that link phytoplankton community structure and
can take up phosphorus is an important determinant of its key traits to biogeochemical cycles. Finally, we describe
competitive ability in environments where phosphorus limits major global change stressors in aquatic environments and
growth. Integrated over the community, these uptake rates discuss how they can change phytoplankton communities,
feed back to influence external phosphorus concentrations. In selecting for groups and species with certain traits, with con-
other cases, the link between biogeochemistry and ecological sequencesfor biogeochemistry.
success is less direct, and it may be useful to distinguish
between traits that affect biogeochemical cycles (effect traits)
Major phytoplankton groups and their
and the traits that determine how abundances of these groups
biogeochemical signatures
would respond to changing conditions (response traits)
(Lavorel & Garnier 2002). Many phytoplankton traits are Phytoplankton are a paraphyletic group of photoautotrophs
both response and effect traits, but many are only one or the with a complex evolutionary history extending across
other. For example, the optimal temperature for growth is a 2.5–3.5 billion years(Olson&Blankenship2004;Yoon et al.
purely response trait (because temperature affects growth but 2004). Despite this paraphyly, they fall into evolutionarily
not vice versa), and carbon export efficiency is an effect trait distinct functional groups, including one major prokaryotic
that is not tightly linked to a particular response trait. Under- group (the cyanobacteria) and a number of eukaryotic groups
standing how response and effect traits are related will allow (diatoms, green algae, coccolithophorids, dinoflagellates and
us to understand the links between the community structure others).
of primary producers and biogeochemistry in a mechanistic The evolution of oxygenic photosynthesis in cyanobacteria
way. was a major advance in metabolic strategy that changed the
Many groups of primary producers differ both in their fate of our planet forever. This major evolutionary innovation
response and effect traits and, consequently, may have differ- likelyhappened onlyonceandchanged the atmosphere of our
ent impacts on biogeochemical cycling. For example, free liv- planet from anoxic to oxygenic after two billion years in the
ing or symbiotic nitrogen-fixers can fix atmospheric nitrogen former state (Knoll 2003). Vast amounts of solar energy were
(N) and do not require other forms of N. Thus, their N subsequently channelled into driving geochemical cycles
response traits are distinct from those of non-N-fixers. While (Rosing et al. 2006), reducing atmospheric carbon dioxide to
non-fixers consume available N, N-fixers can significantly awiderangeoforganicsubstances(Holm(cid:1)en1992).Significant
increase N concentration in the environment (soil or water), quantities of molecular oxygen started to accumulate in the
thus having contrasting N effect traits as well. The N fixation atmosphere about 2.2–2.4 billion years ago (Catling & Zahnle
response and effect traits are tightly linked, which is true for 2002;Holland2006).ThetimingofEarth’soxygenationcoin-
other resourceacquisition traits. cided with the disappearance of large non-mass-dependent
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
1386 E.Litchman et al.
sulphur isotope (33S and 36S) fractionations (Holland 2006) Prochlorococcus andSynechococcus play an important role in
andofironbandedformations(Isley&Abbott1999),showing the carbon cycle, because they are major components of the
theimpactsofoxygenationonotherelementcycles. photosynthetic biomass in the oligotrophic oceans (Johnson
This process of oxygenation was largely driven by the cy- et al.2006).
anobacteria, which remained the dominant phytoplankton for The eukaryotic taxa originated with the engulfment of a
well over a billion years and strongly influence elemental cyanobacterium by a heterotrophic protozoan, leading to the
cycles today. They are the only phytoplanktonic group with formation of a symbiotic relationship between the two,
members capable of atmospheric nitrogen fixation (the approximately 1.5 billion years ago (Yoon et al. 2004). The
absence of N fixation in eukaryotes is poorly understood, endosymbiotic cyanobacterium subsequently evolved into the
Schopf 1983) that has a major impact on global nitrogen contemporary chloroplast. Thereafter, this eukaryotic clade
cycle. Nitrogen fixation is one of the most metabolically diverged into green and red lineages that differ based on their
expensive processes in biology (16 ATPs are hydrolysed per pigment composition (Delwiche 1999). Subsequent engulf-
N fixed) (Simpson & Burris 1984) and is crucial for Earth’s ment of these green and red eukaryotes by heterotrophs led to
2
nitrogen budget and primary productivity. The evolution of secondary and even tertiary endosymbioses: diatoms, for
the ability to fix nitrogen is thought to be extremely ancient example, are the product of an endosymbiotic event between
(Staley & Orians 1992), possibly older than oxygenic photo- a heterotroph and a red alga (Archibald & Keeling 2002). As
synthesis. Several authors infer that the nitrogenase family a consequence, contemporary eukaryotic phytoplankton are
had already evolved in the last common ancestor of extant composed of two superfamilies. The green superfamily con-
organisms (Normand et al. 1992; Fani, Gallo & Lio 2000), tains the green algae and groups formed by the engulfment of
though another hypothesis suggests a later origin (see Ray- a green alga by a heterotroph, such as the euglenophytes. The
mond et al. 2004). Because nitrogen fixation is a process red superfamily contains the red algae (now largely benthic)
highly sensitive to the presence of oxygen, the evolution of and groups containing red plastids, including diatoms, crypto-
oxygenic photosynthesis posed a major physiological burden phytes and coccolithophores. While both green and red super-
on nitrogen fixation in cyanobacteria. This limitation was families primarily use chlorophyll a, the former also
overcome by fixing nitrogen during the night (in the absence possesses chlorophyll b, while the latter uses chlorophyll c
of oxygen production), hence separating N fixation and pho- and several accessory pigments that absorb blue and green
tosynthesis in time. Another strategy was the separation of wavelengths(Falkowski et al.2004; Katzet al. 2004).
