882

Notes

Limnol. Oceanogr.. 37(4), 1992, 882-889

0 1992, by the American Society of Limnology

Nutrient

concentration

and Oceanography,

Inc

of aquatic plants: Patterns across species

Abstract-An extensive compilation ofdata for

96 phytoplankton species, 46 macroalgal species,
27 seagrassspecies, 11 species of freshwater angiosperms, and several mixed phytoplankton and
macroalgal communities revealed a tendency toward higher concentrations of N and P in phytoplankton compared to those of macrophytes.
The depletion of P, and to a lesser extent N, in
macrophytes, particularly macroalgae, appears to
reflect a greater degree of P and N limitation of
growth of natural macrophyte populations, rather
than an intrinsic difference in their chemical
composition relative to that of phytoplankton.
Close associations between nutrients, particularly
a strong linear relationship between concentrations of N and P, reflect the similar biochemical
basis of the different aquatic plant groups and
appear to represent a fundamental characteristic
of the plant kingdom. The results obtained indicate, therefore, that aquatic plants form a continuum across a unique pattern of change in nutrient concentrations, despite considerable
differencesin their architectural, evolutionary, and
life histories, and the growth conditions encountered in their habitats.

The dominant role of nutrient availability, primarily of N and P, in controlling the

growth and abundance of phytoplankton
(Hecky and Kilham 1988), macroalgae (e.g.
Lapointe and OConnell 1989), and marine
(e.g. Perez et al. 199 1) and freshwater angiosperms has been established unambiguously.
Because the nutrient status of aquatic
plants is often assessed by examining the
nutrient concentrations of plant tissues (e.g.
Gerloff and Krombholz
1966), there is a
wealth of data on the elemental composition of aquatic plants. However, attempts
to compare the nutrient concentration of
different aquatic plant groups have been few
(e.g. Atkinson and Smith 1984) and limited
in scope. Yet, comparative analysis across
plant groups is a powerful tool to place
available information
in perspective (e.g.

Acknowledgments
This research was funded by a grant from the Ramon
Areces Foundation.
I thank J. C. Goldman for criticisms.

Nielsen and Sand-Jensen 1990), and the

comparative analysis of nutrient concentrations across species and groups of aquatic
plants is likely to reveal consistent patterns,
for the similar biochemical pathways present in aquatic plants should result in close
association between concentrations
of N
and P.
I report here the existence of fundamental
similarities in the relationships among nutrient (C, N, and P) concentrations and nutrient ratios, across aquatic plant groups,
despite order-of-magnitude
differences in
internal concentrations.
Data on C, N, and P concentrations of
phytoplankton, macroalgae, seagrass leaves
(largely derived from the compilation
of
Duarte 1990), and freshwater submerged
angiosperms were compiled from the literature. Nutrient concentrations are reported
here as percentage of dry weight- the unit
most often reported in the literature. Thus,
an important fraction of the existing data
on nutrient concentrations of phytoplankton, which are reported as contents per unit
cell volume or nutrient ratios (i.e. C : N, C : P,
and N : P), could not be compared here. Analytical differences among data sources were
ignored, for the error introduced by differences among techniques should be small
compared to the very large (> 1O-fold) range
of nutrient concentrations in the data set.
Differences in nutrient concentrations
among aquatic plant groups were tested with
ANOVA and the relationships among nutrient concentrations and their ratios in the
plants were described with least-squares regression analysis of the logarithmically
transformed
data. Logarithmic
transformation of the data was necessary to avoid
heteroscedasticity
in these analyses. The
strength of the relationships obtained was
described by the coefficient of determination (R2), and their precision was described
by the standard error of the regression estimate; comparisons among regression coefficients were based on the Students t-test.
The resulting data set, which is available

883

Notes

80

R = 23.6 - 43
m = 33.5W.4

60

'

iij
l2
3

10

20

30

40

50

60

Freshwater
angiosperms
R=12-55
m = 38.Ok7.4
n = 104

25
m = 34.1k12.2

E 20

15
10

'

