ICES mar. Sei. Symp., 197: 63-68. 1993
The relationship between phytoplankton growth rate and
production with emphasis on respiration and excretion
Egil Sakshaug
Sakshaug, E. 1993. The relationship between phytoplankton growth rate and pro­
duction with emphasis on respiration and excretion. - ICES mar. Sei. Symp., 197: 6 3 -
68 .
Rates o f respiration and production o f extracellular matter represent losses from
phytoplankton, dep end on the growth regime, and may becom e particularly high in
stressed cells. They are also species-dependent to an extent that should be taken into
consideration in models; species dependence in respiration rates to som e extent may
reflect differences in strategies for the uptake o f nitrogen. In som e species the
mitochondrial respiration rate in the light is considerably higher than in the dark. For
such species calculations on the basis o f measurements o f oxygen uptake in darkness
may lead to underestimation o f the gross photosynthetic rate in terms of oxygen
evolution and. conversely, underestimation o f net carbon uptake on the basis o f data
for gross carbon uptake. Studies o f laboratory cultures o f three diatom species indicate
that net particulate carbon uptake on average may be as low as about 50% o f gross
carbon uptake. This implies that the photosynthetic efficiency (a ) and the maximum
photosynthetic rate (Pm) for net particulate uptake should be that much lower than the
corresponding values relevant for gross carbon uptake.
Egil Sakshaug: Trondheim Biological Station, The M useum , University o f Trondheim ,
Bynesveien 46, N 70 I8 Trondheim , N orw ay.
Introduction
Respiration
Phytoplankton biomass (Bc ) at any given instant is given
by the equation
dBc/dt = (PCD - LC)BC
(1)
where Pc is the gross hourly photosynthetic rate and Lc
the sum of daily loss rates (superscript C denotes nor­
malization to carbon). For simplicity, a light on/light off
system has been assumed with D as the number of
illuminated hours d~'. Obviously, if the gross photosyn­
thetic rate is low, as in early spring in high-latitude
waters and generally in deeply mixed water columns,
small changes in Lc can have profound effects on the
dynamics of the algal stock (Sakshaug et al., 1991a). It is
thus as important to know loss rates as the gross photo­
synthetic rate if algal biomass is to be predicted.
The total loss rate L is the sum of grazing, sedimen­
tation, and respiration rates as well as the production of
extracellular matter. This paper deals with the latter two
with emphasis on modelling of phytoplankton growth.
For more information about these two rates, see Geider
and Osborne (1989), Weger et al. (1989), Zlotnik and
Dubinsky (1989) and references therein.
Respiration is usually measured in terms of oxygen
consumption. The most important process is mitochon­
drial respiration (usually and misleadingly called dark
respiration); photorespiration and the Mehler reaction
may occur mainly in strong light, i.e., in the very
uppermost meters of the water column (Tolbert, 1974;
Raven and Beardall, 1981; Glud e ta l., 1992).
The hourly mitochondrial respiration rate in darkness
(rh) appears to be closely related to the hourly maximum
gross photosynthetic rate Pm (Myers and Graham , 1971;
Platt and Jassby, 1976). The bulk of data for the rh/Pm
ratio vary from below 0.01 to 0.5 (Humphrey, 1975,
1979; G eider and Osborne, 1989 and references there­
in). Dinoflagellates exhibit particularly high ratios
(>0.25), as may also large diatom species such as Ditylum brightwellii and Thalassiosira nordenskioeldii (Falkowski and Owens, 1978; Grande e ta l., 1989). Cyano­
bacteria exhibit particularly low ratios, i.e., <0.1
(Geider and Osborne, 1989).
The rh/Pm ratio (oxygen measurements) of some
species may be virtually independent of the growth
irradiance. This apparently holds for the Woods Hole
clone of the diatom Skeletonema costatum and the chlor-
64
E. Sakshaug
I C E S m a r . Sei. S y m p . . 197 ( I 9 M )
ophyte Dunaliella tertiolecta, which exhibit ratios of
about 0.14 and 0.11 (oxygen measurements), respect­
ively, at 14:10 h daylength and 15°C (Falkowski and
Owens, 1980). The rh/Pm ratio varies with daylength,
however. M. Gilstad etal. (unpublished data) found for
a Trondheimsfjord, Norway, clone of S. costatum ratios
of 0.06 and 0.11 for 12 h daylength and continuous light,
respectively, at 15°C.