photosynthesis and N fixation in space, by performing N fixa- The eukaryotic superfamilies exhibit distinct stoichiometries
tion in anaerobic specialized cells, heterocysts, during day- from each other and the cyanobacteria. Members of the green
light and photosynthesis in vegetative cells. There could still superfamily possess higher C: P and N: P ratios than their
beother undiscoveredstrategies. counterparts in the red superfamily as well as higher require-
Marine cyanobacteria are responsible for 25–50% of ments for some micronutrients (Fe, Cu and Zn) and lower
natural (i.e. not anthropogenic via the Haber–Bosch process) requirements for others (Cd, Co and Mn; Quigg et al. 2003).
global nitrogen fixation, or approximately 4.5–9 9 These differences in stoichiometry are thought to be related to
1012 mol N year(cid:1)1 (Mahaffey, Michaels & Capone 2005; oceanic environmental conditions when these groups diversi-
Canfield, Glazer & Falkowski 2010; Zehr 2011). This spatial fied, and have important implications for biogeographic pat-
extentof nitrogenfixation islimited bothbytemperature(Sta- terns in ocean N: P ratios, which they both influence and are
al, Meysman & Stal 2003) and by the availability of iron, influenced by Weber & Deutsch (2010). Because functional
which is needed for the production of the nitrogenase enzyme groups also differ in their response to other environmental
(Berman-Frank et al. 2001; Kustka et al. 2003). Conse- variables (characterized by their traits), environment-driven
quently, nitrogen fixation occurs most strongly in the tropical shifts in functional group composition are likely to drive
and subtropical oceans, and in regions with high Fe: N ratios changes in biogeochemical cycles due to shifts in the average
(Monteiro, Dutkiewicz & Follows 2011; Ward et al. 2013). cell stoichiometry. We discuss a few of the major eukaryotic
The process of nitrogen fixation is leaky; between 50 and groupshere, but note that other less studied groups may be of
90% of fixed nitrogen may be released to surrounding waters considerable biogeochemical importance, though we lack data
in the form of dissolved organic nitrogen (Glibert & Bronk with which to draw broad conclusions. These include the
1994; Mulholland & Bernhardt 2005), thereby subsidizing non-calcifying haptophytes,chrysophytes, cryptophytes, raphi-
non-fixers. The cyanobacteria possess the highest N: P ratio dophytes,rhodophytesandeuglenophytes, amongothers.
of any phytoplankton group, with an average N: P ratio of Green algae, the group that gave rise to terrestrial plants,
around 22:1, relative to 13:1 in eukaryotic taxa (data com- evolved >1 billion years ago and comprised a large propor-
piled from earlier studies by Deutsch & Weber 2012). This is tion of the phytoplankton community till the Mesozoic era,
considerably higher in the nitrogen-fixing Trichodesmium sp., approximately 250 million years ago. Thereafter, they
which may be >40:1 due to the high nitrogen requirement for declined in abundance and diversity in the oceans, being
light-harvesting machinery (Letelier & Karl 1996; data com- apparently out-competed by members of the red superfamily
piled from earlier studies by Klausmeier et al. 2004). groups that began to rise in prominence (Falkowski et al.
Although nitrogen fixation is a unique trait of cyanobacteria, 2004; Katz et al. 2004). This decline has been linked to
not all cyanobacteria fix nitrogen. Among those that do not, changes in the redox state of the oceans, with their high trace
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
Globalbiogeochemical impactsof phytoplankton 1387
metal requirements possibly constraining their present marine uptake of silica is responsible for the undersaturation of silica
distribution and diversity (they remain abundant, diverse and in the surface oceans and leads to the burial of
broadly distributed in freshwaters). Unlike the other groups 6.3 9 1012 mol Si year(cid:1)1 through sinking (Tr(cid:1)eguer & De La
described here, they perform no distinctive biogeochemical Rocha 2013). They have low N: P ratios characteristic of the
functions to our knowledge. They are thought to be excep- red superfamily, with an average of approximately 10:1
tionally plastic in their biomass N: P ratio, but this is based (Sarthou et al. 2005), and are most abundant in unstable,
largely on experiments with a single freshwater species, nutrient-rich waters with similarly low N:P ratios, typically at
Scenedesmussp.(Rhee 1978). highlatitudes andincoastal oceans (Arrigo2005).
