Journal of Plankton Research Vol.18 no.6 pp.1041-1045.1996
SHORT COMMUNICATION
The relative preference index (RPI) for phytoplankton nitrogen
use is only weakly related to physiological preference
Willem Stolte and Roel Riegman
Netherlands Institute for Sea Research, Department of Biological Oceanography,
PO Box 59,1790 AB Den Burg, The Netherlands
Abstract In field studies where the uptake of different nitrogen compounds in phytoplankton is
studied, a relative preference index (RPI) is often used which describes uptake relative to the abundance of a particular nitrogen compound, usually ammonium. This index can easily be misused when it
is applied as a physiological preference indicator. In this study, it is shown that the index may be more
dependent on nutrient concentrations than on the algal preference for ammonium under certain
circumstances.
In marine environments, nitrogen is available for phytoplankton in different
forms. Ammonium is the most reduced form and preferentially used by phytoplankton. Nitrogen recycling within the photic zone is via ammonium or organic
nitrogen. Nitrate, the most oxidized form, is considered to be formed below the
photic zone. In stratified waters, the use of nitrate for phytoplankton growth relative to the total nitrogen uptake is often used to determine the new production
(Dugdale and Goering, 1967), i.e. the import of nitrogen into the photic zone.
The relative preference index (RPI), originally introduced by McCarthy et al.
(1977) was meant to compare the utilization of a nitrogen compound (originally
ammonium) relative to availability [equation (1)].
PA
N +A
where pA and pN are the cellular ammonium and nitrate uptake rates, and A and N
are the ambient concentrations of ammonium and nitrate, respectively. In the
original paper, it is suggested that this index could be a useful measure of the nitrogen sufficiency of the environment (McCarthy et al., 1977). In other field studies
(Glibert et al., 1982; Probyn, 1985; Probyn and Painting, 1985; Lancelot et al., 1986;
Smith and Nelson, 1990; Owens et al., 1990), the RPI has often been used. In this
note, we want to stress that care has to be taken not to use the RPI as an indicator of
algal preference for a nitrogen species. The explanation for this lies in the fact that
nutrient uptake is a non-linear function of the concentration of that particular
nutrient. If we assume Michaelis-Menten kinetics for ammonium and nitrate
uptake, then equation (1) can be expressed as:
© Oxford University Press
1041
W.Stolte and R.Riegman
KA+A
RPI =
•
A+N
(2)
VA-AjVN-N
KA + A
A
where VA and VN are the maximum uptake rates for ammonium and nitrate,
respectively. KA and KN are the half-saturation constants for uptake of ammonium
and nitrate, while A and Ware the concentrations of ammonium and nitrate in the
bulk water phase. The half-saturation constants of ammonium and nitrate are in
general not very different (Eppley etal., 1969). Here, we assume that KA = KN = K.
The maximum uptake rates of ammonium and nitrate can be very different,
depending on their physiological status (Caperon and Meyer, 1972). Suppose that
VA = a • VN (note that a represents the physiological preference of the organism
for ammonium relative to nitrate); in this case, equation (2) becomes:
a • VN -(A + N)
K+A
RPI =
a • VN • A
K+A
VN • N
K+N
a-(A+N)
CL-A
N
(K
x + A)
' \K + A K + N,
which equals
a-(A+N)
a-A-(K
K+A
+ A)
N-(K + A)
K+N
or
Rpi
=
a-(A+N)
(3)
. N-(K + A)
a A +
^
K+N
From equation (3), it is clear that the RPI is a function of a (the real preference
for ammonium) as well as the ammonium and nitrate concentrations. To examine
the effects of nutrient concentration on this index, we consider three cases:
In that case, equation (3) yields:
K +N
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Relative preference index for phytoptankton N
When the concentration of nitrate is also much higher than the half-saturation
constant for uptake, than equation (3) can be expressed as:
RPI=
Under these circumstances, the RPI is positively correlated to the nitrate concentration when A and K are constant. This is the reason for the sometimes very high
RPI values in upwelling systems where nitrate concentrations are 20 u.M or higher
(Probyn, 1985; Probyn and Painting, 1985).
(u)N = A
In that case, equation (3) becomes:
(6)
a+1
When the algae do not have any preference for ammonium (a = 1), then RPI = 1.
When there is a very high preference for ammonium (a = °°), then RPI = 2.
(iii) N is much lower than A.
In that case, equation (3) becomes:
RPI =
^
(7)
K+N
which makes it a complex function of the ambient nitrate and ammonium concentrations, the preference for ammonium (a) and the half-saturation constant for
uptake (K). RPI approaches one when the nitrate concentration approaches zero.