T he respiration rate in darkness depends on tem pera­
ture (T°C), usually in an exponential fashion (Raven,
1974):
rh T = a ■ ekl
(2)
According to many investigations the daily respiration
rate rd is virtually linearly related to the net growth rate ii
(Laws and Caperon, 1976; Bannister, 1979; Verity,
1982a, b; Laws et al., 1983; Falkowski et al., 1985;
Langdon, 1987):
rd = rQ +
ku
(3)
rd, the intercept rQ (the respiration rate at zero net
growth), and have units d~' while k is dimensionless.
This relationship appears to hold fairly well for a variety
of growth irradiances and daylengths (Verity, 1982b; M.
Gilstad et a l., unpublished d ata). Among data compiled
by Langdon (1988) r0 ranges from 0.03 to 0.44 d~'. The
highest value in their survey belonged to the dinoflagellate Alexandrium excavatum (= Gonyaulax tamarensis),
while species belonging in other algal groups had values
below 0.22, averaging 0.11 ± 0.05 d “ 1. G. tamarensis
also had the highest value for the slope k , i.e. 0.40,
whereas the other species averaged 0.18 ± 0.03.
It is not known to what extent Equation 3 is relevant
when tem perature is variable. On the one hand
Equation 3 might be appropriate because growth and
respiration rates both decrease when the tem perature
decreases. However, rQ is likely to decrease with tem ­
perature, and growth and dark respiration rates may
have different Q 10 values (Langdon, 1988). In Leptocylindrus danicus Q 10 for respiration is lower than for
growth (Verity, 1982a), whereas in some polar phyto­
plankton communities the opposite may be true (Neori
and Holm-Hansen, 1982; Tilzer and Dubinsky, 1987). In
any case, stressed algae (e.g. algae grown in strong light
in long days) may exhibit anomalously high respiration
rates (Sakshaug et al., 1991b). There is clearly a need for
more culture-based data sets for systematic study of the
variations in the dark respiration rate.
It is usually assumed that the dark respiration rate is
the same whether in darkness or in light, i.e. that the
daily mitochondrial respiration rate equals 24 rh. This,
however, is not generally true. Recent investigations
involving mass spectrometric analysis of gas exchange
have shown that mitochondrial respiration rates may be
considerably higher in the light than in darkness
(G rande et al., 1989; Weger et al., 1989). Because of
this, adding the respiration rate in darkness to the net
oxygen evolution rate would result in 25% too low a
value for the gross photosynthetic rate in the case of the
diatom Thalassiosira weissflogii (Weger eta l., 1989). For
such reasons, coefficient values given by Langdon (1988)
for Equation 3 may also yield too low a gross growth rate
for some species. On the other hand, G rande et al.
(1989) observed that mitochondrial respiration rates in
darkness and light do not differ significantly in the
diatom Skeletonema costatum and the coccolithophorid
Emiliania huxleyi\ however, their data set exhibited
considerable scattering.
Studies of N-starved cells of the chlorophyte Selenastrum m inutum have revealed that the addition of nitro­
genous nutrients in the light, w hether ammonium,
nitrite, or nitrate, grossly enhances the activity of the
tricarboxylic acid cycle, thus C 0 2 release is enhanced.
Cytochrome electron transport (i.e., 0 2 uptake) in con­
trast is enhanced mainly when ammonium is added
(Turpin eta l., 1988; Weger and Turpin, 1989; Weger et
al., 1988). This may imply that high respiration rates in
darkness, for instance in dinoflagellates, are related to
high dark uptake rates for nitrogen, especially of am­
monium, as reported by Paasche et al. (1984). They
found in five of seven species that N-sufficient cells in
darkness incorporated ammonium at a rate of about
65% of the rate in light (in terms of nitrate: 45%).