10

20

30

40

50

60

60

Carbon content (% dry wt )

Fig. 1. Frequency distribution of C content in different aquatic plant groups: R-range; m-mean
y1- number of observations.

on request, included 892 reports of nutrient

concentrations of aquatic plants, comprising data for 96 phytoplankton
species, 46
macroalgal species, 27 seagrass species, 11
species of freshwater angiosperms, and several mixed phytoplankton
and macroalgal
communities. The data set included nutrient concentrations in plants sampled along
a wide variety of aquatic environments, but
while most data on nutrient content of macrophytes represented analyses of plants collected in the field, a significant fraction of
the data for phytoplankton
was obtained
from laboratory cultures.
Concentrations
of C, N, and P ranged
widely (> 1O-fold) across aquatic plants
(Figs. l-3). Variability in concentration of
P was, however, much greater (C.V., 194%)
than in concentrations of N (C.V., 69%) and
C (C.V., 30%). A similar gradation in variability, from highest for P concentration to
lowest for C concentration and intermediate
for N concentration, was observed when data
for different groups of aquatic plants were
examined separately (Figs. l-3).
Nutrient concentrations differed significantly across plant groups (ANOVA, P <

(+ SD);

0.00 1; Figs. l-3). Among-group differences

were smallest for C concentrations, which
were normally distributed within groups
(Fig. 1). Macroalgae were characterized by
lower concentrations of C than angiosperms
(Fig. l), and phytoplankton
showed a
broader range of C concentrations (Fig. l),
some algae (mostly diatoms) having low and
others (mostly dinoflagellates and green algae) having high concentrations of C (ANOVA, P < 0.00 1). These differences in C concentration among, and probably within,
aquatic plant groups are probably attributable to differences in the importance of
structural C relative to that associated with
metabolic compounds. The high C content
of aquatic angiosperms probably results
from their relatively high contents of lignin
and cellulose (e.g. Hutchinson 1975; Dawes
et al. 1987) and the high C content of dinoflagellates may be attributable, in turn, to
the external cellulose plates present in many
of them (Taylor 1987).
Macrophytes were also characterized by
low concentrations of N relative to those of
phytoplankton
(Fig. 2; ANOVA,
P <
O.OOOl), which showed a bimodal distri-

Notes

884
70

70

60

60

50

50

40

40

30

30

-g

20

20

10

10

a%

O 0.2

1.2

2.2

3.2

4.2

5.2

6.2

7.2

6.2

9.2 10.2

' 0.2

1.2

2.2

3.2

4.2

6.2

5.2

7.2

9.2 10.2

8.2

16
14

30

12

angiosperms

25

10

R = 1.0 - 4.3
m = 2.4kO.7
n =104

20

8
6
4
2
0

0.2

1.2

2.2

3.2

4.2

5.2

6.2

7.2

8.2

9.2 10

.2

1.2

2.2

3.2

4.2

5.2

6.2

7.2

8.2

9.2 10.:

Nitrogen content (% dry wt )

Fig. 2. As Fig. 1, but of N content.

bution of N concentrations (Fig. 2), diatoms

having low N contents and green algae
showing a tendency toward high N contents
(ANOVA, P < 0.001). The skewed distri-

bution of N concentrations in macrophyte

tissues (Fig. 2), which corresponded largely
to field populations, indicates that many
natural populations
of macroalgae have
70,

I
Seagrass
R = 0.06 - 0.78
m = 0.24a0.13
n =141

6050 40 30.-

20-

xL

20

%
g

lo0

0.2

0.4

0.6

0.8

1 .01.21.41.61.82.0

OL0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

Phosphorus content (% dry wt )

Fig. 3. As Fig. 1, but of P content.

