Journal of
Plankton Research
plankt.oxfordjournals.org
J. Plankton Res. (2013) 35(1): 3 –11. First published online September 12, 2012 doi:10.1093/plankt/fbs062
HORIZONS
Misuse of the phytoplankton –
zooplankton dichotomy: the need
to assign organisms as mixotrophs
within plankton functional types
KEVIN J. FLYNN1*, DIANE K. STOECKER2, ADITEE MITRA1, JOHN A. RAVEN3, PATRICIA M. GLIBERT2, PER JUEL HANSEN5,
EDNA GRANÉLI4 AND JOANN M. BURKHOLDER6
1
2
CENTRE OF SUSTAINABLE AQUATIC RESEARCH (CSAR), SWANSEA UNIVERSITY, SWANSEA SA2 8PP, UK, UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL
3
SCIENCE, HORN POINT LABORATORY, PO BOX 775, CAMBRIDGE, MD 21613, USA, DIVISION OF PLANT SCIENCES, UNIVERSITY OF DUNDEE AT THE JAMES
4
HUTTON INSTITUTE, INVERGOWRIE, DUNDEE DD2 5DA, UK, MARINE SCIENCES CENTRE, LINNAEUS UNIVERSITY, 39182 KALMAR, SWEDEN,
5
6
MARINE BIOLOGICAL SECTION, UNIVERSITY OF COPENHAGEN, STRANDPROMENADEN 5, DK-3000 HELSINGØR, DENMARK AND CENTER FOR APPLIED AQUATIC
ECOLOGY, NORTH CAROLINA STATE UNIVERSITY,
620
HUTTON STREET, SUITE
104, RALEIGH,
NC, USA
*CORRESPONDING AUTHOR: [email protected]
Received April 3, 2012; accepted August 17, 2012
Corresponding editor: Marja Koski
The classic portrayal of plankton is dominated by phytoplanktonic primary producers and zooplanktonic secondary producers. In reality, many if not most plankton
traditionally labelled as phytoplankton or microzooplankton should be identified
as mixotrophs, contributing to both primary and secondary production. Mixotrophic protists (i.e. single-celled eukaryotes that perform photosynthesis and graze
on particles) do not represent a minor component of the plankton, as some form
of inferior representatives of the past evolution of protists; they represent a major
component of the extant protist plankton, and one which could become more
dominant with climate change. The implications for this mistaken identification, of
# The Author 2012. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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the incorrect labelling of mixotrophs as “phytoplankton” or “microzooplankton”,
are great. It extends from the (mis)use of photopigments as indicators of primary
production performed by strict photoautotrophs rather than also (co)locating mixotrophic activity, through to the inadequacy of plankton functional type descriptions
in models (noting that mixotrophic production in the individual organism is not a
simple sum of phototrophy and heterotrophy). We propose that mixotrophy should
be recognized as a major contributor to plankton dynamics, with due effort
expended in field and laboratory studies, and should no longer be side-lined in
conceptual food webs or in mathematical models.
KEYWORDS: phytoplankton; microzooplankton; primary production; secondary
production; mixotroph; model; plankton functional type
I N T RO D U C T I O N : D E F I N I N G
T E R M S I N P L A N K TO N E C O LO G Y
refer to protists that feed on particles through phagotrophy. This conflicts with the allometric division because
some “microzooplankton” are larger than early life
stages of many “mesozooplankton”; they may, unlike
metazoan zooplankton, also predate much larger particles than themselves (including mesozooplankton and
large detritus particles (Poulsen et al., 2011; Berge et al.,
2012) and so disturb conventional expectations of allometric scaling in trophic dynamics. Despite the fact that
protist-microzooplankton grazing on “phytoplankton” is
at least as important as that undertaken by mesozooplankton (Calbet and Landry, 2004), and that copepods
(and their allies) obtain much of their food by grazing
on protists (Calbet and Saiz, 2005; Fileman et al., 2010),
it is the copepods that are still typically accorded the
term “herbivore”, suggesting that they are the major
secondary producers.
