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Oxyrrhis marina growth, sex
and reproduction
DAVID J. S. MONTAGNES1*, CHRIS D. LOWE1, LAURA MARTIN1, PHILLIP C. WATTS1, NAOMI DOWNES-TETTMAR1,
ZHOU YANG2, EMILY C. ROBERTS3 AND KEITH DAVIDSON4
1
2
SCHOOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF LIVERPOOL, BIOSCIENCES BUILDING, LIVERPOOL L69 7ZB, UK, JIANGSU PROVINCE KEY LABORATORY FOR
3
BIODIVERSITY AND BIOTECHNOLOGY, SCHOOL OF BIOLOGICAL SCIENCES, NANJING NORMAL UNIVERSITY, 1 WENYUAN ROAD, NANJING 210046, CHINA, PURE
4
AND APPLIED ECOLOGY, SWANSEA UNIVERSITY, SINGLETON PARK, SWANSEA SA2 8PP, UK AND SCOTTISH ASSOCIATION FOR MARINE SCIENCE, OBAN, ARGYLL
PA37
1QA,
UK
*CORRESPONDING AUTHOR: [email protected] or [email protected]
Received May 13, 2010; accepted in principle July 8, 2010; accepted for publication August 1, 2010
Corresponding editor: John Dolan
We examine the literature on Oxyrrhis marina cell and life cycles, population growth
and production. We then provide an overview of what is known regarding aspects
of O. marina growth, indicate where information is needed and suggest ways in
which this species can and cannot be used as a general model, in this respect.
Little is known about the O. marina life cycle; it is even unknown if cells are
haploid, diploid or polyploid, although there is one report that sex occurs by
homothallic isogamy. There is considerable information on the cell cycle, which
we briefly review and provide a guide to the literature for details. We briefly
discuss and provide guidance to information on: (i) population cell size distributions; (ii) cannibalism; (iii) our first report of “mini-cells” in cultures (8 mm)
and their possible role in the life cycle; (iv) cysts, and their possible role in the life
and cell cycles; (v) biotic influences on growth, such as food type and abundance,
assimilation efficiency, prey stiochiometry, strain differences, population growth
and starvation and nutritional shifts; (vi) abiotic factors that affect growth, such as
temperature, salinity, pH, light and turbulence. We then reflect on the consequences of interactions between the above factors and review data on population
growth of O. marina in the field and laboratory. Finally, we evaluate the use of
O. marina as a model organism to examine cell and life cycles and ecological processes. Throughout the paper, we suggest areas that need evaluation.
KEYWORDS: model organism; dinoflagellate; protozoa; life history; Oxyrrhis
I N T RO D U C T I O N
There is now, and has been for some time, compelling
evidence that protozoa hold a key position and are an
essential link in pelagic food webs (e.g. Calbet, 2008).
Furthermore, there is a growing awareness that heterotrophic flagellates and specifically dinoflagellates are a
significant component of the protozoa in planktonic
ecosystems (Laybourn-Parry and Parry, 2000; Sherr and
Sherr, 2007). It is, therefore, important for researchers
interested in plankton dynamics to have at least a basic
knowledge, and at times a detailed understanding, of
the life and cell cycles of these organisms.
Protozoa differ from most metazoa in that reproduction
(and hence population growth) and sex are typically
decoupled (Fig. 1). The protozoan cell cycle sensu stricto
refers to mitotic cell division, and hence binary, asexual,
reproduction (of either diploid or haploid cells). In contrast, the protozoan life cycle sensu stricto may include a
number of cell cycles and ends–begins with sex; i.e. the
recombination of genetic material, through syngamy or
doi:10.1093/plankt/fbq111, available online at www.plankt.oxfordjournals.org. Advance Access publication August 26, 2010
# The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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Fig. 1. Dinoflagellate life cycle variations, redrawn from Pfiester and
Anderson (Pfiester and Anderson, 1987). The haplontic cycle is
represented by a stylized gymnodinoid dinoflagellate, while the
diplontic cycle is represented by a stylized form of Noctoluca. See text
for an explanation of terms.
conjugation, where two cells exchange, or combine,
gametic nuclei, either by fusing into a single cell, as is the
case for dinoflagellates, or temporarily fusing and then
separating, as is the case for ciliates. Of course, growth
also occurs by cells increasing in size during the cell cycle,
where maximum, pre-division cell size is determined by
biotic and abiotic factors, such as food abundance and
ambient temperature (e.g. Kimmance et al., 2006).
Beyond their importance in pelagic food webs, protozoa are also useful tools to understand fundamental biological processes. Because of their tractability, protozoa
(including planktonic taxa) have been employed as
models to examine cell cycles (e.g. Berger, 2001), life
cycles (e.g. Bell, 1988) and the constraints of external
factors on optimal size (e.g. Atkinson et al., 2003).
Furthermore, repeated cell cycles result in population
growth, and protozoa have historically been, and
continue to be, used as models to examine concepts
associated with population dynamics (e.g. Gause et al.,
1936; Fenton et al., 2010). Thus, uncovering the mechanisms underlying the cell and life cycles of planktonic
protozoa is useful to understand both ecological and
fundamental biological processes.
Why then should we focus on the heterotrophic dinoflagellate Oxyrrhis marina? First, this species is planktonic:
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it remains in the water column, is moved by currents
and behaves (swimming, growth, feeding) like many
planktonic protozoa including other heterotrophic flagellates. Although O. marina blooms occur in large bays,
producing “red tides” (105 cells mL21) and it can regularly be found in estuaries at abundances of 10–
100 mL21 (Fenchel et al., 1995; Johnson et al., 2003;
Begun et al., 2004), O. marina rarely occurs in the open
ocean. Rather, O. marina is typical of shallow waters and
littoral and supralittoral pools (Johnson, 2000;
Kimmance et al., 2006). Thus, at times O. marina may
be trophically important as a grazer and prey for other
organisms, but in terms of open-ocean plankton
dynamics assessing the specific importance of O. marina
is of a lesser concern. There are, nonetheless, significant
benefits to using O. marina as a model for other openocean species, as, unlike many planktonic protozoa, it is
easy to obtain from natural samples, identify, maintain
in culture and manipulate in experiments.
Directly pertinent to this review, over the past 100
years, O. marina has been extensively studied, and much
of this research has been associated with the cell cycle
and population growth; in contrast, far less work has
been conducted on its life cycle (Montagnes et al.,
2010). Here we examine the literature on O. marina cell
and life cycles, population growth and production
(growth rate cell size). Our aim is to provide an overview of what is known regarding aspects of O. marina
growth, indicate where information is needed and
suggest ways in which this species can and cannot be
used as a general model, in this respect.
L I F E C YC L E
The generalized life cycle of dinoflagellates includes
several stages (Pfiester and Anderson, 1987; Fig. 1).