Excretion of organic m atter
Production of organic extracellular m atter represents a
loss to phytoplankton and a substrate for heterotrophic
microorganisms (Wiebe and Smith, 1977; Azam and
A m m erm ann, 1984). Main constituents of extracellular
matter are glycollic acid, polypeptides, amino acids,
lipids, and various polysaccharides, in the main lowmolecular compounds (Aaronson, 1971; Myklestad et
al., 1972; Ignatiades and Fogg, 1973; Smestad et al.,
1974; W atanabe, 1980; Smestad Paulsen eta l., 1992).
Phytoplankton release extracellular organic products
mainly in the light; in darkness photosynthetates are
used mainly in biosynthesis (Hellebust, 1965); m ore­
over, production of extracellular m atter may be higher
in fluctuating than in continuous light (Cosper, 1982).
Algal cells may exude 60-90% of the fixed carbon in
extreme cases, but such high percentages usually pertain
to growth in marginally low light, i.e., when carbon
fixation is very small, and may also reflect methodologi­
cal problems (Fogg, 1977; W atanabe, 1980; Zlotnik and
Dubinsky, 1989). Relatively high rates of extracellular
production may occur in nutrient-deficient cells; this,
Phytoplankton growth and production
I C E S m a r . Sei. S y m p .. 197 (19 93)
however, is highly species-dependent. In cultures of
stationary phase diatom cells the ratio of extracellular to
cellular carbohydrate was 0.3-1.5 in four species of
Chaetoceros and only 0.01-0.07 in Skeletonema costa­
tu m , Thalassiosiragravida, and T.fluviatilis (Myklestad,
1974).
Although high percentages of extracellular pro­
duction relative to gross carbon uptake, i.e ., 10-50, have
been reported in nature, particularly in oligotrophic
waters (Anderson and Zeutschel, 1970; Thomas, 1971;
Berman and Holm-Hansen, 1974; Mague et al., 1980),
the bulk of field and laboratory data indicate percent­
ages of only 3-10 unless cells are stressed (Sellner, 1981 ;
Zlotnik and Dubinsky, 1989 and references therein).
Laboratory data for Leptocylindrus danicus (Verity,
1981) and Isochrysis galbana, Chlorella vulgaris, and
Synechococcus sp. (Zlotnik and Dubinsky, 1989) con­
flict with respect to the effect of temperature. The
production of extracellular matter in absolute terms is
relatively independent of temperature in L. danicus,
while that relative to the gross photosynthetic rate
decreases from 3-20% at 5°C to 1-3% at 20°C. In the
other three species the production of extracellular m at­
ter relative to the gross photosynthetic rate is relatively
independent of temperature. Such characteristics are
clearly species-dependent.
M od ellin g
The relationship between growth, photosynthesis, and
losses may be modelled in terms of carbon-specific rates:
H = D PC - rc - D dc
(4)
Pc is the hourly gross photosynthetic rate, actually a P-I
function, rc is the daily respiration rate, dc the hourly
rate of production of extracellular matter assuming that
it takes place only in the light, and D is daylength (h). rc
may be substituted by Equation (3); however, rQ and k
will then have to be determined and, at least in the case
of some species, differences in the mitochondrial respir­
ation rate in the dark and light phases will have to be
accounted for (Langdon. 1992). It is thus virtually im­
possible to estimate all terms in Equation (4) accurately.
In fieldwork, one therefore has to resort to simple
empirical models and coefficient values which are
approximate.
One simple alternative is to keep only the term D P C,
i.e., daylength and the P-I formulation in Equation (4)
and instead scale Pc so that it expresses only the fraction
of the daily photosynthetic rate which is appropriate for
the method of measurement in use or the problem in
question, for instance one scaling for gross photosyn­
thesis, another for net photosynthesis, etc. This can be
done by defining appropriate values for the maximum
65
quantum yield ø max which is implicit in all P -I formu­
lations (Sakshaug et al., 1991b, Sakshaug and Slagstad,
1991). cpmm thus becomes a scaling factor (functional
ø m a x ) - Because ø max is implicit in the photosynthetic
efficiency (a) and the maximum photosynthetic rate
(Pm), variations in functional ø max imply pro rata vari­
ations in a and Pm, while Ik, the light saturation index, is
unchanged. Biologically dependent variation in ø max
will not be considered here (see Welschmeyer and
Lorenzen, 1981; Langdon, 1988 for review).