Coccolithophorids first occur in the fossil record approxi- Dinoflagellates belong to the red superfamily and became a
mately 220 million years ago and rose to prominence through major component of the phytoplankton community over
the Mesozoic era and then declined in diversity as the dia- 200 million years ago, but have decreased in diversity over
toms diversified (Bown, Lees & Young 2004; Falkowski the past 40–60 million years (Katz et al. 2004). They exhibit
et al. 2004; Katz et al. 2004). They form a major portion of exceptionally complex genomes and metabolic capabilities:
high latitude phytoplankton communities today, with massive members of this motile group exhibit mixotrophy (and even
blooms of one major species, Emiliania huxleyi, occurring pure heterotrophy), toxin production, bioluminescence and
over areas of hundreds of thousands of square kilometres tertiary endosymbiosis with complex symbionts such as dia-
(Brown & Podest(cid:1)a 1997). They play a dominant role among toms and prasinophytes (Wisecaver & Hackett 2011). Despite
the phytoplankton in the marine calcium cycle through the belonging to the red superfamily, they also contain members
formation of calcium carbonate plates (coccoliths), which are that have appropriated plastids belonging to the green lineage
responsible for the formation of calcium carbonate rock for- (Falkowski et al. 2004). They possess among the largest phy-
mations across the globe. Although coccolith sinking may be toplankton cells and are typically poor competitors for nutri-
expected to lead to considerable carbon export, the extent of ents and slow growers under autotrophic conditions
the export is a function of sea floor depth and calcium com- (Litchman et al. 2007); mixotrophy allows them to persist
pensation depth. If the ocean floor is lower than the compen- despite this inefficiency, particularly in environments with
sation depth, coccoliths dissolve, returning carbon to the highnutrient andorganic matter concentrations.
water. In total, they are thought to be responsible for approxi-
mately 10% of carbon export to the deep ocean (Jin et al.
Biogeochemical models of phytoplankton
2006). At the same time, calcification reduces total alkalinity,
functional types
reducing the ability of the surface ocean to take up atmo-
spheric CO (Passow and Carlson 2012). Coccolithophores Biogeochemical models aim to explain how biogeochemical
2
also produce dimethylsulfoniopropionate (DMSP), a precursor cycles operate today and operated in the past, and predict
to dimethyl sulphide (DMS), a cloud condensation nucleus. how they will respond to anthropogenic stressors such as cli-
Though there is a clear mechanistic link between coccolitho- mate change. Much of the foundational and current work
phorid growth and climate in this case, the evidence for it as on marine ecosystem models has used a NPZ (nutrient–
a regulator of climate is weak, though it may still play a phytoplankton–zooplankton) structure, where phytoplankton
minor role (Charlson et al. 1987; Ayers & Cainey 2007; are modelled as a single population that consumes a single
Quinn& Bates2011; Rapet al. 2013). limiting nutrient (typically representing nitrogen) and are con-
Diatoms are believed to have originated 160–200 million sumed by a single zooplankton population (Evans and Par-
years ago and diversified strongly in the past 60 million slow 1985, Fasham et al. 1990, Franks 2002). NPZ models
years, at the expense of other groups (Kooistra & Medlin are formulated and parameterized by combining laboratory
1996; Falkowski et al. 2004; Sims, Mann & Medlin 2006). data on plankton traits, field observations of bulk stocks and
Their recent dominance may be a result of their ability to rates, and theoretical considerations such as dynamical stabil-
store pulses of nutrients in a large vacuole supported by the ity. Although they greatly simplify biological complexity,
silica cell wall and/or protection from predation accorded by NPZ models are useful for theoretical exploration and have
their silica shells (Smetacek 1999; Thingstad et al. 2005; successfullyrepresentedecosystem patternsinmanysituations
Litchman, Klausmeier & Yoshiyama 2009). As other func- (Franks 2002). More complex models have been developed to
tional groups do not use silica, the ability to compete for this address questions such as the role of multiple limiting nutri-
element does not contribute to their success against other ents and their biogeochemical coupling, because iron, phos-
functional groups, but may contribute towards determining phorus and silicon may all limit phytoplankton growth in
which diatom species predominate. Globally, they play a additionto nitrogen (Flynn2003,Mooreet al.2013).
dominant role in the carbon cycle, contributing an estimated It has also become clear that incorporating the functional
20–25% of global primary productivity (Nelson et al. 1995; diversity of phytoplankton is important for modelling biogeo-
Smetacek 1999). Their relatively large cell sizes lead to a chemical cycles, because community structure varies greatly
highsinkingratewhichcontributestomajorportionofcarbon in time and space, and different kinds of phytoplankton have
export to the deep oceans (Nelson et al. 1995). They are also distinct effects on carbon fixation and export, as well as the
the primary phytoplankton group associated with the global cycling of N and Si among other elements (Le Qu(cid:1)ere et al.
silica cycle (with silicoflagellates playing a minor role). This 2005, Hood et al. 2006). The most common way biogeo-
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
1388 E.Litchman et al.
chemical models have incorporated functional diversity is by The higher nutrient affinity of smaller cells has a sound
including multiple plankton functional types (PFTs) in the theoretical basis (Pasciak & Gavis 1974) with empirical sup-
ecosystem (Le Qu(cid:1)er(cid:1)e et al. 2005). These types are given port (Edwards et al. 2012). What traits allow larger phyto-
parameters that represent response traits and effect traits, with plankton to prosper in seasonal environments, upwelling
values derived from laboratory and field experiments, guesses regions and productive continental shelves, and how are these
based on observed distributions and post hoc tuning to bring traits incorporated into biogeochemical models? Interestingly,
modelled distributions in line with the available data (Moore this appears to be a somewhat unresolved question, as there
et al. 2002; Aumont et al. 2003; Gregg et al. 2003; Le Qu(cid:1)er(cid:1)e are multiple mechanisms that could allow larger phytoplank-
et al. 2005; Litchman et al. 2006). We cannot review all ton to become abundant, and some or all of these have been
approaches to modelling PFTs in this article, but we will incorporated in different models. We summarize these mecha-
compare a number of representative models to explain how nismsas follows:
traitvariation is translated intomodel parameterization. 1. Larger phytoplankton experience a lower per capita graz-
Plankton functional types models are an excellent first step ing rate, which allows them to become relatively more
to introducing trait diversity into biogeochemical models, abundant if resources are not strongly limiting (Kiørboe
due to the distinct roles of these types in biogeochemical 1993; Smetacek1999).