Under favoured conditions (e.g. sufficient nutrients),
cells (which are typically but not always haploid) divide
vegetatively by binary fission, allowing population
growth. Due to some trigger (e.g. lack of nutrients, shift
in temperature), haploid cells act as gametes and fuse to
form a diploid zygote that may continue to be motile
but in some cases forms a resting cyst. Diploid cells
then undergo a single meiotic division to produce
haploid cells—note that some dinoflagellates, such as
Noctaluca, are diploid, and thus do not follow this generalized dinoflagellate model (Fig. 1). Most dinoflagellates
are homogamous (i.e. gametes do not differ from vegetative cells), but some are isogamous (i.e. gametes differ
from vegetative cells in size, pigmentation or presence
of a theca but are similar to each other), and others
may be anisogamous (gametes differ from each other).
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Furthermore, although most dinoflagellates are monoecious (homothallic), some may be dioecious (heterothallic), not being able to conjugate within a clone.
As indicated above, we know little about the life cycle
of O. marina. It is even unknown whether the cells are
haploid, diploid or polyploid (Sano and Kato, 2009). To
our knowledge, only one researcher has reported on sex
in O. marina (von Stosch, 1972a,b): O. marina is isogamous, with gametic cells being “considerably” smaller
than vegetative cells, and gametes were suggested to be
formed by two typical meiotic divisions (although data
were lacking to support this); the zygote enlarges after
fusion (von Stosch, 1972a). Zygotes are motile during
meiosis, and both flagella are retained in a “skiing-track
fashion” and are “distributed singly to the daughter cell
of the first meiotic division” (von Stosch, 1972b). Below,
we quote directly from von Stosch (von Stosch, 1972a),
as we are unsure of his meaning (no illustrations accompany his text), but “as chance favours the prepared
mind” (L. Pasteur), we provide his description in the
hope that a keen observer will make sense of it: “In
Oxyrrhis, however, the chromosomes could not be seen in the
living meiocyte and only circular motion of the nucleoli, which
are driven around with the chromosomes, could be observed.
The cytology of fertilization and meiosis in this organism is
rather well, if not completely, known to us, and older zygotes or
meiocytes respectively can easily be recognized by large size attained
by voracious feeding . . . . Even in Oxyrrhis, where the chromosomes appear short in vegetative interphase, they are considerably
stretched in zygotene”. Sex may be induced by changing
food type, from Pyraminonas to Dunaliella (von Stosch,
personal communication in Pfiester and Anderson,
1987).
To the observations above, we can add one new
insight: we routinely observe conspicuously small
O. marina cells (8 mm) in many of our cultures, occurring across all of the currently recognized Oxyrrhis phylotypes (see Lowe et al., 2010 for a description of the
major genetic lineages). The small cells may be gametes
(see Mini-cells, below; Fig. 2); however, we have not discovered the factors that stimulate their production,
observed fusion of these mini-cells, nor ascertained their
ploidy. Clearly, there is a great scope for the study of the
life cycle of O. marina. The implications of sex in cultures are worth considering, as a clonal culture unable
to have sex may reduce in fitness over time (Bell, 1988);
possibly undetected sex is the reason for O. marina cultures surviving for years. Likewise, if it becomes possible
to perform mating experiments with O. marina, a new
field of studies, associated with classical genetic recombination and survival strategies (e.g. Bell, 1988), will be
opened to plankton researchers using this species.
Given the existing, extensive, application of O. marina as
Fig. 2. An indication of Oxyrrhis marina cell sizes and shapes. (a) a
large cell; (b) mini-cells; (c) a normal cell; (d) a large cell, possibly a
cyst; (e) a dividing cell. Note that the mini-cells are likely less than
half the size of the dividing cell, suggesting that they are not simply
young daughter cells. Cells were fixed with 2% Lugol’s iodine, which
may result in cells being 90% of their live-linear dimensions
(Montagnes et al., 1994). Scale bar ¼ 10 mm.
a model for planktonic species (Montagnes et al., 2010),
the added ability to examine life cycle traits would
broaden its utility to assess planktonic processes.
C E L L C YC L E
Here we do not provide a detailed description of the
cell cycle but indicate some major features and offer a
guide to the extensive literature on the subject. For a
review of the dinoflagellate cell cycle, see Pfiester and
Anderson (Pfiester and Anderson, 1987).
Cell division
Over the past 100 years (e.g. Senn, 1911; Hall, 1925;
Triemer, 1982; Gao and Li, 1986; Whiteley et al., 1993;
Kato et al., 1997, 2000; Sano and Kato, 2009), there
have been a number of detailed descriptions of the
intracellular processes and stages involved in the cell
cycle of O. marina, and we direct the interested reader to
these works. Cell division in O. marina is transverse, and
during the cell cycle the chromosomes are always condensed, as is typical for dinoflagellates, but there are
differences from other dinoflagellates in the structural
organization of division that make O. marina phylogenetically unique (see the above references).
As is typical of eukaryotes, in exponentially growing cultures of O. marina, there are three phases to the cell cycle:
G1 (between the end of mitosis and the beginning of DNA
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replication), S (DNA replication) and G2 (between the end
of DNA replication and the beginning mitosis) þ M
(meiosis) (Whiteley et al., 1993; Sano and Kato, 2009).
Most of the cell cycle, of exponentially growing cells, is
spent in G2 þ M, and G1 is reduced (Whiteley et al., 1993;
Sano and Kato, 2009). However, Whiteley et al. (Whiteley
et al., 1993) indicate that stationary-phase cells accumulate
in G1 and G2, and nutrient-limited cells accumulate at G2,
rather than G1; they conclude that nutrient-dependent
control points exist at both G1 and G2, with the main
control point in G2. Their data led Whiteley et al.
(Whiteley et al., 1993) to suggest that this is a mechanism
adapted to feast-or-famine conditions, often experienced
by protozoa; they proposed a dual limitation of the cell
cycle that would allow cells to slowly progress through G1
to G2 when key nutrients are limited but not absent, allowing cells to accumulate in G2 in anticipation of feast conditions, when they could rapidly divide and exploit the
resource.
Intra- and inter-population size
distributions
Cell size (i.e. volume) changes during the cell cycle; this
is expected and clearly depicted in early observations of
dividing O. marina (e.g. Hall, 1925) and in cell-size distributions revealed by more modern techniques, such as
flow cytometry (e.g. Sano and Kato, 2009). However, it
should be noted that cell size of O. marina also changes
with nutritional state (see Biotic factors and Abiotic
factors, below) and, temperature (Kimmance et al.,
2006); it also appears, from our initial evaluation of
400 isolated strains of O. marina, that strains may vary
in maximum size (Lowe, unpublished results).
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routine observations of the 400 isolates of O. marina that
we are presently maintaining (at the University of
Liverpool, School of Biological Sciences), small cells
(8 mm) occur, compared to the typical 20–30 mm cells
(Fig. 2). These have been confirmed to be O. marina, by
PCR sequencing of 5.8S ITS rDNA fragments (following
methods outlined in Lowe et al., 2005, 2010), and are
observed in all four clades of Oxyrrhis, including the
lineage we have suggested to be a different species (Lowe
et al., 2011a). As indicated above, we do not know the
origin of these mini-cells and can only speculate that they
may be gametic (see Life Cycle, above).