Values for functional <pmd% may depend on incubation
time and may become anomalously low for stressed
populations because of susceptibility to manipulation
(Sakshaug et al., 1991b). Nevertheless, on the basis of
reported values for ø max (Welschmeyer and Lorenzen,
1981; G eider et al., 1985; G eider and Osborne, 1986;
Langdon, 1988; Sakshaug et al., 1991b; M. Gilstad etal.,
unpublished data), a methodologically dependent hier­
archy of values for functional cpmax may be suggested
(Table I).
Table 1 indicates primarily that functional ø max be­
comes smaller the less the flow of m atter the method of
measurement intercepts. Thus some of the flow from
PSII, where oxygen is released, is spent on nutrient
uptake, particularly nitrate, so that there is less left for
carbon uptake, causing functional ø max for gross carbon
uptake, c ømaxi to become lower than ø max for gross
oxygen evolution, ° ø max. This may be particularly evi­
dent at low irradiances (Megard etal., 1985). Moreover,
carbon uptake measurements based on filtered samples
intercept less of the carbon flow than those based on
unfiltered samples because extracellular products will
not be included in the latter (this difference may be close
to nil for short-term carbon uptake, i.e., < 1/2 h,
assuming negligible photoinhibition). Finally, func­
tional ø max for net particulate carbon uptake and the net
growth rate, " ø max, will be the lowest because it rep­
resents what is left (i.e. reproducing carbon) after all
internal losses.
The ratio between c ø max and °<pmax in Table 1 corre­
sponds to a photosynthetic quotient (g-at C : mol 0 2) of
about 0.6 and is in good agreement with averages for
large sets of data for marine phytoplankton (Platt et a l.,
Table 1. Suggested method-dependent hierarchy o f functional
values for the maximum quantum yield, </>max [mol 0 2 or g -a t C
(mol p h o to n s)1].
Theoretical maximum (ÿ>max )
Gross oxygen release ( ° ø max)
Gross carbon uptake (unfiltered sam ples), (c ø max)
Gross carbon uptake (filtered samples), (sømnx)
(gross growth rate-relevant)
Net growth rate ( > raax)
0.125
0.10-0.11
0 .0 6 -0 .0 7
0 .0 5 -0 .0 7
0.0 3 -0 .0 4
66
I C E S m a r . Sei. S y m p .. 197 (19 93 )
E. Sakshaug
1987; Langdon, 1988). On the basis of studies of fresh­
water assemblages dominated by dinoflagellates, i.e.,
Peridinium spp., a “typical” quotient of about 0.5 has
been suggested (Megard et al., 1985), i.e., that c ø max is
about half of ° ø maxShort-term radiocarbon experiments, i.e. < i h (Lewis
and Smith, 1983), may yield real gross values for carbon
uptake (Li and Goldman, 1981). However, as noted by
Weger et al. (1989), problems may arise in the esti­
mation of net particulate carbon uptake on the basis of
data for gross carbon uptake if the respiration rate is
higher in the light than in darkness. As a consequence,
subtraction of the respiration rate in darkness from the
gross carbon uptake rate will yield too high a rate for net
particulate production. It also follows that estimations
of the gross growth rate ( a -I- r), which is explicit in many
models for algal growth (Bannister, 1979; Kiefer and
Mitchell, 1983; Laws and Bannister, 1980; Sakshaug et
al., 1989; Cullen, 1990), by adding the daily respiration
rate on the basis of measurements in darkness (i.e., 24
rh) to the measured growth rate will yield a gross growth
rate which is too low. This implies that functional ø max
for the gross particulate carbon uptake rate and the gross
growth rate, gø max, becomes too low. In principle, the
difference between c </>max and gø max should correspond
to extracellular production and under normal circum­
stances make up < 10% o f ( f/>maxIn nutrient-sufficient cultures of the Barents Sea dia­
toms Thalassiosira nordenskioeldii and Chaetoceros furcellatus, c 0 max is 0.077 and 0.055, respectively, while
g0max7 as calculated on the basis of fi + r, is only 0.04
(Sakshaug et al., 1991b). Although a high rate of pro­
duction of extracellular m atter cannot be excluded, it is
likely that the low value for gø max relative to c 0 max may
be due to underestimation of the respiration rate in the
light. In Skeletonema costatum, in contrast, gø max is as
high as 0.076 (M. Gilstad et al., unpublished data),
which may reflect that the respiration rate of this species
is about the same in the light as in darkness (G rande et
al., 1989) and that production of extracellular matter is
small (Myklestad, 1974).