cycles, but still neglect finer-scale diversity within each 2. Some larger phytoplankton (e.g. diatoms) have a higher
group. There are additional emerging trait-based modelling maximum growth rate, which allows them to capitalize on
frameworks that can include greater trait diversity. These transiently high nutrient concentrations (Mara~n(cid:1)on2014).
include random selections from a high-dimensional trait 3. Large phytoplankton (diatoms) have greater nutrient
space (Follows et al. 2007), continuous trait distributions (nitrate) storage capabilities that afford a competitive
parameterized with putative trade-offs (Bruggeman & Kooij- advantage under fluctuating nutrient regimes (Litchman,
man 2007; Ward et al. 2012), flexible physiological alloca- Klausmeier & Yoshiyama 2009).
tion strategies (Klausmeier et al. 2004; Clark et al. 2013), 4. Small and large phytoplankton are eaten by different gra-
optimality approaches (Smith et al. 2011) and approaches zer species (different size classes of grazers). As nutrient
from evolutionary game theory (Litchman, Klausmeier & supply increases, small phytoplankton are controlled by
Yoshiyama 2009). The focus of these fully trait-based theirgrazers, leavingsufficientremainingnutrientsfor lar-
approaches shifts from modelling the dynamics and distribu- gerphytoplankton topersist (Armstrong 1994).
tion of species or functional groups to modelling the distri- 5. Larger phytoplankton are eaten by slower-growing meta-
bution of traits. Synthesizing these more flexible approaches zoangrazers,whichallowsthemtotransientlyescapegraz-
with distinct functional categories will likely be an important ingcontrolwhennutrientsandlightaresufficient(Irigoien
future direction, although realistic parameterization of multi- 2005).
dimensional trait variation among multiple groups remains a
significant empirical challenge. Different combinations of these mechanisms appear in dif-
A major form of functional diversity derives from phyto- ferent models. For example, Follows et al. (2007) have a lar-
plankton cell size. Cell volume varies over nine orders of ger diatom-like class and a smaller picocyanobacteria-like
magnitude and is a ‘master trait’ that affects metabolic rates, class, and the former is given a higher mean maximum
light absorption, nutrient uptake, sinking rate and interaction growth rate. This allows them to dominate under variable
with grazers (Chisholm 1992, Litchman and Klausmeier nutrient supply, that is as ‘opportunists’ as opposed to the
2008, Finkel et al. 2010). Size plays a central role in biogeo- small ‘gleaners’ (Grover 1991; Dutkiewicz, Follows & Bragg
chemistry because phytoplankton of different sizes have dis- 2009; Litchman, Klausmeier & Yoshiyama 2009). Although
tinct biogeographies and effects on the carbon cycle. Models the general allometric trend is for larger species to grow more
often incorporate this variation by using two or three size slowly (Edwards et al. 2012), the smallest phytoplankton tend
classes (Moore et al. 2002; Aumont et al. 2003; Blackford, togrowmoreslowlythanintermediate-sized diatomsandcoc-
Allen & Gilbert 2004), or by using functional types whose colithophores (Ward et al. 2012; Mara~n(cid:1)on 2014), which is
parameterization is based in part on size differences (e.g. consistent with this modelling approach. This model also has
mixed phytoplankton, diatoms, coccolithophores; Le Qu(cid:1)er(cid:1)e two size classes of grazers, which will allow mechanisms 3
et al. 2005). Smaller size classes are typically given lower and 4 to operate as well. In contrast, in the biogeochemical
half-saturation constants for nutrient-limited growth or nutri- element cycling model of Moore et al. (2002), the diatoms
ent uptake (Moore et al. 2002; Dutkiewicz, Follows & Bragg and nanophytoplankton have the same maximum growth rate
2009; Buitenhuis, Hashioka & Le Quere 2013). This has the and are eaten by the same grazer, but the grazer feeds more
effect of making smaller phytoplankton better competitors for slowly on diatoms. This implies that mechanisms 1 and 4 can
nutrients under chronic limitation, that is they have a lower operateinthis model.
R* (Tilman 1982, Litchman 2007, Litchman et al. 2007, Du- Although size is a master trait that affects many ecological
tkiewicz, Follows & Bragg 2009). In models, a lower R* processes, there are other kinds of functional variation that
allows smaller phytoplankton to dominate in permanently are important for biogeochemical models. Diatoms, in addi-
stratified or chronically iron-limited regions (Moore et al. tion to being relatively large on average, require silica for
2002; Dutkiewicz,Follows &Bragg 2009). growth. This dependency is often modelled as an additional
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
Globalbiogeochemical impactsof phytoplankton 1389
nutrient limitation term, and this can cause their regional pat- traits will lead to diazotroph occurrence in stably stratified
terns of growth limitation to be distinct from other phyto- regions with a low supply ratio of N: Fe and N: P (Ward
plankton types, due to variation in the supply of Si relative to et al. 2013). Although most ocean biogeochemical models
other elements (Moore et al. 2002; Aumont et al. 2003; represent diazotrophs by a single group, some models
Blackford, Allen & Gilbert 2004). They are also thought to include different diazotroph types with distinct traits, such as
contribute disproportionately to carbon export from the filamentous Trichodesmium, unicellular N-fixers and symbi-
euphotic zone, due to a number of potential factors: their lar- otic N-fixers living inside diatoms (e.g. Monteiro, Follows
ger size (on average), the boom-and-bust phenology of some & Dutkiewicz 2010).
species, the ‘ballasting’ effect of the silica frustule and
reduced grazing rates (Smetacek 1999; Assmy et al. 2013).