Notes

885

Table 1. Regression equations (Y = aX) describing relationships between nutrient concentration (as % dry
wt) and nutrient ratios (by atoms) in aquatic plants. Also shown, coefficient of determination (R*), standard
error of the slope (SE,), probability level (I), and number of observation pairs in the regression equation, IV.
Plant type

C:N

C:P

N:P

C:P

C:N

Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall
Freshwater angiosperms
Macroalgae
Phytoplankton
Seagrasses
Overall

1.52
1.32
1.07
1.45
1.39
1.57
1.40
1.55
1.50
1.62
- 1.23
- 1.23
-0.59
-0.86
-1.10
1.59
1.38
1.14
1.52
1.46
2.02
1.80
1.97
1.89
2.05
0.91
1.oo
1.11
-1.10
1.03
0.49
0.06
0.18
0.19
0.15

concentrations of N below the critical concentration for maximum macroalgal growth

(N 1.5% dry wt; Fujita et al. 1989), although
nutrient concentrations in macrophyte tissues may reach values comparable to those
observed for phytoplankton
(Fig. 2).
The concentration of P of macrophyte tissues also showed a skewed distribution and
tended to be lower than that for phytoplankton (Fig. 3; ANOVA, P < 0.001). The P
concentrations of macrophytes, particularly
macroalgae, were often well below the critical level for maximum growth (0.13% dry
wt for angiosperms, Gerloff and Krombholz
1966), suggesting that macrophyte growth
may often be P limited in nature. The P
content of phytoplankton
differed among

0.12
0.22
0.64
0.21
0.24
-0.03
0.03
0.28
-0.02
0.18
1.65
0.60
0.58
0.67
1.07
-0.87
-0.76
-0.36
-0.78
-0.75
-1.03
-1.00
-0.73
-1.05
-0.82
-0.72
-0.62
-0.57
1.07
-0.57
0.30
0.39
0.34
0.43
0.39

0.02
0.10
0.40
0.08
0.18
0.02
0.00
0.10
0.00
0.26
0.45
0.24
0.23
0.25
0.46
0.58
0.58
0.15
0.55
0.70
0.98
0.64
0.37
0.68
0.88
0.85
0.40
0.34
0.46
0.62
0.52
0.38
0.45
0.48
0.47

SE,

0.07
0.03
0.08
0.05
0.02
0.01
0.06
0.10
0.05
0.01
0.21
0.10
0.12
0.10
0.06
0.07
0.04
0.09
0.05
0.02
0.02
0.07
0.13
0.06
0.01
0.03
0.07
0.09
0.06
0.02
0.03
0.04
0.03
0.04
0.02

0.08
<O.OOl
<O.OOl
<O.OOl
<O.OOl
0.1
0.60
0.015
0.70
<O.OOl
co.00 1
<O.OOl
<O.OOl
<O.OOl
co.00 1
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
<O.OOl
co.00 1
<O.OOl
<O.OOl
co.00 1

104
298
85
197
684
72
125
52
123
370
72
125
69
135
399
104
298
85
197
684
72
125
52
123
370
72
125
69
104
416
72
127
103
116
416

algal groups, green algae having the highest

contents and blue-greens the lowest (ANOVA, P < 0.001).
Examination of the central tendency (as
described by the average C concentration,
and geometric mean N and P concentrations) of the C: N: P ratios of different
aquatic plant groups showed phytoplankton
to have tissues enriched in N and P relative
to C (median phytoplankton C : N : P = 110 :
16 : l), in proportions remarkably close to
the Redfield ratio (106 : 16 : 1, Redfield et
al. 1963) characteristic of oceanic seston and
phytoplankton
growing at maximal rates
(Goldman et al. 1979; Goldman 1980). In
contrast, freshwater and marine angiosperms exhibited C : N : P ratios indicative

Notes

886

3
.

.
3

.k %'. .