Adding to this complexity (and confusion) are the
terms “microbe” and “microbial loop”. A microbe is an
organism that is microscopic, which by definition
includes all of the above-mentioned organisms (excepting
the larger mesozooplankton), and not just bacteria or a
bacterial-centric trophic pathway. The term “microbial
loop” (Azam et al., 1983; Jiao et al., 2010) encapsulates
the concept of return of dissolved organic carbon to
higher trophic level via its incorporation into bacterial
biomass, but it is really a description of organic carbon
recycling through the microbial food web consisting of
bacteria, cyanobacteria, viruses and protists.
Then there are the physiological terms of “autotroph” and “heterotroph”. The meanings of autotrophy
and heterotrophy have clear definitions, and groups of
plankton are typically described (or assumed) as being
solely of one or other nutritional (functional) type.
However, confusion arises when both nutritional pathways co-occur within a single organism, i.e. within the
“mixotrophs”. The term “mixotroph” is used here to
describe an organism that undertakes some
In both teaching and research, the open water
planktonic food web is typically characterized as
containing predominantly bacteria, phytoplankton,
microzooplankton and mesozooplankton. We all know
what these terms mean; or do we? And does our terminology and use of these terms reflect our current
state of knowledge? We commence by considering
the meaning of common descriptors in plankton
research, for it is within that framework that the mixotrophic protists, which are the subject of this commentary, reside.
Bacteria as a group should be readily and clearly
defined, and yet, depending on the application, this
group may or may not include cyanobacteria, which
may or may not be included within phytoplankton;
cyanobacteria (usually, but not always, considered
functionally to include Prochlorococcus) may, or may not,
be accorded their own group. Phytoplankton, i.e. the
planktonic photosynthetic eukaryotes and prokaryotes,
are often (at least colloquially) considered to perform a
role analogous to that of higher plants in terrestrial
ecology. In older texts, phytoplankton biomass may
even be given units of “plant pigments” (Cushing, 1975),
and are thus fed upon by “herbivorous” zooplankton
(Cushing, 1975; Fasham, 1995). Microzooplankton and
mesozooplankton are, according to the prefix of each
term, delimited by size. In practical terms, as divided
using filters and meshes, the range for microzooplankton is generally considered to be 20– 200 mm (nanoplankton at 2– 20 mm), with mesozooplankton in the
range of 200 – 2000 mm; these sizes equate to wet
weight ranges (nanoplankton weigh nanogram, microplankton weigh microgram etc.) (Gifford and Caron,
2000). However, the term “microzooplankton” can also
be taken to mean unicellular zooplankton, and thus
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combination of both photoautotrophic and heterotrophic activity. Technically, the heterotrophic component
may involve osmotrophy (using dissolved organic substrates) and/or phagotrophy. However, almost certainly,
all “phytoplankton” (eukaryote and prokaryote) are in
part osmotrophs, not least by virtue of being auxotrophic; many need external sources of one or more vitamins
(Croft et al., 2006). Further, in the majority that have
been surveyed, “phytoplankton” exhibit significant
levels of non-auxotrophic osmotrophy, especially with
respect to the uptake of amino acids and other primary
metabolite compounds (Flynn and Butler, 1986;
Berman and Bronk, 2003; Mulholland et al., 2003;
Glibert and Legrand, 2006; Lindehoff et al., 2011).
Likewise, protist “microzooplankton” can also engage in
osmotrophy (Droop, 1959; Sanders, 1992). The use of
osmotrophy as a discriminating feature of mixotrophy
in planktonic protists thus appears weak (de facto all
phytoplankton are mixotrophs by such a definition),
and hence in practice, phagotrophy coupled with
phototrophy is a more useful discriminator. (In passing,
it should be noted that phagotrophy is not a processes
seen in prokaryotes, thus cyanobacteria could not be
considered as mixotrophs by virtue of phototrophy þ
phagotrophy.) Phagotrophy, especially when it involves
the death of another organism, not only has implications for the growth of the mixotroph, but it also has
other important impacts on trophic dynamics.