Responses of phytoplankton communities to
Some of these effects will emerge naturally if the functional
global environmental change and implications
type representing diatoms is given a higher maximum growth
for biogeochemistry
rate or lower grazing rate, as described above. The increase in
export due to larger size or ballasting can be modelled with Themanydimensionsofglobalchangeareincreasinglyaffect-
anincreasedsinkingrateofnon-grazedand/orgrazedbiomass ing marine environments and the phytoplankton communities
(Moore et al. 2002; Litchman et al. 2006; Follows et al. that inhabit them. In the following section, we briefly summa-
2007). rizethemostimportantaspectsoftheoceanthatarechanging,
Coccolithophoresplay adistinct biogeochemical roledueto including temperature, acidity and nutrient availability. The
calcification and ballasting of organic matter and have a dis- traitsandfunctionsofphytoplanktongroupsandspeciesdeter-
tinct (and likely varied) ecology that is still being unravelled mine both how they are affected by global change and how
(Boyd et al. 2010). Their traits have been modelled in a vari- their responses in turn alter global biogeochemistry. In the
ety of ways, although a general aim is to reproduce the fact remaining text, we discuss how global change stressors influ-
that they bloom undermore stratifiedconditions than diatoms, ence phytoplankton across different levels of biological orga-
but are likely poorer nutrient competitors than picophyto- nizationfromfunctionalgroupstospecies.
plankton. Gregg & Casey (2007) give coccolithophores a Global change is multifaceted and includes not just CO
2
half-saturation constant for nitrogen-limited growth that is emissions and climate change, but also anthropogenic effects
higher than that of cyanobacteria but lower than that of dia- thatareindependentofthesefactors.Acidification,risingtem-
toms,aswellasanintermediatemaximumgrowthrate(which peratures and changes in the supply of nutrients and light will
is highest for diatoms in this case) and a relatively high irra- posethe greatest challenges for marine ecosystems and phyto-
diance requirement. In this formulation, they essentially have plankton communities. Several reviews have examined these
an intermediate position on a gleaner–opportunist trade-off effects in greater detail (e.g. Hoegh-Guldberg & Bruno 2010;
axis (Margalef 1978; Kudela 2010; Edwards, Klausmeier & BoydandHutchins2012,Doneyet al.2012),sooursummary
Litchman 2013). In contrast, the PlankTOM10 model gives is brief. World-wide, oceans act as a major sink for both the
coccolithophores a relatively slow maximum growth rate, rising levels of atmospheric CO and the increased amount of
2
intermediate nutrient affinity traits and a minimum tempera- heat trapped by this CO and other greenhouse gasses. Nearly
2
ture threshold that is lower than that of the picocyanobacteria 1/3 of anthropogenic CO is being absorbed into the oceans,
2
that are the best nutrient competitors (Kwiatkowski et al. where it interacts with water, altering seawater carbonate
2014, http://lgmacweb.env.uea.ac.uk/green_ocean/model/ chemistryanddrivingoceanacidification(Riebesell2004;Do-
code_description/PFT/fluxes.html). An increased efficiency of ney et al. 2009; Hoegh-Guldberg & Bruno 2010). Tempera-
carbon export for coccolithophores, due to ballasting, can be tures have risen by ~0.6 °C over the last 100 years within the
implemented with a higher sinking rate (Moore et al. 2002; surface layers of the ocean (Hoegh-Guldberg & Bruno 2010)
Gregg &Casey 2007). andarepredicted to increase byanother 1–3 °C bythe end of
Diazotrophs (nitrogen-fixers) are an important functional the century (IPCC; Collins et al. 2013). Temperature plays an
type, due to their unique role in the nitrogen cycle. They important role in physical ocean processes, driving mixing,
are thought to prosper under extreme nitrogen limitation, vertical stratification and currents. In tropical and temperate
while suffering a number of disadvantages described earlier. regions, warmer temperatures lead to stronger stratification
They are often modelled as having a relatively high iron and shallower mixed layers, simultaneously intensifying nutri-
requirement, which makes them poor competitors when iron ent limitation and reducing light limitation (as plankton avoid
supply is low relative to N and P (Moore et al. 2002; Ward being mixed to deeper, darker regions) (Beardall, Stojkovic &
et al. 2013). They are also typically given a low maximum Larsen 2009). Regionally, warming may strengthen coastal
growth rate, which means they cannot take advantage of upwellingandnutrientsupplyandalterthedepthofmixingin
variable nutrient supply (Tyrell 1999, Moore et al. 2002; polar oceans (Hoegh-Guldberg & Bruno 2010). Temperature
Monteiro, Dutkiewicz & Follows 2011). It may also be and pH also influence the chemistry of seawater; changes in
important for diazotrophs to be poor P competitors (Tyrrell both of these variables will alter the solubility and oxidation
1999; Lenton & Klausmeier 2007; Ward et al. 2013), stateoftracemetalssuchasironinwaysthatarenotyetfully
although a relatively low P stoichiometry will at least par- understood(Hoffmannet al.2012).Thesechangeswillbesig-
tially offset this (Moore et al. 2002). In combination, these nificant for marine organisms requiring these trace metals