Functional ø max for the net growth r a t e / ø max, can be
calculated on the basis of models such as presented by
Sakshaug et al. (1991b) by neglecting the respiration
term. Values for T. nordenskioeldii, C. furcellatus, and
Skeletonema costatum are 0.031, 0.033, and 0.040, re­
spectively, and, thus, remarkably similar considering
that the former two species were grown at 0.5°C and the
latter at 15°C (Sakshaug et al., 1991b; M. Gilstad et al.,
unpublished data).
The ratio
is 0.43 and 0.65 for T. nordens­
kioeldii and C. furcellatus, respectively, and about 0.5
for S. costatum, i.e., on average about 0.5 for the three
species. These results imply that net particulate pro­
duction as an average for the three species may be only
about half the gross carbon uptake, thus gross carbon
uptake values for a and Pm should be halved for the
calculation of net particulate carbon uptake. For some
dinoflagellate species the ;'ømax/c <Amax ratio is likely to
be even lower because of their very high respiration
rates. It is impossible to suggest corresponding rules for
the relationship between carbon uptake and growth rate
for longer incubation times because carbon uptake ap­
proaches net uptake as the incubation time increases.
C on clu d in g remarks
Rates of cellular (net particulate) production and extra­
cellular production are paramount variables in ecosys­
tem studies because they represent inputs of m atter to
the ecosystems, whether the grazing chain or the mi­
crobial loop. Unfortunately, determination of these
rates is not trivial, and the problems discussed here bear
relation to any marine productivity budget, including
global budgets for the biological “carbon pum p” . While
real gross carbon uptake may be determined by short­
term incubations, it is impossible to measure algal res­
piration rates separately from those of heterotrophs in
the field; besides, different respiration rates in the light
and in darkness present a major problem with respect to
some species. Thus net production is hard to determine
in the field. M oreover, there are major problems in the
determination of extracellular production. W hether
with respect to respiration or production of extracellular
matter, species- and life stage-dependent differences
appear too large to be overlooked. Presumably, im port­
ant information can be had from studies of cultures such data, however, are scarce relative to the many non­
interpretable data sets from field studies. On the basis of
a few data presented here it appears that net particulate
production on average may be as low as half the gross
production, while extracellular production may consti­
tute <10% of the gross production under “normal”
circumstances.
R e fe re n c e s
A aronson, S. 1971. The synthesis o f extracellular macromol­
ecules and membranes by a population o f the phytoflagellate
O ch rom on as danica. Limnol. O ceanogr., 16: 1-9.
Anderson, G. C ., and Zeutschel, R. P. 1970. Release o f
dissolved organic matter by marine phytoplankton in coastal
and offshore areas o f the Northeast Pacific Ocean. Limnol.
O ceanogr.. 15: 402^107.
A za m . F., and Am m erm ann, J. W. 1984. Cycling o f organic
matter by bacterioplankton in pelagic marine ecosystems:
microenvironmental considerations. In Flows o f energy and
material in marine ecosystem s, pp. 345-360. Ed. by M. J. R.
Fasham. Plenum Press, N ew York and London. 733 pp.
Bannister, T. R. 1979. Quantitative description o f steady-state
nutrient-saturated algal growth, including adaptation. Lim­
nol. O ceanogr., 24: 76-96.
I C E S m a r . Sei. S y m p ., 197 ( 1993)
Berman. T., and Holm -H ansen. O. 1974. Release o f photoassi­
milated carbon as dissolved organic matter by marine phyto­
plankton. Mar. Biol., 28: 305-310.