Clearly, the terminology we use in our science has
not evolved in step with our understanding of plankton
ecophysiology, and certainly not with advances in our
appreciation of nutritional diversity in protists. Emerging
out of concepts in which planktonic “plants” and
“animals” were thought to be easily distinguished, the research arena now has a mess of sloppy, loosely defined,
terms with which we typically describe members of
plankton and their processes. As we shall see, it is becoming increasingly apparent that photosynthetic protists
should by default be regarded as mixotrophs and not as
phototrophs. That this situation has not been given its
due appreciation in the past is most likely due in large
measure to problems in nomenclature enforcing the retention of stereotypes in functionality. The mixotrophic
protists combine all the complexities of phototrophs,
osmotrophs and phagotrophs, together within a single
cell, and yet packaged in a bewildering array of functional and taxonomic groups (Jones, 1997; Stoecker, 1998;
Stoecker et al., 2009; Granéli et al., 2012). In a subject in
which the search for scientific clarity is a prime motivator, one may be excused for glossing over these organisms with their complex and often perplexing physiology.
However, here we argue the importance of mixotrophy
needs to be acknowledged and clarifying their
descriptions (and indeed that of their planktonic consorts) is as good a place as any to start.
T H E M I XO T RO P H I C P RO T I S T S
In teaching and research in aquatic ecology, limnology
and oceanography, the term “mixotroph” only occasionally surfaces, typically as a curio, not least to fascinate students with videos of protists eating other protists,
and with the spectre of potentially harmful algal bloom
(HAB) species in the field eating other plankton, if not
killing organisms at higher trophic levels. The group
most closely aligned with the term “mixotrophs” are the
dinoflagellates (Burkholder et al., 2008; Jeong et al.,
2010b; Hansen, 2011). Generally, however, in the
science literature and in textbooks, the protists are distributed between “phytoplankton” and “microzooplankton”, between those that cannot eat and those that can
(Sarmiento and Gruber, 2006; Miller and Wheeler,
2010). This categorization, conveniently for ecologists
and modellers, also splits protists between primary
and secondary producers (Fig. 1). In fact, however, the
protists that inhabit illuminated waters are far from
being distributed cleanly between primary and secondary producers (Fig. 1), but are smeared across a continuum (Fig. 2). Mixotrophy is not limited to a few
groups, such as the dinoflagellates, it is almost everywhere in the illuminated water column, for much of the
time (e.g. Hartmann et al., 2012). Or at least, it is potentially there; the organisms are there though their mode
of operation at any instant is rarely characterized and
will likely depend on the presence of conditions conducive to one or other, or both, nutritional pathways.
Fig. 1. Schematic showing the classic misrepresentation of the
functional classification of planktonic protists as contributors to
primary production (on the right) or to secondary production (on the
left). Only some dinoflagellates, forams, radiolaria and acantheria are
accorded a mixotrophic status, and these are down-played (usually
ignored) in models.
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our understanding of the system, has failed to enter
mainstream plankton research. Why this is so is not
clear. While there is a time and place for all concepts,
maybe part of the problem has been that previous commentaries have been directed at the mixotroph researchers and at the breadth of diversity within mixotrophs,
rather than at the full breadth of plankton scientists
(from laboratory to field to modellers) and at the
breadth of diversity within aquatic protists. Doubtless,
the issue has also not been helped by the sheer diversity
of mixotroph strategies that are described in these
earlier works, together with the stereotypical descriptors
used in plankton research discussed earlier.
The core point that we make here is that the default
expectation for photosynthetic protists living in illuminated water is that they are mixotrophs. The exceptions
(in total contrast to commonly voiced wisdom) are those
species that cannot also engage in phagocytosis, and not
those that can eat. That the default nutritional expectation should indeed be mixotrophy is underscored by
the fact that a notable feature of the protists is their remarkable series of repeated evolutionary gains and
losses of phototrophic potential (Sanchez-Puerta and
Delwiche, 2008). A defining feature of protist evolution
has been genetic (re)combination and exchange of functionality supported through mixotrophy. The implication
is that mixotrophy has, and continues to be, an important nutritional option for these planktonic protists.