In the hypothetical case that there would not be any preference for ammonium
(so a= 1), the RPI varies with nitrate and ammonium concentrations (Figure 1).
Note that RPI can become very high, although there is no preference at all for
either nitrate or ammonium under the circumstance that nitrate concentration is
high compared to the ammonium concentration [case (i)]. When a = 5, so VA = 5 x
VN, RPI is above unity, except at very low nitrate concentrations (Figure IB). A
lower value of KA results in a higher preference for ammonium at low ammonium
concentrations, which is reflected in higher values of the RPI (Figure 1C), whereas
the effect of a lower KN results in lower RPI values (Figure ID). From these
examples, it is clear that the RPI and the physiological preference of algae for a
nitrogen source are not always the same.
In our view, the present use of the RPI is at least doubtful. Great care has to be
taken that it does not describe concentrations rather than the ammonium preference of a population. For example, Probyn and Painting (1985) conclude that
ammonium is the preferred nitrogen source because the RPI is above unity.
Although they are probably right in that ammonium is the preferred nitrogen
source, it is not possible to conclude this from an RPI above one. In their study,
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0.1
110-100
n-10
n
0.1-1
Fig. 1. Calculated relative preference index as a function of ambient ammonium and nitrate concentrations of a theoretical phytoplankton population with equal ammonium and nitrate uptake kinetics
(A), a 5-fold preference of ammonium over nitrate (B), and with a 5-fold lower Km for uptake of
ammonium (C) or nitrate (D).
nitrate concentrations were very high (most probably saturating for uptake by
phytoplankton), while ammonium concentrations were very low, probably not
saturating. This case is described above as case (i). Under these circumstances, the
RPI is more dependent on the nitrate concentration than on any uptake characteristic and can therefore not be used.
One of the useful applications of the RPI is to compare ammonium preference in
different size classes. However, since in one sample the bulk nutrient concentration does not differ for different size classes, comparing RPIs becomes independent of the concentration of nutrients. In that case, the uptake ratio alone gives
exactly the same information on the partitioning of phytoplankton nitrogen
sources because:
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Relative preference index for phytoplankton N
PAI
PAI
+
PNI
PAI
A+N
j
PA2
\
PA2 + PN2
=
\ p A , + pN,
(
PA2 + PN2
A +N
where the indices 1 and 2 stand for different size classes of the plankton. Apparently, it is not more useful to compare RPIs of different size classes than uptake
ratios when size-dependent nitrate or ammonium preference is studied.
References
CaperonJ. and MeyerJ. (1972) Nitrogen-limited growth of marine phytoplankton—II. Uptake kinetics and their role in nutrient limited growth of phytoplankton. Deep-Sea Res., 19,619-632.
Dugdale.R.C. and GoeringJ.J. (1967) Uptake of new and regenerated forms of nitrogen in primary
productivity. Limnol. Oceanogr., 12, 196-206.
Eppley.R.W., RogersJ.N. and McCarthyJ J. (1969) Half-saturation constants for uptake of nitrate and
ammonium by marine phytoplankton. Limnol Oceanogr., 14,912-920.
Glibert.P.M.. GoldmanJ.C. and Carpenter,EJ. (1982) Seasonal variations in the utilization of
ammonium and nitrate by phytoplankton in Vineyard Sound, Massachusetts, USA. Mar. Biol., 70,
237-249.
Lancelot.C, Mathot.S. and Owens.NJ.P. (1986) Modelling protein synthesis, a step to an accurate
estimate of net primary production: Phaeocystis pouchelii colonies in Belgian coastal waters. Mar.
Ecol. Prog.Ser.,32, 193-202.
McCarthyJ J.. Taylor.W.R. and TaftJ.L. (1977) Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnol. Oceanogr.. 22.996-1011.
Owens,NJ.P., Woodward,E.M.S., Aiken J., Bellan.I.E. and Rees.A.P. (1990) Primary production and
nitrogen assimilation in the North Sea during July 1987. Neth. J. Sea Res., 25, 143-154.
Probyn.T.A. (1985) Nitrogen uptake by size-fractionated phytoplankton populations in the southern
Benguela upwelling system. Mar. Ecol. Prog. Ser, 22,249-258.
Probyn.T.A. and Painting.SJ. (1985) Nitrogen uptake by size-fractionated phytoplankton populations
in Antarctic surface waters. Limnol. Oceanogr., 30, 1327-1332.
Smith.W.O., Jr and Nelson,D.M. (1990) Phytoplankton growth and new production in the Weddell Sea
marginal ice zone in the austral spring and autumn. LimnoL Oceanogr., 35, 809-821.
Received on September 20, 1995; accepted on January 15, 1996
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