C o sp e r.E . 1982. Influence o f light intensity on diel variations in
rates o f growth, respiration and organic release o f a marine
diatom: comparison o f diurnally constant and fluctuating
light. J. Plank. R es., 4: 705-724.
Cullen, J. J. 1990. On models o f growth and photosynthesis.
Deep -S ea R es., 37: 667-683.
Falkowski, P. G ., Dubinsky, Z ., and Wyman, K. 1985.
Growth-irradiance relationships in phytoplankton. Limnol.
O ceanogr., 30: 311-321.
Falkowski, P. G ., and O wens, T. G. 1978. Effects o f light
intensity on photosynthesis and dark respiration o f marine
phytoplankton. Mar. Biol., 45: 289-295.
Falkowski, P. G ., and O w ens, T. G. 1980. Light-shade adap­
tation: two strategies in marine phytoplankton. Plant
Physiol., 66: 592-595.
Fogg, G . E. 1977. Excretion o f organic matter by phyto­
plankton. Limnol. O ceanogr., 22: 576-577.
Geider, R. J., and Osborne, B. A . 1986. Light absorption,
photosynthesis and growth o f Nannochloris atom us in
nutrient-saturated cultures. Mar. Biol., 93: 351-360.
G eider, R. J., and Osborne, B. A. 1989. Respiration and
microalgal growth: a review o f the quantitative relationship
between dark respiration and growth. N ew Phytol., 112:
327-341.
Geider, R. J., Osborne, B. A . , and Raven, J. A . 1985. Light
dependence o f growth and photosynthesis in P haeodactylum
tricornutum (Bacillariophyceae). J. Phycol., 21: 609-619.
Glud, R. N i, Ramsing, N. B ., and Revsbech, N. P. 1992.
Photosynthesis and photosynthesis-coupled respiration in
natural biofilms quantified with oxygen microsensors. J.
Phycol., 28: 51-60.
Grande, K. D . , Marra, J., Langdon, C ., H einem ann, K., and
Bender. M. L. 1989. Rates o f respiration in the light
measured in marine phytoplankton using an lxO isotopelabelling technique. J. exp. mar. Biol. E col., 129: 95-120.
Hellebust, J. A. 1965. Excretion o f som e organic compounds
by marine phytoplankton. Limnol. O ceanogr., 10: 192-206.
Humphrey, G. F. 1975. The photosynthesis:respiration ratio o f
som e unicellular marine algae. J. exp. mar. Biol. E c o l., 18:
111-119.
Humphrey, G. F. 1979. Photosynthetic characteristics of algae
grown under constant illumination and light-dark regimes. J.
exp. mar. Biol. E col., 40: 63-70.
Ignatiades, L.. and Fogg, G. E. 1973. Studies on the factors
affecting the release o f organic matter by S keletonem a costa­
tum (G rev.) Cleve in field conditions. Mar. biol. Ass. U K ,
53: 923-935.
Kiefer, D. A . , and Mitchell, B. G. 1983. A simple steady state
description o f phytoplankton growth rates based on absorp­
tion cross section and quantum efficiency. Limnol. O cea ­
nogr., 28: 770-776.
Langdon, C. 1987. On the causes of interspecific differences in
the growth irradiance relationship for phytoplankton. I. A
comparative study o f the growth irradiance relationship of
three marine phytoplankton species: Skeletonem a costatum ,
Olisthodiscus luteus and G onyaulax tam arensis. J. Plank.
R es., 9: 459-482.
Langdon, C. 1988. On the causes o f interspecific differences in
the growth-irradiance relationship for phytoplankton. II. A
general review. J. Plank. R es., 10: 1291-1312.
Langdon, C. 1992. The significance o f respiration in production
measurements based on both carbon and oxygen (this vol­
ume).
Laws, E. A . , and Bannister, T. T. 1980. Nutrient- and lightlimited growth o f Thalassiosira fluviatilis in continuous cul­
Phytoplankton growth and production
67
ture, with implications for phytoplankton growth in the
ocean. Limnol. O ceanogr., 25: 457-473.