Alas, our detailed understanding of protist ecophysiology is not aided by the emphasis on axenic clones of
phototrophic protists held in culture collection, a practice which will select against mixotrophy. Meanwhile,
those protists deemed to be heterotrophs are held under
conditions selecting for that mode of nutrition. It is also
notable that organisms that are strongly mixotrophic (in
some instances, obligate mixotrophs) are rarely held in
culture collections for any period of time; we do not
understand enough about their nutritional needs,
further hindered by the emphasis towards maintaining
axenic cultures.
All this leads to a circular situation; because we do
not know how important the process is, it is difficult to
justify studying it, and yet we will never know how important it is, unless we do expend that research effort.
What we can be sure of is that the factors stimulating
mixotrophy need not be simply the supply of C (which
lies at the heart of the classic definition of “mixotrophy”), but that the acquisition of other nutrients is likely
to be at least as important. Indeed, the contribution of
C could be minor, but that of other N, P and Fe could
be highly significant both for mixotroph nutrition and
for trophic dynamics (Maranger et al., 1998; Smalley
et al., 2003; Stoecker et al., 2006; Zubkov and Tarran,
Fig. 2. Schematic of the functional classification of planktonic
protists as contributors to primary production (on the right) and/or to
secondary production (on the left). Note that in contrast to the classic
misrepresentation (Fig. 1), the potential for individual organisms to
contribute both to primary and secondary production is now
acknowledged. References in support of this description are as follows:
Acantharia (Caron et al., 1995; Stoecker et al., 1996); Chrysophyceae
(Kristiansen, 2005) with mixotrophy common in Chrysophyceae sensu
stricto, i.e. excluding the photolithophic Synurophyceae (Bhatti and
Colman, 2008); Ciliates (Bernard and Rassoulzadegan, 1994; Stoecker
et al., 1996, 2009; Perez et al., 1997; Esteban et al., 2010); Cryptophyta
(Laybourn-Parry et al., 2005; Callieri et al., 2006). Dinophyta (Callieri
et al., 2006; Park et al., 2010; Jeong et al., 2010b; Hansen, 2011;
Minnhagen et al., 2011); Foraminifera (Caron et al., 1995; Stoecker
et al., 1996, 2009); Pavlovophyceae (Callieri et al., 2006);
Prasinophyceae (Bell and Laybourn-Parry, 2003), though mixotrophy
appears rare in the Prasinophyceae; Prymnesiophyceae (Hansen and
Hjorth, 2002; Carvalho and Granéli, 2010; Granéli et al., 2012
Rokitta et al., 2011), though mixotrophy is very rare in
coccolithophores, occurring only in some non-calcified species, it is
common in the sister class Pavlovophyceae); Radiolaria (Caron et al.,
1995). Also, not shown in the figure: mixotrophy occurs in the
Chlorarachniophyta (Calderon-Saenz and Schnetter, 1989) and
Raphidophyceae (Jeong et al., 2010a; Jeong, 2011). For an overview of
the phylogenetic occurrence of mixotrophy, see Table II of Raven et al.
(Raven et al., 2009).
An analysis of the organisms traditionally termed eukaryote “phytoplankton” reveals that, not only are they
all osmotrophs, but that the majority are to a lesser or
greater degree potentially also phagotrophic (Fig. 2).
Certainly, studies over the last decade have shown that
many flagellate species are ferocious phagotrophs, such
as the haptophyte Prymnesium parvum (Carvalho and
Granéli, 2010; Granéli et al., 2012). The mixotrophic
status may even include both haploid and diploid
Emiliania huxleyi, which appear capable of phagotrophy
late in batch culture (Rokitta et al., 2011). Likewise,
many organisms traditionally termed “microzooplankton” have been shown to exhibit some level of phototrophic activity [typically through kleptoplastidy or
endosymbiosis (Stoecker et al., 2009)] and hence also
exhibit mixotrophic capabilities (Fig. 2, cf. Fig. 1).