Cysts
Post-conjugation resting cysts form in many dinoflagellates (Pfiester and Anderson, 1987; Fig. 1). Although
Goodman (Goodman, 1987) suggests Oxyrrhis does not
produce cysts, there are reports in the literature of cysts.
However, neither of the two descriptions of cyst formation
in Oxyrrhis are related to sex. Although we are not convinced that we have ever seen cysts (but see Fig. 2), and to
our knowledge neither have other recent studies,
O. marina may form thin-membrane covered cysts (Fig. 3)
induced by both excess and lack of food (Hall, 1925). A
more recent study indicated that Oxyrrhis sp. ( possibly not
O. marina; see Lowe et al., 2005, 2010), found in intertidal
rock pools, formed robust adherent cysts (Jonsson, 1994)
that were speculated to allow the dinoflagellate to maintain its place in the pools when they were flushed by the
incoming tide. We suggest that, as for observations of
the life cycle, researchers also should be vigilant for the
occurrence of cysts when they examine cultures;
Cannibalism
Large cannibals in O. marina populations can occur
(Öpik and Flynn, 1989; Flynn and Davidson, 1993a;
Martel and Flynn, 2008): a few cells (2% in a population; Martel and Flynn, 2008) are cannibalistic, and
this may depend on available prey and the nutritional
state of O. marina. Clearly, the occurrence of cannibals
will alter the distribution of cell sizes in a population
and potentially alter population growth (see below).
However, it is unknown whether cannibals initially grow
larger and then ingest other O. marina or whether the
increase in size is a consequence of prey consumption.
Mini-cells
Here we provide, to our knowledge, the first report of
mini-cells occurring within O. marina cultures. Within our
Fig. 3. Temporary cysts of Oxyrrhis marina, from Hall (Hall, 1925);
note the lack of flagella and the thin membrane around the cells.
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indications of conditions that encourage cyst formation
would direct future research into the biological relevance,
if at all, of this stage in the life cycle.
2010), and consequently there is a need to determine
how biotic and abiotic factors alter assimilation.
Biotic factors
G ROW T H R AT E , C E L L S I Z E ,
P RO D U C T I O N A N D
A S S I M I L AT I O N
Food type and abundance
Below, we examine factors that alter the specific growth
rate, cell size, production and assimilation of O. marina
under various biotic and abiotic conditions. Specific
growth rate, or per capita growth rate, is typically determined as the slope of the relationship of the natural log
of abundance versus time, in exponentially growing cultures; it is often examined in relation to prey abundance
(the numerical response) but is also examined in
response to abiotic factors (e.g. temperature). Cell size
(i.e. volume), estimated from linear measurements made
with a microscope, or by automated means such as electronic particle counters or flow cytometers is often used
as a proxy for biomass and may be converted to carbon
(see Menden-Deuer and Lessard, 2000). Given that both
specific growth rate and volume may be influenced by
biotic and abiotic factors, some authors (e.g. Kimmance
et al., 2006) have examined their product (growth rate volume) to determine production; i.e. the amount of
biomass elaborated per time. Finally, the amount of
material assimilated by an organism is a key component
of most population models (Turchin, 2003; Fenton et al.,
Oxyrrhis marina will grow on a wide range of taxa (from
bacteria to cells of its own size) and prey abundances;
clearly though, some prey elicit a higher growth rate
than others (Fig. 4, Table I; Tarran, 1991).
Furthermore, the quality of the prey, in terms of nutrient stoichiometry and chemical cues, may alter uptake
and presumably then growth (this topic is beyond the
scope of the present review, and the interested reader is
directed to the reviews on this topic: Davidson et al.,
2011; Roberts et al., 2011).
Cell size and production also vary with prey concentration, both following a similarly shaped, rectangular
hyperbolic response, akin to the functional response
(Kimmance et al., 2006). Surprisingly, O. marina cell size
rarely reaches an asymptote over the prey abundance
range where growth rate has become asymptotic (e.g.
Jeong et al., 2001; Kimmance et al., 2006; Fig. 5,
Table II), which results in biomass production continuing to increase with prey abundance, even when the
growth rate is constant. Thus, in this case, O. marina has
provided a model to illustrate that both the growth rate
and cell size must be measured when studies are
Fig. 4. A comparison of numerical responses of Oxyrrhis marina feeding on a range of prey, over a range of prey biomass, all conducted at 20–
218C. Responses are for Amphidinium carterae (Jeong et al., 2001); Heterosigma akashiwo (Jeong et al., 2003); Pfiesteria piscicida, Stoeckeria algicida (Jeong
et al., 2007a); Cafeteria sp. (Jeong et al., 2007b); mixed natural bacteria (Jeong et al., 2008); Dunaliella primolecta, Chlamydomonas spreta, Brachiomonas
submarina, Nanochloropsis oculata (Fuller, 1990); Isochrysis galbana (Kimmance et al., 2006); Dunaliella primolecta*, Dunaliella primolecta** (unpublished
data, Yang and Montagnes, using two strains of O. marina as predators, *351_FAR01, **45_BOG01, Univ. Liverpool cultures of O. marina). All
responses were fit to the equation r ¼ rmax (P 2 P0 )/(k þ P 2 P0 ), where r is growth rate and rmax is the asymptotic growth maximum (both
with units of day21), P is prey concentration, P0 is the prey concentration where growth rate is zero and k is a constant; P, P0 and k have units of
(ng carbon mL21).
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Table I: Parameters for
responses depicted in Fig. 4
the
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Table II: Parameters for the volume responses
depicted in Fig. 5
rmax (day21)
p0 (ng C mL21)
k (ng C mL21)
Prey
Vmax (mm23)
V0 (mm23)
k (ng C mL21)
1.43
1.17
0.19
0.66
0.22
1.47
0.53
0.73
1.31
0.94
0.50
0.77
8.0
1.3
0.06
0.4
5.0
222
146
40.8
2114
44.5
46.2
21.3
104
12.5
0.48
21.0
21.0
458
387
57.6
626
98.7
91.8
49.4
Heterosigma akashiwo
Amphidinium carterae
Cafeteria sp.
Pfiesteria piscicida
Stoeckeria algicida
Dunaliella primolecta
Chlamydomonas spreta
Brachiomonas submarina
Nanochloropsis oculata
Isochrysis galbana
Dunaliella primolecta*
Dunaliella primolecta**
4770
5910
6710
8750
908
1800
5890
4160
378
2510
3970
1280
See Fig. 4 legend for an explanation of the parameters and sources of
the data.
2011
Amphidinium carterae
Isochrysis galbana
Dunaliella primolecta*
Dunaliella primolecta**
See Fig. 5 legend for and explanation of the parameters and sources of
the data.