Laws, E. A . , and Caperon, J. 1976. Carbon and nitrogen
metabolism by M onochrysis lutheri: measurement o f growth
rate dependent respiration rates. Mar. Biol., 36: 85-97.
Laws, E. A ., Redalje, D . G ., Karl, D. M ., and Chalup, M. S.
1983. A theoretical and experimental examination o f two
recent models o f phytopiankton growth. J. theor. Biol., 105:
469-491.
Lewis, M. R.. and Smith, J. C. 1983. A small volum e, shortincubation-time method for measurement o f photosynthesis
as a function o f incident irradiance. Mar. Ecol. Prog. Ser.,
13: 99-102.
Li, W. K. W .. and G oldm an, J. 1981. Problems in estimating
growth rates o f marine phytopiankton from short-term 14C
assays. Microb. E col., 7: 113-121.
Maguc, T. H ., Friberg, F., Hughes, D. J., and Morris, I. 1980.
Extracellular release o f carbon by marine phytopiankton: a
physiological approach. Limnol. O ceanogr., 25: 262-279.
Megard, R. O .. Berman, T ., Curtis, P. J., and Vaughan, P. W.
1985. D ep en d en ce o f phytopiankton assimilation quotients
on light and nitrogen source: implications for oceanic pri­
mary productivity. J. Plank., R es., 7: 691-702.
Myers, J., and Graham , J. R. 1971. The photosynthetic unit in
Chlorella measured by repetitive short flashes. Plant
Physiol., 48: 282-286.
Myklestad, S. 1974. Production o f carbohydrates by marine
planktonic diatoms. I. Comparison o f nine different species
in culture. J. exp. mar. Biol. E col., 15: 261-274.
Myklestad, S., Haug, A . , and Larsen, B. 1972. Production o f
carbohydrates by the marine diatom C haetoceros affinis var.
willei (Gran) Hustedt. II. Preliminary investigation o f the
extracellular polysaccharide. J. exp. mar. Biol. E c ol., 9: 137—
144.
Neori, A . , and Holm-Hansen, O. 1982. Effect o f temperature
on rate o f photosynthesis in Antarctic phytopiankton. Polar
B iol., 1: 33-38.
Paasche, E ., Bryceson, I., and Tangen, K. 1984. Interspecific
variation in dark nitrogen uptake by dinoflagellates. J. Phy­
col., 20: 394-401.
Platt, T ., Harrison, G ., Horne, E. P. W ., and Irwin, B. 1987.
Carbon fixation and oxygen evolution by phytopiankton in
the Canadian High Arctic. Polar B iol., 8: 103-113.
Platt, T ., and Jassby, A . 1976. The relationship between
photosynthesis and light for natural assemblages o f coastal
marine phytopiankton. J. Phycol., 12: 421-430.
Raven, J. A . 1974. Carbon dioxide fixation. In Algal physi­
ology and biochemistry, pp. 434-455. Ed. by W. D. P.
Stewart. University o f California Press, Los A ngeles.
Raven, J. A . , and Beardall, J. 1981. Respiration and photores­
piration. In Physiological bases o f phytopiankton ecology,
pp. 55-82. Ed. by T. Platt. Can. Bull. Fish, aquat. Sei., 210.
Sakshaug, E ., Andresen, K., and Kiefer, D . A . 1989. A steady
state description o f growth and light absorption in the marine
plankton diatom Skeletonem a costatum . Limnol. O ceanogr.,
3 4 :1 9 8 -2 0 5.
Sakshaug, E ., Johnsen, G ., A ndresen, K., and Vernet, M.
1991b. Modeling o f light-dependent algal photosynthesis and
growth: experiments with the Barents Sea diatoms Thalassio­
sira n ordenskioeldii and Chaetoceros furcellatus. D eep-Sea
R es., 38: 415^130.
Sakshaug, E ., and Slagstad, D . 1991. Light and productivity of
phytopiankton in polar marine ecosystems: a physiological
view. Polar R es., 10: 69-85.
Sakshaug, E ., Slagstad, D . , and H olm-H ansen, O . 1991a.