It must be said that the concept of a continuum of
mixotrophy within aquatic protists is not new (Sanders,
1991, 1992, 2011; Jones, 1994; Stoecker, 1998). However, the message, and the critical importance of it in
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2008; Lindehoff et al., 2011; Stukel et al., 2011;
Hartmann et al., 2012). For example, when growing
under P and or N deficiency, the haptophyte P. parvum
has been shown to incorporate more than 70% of P
and N by ingesting prey (Carvalho and Granéli, 2006,
2010).
Whether some significant fraction of the pigment signature, and thus a fraction of the process of primary production, is associated with organisms that are actually
mixotrophs invariably does not enter into the analysis.
Certainly, when considering the process of C-fixation, it
does not matter so much, but when we need to understand, and model, the processes of primary production
(which is more than just photosynthesis) then it certainly
does matter. This is because it affects our understanding
of the flow of nutrients supporting primary production,
affecting the classic perception that primary production
is supported by only inorganic nutrition. On the contrary, it appears that primary production in many ocean
areas is actually supported by P and Fe derived directly
from phagocytosis (Maranger et al., 1998; Hartmann
et al., 2012). It also affects our understanding of the
support and fate of secondary production. The situation
is exacerbated on acceptance that a significant part of
the classic “microzooplankton” fraction is also photosynthetic (Figs 1 versus 2). Just as primary production is
uncritically linked to phytoplankton, so the term “predation” has also become uncritically linked to a group of
organisms rather than properly remaining as a descriptor
of a rate process.
The net result of all this is a perpetuation of the perception of the pelagic ecosystem as one dominated by
the groups phytoplankton and microzooplankton
( perhaps with minor inclusion of mixotrophs), rather
than dominated by the processes of phototrophy and
phagotrophy (which may or may not operate concurrently in the same organism). The problem does not
only reside with the use of chlorophyll as a marker for
characterization of protist functionality; molecular
screening approaches also need careful interpretation,
not least because of the complexity of protist evolution
(Sanchez-Puerta and Delwiche, 2008; Stoecker et al.,
2009) which results in genomic and proteomic signatures being smeared across protist groups.
Where researchers have specifically sought to identify
mixotrophy, and/or to identify and hence characterize
actual organisms, the contributions of mixotrophs to
system dynamics and functionality have been shown to
be important (Stoecker et al., 1997; Jeong et al., 1999,
2005a, b, 2010a, b; Gisselson et al., 2002; Smalley et al.,
2003; Zubkov and Tarran, 2008; Glibert et al., 2009;
Rokitta et al., 2011; Hartmann et al., 2012). The implication is that the more we look, the more we will find evidence for mixotrophy. It is perhaps ironic that in the
situations where mixotrophs are best known to be of importance (Burkholder et al., 2008), our terminology lets
us down; “HAB” is a rather unfortunate descriptor in
this capacity, with the term “algae”, like “phytoplankton”, being synonymous with a plant-like phototrophic
O RG A N I S M
C H A R AC T E R I Z AT I O N S A N D
T RO P H I C F U N C T I O N A L I T Y
Not only does the classic characterization of protists
divide them neatly into “phytoplankton” and “microzooplankton”, but it further distinguishes between those
contributing to primary production and to secondary
production (Fig. 1). As may be deduced from the corrected revised portrayal (Fig. 2), our mistaken categorization of protist plankton as either “phytoplankton” or
“microzooplankton” has various ramifications and
implications for key questions in plankton ecology and
oceanography. Critically, it now becomes clear that
many, if not on occasion most, protists in the photic
zone contribute to both primary and secondary production simultaneously, in the same single-celled organism.