Kimmance et al., 2006), with values ranging between 0
and 70%, depending on prey concentration and
temperature (see Abioitc factors, below). However,
recently, using data on O. marina (from Kimmance et al.,
2006), Fenton et al. (Fenton et al., 2010) have provided a
means to calculate assimilation efficiency when data are
available for both the functional (i.e. ingestion versus
prey abundance) and numerical responses. For
O. marina, this analysis indicated a significant decrease
in assimilation efficiency with increasing prey abundance (from 1 to 0.5 over a range of 0 to 105
Isochrysis galbana mL21). Thus, using O. marina, Fenton
et al. (Fenton et al., 2010) have paved the way for
exploration of this phenomenon in other protozoa.
Prey stoichiometry
Fig. 5. A comparison of volume responses of Oxyrrhis marina feeding
on a range of prey, over a range of prey biomass, all conducted at
208C. Responses are for Amphidinium carterae (Jeong et al., 2001);
Isochrysis galbana (Kimmance et al., 2006); Dunaliella primolecta*,
Dunaliella primolecta** (unpublished data, Yang and Montagnes, using
two strains of O. marina as predators,*45_BOG01, **351_FAR01,
Univ. Liverpool cultures of O. marina). All responses were fit to the
equation V ¼ (Vmax P/k þ P) þ V0, where V is cell volume, Vmax is
the asymptotic maximum volume and V0 is cell volume at zero prey
(all three with units of mm3), P is prey concentration and k is a
constant (both with units of ng carbon mL21).
concerned with the biomass production of planktonic
protozoa.
Assimilation and gross growth efficiency
The proportion of ingested material assimilated by protozoa is exceedingly difficult to determine, as measurements of this parameter typically require estimates of
egestion, which is not easily measured in protozoa.
Rather, gross growth efficiency (or yield), the proportion
of ingested material converted to consumer biomass, is
typically determined for protozoa, and this has been
done for O. marina (Fuller, 1990; Tarran, 1991;
The “quality” of phytoplankton ( prey for O. marina and
other protozoa), in terms of nutrient and metabolic
composition, changes within the growth cycle and as a
response to various biotic and abiotic factors (Davidson
et al., 1992; Flynn et al., 1993). This variability can be a
major factor influencing the growth of protozoa
(Goldman and Dennett, 1992; John and Davidson,
2001; Montagnes et al., 2008). While the composition of
a range of metabolites may be important in this
process, the stoichiometric balance of bulk cell carbon
and nitrogen are often chosen as indices of prey quality,
being relatively easily quantified and composing a large
fraction of the biomass of the cell.
A number of studies based on O. marina have investigated this topic. Flynn and Davidson (Flynn and
Davidson, 1993b) noted that a proportion of ingested C
is lost through respiration associated with the energy
demands of growth and motility. Carbon is also lost
through the formation of C-rich “micro-particles” that
void excess C when prey are N deplete. Davidson et al.
(Davidson et al., 1995), using a combined experimentalmodelling approach, suggested that O. marina optimizes
growth by maintaining a balanced C:N ratio, and
Hammer et al. (2001) have used O. marina grazing and
growth as an experimental model system to study
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artificial carbohydrate-protein food particles that mimic
natural C:N stoichiometry of prey. Further studies
(Goldman et al., 1989; Davidson et al., 2005) have highlighted the differential regeneration of N by O. marina as
a function of prey stoichiometry as a means of optimizing growth. Finally, a range of mathematical modelling
studies (e.g. Mitra et al., 2003; Mitra and Flynn, 2005)
based on O. marina experimental data have investigated
the role of prey stoichiometry in governing protozoan
growth. Thus, in this sense, O. marina has acted as a
useful model to examine the effects of prey stoichiometry on growth.
Strain differences
Primarily through our work, there is a growing awareness that there are genetically distinct strains of
O. marina (see Lowe et al., 2005, 2010), and many of
these exhibit distinct growth responses (Lowe et al.,
2005; Yang et al., in preparation). Our main methodological conclusion from this is that researchers examining biological parameters, including those associated
with growth, must define the strain of O. marina that
they are working on (see Lowe et al., 2010).
Population growth
To our knowledge, there are no data that illustrate a
typical sigmoidal logistic-growth response (i.e. abundance versus time) for O. marina (but see Fig. 6); such
responses occur when resources (e.g. prey for O. marina)
are replete, and it is the population abundance of the
target organism that influences its own growth rate.
However, from the literature, we can estimate
maximum growth rate (r) that may range around 1.0
day21 (Fig. 5); this figure agrees with general estimates
for protozoa (and specifically dinoflagellates and other
heterotrophic flagellates) of a similar size (Hansen et al.,
1997), supporting the suitability of O. marina as a model,
in this respect. The carrying capacity (K) may be up to
105 O. marina mL21 (Begun et al., 2004; Fig. 6; Lowe;
Davidson; Roberts, unpublished data). Combined, these
estimates allow us to make some predictions of logistic
growth, assuming that the growth rate decreases linearly
with increasing O. marina abundance (but see Sibly and
Hone, 2002, for modifications on the general logistic
growth curve that allow growth rate to decrease in a
nonlinear manner with increasing prey abundance).
However, it is unlikely that under most conditions
(natural or batch cultures in the laboratory), resources
will remain replete, and thus logistic growth is an unlikely scenario. Most of our laboratory data on population dynamics of O. marina and its prey indicate that
either predators and prey exhibit population cycles or
populations become roughly stable (Montagnes,
unpublished results). Similarly, models of O. marina
based on functional and numerical response data
suggest when O. marina is incubated with a single prey,
population cycling occurs (Davidson et al., 1995;
Kimmance et al., 2006; Yang et al., in preparation). As is
discussed in detail by Davidson et al. (Davidson et al.,
2011), O. marina lends itself to such population studies
(e.g. Kimmance et al., 2006) and may act as a model to
assess protozoan, and possibly more general, population
phenomena.
Starvation and nutritional shifts
Little is known regarding the response of O. marina to
low prey concentrations, where it starves. Studies such
as that by Kimmance et al. (Kimmance et al., 2006)
provide a threshold level, where food is just sufficient to
sustain the cells (Table I), and a mortality response at
sub-threshold concentrations (see Montagnes, 1996).
However, to our knowledge, there are no data on how
O. marina will respond to changes in prey levels (either
nutritional shifts up or down). Some protozoa will
respond in a non-intuitive way to these shifts: e.g. ciliates may initially increase in numbers (but get smaller)
when starved, and they may increase in cell size and
not divide when they experience an increase in food
(e.g. Lynn et al., 1987).
Our own perception is that O. marina has a long lagphase when transferred to increased prey levels or a
different prey type (Lowe, Roberts, unpublished data).
This is in agreement with the above argument made for
ciliates but seems to contradict the speculations of
Whiteley et al. (Whiteley et al., 1993) that the population
progresses to G2-phase, to allow rapid exploitation of
new resources (see Cell Division, above). Clearly, to
understand its population dynamics, it will be beneficial
to develop studies to examine the response of O. marina
to transitional and rapidly shifting prey levels; these can
then be compared to other planktonic protozoa to assess
the utility of O. marina as a model. Researchers interested
in pursuing this area are directed to the classic works of
Fenchel (e.g. Fenchel, 1982; Fenchel, 1990).