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
1390 E.Litchman et al.
often as catalysts for critical biochemical processes. The sup- of diverse and interacting species, are exceedingly complex in
ply of more abundant (though no less important) nutrients their own right. We can organize this complexity by consider-
suchasnitrogenandphosphateisalsobeingalteredbyhuman ing how global change affects phytoplankton at different eco-
activities. This occurs most dramatically in coastal regions, logical resolutions,ranging fromthe collective response of the
through the influx of agricultural run-off and sediments from phytoplankton as a whole to the fine-scale reactions of indi-
rivers, but also includes atmospheric deposition of dust and vidual species (Fig. 1). These categories roughly correspond
combustion by-products. Ultimately, these nutrients affect to the level of detail included in different biogeochemical
microbial communities producing areas of hypoxia, especially models of phytoplankton communities as discussed in ‘bio-
in coastal regions (Diaz & Rosenberg 2008), and altering bio- geochemical models of phytoplankton functional types’,
geochemical processes. Finally, climate-driven changes in which range from as coarse as one or a few functional
weather patterns and cloud cover, among other factors, alter groups, to dozens of species. Determining the appropriate
theamountoflight(andespeciallyultravioletradiation)reach- level of detail to resolve is a critical open research question,
ing and penetrating the ocean surface (Beardall, Stojkovic and which likely depends on which ecological or biogeochemical
Larsen2009). features are of interest, and the degree of precision required.
Adding to the complexity of global change is the fact that Thefollowing discussion examines eachof these categories in
few environments will experience only one of these changing turn,startingwith the broadest andmost simplifiedview.
stressors: marine organisms may simultaneously face rising At the coarsest scale, briefly setting aside the particulars of
temperatures, changing nutrient levels and acidification (Halp- species or functional group identity, photoautotrophs such as
ern et al. 2008). The combined effects of multiple stressors phytoplankton are united in their requirement for light, nutri-
can be non-additive and nonlinear, so global change studies entsandCO tosupporttheirgrowthandproductivity.Ifbasic
2
for most environments or species must consider the effects of requirements are either not met or dramatically exceeded (e.g.
a suite of stressors (Crain, Kroeker & Halpern 2008; Boyd photoinhibition or nutrient toxicity), whether through regional
2013; Boyd et al. 2015). Many aspects of global change also variationorglobalchange,growthandproductivityarelimited
exhibit significant regional variability on top of underlying (Fig. 1a).Modellingstudiesthatincludeagenericphytoplank-
global trends (Hansenet al. 2006). ton component, with parameters based on these requirements,
As complex as global change is, understanding its effects improve biogeochemistry models and can reproduce empirical
on phytoplankton and marine ecosystems presents an even patternsofnutrientdistributions(Kriest,Khatiwala&Oschlies
greater challenge, becausethese ecological systems, composed 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 influencing 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.Changesinbulkpropertiesofphytoplankton,suchastheirproductivity,canalterenergyfluxesandcarboncycling.Increas-
ing stratification can reduce productivity in temperate and tropical oceans. (b) Intergroup. Functional groups within phytoplankton communities
canresponddifferentlyto sharedstressors, alteringtheir relative abundance.Diazotrophsmay becomemorecommoninnitrogen-limited waters,
alteringNcycling.(c)Intragroup.Turnoverintheidentityandabundanceofparticularspecieswithinagroupmayalteritsfunctioning.Nutrient
limitationfavourssmall-celledspecies,influencingratesofzooplanktonpredationandcarbonexporttothedeepocean.(d)Intraspecific.Individ-
ualspeciesmaychangetheirtraitsandfunctionasaresultofglobalchange,throughplasticityorrapidevolution.AswithC,thiscouldleadto
smallercellsizesinthecaseofnutrientlimitation.