While it is without doubt that the existence of mixotrophic protists is well known, and that these organisms
have been included within various conceptual food
webs and mathematical models (e.g. Thingstad et al.,
1996; Baretta-Bekker et al., 1998; Stickney et al., 2000;
Hammer and Pitchford, 2005; Jeong et al., 2010b), more
typically mixotrophs are hardly mentioned. As examples, mixotrophs are absent from a recent review of the
microbial loop (Jiao et al., 2010), and from recent text
books and compendia (e.g. Sarmiento and Gruber,
2006; Steele et al., 2010). Inevitably, then, discussion
and analysis of rate processes of primary and secondary
production typically ignores the role of mixotrophy.
The greatest emphasis in biological oceanography is
on primary producers, and primary production. In part
through convenience, and because of the ways in which
field analyses are conducted, from molecular analyses to
remote sensing technologies, there has been a blurring of
the descriptors “phytoplankton”, “primary production”
and “chlorophyll”. The result is that the rate process of
“primary production” has become uncritically associated, almost as a synonym, with the state variable
“phytoplankton”. Further, “chlorophyll” all-too-often
has become synonymous with “phytoplankton biomass”.
Indeed, because of the operational difficulty in measuring phytoplankton biomass in the field, colloquially at
least, “chlorophyll” is phytoplankton biomass (Falkowski
and Kiefer, 1985; Aiken et al., 2008).
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life style ( perhaps with some osmotrophy, but not with
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primary producers, which are used to tune and validate
the P box. Data for the biomass of grazers, and for
grazing activity, are far fewer in number and scope (e.g.
Lochte et al., 1993), and are less robust. We thus rely
critically on the structure of the model to infer what
trophic levels above primary production are doing: and
that feeds back around the loop through predator– prey
cycles, through nutrient regeneration and sedimentation
processes. The problem that now becomes clear is that
the chlorophyll signal originates from functionally
rather diverse organisms. Yes, it is associated with
primary production, but often it is also associated with
secondary production within the same organism, if not
(for kleptochloroplastidic protists) associated with a
complex interaction between primary producers and
phagotrophs (Park et al., 2010; Minnhagen et al., 2011;
Hansen et al., 2012).
As we move increasingly towards the development
and the use of so-called plankton functional type models,
with all the challenges that presents (Flynn, 2006), where
are the state variables for the organism groups shown in
Fig. 2? Where are these mixotrophs? Where are the rate
processes for mixotrophy? And where does this throw
the concept of adaptive modelling, of considering trait
tradeoffs based upon resource optimization? There are
profound differences between the individual processes of
primary and secondary production occurring within the
same organism, rather than in separate organisms.
Within a mixotroph, the two processes do not simply
add up, and neither do they simply compete; rather
there is a level of cooperation between them (Flynn and
Mitra, 2009; Mitra and Flynn, 2010). The implication is
that the activity of mixotrophs certainly cannot be
summed by adding together the contents and activities
of the strict phototrophic “P” and strict phagotrophic
“Z” boxes in models. Or to be pragmatic, we certainly
should not assume that they can be summed unless we
have proven it. One thing is for certain; we lack complete data sets to critically test models of mixotrophy.
That includes not only data for the mixotroph itself, but
for its prey (Flynn and Mitra, 2009).
When such a large fraction of the primary production
signal (as photopigment) is incorrectly assigned within
the model structure, how sure can we be of the reliability
of the whole model? Hindcasts provide a validation
method for climate change models (Ciavatta et al., 2011),
but to accept that as a methodology, we need to assume
that under climate change, the balance of strict phototrophs, mixotrophs and strict phagotrophs remains unchanged. We clearly cannot do that with any surety.