Abiotic factors
Temperature
Classically, biotic rate processes are expected to increase
exponentially with temperature, following a Q10 or
Arrhenius response, but Montagnes et al. (Montagnes
et al., 2003) have argued that the response of protozoan
growth rate to temperature is better modelled by a
linear response. Data on O. marina seem to support the
linear model (Kimmance et al., 2006). Atkinson et al.
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Fig. 6. Mixing and turbulence effects on Oxyrrhis marina and the prey flagellate Isochrysis galbana populations. Population dynamics were followed
in three replicate flasks (250 mL) at 168C and 30–35 mmol photons m22 s21 of 24 h light. Flasks contained 200 mL of 32 PSU artificial
seawater, enriched with f/2 media (Sigma). Daily, 3-mL sample were collected, fixed with Lugol’s Iodine (2% final concentration) and cells were
counted. Treatments, quantified as dissipation (1) m3 s21 were: “No mixing”, gently mixed once per day (1 ¼ 0); “Low mixing”, rotated on a
plankton wheel (1 ¼ 5.3 1025); and shaken on agitating tables (1 ¼ “Medium mixing”, 8.2 1023; “High mixing”, 2.32 1022).
Calculations of dissipation are described in Downes-Tettmar and Montagnes (2008).
(Atkinson et al., 2003) have indicated another general
temperature rule: protist cell size decreases linearly with
increasing temperature, and again data on O. marina
follow this trend (Kimmance et al., 2006). Thus, O. marina
has been useful in helping to further assess these general
trends.
Oxyrrhis marina is able to grow between 8 and 308C
(Droop, 1959; Kimmance et al., 2006), with notable
differences between clones (Lowe, Montagnes, Yang,
et al., in preparation), so this range may not be as great
for any one isolate. The estuarine and intertidal
environments in which O. marina occurs (e.g. Droop,
1959; Jonsson, 1994; Johnson et al., 2003; Begun et al.,
2004) will vary, rapidly and extensively, in temperature
(e.g. as air temperatures change), compared with typical
water column conditions, possibly explaining why this
species is eurythermal.
Salinity
In general, O. marina grows over a wide range of salinities, between 4 and 130 PSU, with maximum growth
at 20, although there are strain-specific responses
(Droop, 1959; Lowe et al., 2005). Furthermore, O. marina
is better at surviving transfers to lower salinities, rather
than to higher salinities. Given its apparent global distribution and prevalence in intertidal pools and estuaries (Fenchel et al., 1995; Johnson et al., 2003; Lowe
et al., 2005, 2010, unpublished results on 400 isolates
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OXYRRHIS MARINA GROWTH, SEX AND REPRODUCTION
from around the globe), it is not surprising that
O. marina is euryhaline and adaptable.
pH
The two studies that have investigated the effect of pH
on O. marina growth indicate that it can tolerate a wide
range, growing between 7.8 and 9.8, but it dies below
7.5 (Droop, 1959; Pedersen and Hansen, 2003). Like the
data on salinity, these should not be surprising, as rock
pools often exhibit a wide range of pH, due to high
levels of photosynthetic activity, altering CO2 production – consumption, which in turn alters pH. Given
the interest in pH shifts in the ocean and its effect on
microbes (Joint et al., 2010), O. marina may be useful as a
study organism to assess short- and long-term phenotypic and genotypic changes on protists.
Light
Strom (Strom, 2001) indicated that light may increase
population growth of heterotrophic protists, and Klein
et al. (Klein et al., 1986) found that light enhanced alloxanthin and chlorophyll c degradation by O. marina,
suggesting that light may have an effect on its growth
rate. Furthermore, Jakobsen and Strom (2004) indicated
that O. marina exhibits a light-induced deil cycle in its
feeding and growth rates. As O. marina contains rhodopsin, it may be that this protozoan can use light to facilitate cellular processes that increase growth rate
(C. H. Slamovits et al., unpublished results). Clearly, this
is an area for future study, not just for O. marina but to
generally assess aspects of light-mediated metabolism in
planktonic heterotrophs.
Oxygen
There is one report of O. marina being associated with
the microaerophilic zone of a Danish fjord (Fenchel
et al., 1995). Although O. marina occurred in abundance at this interface, there was no indication that it
was growing, and given this flagellate’s ability to
migrate and accumulate at interfaces (Menden-Deuer
and Grünbaum, 2006), it may be as Fenchel et al.
(Fenchel et al., 1995) suggest: O. marina was abundant
at this site because there were few predators. The
ability of plankton to relocate to thin-layer conditions
where growth is optimal, due to lack of predation or
an increase in growth rate, is undoubtedly another
area of research where O. marina could be employed as
a model.
Mixing and turbulence
There is an expected negative effect of high turbulence
on protozoan growth, although increased encounter
with prey due to low-level turbulence may increase
ingestion, and hence growth (see Peters and Marrasé,
2000). Havskum (Havskum, 2003) found that O. marina
growth significantly decreased, by 20%, at high but
not low turbulence (dissipation, 1, was 1 and
522 cm2 s3, respectively). We also found that turbulence, measured as dissipation, had no apparent effect
on the growth of O. marina, except at very high levels
(Fig. 6). Note also, that our previous work
(Downes-Tettmar and Montagnes, 2008) indicated no
effect of turbulence (i.e. mixing) on Isochrysis galbana,
one of the prey routinely used to grow O. marina (e.g.
Kimmance et al., 2006).
It might be expected, given that one of the natural
habitats of O. marina is intertidal pools (e.g. Droop,
1959; Jonsson, 1994), that it would be robust to mixing
(turbulence), as a consequence of wave action and wind
mixing. This ability to grow when mixed vigorously
means that O. marina is probably a poor model organism
to study the effect of turbulence on “planktonic”
species. However, our data (Fig. 6) and those of
Havskum (Havskum, 2003) indicate that researchers
need not concern themselves with detrimental influences of routine mixing when examining the effects of
other parameters (e.g. temperature, prey levels), making
O. marina a useful model, in this respect. It is also important to note that continuous mixing on a plankton
wheel produced different population dynamics to those
in containers that were only mixed once per day
(Fig. 6); this may be due to increased encounter by predators and prey in the continually mixed cultures, but it
could equally be due to aggregation of predators and
prey on the bottom of cultures that were not mixed.
These data, on O. marina, illustrate the benefits of continually mixed cultures, a fact well-recognized by most
planktologists.
Interactions between biotic and abiotic
factors
Most population and ecosystem models that include
both abiotic and biotic factors do so in an additive
fashion, as there are rarely measurements that allow
parameterization of interactive effects. However, interactions may produce surprising results. For instance, the
intensive work on O. marina by Kimmance et al.
(Kimmance et al., 2006) is a good example of how
abiotic (temperature) and biotic factors ( prey concentration) influence growth rate, cell size and ultimately
production and population dynamics of organisms, in
non-intuitive ways: briefly, the responses were not additive, and there were non-linear responses to a number
of variables, including gross growth efficiency. It might,
thus, be expected that combinations of other biotic and
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abiotic factors (see above) will also yield non-intuitive
information about how protozoa respond to their
environment. In this sense, O. marina may prove useful
to explore such interactions.