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
Globalbiogeochemical impactsof phytoplankton 1391
change-driven shifts in the abundance, productivity and func- tional groups with traits required to compete effectively for
tion of phytoplankton as a whole. Empirical evidence of such nutrients or access unique resources. Major functional groups
broadtrendsisactivelybeingsoughtandevaluated.Forexam- differ in their sizes: diatoms and dinoflagellates typically have
ple, studies combining in situ and satellite measurements of cell volumes that are orders of magnitude larger than cyano-
chlorophyll have shown a negative relationship between sea bacteria, while green algae and haptophytes are intermediate
surface temperature and net primary productivity (from 1999 in size (Diaz & Rosenberg 2008; Finkel et al. 2009). Large
to2004,Behrenfeldet al.2006),andpotentialdeclinesinpro- diatoms and other large-celled species perform well in sea-
ductivity over the last 100 years (Boyce, Lewis & Worm sonal environments with significant, albeit periodic, supplies
2010; but see McQuatters-Gollop et al. 2011 and Mackas of nutrients (Beardall, Stojkovic and Larsen 2009, Litchman,
2012). The former result holds across three quarters of the Klausmeier & Yoshiyama 2009). However, as stratification
world’s permanently stratified oceans and is hypothesized to intensifiesandnutrient-limited oceanregionsexpandwithglo-
be driven by increases in stratification and nutrient limitation bal change (Behrenfeld et al. 2006; Halpern et al. 2008;
(Behrenfeld et al. 2006). However, these trends are debated; Irwin & Oliver 2009), smaller-celled species and groups and
they are influenced by changes in instrumentation (Beaulieu nitrogen-fixing cyanobacteria will be competitively favoured
et al. 2013) and may not be large enough to exceed the range and increase in abundance at the expense of other groups,
of ‘natural’ background variability (Henson et al. 2010). If such as diatoms (Bopp et al. 2005; Crain, Kroeker & Halpern
such trends hold, isolating and determining their causes may 2008; Mor(cid:1)an et al. 2010). Potential increases in the abun-
stillrequireamoredetaileddescriptionofphytoplanktoncom- dances of nitrogen-fixers would have obvious, direct effects
munities. We next consider trait differences at the functional on nitrogen cycling. Changes in the size-structure of phyto-
group level, highlighting how variation influences their plankton communities may be just as significant for biogeo-
response to different stressors, highlighting acidification and chemical cycling. Smaller phytoplankton, especially those
nutrientlimitationasexamples. withouthardshells, arelesslikelytosink,limiting theirdirect
The distinct traits of different functional groups may cause contributions to carbon export. Indeed, Bopp et al. (2005)
functional groups to respond differently to global change found that as oceans warm, small phytoplankton replaced dia-
stressors, altering their relative abundances, community func- toms in an ocean biogeochemical model, leading to increased
tion and ultimately global biogeochemical cycling (Fig. 1b) rates of carbon and nutrient recycling and decreased export
(Doney et al. 2009; Hoegh-Guldberg & Bruno 2010; Litch- ratios. These results are supported by another modelling study
man et al. 2012). Functional groups differ in their ability to documenting increases in groups of phytoplankton species
competefor CO ,ranging frompassiveCO uptaketosophis- that are small (and good nutrient competitors) due to nutrient
2 2
ticated mechanisms for actively collecting CO and bicarbon- limitation, with regional exceptions driven by iron supply
2
ate (HCO (cid:1)). While many groups (including diatoms) are not (Dutkiewicz,Scott & Follows2013).
3
carbon limited, others, such as the coccolithophorids, show The effects of global change on size-structure and subse-
dramatic increases in photosynthetic rate with increases in quentlyonproductivityandbiogeochemistrycanalsobeampli-
CO (Rost et al. 2003; Riebesell 2004; Doney et al. 2012). fiedbytrophicinteractions(Hansen et al.2006; Stock,Dunne
2
Suchtrait differences likely explain shiftsfrom diatomto coc- & John 2014). Smaller phytoplankton support different zoo-
colithophoriddominanceduetoCO enrichmentinmesocosm plankton predators, primarily smaller crustaceans and gelati-
2
experiments (Riebesell 2004; Hoegh-Guldberg & Bruno nous species (micro- and mesozooplankton) compared to the
2010). Shifting elemental ratios within sedimenting particles larger crustaceans that dominate in seasonal and polar regions
in the North Atlantic suggest that abundances of diatoms and (Redfield 1958; Richardson 2008). This alters food chain
coccolithophores are already changing (Antia et al. 2001; length,leadingtolessproductivezooplanktoncommunitiesthat
Beardall, Stojkovic and Larsen 2009). While increased CO provide a poorer resource for higher trophic levels. It can also
2
appears to favour coccolithophorid growth, ocean acidification influencetheamountofcarbonexportresultingfrompredation;
increases the difficulty and energetic costs of forming the cal- some zooplankton groups produce faecal pellets that rapidly
cium carbonate plates after which they are named. The eco- sink from the surface exporting carbon, while others excrete
logical consequences of producing thinner, deformed shells more labile forms of carbon that persist in the water column.
due to acidification (Riebesell 2004; Hoegh-Guldberg & Rising temperatures associated with stratification and nutrient
Bruno 2010) are not conclusively known, but may include limitation may also alter the stoichiometry of phytoplankton,
increased susceptibility to predation. Ultimately, the net effect changing their value as a resource for zooplankton (Kriest,
of these organisms on carbon cycling depends on the balance Khatiwala&Oschlies2010;Yvon-Durocheret al.2015).
between carbon export to deep waters and carbon emissions Functional groups themselves are composed of many
during calcification, determined by interactions between their individual species representing significant amounts of trait
sensitivity to CO , acidification and competition with other variation and subject to trade-offs between traits. Global
2
groups (Riebesell 2004; Beardall, Stojkovic and Larsen 2009, change has the potential to affect both the presence/absence
Hoffmann et al.2012). and abundance of particular species within a functional group
Acidification is not the only stressor influencing the relative in a given location or environment (Fig. 1c). Environmental
abundance of functional groups. Nutrient limitation, intensi- conditionsandcompetitiveinteractions winnowoutsome spe-
fied by stratification due to rising temperatures, favours func- cies, while creating opportunities for others. When changing
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
1392 E.Litchman et al.
community composition alters the functional contributions of previously. In addition to physiological changes, evolutionary
a group, global change can affect biogeochemistry at the in- responses are likely within the phytoplankton due to their
tragroup level. Such dynamics occur in response to climate small size, huge populations and rapid generation times.