One could argue that there are enough problems,
enough challenges, in marine science without introducing mixotrophs as a plankton functional type. Others
GETTING IT RIGHT
Does it matter that the ecosystem functionality of protists is incorrectly assigned, that so many organisms that
are actually mixotrophs are put into the wrong bucket,
so to speak? On point of principle, yes of course, it
matters. It is beholden on scientists to describe and
characterize the workings of nature correctly. That is all
the more so when an incorrect characterization may
lead to a deeper misunderstanding of how systems function, and in the modern context, to a potential misunderstanding of the consequences of climate change. If
there are to be simplifications, then they need to be well
argued and evidence-based. Who is to say how the
balance of protist nutrition (and which nutrition; C, N,
P, Fe) may change in the future, between phototrophic
versus phagotrophic versus mixotrophic modes?
The proper identification of the organisms responsible for biogeochemical processes, for supporting
primary and secondary production (etc.) affects our
perception of nutrient cycling, of what proportion of
primary production flows from regenerated production (low f-ratio) and of how much regeneration is
short-circuited directly from secondary production to
primary production within the same organism functional type. It affects our understanding of who eats who,
and the drivers for that interaction. It affects our understanding of the “microbial loop”. A recognition of mixotrophy is also critically important in understanding
how microbes moderate stoichiometric imbalances
within the plankton, likely making primary production
packaged within a mixotroph better balanced (less
extreme) than that packaged within a strict nonphagotrophic phototroph (e.g. Glibert and Burkholder,
2011). If, as we suggest, it is important to correctly identify the organisms responsible for biogeochemical processes and for production, then surely this perception
should also affect how we model these ecosystems.
Models of planktonic systems traditionally (and
usually still do) have as state variables parameters that
describe organisms performing strict phototrophy and
strict grazing (the phytoplankton “P” and zooplankton
“Z” boxes, respectively; Fasham et al., 1990; Fasham,
1995). The major mechanism for the truthing of the
biological component of plankton models is by the use
of data from the monitoring of photopigments (mainly
chlorophyll), either by in situ or remote monitoring
(Lochte et al., 1993; Aiken et al., 2008). These data have
been used to derive estimates for the “biomass” of
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Bell, E. M. and Laybourn-Parry, J. (2003) Mixotrophy in the Antarctic phytoflagellate, Pyramimonas pedicola (Chlorophyta: Prasinophyceae).
J. Phycol., 39, 644–649.
would surely argue that this is a challenge that should
be met, that mixotrophs cannot continue to be sidelined
as throwback freaks, as extant representatives of the evolution between phagotrophic protists and strict phototrophic
(or
perhaps
more
accurately strict
non-phagotrophic) protists. The fact is that, a very significant minority if not the majority (depending on the
time and place) of the protist plankton are actively mixotrophic (Caron et al., 1995; Stoecker et al., 1996, 2009;
Jeong et al., 2010b; Jeong, 2011; Hartmann et al., 2012).
It is not that a group of organisms new to science has
been identified; it is that members of existing groups
have been widely misidentified with respect to their
functionality. While it may be argued that the term
“mixotroph” is unfortunate as it does not distinguish
between those photoautotrophs that have heterotrophic
tendencies and those heterotrophs that have autotrophic
tendencies, the critical issue is that we recognize that
among the photic-zone dwelling planktonic microbes,
there are few strict photoautotrophic or strict heterotrophic protists. (Indeed, including osmotrophy to
support growth in non-phagotrophs such as diatoms
would identify all phototrophic protists as mixotrophs.)
Once we achieve that recognition for mixotrophy in
protists, then we can determine the contribution, the
fluxes of C, N, P, Fe (etc.), that flows through them.
Accordingly, we suggest that it is time to recognize the
role of mixotrophy in field work, to reflect it in laboratory studies and describe it in conceptual and mathematical models.
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FUNDING
Carvalho, W. F. and Granéli, E. (2010) Contribution of phagotrophy versus autotrophy to Prymnesium parvum growth under nitrogen and phosphorus sufficiency and deficiency. Harmful Algae, 9,
105 – 115.
This work was funded by a Leverhulme Trust
International Workshop. D.K.S. was partially supported
by NSF award 1031344. This is contribution number
4701 from UMCES. The University of Dundee is a
registered charity, No SC 10596.
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