Population growth in the environment
There are few data that examine population growth of
O. marina in the environment. Kimmance (Kimmance,
2001) recorded seasonal variation in O. marina abundance in intertidal pools on the Isle of Man and indicated peaks in abundance during late June and between
late July and September, when prey would have been
abundant. Begun et al. (Begun et al., 2004) followed
bloom dynamics of O. marina for 2 months in an
enclosed bay in the Sea of Japan; they suggested that
reduced salinity, caused by freshwater inflow, may have
stimulated blooms that reached as high as 4 105
O. marina mL21, although their data are also in keeping
with the notion that freshwaters increased nutrient
levels and thus increased the abundance of autotrophic
(or bacterial) prey that stimulated blooms. Finally,
Johnson et al. (Johnson et al., 2003), examining summer
plankton in Chesapeake Bay, USA noted that O. marina
was at times abundant (0 – 100 mL21) and was positively correlated with its prey, but it also was most abundant at lower salinities (10– 14 PSU). From these
studies, we might conclude that there are interactive
effects of salinity and prey concentration on the abundance (a proxy for growth in the natural environment),
as well as the known interactions between prey abundance and temperature on growth (Kimmance et al.,
2006). These field data emphasize the need for further
long-term collections of O. marina, to improve our
understanding of this species and appreciate it as a
potential model.
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cycle attributes were better understood, they too would
be illuminating. Finally, if O. marina is to be used as a
model for other processes (see Ecology, below), there is a
need to understand both its life and cell cycles; for
instance, if, as for most dinoflagellates, O. marina is homothallic, and the mini-cells that we have observed are,
indeed, gametes, then sex within clonal cultures may
bias long-term studies. We, therefore, strongly recommend that future research is conducted on these processes and support the ongoing efforts of those
researchers who are pursuing this work.
Ecology
Oxyrrhis marina is used as a model organism to examine
ecological processes (Montagnes et al., 2011). Reasons
for this are: its ability to be recognized and isolated
from the environment, its ease of culturing and its
ability to be maintained for many years in culture (for
details on culturing beyond the scope of this review, see
Lowe et al., 2011b). The last of these factors might be
attributed to sex within clones, as protozoa often exhibit
clonal decline when sex is prevented (Bell, 1988).
Furthermore, O. marina responds to many biotic and
abiotic factors that are considered important drivers of
marine productivity in pelagic environments (see above)
and is able to survive over a wide range of these, possibly because in nature it experiences extremes. Thus,
although O. marina is not routinely found in open-ocean
waters, it is potentially useful as a proxy to model the
range of environmental factors experienced by planktonic protozoa, including the effects of environmental
perturbations. Given that many truly planktonic protozoa are notoriously difficult to maintain for extended
periods, O. marina seems well suited as a model organism to examine both aut- and synecological processes
associated with their growth.
OX Y R R H I S A S A M O D E L
AC K N OW L E D G E M E N T S
Cell and life cycles
The Authors would like to thank Mark Breckels,
Claudio H. Slamovits, Michael Steinke and Ewan
Minter for their constructive comments on this manuscript. We would also like to thank the anonymous
reviewers for their suggestions.
Oxyrrhis marina is an unusual dinoflagellate, having a
basal position within this group (Saldarriaga et al., 2003)
and, therefore, is not necessarily an ideal candidate to
act as a model of either the cell or life cycle of dinoflagellates. Furthermore, the lack of data available on O. marina
reduces its immediate use to elaborate cell or life cycle
patterns, in general. Thus, at present, in this respect, O.
marina is a poor model. However, the basal position of O.
marina in dinoflagellate phylogeny makes it a target for
further evolutionary study, and specific cell cycle processes have illustrated its unique position; possibly if life
FUNDING
This work was, in part, supported by: a UK NERC
grant (NE/F005237/1) awarded to P.C.W., C.D.L. and
D.J.S.M.; a Project of International Cooperation and
Exchanges from the National Natural Science
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D. J. S. MONTAGNES ET AL.
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OXYRRHIS MARINA GROWTH, SEX AND REPRODUCTION
Foundation of China (30970500) awarded to Y.Z.;
SAMS/NERC Oceans 2025 programme awarded to
K.D. and NERC grants NE/C519438/1 and NE/
G010374/1 awarded to E.C.R.
REFERENCES
Atkinson, D., Ciotti, B. J. and Montagnes, D. J. S. (2003) Protists
decrease in size linear with temperature: ca. 2.58C21. Proc. R. Soc.,
270, 2605–2611.
Begun, A. A., Orlova, T. Y. u. and Selina, M. S. (2004) A “bloom”
in the water of Amursky Bay (Sea of Japan) caused by the dinoflagellate Oxyrrhis marina Dujardin, 1841. Russ. J. Mar. Biol., 30,
51–55.
Bell, G. (1988) Sex and Death in Protozoa. Cambridge University Press,
Cambridge, pp. 199.
Berger, J. D. (2001) Riding the ciliate cell cycle -a thirty-five-year prospective. J. Eukaryot. Microbiol., 48, 505–518.
Calbet, A. (2008) The trophic roles of microzooplankton in marine
systems. ICES J. Mar. Sci., 65, 325– 331.
Davidson, K., Flynn, K. J. and Cunningham, A. (1992) Non-steady
state ammonium-limited growth of the marine phytoflagellate,
Isochrysis galbana Parke. New Phytol., 122, 433–438.
Davidson, K., Cunningham, A. and Flynn, K. J. (1995) Predator–
prey interactions between Isochrysis galbana and Oxyrrhis marina III.
Mathematical modelling of predation and nutrient regeneration.
J. Plankton Res., 17, 465– 492.
Davidson, K., Roberts, E. C., Wilson, A. M. et al. (2005) The role of
prey nutritional status in governing protozoan nitrogen regeneration
efficiency. Protist, 156, 45– 62.
Davidson, K., Sayegh, F. and Montagnes, D. J. S. (2011) Oxyrrhis
marina-based mathmatical models as a tool to interpret protozoan
population dynamics. J. Plankton Res., 33, 651– 663.
Downes-Tettmar, N. and Montagnes, D. J. S. (2008) How might
mixing bias protozoan-experiments that use the common microalga Isochrysis galbana? Acta Protozool., 47, 287–291.
Droop, M. R. (1959) A note on some physical conditions for cultivating Oxyrrhis marina. J. Mar. Biol. Ass. UK, 38, 599– 604.
Fenchel, T. (1982) Ecology of heterotrophic microflagellates. III.
Adaptations to heterogeneous environments. Mar. Ecol. Prog. Ser., 9,
25–33.
Fenchel, T. (1990) Adaptive significance of polymorphic life cycles in
Protozoa: responses to starvation and refeeding in two species of
marine ciliates. J. Exp. Mar. Biol. Ecol., 136, 159– 177.