change within an intermediate complexity Earth system These responses might allow species to adapt to conditions
model, as the ranges of individual species expand and con- imposed by global change, suggesting that (over longer
tract based on their trait differences (including growth rates, time-scales) communities might recover from short-term per-
temperature optima, size and half-saturation constants), lead- turbations. Understanding the effects of evolutionary
ing to substantial turnover in the composition of local com- responses to global change is a complex process, requiring
munities (Dutkiewicz, Scott & Follows 2013). Several detailed, specific knowledge of how environments will
examples exist of between-species trait variation with the change, how quickly phytoplankton can adapt and what
potential to produce intragroup level biogeochemical effects, genetic constraints or trade-offs limit them. Experiments
limited seemingly only by the number of traits and environ- designed to investigate these questions are becoming more
mental factors studied so far. Biogeochemical rates are funda- common,but muchwork remains tobedone.
mentally linked to biological rates, such as growth rate. Ultimately, understanding how the effects of global change
Growthratesarestronglylinkedtotemperature,yetindividual will propagate through phytoplankton communities to influ-
species often differ dramatically in their temperature depen- ence biogeochemical cycling requires understanding the indi-
dence (Thomas et al. 2012; Boyd et al. 2013). In turn, these vidual and combined effects of stressors on phytoplankton
differences lead to predicted range shifts as oceans warm from species to functional groups. The key to obtaining this
(Thomas et al. 2012). Looking beyond temperature, different knowledge rests on elucidating the links between environ-
coccolithophorid species and strains engage in calcification to ment, species traits and trade-offs, and their performance and
varying degrees, with important consequences for productivity function.
and carbon cycling. In nitrogen-fixing cyanobacteria,
responses toCO are diverse: elevated CO stimulated growth
2 2 Conclusions
and N fixation in Trichodesmium species and Crocosphaera
2
watsonii, important open ocean diazotrophs (Behrenfeld et al. Understanding the feedbacks between phytoplankton commu-
2006; Beardall, Stojkovic and Larsen 2009, Hutchins et al. nity structure and biogeochemistry is a burgeoning area of
2013), but inhibited these processes in coastal Nodularia research. Distinct functional groups have been shaping the
spumigena (Czerny, Barcelos e Ramos & Riebesell 2009; biogeochemistry of our planet, from the period of oxygena-
Boyce,Lewis&Worm2010).Inthiscase,turnover incyano- tion ushered in by the cyanobacteria to contemporary patterns
bacteria species driven by rising CO might actually support ofNfixation andcarboncycling intheoceans. Understanding
2
consistentlevelsof function(N fixation)inthefaceof global the physiology and ecology of these groups is continuing. We
2
change. Overall, the effects of species turnover within func- are still learning about new members of the phytoplankton
tional group will depend on which species are favoured by (Cuvelier et al. 2010), the environmental sensitivities and
the combinations of global change stressors experienced by traits of even the well-studied groups (Boyd et al. 2010),
communities regionally and how these species contribute to approaches for efficiently modelling diverse plankton commu-
ecosystem function. nities and multiple element cycles (Stock, Dunne & John
Finally, within a functional group, individual species need 2014), and methods for conceptually managing complex glo-
not have fixed traits (Fig. 1d). Even within primarily asexual bal change (Boyd et al. 2015). These are crucial problems in
phytoplankton, species consist of multiple strains with differ- an era of global change. Quantifying the traits and trade-offs
ent traits, representing standing genetic and phenotypic varia- that affect functional group composition will help connect
tion. In addition to between-species differences in the communityresponses to biogeochemical causesandeffects.
sensitivity of N fixation rates to pCO , Hutchins et al. (2013) A challenging empirical aspect of this approach is the num-
2
demonstrated significant strain-level variation. Given this vari- ber of important traits that must be gathered, especially given
ation, increasing CO concentrations may select for particular trait variation between functional groups, species and popula-
2
strains, influencing future biogeochemistry in complex ways. tions. Which traits do we need to measure in order to predict
The traits of species also respond to environmental changes functionalgroupdynamics? Predicting theoutcome of compe-
through physiological, behavioural and evolutionary mecha- tition between two populations requires knowledge of traits
nisms. For example, the lipid content of several species of relating to competition for resources (macronutrients,
Antarctic diatom (in the genus Navicula) declines with micronutrients and light) and avoidance of predators, all of
increasing temperature, making them a poorer resource for which differ between groups (Litchman and Klausmeier 2008;
zooplankton(Teoh,Phang&Chu2012).Manyphytoplankton Boyd et al. 2010; Edwards et al. 2012, 2015). However, this
are capable of nutrient storage and exhibit variable stoichiom- task is made easier because of several fundamental con-
etries through a variety of physiological mechanisms. straints, including both allometric and phylogenetic relation-
Changes in the stoichiometry of individual species can be of ships. Many traits scale strongly with cell size and
similar magnitude to effects driven by turnover between spe- temperature, including cellular stoichiometry (Yvon-Durocher
cies (Behrenfeld et al. 2006; Finkel et al. 2009). This can et al. 2015). Due to the physical constraints that size and
influence their value as a food resource as mentioned shape place on cells’ ability to obtain nutrients, cell size cor-
©2015TheAuthors.JournalofEcology©2015BritishEcologicalSociety,JournalofEcology,103,1384–1396
Globalbiogeochemical impactsof phytoplankton 1393
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