Factors controlling the developm ent o f blooms in the Antarc­
tic O c e a n - a mathematical model. Mar. C h em ., 35:259-271.
Sellner, K.. G. 1981. Primary productivity and the flux of
68
E. Sakshaug
dissolved organic matter in several marine environments.
Mar. B iol., 65: 101-112.
Smestad, B ., Haug, A . , and Myklestad, S. 1974. Production of
carbohydrate by the marine diatom Chaetoceros affinis var.
willei (Gran) Hustedt. III. Structural studies of the extra­
cellular polysaccharide. Acta Chem. Scand., B28: 662-666.
Smestad Paulsen, B ., Vieira, A . A . H ., and Klaveness, D.
1992. Structure o f extracellular polysaccharides produced by
a soil C ryptom on as sp. (Cryptophyceae). J. Phycol., 28: 6 1 63.
Thom as, J. P. 1971. R elease o f dissolved organic matter from
natural populations o f marine phytopiankton. Mar. Biol.,
11: 311-323.
Tilzer, M ., and Dubinsky, Z. 1987. Effects o f temperature and
day-length on the mass balance o f antarctic phytopiankton.
Polar B iol., 7: 35-42.
Tolbert, N. E. 1974. Photorespiration. In Algal physiology and
biochemistry, pp. 474-504. Ed. by W. D . P. Stewart. Univer­
sity o f California Press, Los Angeles.
Turpin, D . H .. Elrifi, I. R .. Birch, D. G ., W eger, H. G ., and
H olm es, J. J. 1988. Interactions between photosynthesis,
respiration, and nitrogen assimilation in microalgae. Can. J.
B o t., 66: 2083-2097.
Verity. P. G. 1981. Effects o f temperature, irradiance, and
daylength on the marine diatom L eptocylin dru s danicus
Cleve. II. Excretion. J. exp. mar. Biol. E col., 55: 159-169.
Verity, P. G. 1982a. Effects o f temperature, irradiance, and
daylength on the marine diatom L eptocylindrus danicus
Cleve. III. Dark respiration. J. exp. mar. Biol. E c o l., 60:
197-207.
I C E S m a r . Sei. S y m p .. 197 (1 993)
Verity, P. G. 1982b. Effects o f temperature, irradiance, and
daylength on the marine diatom L eptocylin dru s danicus
Cleve. IV. Growth. J. exp. mar. Biol. E c o l., 60: 2 0 9 2 22 .
W atanabe, Y. 1980. A study o f excretion and extracellular
products o f natural phytopiankton in Lake Nakanuma,
Japan. Int. Rev. ges. H ydrobiol., 65: 809-834.
W eger, H . G ., Birch, D . G . M ., Elrifi, I. R ., a ndTurpin, D . H.
1988. A m m onium assimilation requires mitochondrial res­
piration in the light. A study with the green alga Selenastrum
m inutum . Plant Physiol., 86: 688-692.
W eger, H. G .. Herzig. R ., Falkowski, P. G ., an dTurpin, D . H.
1989. Respiratory losses in the light in a marine diatom:
measurement by short-term mass spectrometry. Limnol.
O cea n o g r., 34: 1153-1161.
W eger, H. G ., a ndTurpin, D . H . 1989. Mitochondrial respir­
ation can support N O j and N O 2 reduction during photosyn­
thesis. Interactions between photosynthesis, respiration and
N assimilation in the N-limited green alga Selenastrum m inu­
tum . Plant Physiol., 89: 409-415.
W elschmeyer, N. A . , and Lorenzen, C. J. 1981. Chlorophyllspecific photosynthesis and quantum efficiency at subsaturating light intensities. J. Phycol., 17: 283-293.
W iebe, W. J., and Smith, D . F. 1977. Direct measurement
o f dissolved organic carbon release by phytopiankton and
incorporation by microheterotrophs. Mar. Biol., 42: 213—
223.
Zlotnik, I., and Dubinsky, Z. 1989. The effect o f light and
temperature on D O C excretion by phytopiankton. Limnol.
O ceanogr.. 34: 831-839.