Fenchel, T., Bernard, C., Estaban, G. et al. (1995) Microbial diversity and
activity in a Danish fjord with anoxic deep water. Ophelia, 43, 45–100.
Fenton, A., Spencer, M. and Montagnes, D. J. S. (2010)
Parameterising variable assimilation efficiency in predator-prey.
Oikos, 119, 1000–1010.
Flynn, K. J. and Davidson, K. (1993a) Predator– prey interactions
between Isochrysis galbana and Oxyrrhis marina I. Changes in particulate d 13C. J. Plankton Res., 15, 455– 463.
Flynn, K. J. and Davidson, K. (1993b) Predator-prey interactions
between Isochrysis galbana and Oxyrrhis marina II. Release of
non-protein amines and faeces during predation of Isochrysis.
J. Plankton Res., 15, 893– 905.
Flynn, K. J., Davidson, K. and Cunningham, A. (1993) Relations
between carbon and nitrogen during growth of Nannochloropsis oculata
(Droop) Hibberd under continuous illumination. New Phytol., 125,
717 –722.
Fuller, A. K. R. (1990) The grazing and growth rates of some marine
protozoa measured in batch and continuous culture with particular
reference to the heterotrophic dinoflagellate Oxyrrhis marina. PhD
thesis. University of London, UK, pp. 296.
Gao, X. P. and Li, J. Y. (1986) Nuclear division in the marine dinoflagellate Oxyrrhis marina. J. Cell. Sci., 85, 161–175.
Gause, G. F., Smaragdova, N. P. and Witt, A. A. (1936) Further
studies of interaction between predators and prey. J. Animal Ecol., 5,
1 –18.
Goldman, J. C. and Dennett, M. R. (1992) Dynamics of prey selection
of an omnivorous flagellate. Mar. Ecol. Prog. Ser., 59, 183 –194.
Goldman, J. C., Caron, D. A. and Gordin, H. (1989) Dynamics of
hervivorous grazing by the heterotrophic dinoflagellate Oxyrrhis
marina. J. Plankton Res., 11, 391–407.
Goodman, D. K. (1987) Dinoflagellate cysts in ancient and modern
sediments. In Taylor, F. J. R. (ed.), The Biology of Dinoflagellates.
Blackwell Scientific Publications, Oxford, pp. 649– 722.
Hall, R. P. (1925) Binary fission in Oxyrrhis marina Dujardin. Univ. Calif.
Publ. Zool., 26, 281–324.
Hammer, A., Grüttner, C. and Schumann, R. (2001) New biocompatible tracer particles: use for estimation of microzooplankton
grazing, digestion, and growth rates. Aquat. Microb. Ecol., 24,
153 –161.
Hansen, P. J., Bjørnsen, P. K. and Hansen, B. W. (1997) Zooplankton
grazing and growth: scaling within the 2-2,000-mm body size
range. Limnol. Oceanogr., 42, 687– 704.
Havskum, H. (2003) Effects of small-scale turbulence n the interactions between the heterotrophic dinoflagellate Oxyrrhis marina and
its prey Isochrysis sp. Ophelia, 57, 125– 135.
Jakobsen, H. H. and Strom, S. L. (2004) Circadian cycles in growth
and feeding rates of heterotrophic protist plankton. Limnol. Oceanogr.,
49, 1915–1922.
Jeong, H. J., Kang, H., Shim, J. H. et al. (2001) Interactions among
the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp.
Mar. Ecol. Prog. Ser., 218, 77–86.
Jeong, H. J., Kim, J. S., Yeong, D. Y. et al. (2003) Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte
Heterosigma akashiwo: a potential biological method to control red
tides using mass-cultured grazers. J. Eukaryot. Microbiol., 50,
274 –282.
Jeong, H. J., Kim, J. S., Song, J. E. et al. (2007a) Feeding by heterotrophic protists and copepods on the heterotrophic dinoflagellate
Pfiesteria pisicicida, Stoeckeria algicida and Luciella masanensis. Mar. Ecol.
Prog. Ser., 349, 199–211.
Jeong, H. J., Song, J. E., Kang, N. S. et al. (2007b) Feeding by heterotrophic dinoflagellates on the common marine heterotrophic nanoflagellate Cafeteria sp. Mar. Ecol. Prog. Ser., 333, 151–160.
Jeong, H. J., Seong, K. A., Du Yoo, Y. et al. (2008) Feeding and
grazing impact by small marine heterotrophic dinoflagellates on
heterotrophic bacteria. J. Eukaryot. Microbiol., 55, 271–288.
John, E. H. and Davidson, K. (2001) Prey selectivity and the influence
of prey carbon:nitrogen ration on microflagellate grazing. J. Exp.
Mar. Biol. Ecol., 260, 93– 111.
625
JOURNAL OF PLANKTON RESEARCH
j
33
VOLUME
Johnson, M. P. (2000) Physical control of plankton population abundance
and dynamics in intertidal rock pools. Hydrobiologia, 440, 145–152.
Johnson, M. D., Rome, M. and Stoecker, D. K. (2003)
Microzooplankton grazing on Prorocentrum minimum and Karlodinium
micrum in Chesapeake Bay. Limnol. Oceanogr., 48, 238– 248.
Joint, I., Doney, S. C. and Karl, D. M. (2010) Will ocean acidification
affect marine microbes? ISME, Published online 10 June.
Jonsson, P. R. (1994) Tidal rhythm of cyst formation in the rock pool
ciliate Strombidium oculatum Gruber (Cilophora, Oligotrichida): a
description of the functional biology and analysis of the tidal synchronization of encystment. J. Exp. Mar. Biol. Ecol., 175, 77–103.
Kato, K. H., Moriyama, A., Huitorel, P. et al. (1997) Isolation of the
major basic nuclear protein and its localization on chromosomes of
the dinoflagellate, Oxyrrhis marina. Biol. Cell, 89, 43–52.
Kato, K. H., Moriyama, A., Itoh, T. J. et al. (2000) Dynamic changes
in microtubule organizations during division of the primitive dinoflagellate Oxyrrhis marina. Biol. Cell, 92, 583– 594.
Kimmance, S. A. (2001) The interactive effects of temperature and
food concentration on growth responses of aquatic protists, with
particular reference to the heterotrophic dinoflagellate Oxyrrhis
marina. PhD Thesis. University of Liverpool, pp. 131.
j
NUMBER
4
j
PAGES
615 – 627
j
2011
Mitra, A. and Flynn, K. J. (2005) Predator-prey interactions: is “ecological stoichiometry” sufficient when good food goes bad?
J. Plankton Res., 27, 393–399.
Mitra, A., Davidson, K. and Flynn, K. J. (2003) The influence of
changes in predation rates on marine microbial predator/prey
interaction: a modelling study. Acta Oecol., 24, S539– S367.
Montagnes, D. J. S. (1996) Growth responses of planktonic ciliates in
the genera Strobilidium and Strombidium. Mar. Ecol. Prog. Ser., 130,
241 –254.
Montagnes, D. J. S., Berges, J. A., Harrison, P. J. et al. (1994)
Estimating carbon, nitrogen, protein, and chlorophyll a from cell
volume in marine phytoplankton. Limnol. Oceanogr., 39, 1044– 1060.
Montagnes, D. J. S., Kimmance, S. A. and Atkinson, D. (2003) Using
Q10: can growth rates increase linearly with temperature? Aquat.
Micob. Ecol., 32, 307–313.
Montagnes, D. J. S., Barbosa, A. B., Boenigk, J. et al. (2008) Selective
feeding behaviour of free-living protists: views on, and avenues for,
continued study. Aquat. Microb. Ecol., 53, 83– 98.
Montagnes, D. J. S., Lowe, C. D., Roberts, E. C. et al. (2011) An introduction to the special issue: Oxyrrhis marina, a model organism?
J. Plankton Res., 33, 549–554.
Kimmance, S., Atkinson, D. and Montagnes, D. J. S. (2006) Do temperature—food interactions matter? Responses of production and its
components in the model heterotrophic flagellate Oxyrrhis marina.
Aquat. Microb. Ecol., 42, 63–73.
Öpik, H. and Flynn, K. J. (1989) The digestive process of the dinoflagellate Oxyrrhis marina Dujardin, feeding on the chlorophyte,
Dunaliella primolecta Butcher: a combined study of ultrastructure and
free amino acids. New Phytol., 113, 43– 151.
Klein, B., Gieskes, W. W. C. and Kraay, G. G. (1986) Digestion of
chlorophylls and carotenoids by the marine protozoan Oxyrrhis
marina studied by h.p.l.c. analysis of algal pigments. J. Plankton Res.,
8, 827– 836.
Pedersen, M. F. and Hansen, P. J. (2003) Effects of high pH on the
growth and survival of six marine heterotrophic protists. Mar. Ecol.
Prog. Ser., 260, 33–41.
Laybourn-Parry, J. and Parry, J. (2000) Flagellates and the microbial
loop. In Leadbeater, B. S. C. and Green, J. C. (eds), The Flagellates.
Unity, Diversity, and Evolution. Taylor and Francis, London, pp.
216–239.
Lowe, C. D., Day, A., Kemp, S. J. et al. (2005) There are high levels of
functional and genetic diversity on Oxyrrhis marina. J. Eukaryot.
Microbiol., 52, 250– 257.
Lowe, C. D., Montagnes, D. J. S., Martin, L. E. et al. (2010) Patterns
of genetic diversity in the marine heterotrophic flagellate Oxyrrhis
marina (Alveolata: Dinophyceae). Protist, 161, 212 –221.
Lowe, C. D., Keeling, P. J., Martin, L. E. et al. (2011a) Who is
Oxyrrhis marina? Morphological and phylogenetic studies on an
unusual dinoflagellate. J. Plankton Res., 33, 555– 567.
Lowe, C. D., Martin, L. E., Roberts, E. C. et al. (2011b) Collection,
isolation and culturing strategies for Oxyrrhis marina. J. Plankton Res.,
33, 569–578.
Lynn, D. H., Montagnes, D. J. S. and Riggs, W. (1987) Divider size
and the cell cycle after prolonged starvation of Tetrahymena corlissi.
Microb. Ecol., 13, 115–127.
Martel, C. M. and Flynn, K. J. (2008) Morphological controls on cannibalism in a planktonic marine phagotroph. Protist, 159, 41–51.
Menden-Deuer, S. and Lessard, E. J. (2000) Carbon to volume
relationships for dinoflagellates, diatoms, and other protist plankton.
Limnol. Oceanogr., 45, 569– 579.
Menden-Deuer, S. and Grünbaum, D. (2006) Individual foraging
behaviors and population distributions of a planktonic predator
aggregating to phytoplankton thin layers. Limnol. Oceanogr., 51,
109–116.
Peters, F. and Marrasé, C. (2000) Effects of turbulence on plankton:
an overview of experimental evidence and some theoretical considerations. Mar. Ecol. Prog. Ser., 205, 291–306.
Pfiester, L. A. and Anderson, D. M. (1987) Dinoflagellate reproduction. In Taylor, F. J. R. (ed.), The Biology of Dinoflagellates. Blackwell
Science, Oxford, pp. 611– 648.
Roberts, E. C., Wooton, E. C., Davidson, K. et al. (2011) Feeding in
the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms. J. Plankton Res., 33, 603 –614.
Saldarriaga, F., McEwan, M. L., Fast, N. M. et al. (2003) Multiple
protein phylogenies show that Oxyrrhis marina and Perkinsus marinus
are early branches of the dinoflagellate lineage. Int. J. Syst. Evol.
Microbiol., 53, 355– 365.
Sano, J. and Kato, K. H. (2009) Localization and copy number of the
protein-coding genes actin, a-tubulin, and HSP90 in the nucleus of
a primative dinoflagellate, Oxyrrhis marina. Zool. Sci., 26, 745–753.
Senn, G. (1911) Oxyrrhis, Nephroselmis und einige Euflagellaten,
nebst Bemerkungen über deren System. Z. Wiss. Zool. Abt. A,
604 –672.
Sherr, E. B. and Sherr, B. F. (2007) Heterotrophic dinoflagellates: a
significant component of microzooplankton biomass and major
grazers of diatoms in the sea. Mar. Ecol. Prog. Ser, 352, 187 –197.
Sibly, R. M. and Hone, J. (2002) Population growth rate and its determinants: an overview. Philos. Trans. R. Soc. Lond. B, 357, 1153–1170.
Strom, S. L. (2001) Light-aided digestion, grazing and growth in herbivorous protists. Aquat. Microb. Ecol., 23, 253– 261.
Tarran, G. A. (1991) Aspects of the grazing behaviour of the marine
dinoflagellate Oxyrrhis marina, Dujardin. PhD Thesis. University
of Southampton, pp. 182.
626
D. J. S. MONTAGNES ET AL.
j
OXYRRHIS MARINA GROWTH, SEX AND REPRODUCTION
Triemer, R. E. (1982) A unique mitotic variation in the marine dinoflagellate Oxyrrhis marina (Pyrrophyta). J. Phycol., 18, 399– 411.
Turchin, P. (2003) Complex Population Dynamics: A Theoretical/Empirical
Synthesis. Princeton University Press, Princeton, NJ, pp. 450.
von Stosch, H. A. (1972b) Observations on vegetative reproduction
and sexual life cycles of two freshwater dinoflagellates, Gymondinium
pseudopalustre Schiller and Woloszynskia apiculata sp. nov. Eur. J. Phycol.,
8, 105–134.
von Stosch, H. A. (1972a) La signification cytologique de la “cyclose
nucléaire” dans le cycle de vie des Dinoflagelles. Mem. Soc. Bot. Fr.,
201–212.
Whiteley, A. S., Burkill, P. H. and Sleigh, M. A. (1993) Rapid method
for cell cycle analysis in a predatory marine dinoflagellate. Cytometry,
14, 909– 915.
627