0.5
1
0.01

r
0.05

0.1

0.5

1.0

I
5.0

Phosphorus content (% dry wt )

r,

I,,
0.5

(,,,,,,,,,,,,
1

10

Nitrogen content (% dry wt )

I
0.01

I
0.02

0.05

0.1

0.5

1.0

2.0

Phosphorus content (% dry wt )

Fig. 4. Relationships between concentration of C

and concentrations of N and P and between concentrations of N and P in aquatic plants.

of depletion in N and, particularly, P relative to C compared to phytoplankton (500 :

24 : 1 and 435 : 20 : 1, respectively; cf. Atkinson and Smith 1984; Duarte 1990). The
extent of P and N depletion was even greater
for macroalgae, as reflected in their high
C : N : P ratio (i.e. 800 : 49 : l), which was
even greater than that reported on the basis

of a more limited data set by Atkinson and

Smith (1984).
The hypothesis that the concentrations of
N and P in aquatic plants should be closely
associated was supported by the finding of
a significant positive correlation between the
concentrations of these elements (Pearson
correlation coefficient, rNmp = 0.67, P <
0.00 1; Table 1; Fig. 4). The relationship between N and P concentrations (Fig. 4) was
linear (H,: slope = 1.O; t-test, P > 0. lo),
indicating that N and P tend to be present
at a ratio of - 12, by weight, in the tissues
of aquatic plants. Moreover, the relationship between N and P concentrations described here (Table 1) is similar, both in
slope and intercept, to the relationship described for a mixture of largely terrestrial
plants (Garten 1976), indicating that it may
reflect a fundamental characteristic of the
plant kingdom.
The relationships of N and P to C concentration were, however, weak (rCsN= 0.43;
rc+ = 0.5 1, P < 0.00 1; Fig. 4) and not statistically significant for some plant groups
(Table 1). Regression analyses showed the
C concentration of aquatic plants to change,
on the average, as the ?$ power of their N
and P concentrations
(Table 1). Phytoplankton, however, showed a faster rate of
increase in C concentration with increasing
N than other aquatic plants (Table l), suggesting a closer coupling between the metabolism of C and N.
The significant correlations between the
concentrations of nutrients in aquatic plants
described here probably reflect their close
association in the basic biochemical processes of the plants, which are similar across
plant groups (Garten 1976). The weaker relationships found between N and C and P
and C concentrations (Fig. 4), compared to
the strong, linear relationship between the
concentrations of N and P (Fig. 4; Table l),
probably reflect the important structural role
of C, which uncouples it from metabolicrelated variation in the concentrations of N
and P. Moreover, N and P are closely associated in plant biochemistry, particularly
through protein synthesis. Thus, plants with
high N but low P concentrations, or vice
versa, should not be able to produce the
proteins, ATP, ADP, NADP, and nucleic

Notes

887
n

Seagrass

1
Phosphorus content (% dry wt )

0.2

I,

10

Nitrogen content (% dry wt )

Fig. 5. Relationships
of P in aquatic plants.

between C : N ratio and concentration

acids necessary for rapid growth. The close

association between the concentrations of
N and P may also explain their close association in growth regulation, as reflected
in the significant interaction between N and
P detected in most experimental enrichment experiments of phytoplankton (e.g. Elser et al. 1990), macroalgae (e.g. Lapointe
and OConnell 1989), and angiosperms (e.g.
Perez et al. 199 1).
Aquatic ecologists often scale the N and
P contents of aquatic plants to their C concentration (i.e. C : N and C : P ratios), and
use the N : P atomic ratio to infer the relative importance of N and P as potential limiting factors for plant growth. However, since

of N and between C : P ratio and concentration

variability
in N and P concentrations
is
much greater than that in C concentration
(Figs. l-3), the variability in C : N and C : P
ratios should be dominated by variability
in the N and P concentrations of the plants,
respectively (Duarte 1990). Thus, C : N and
C : P ratios are expected to show inverse relationships to the concentrations of N and
P, respectively. The existence of strong relationships between the C : N ratio and N
concentration and between the C : P ratio
and P concentration of aquatic plants was
confirmed by the analyses (Fig. 5; Table 1).
However, the relationships obtained (Table
1) deviated significantly (t-test, P < 0.01)
from the inverse relationship postulated (i.e.

Notes

888
60 ------0
.-

50-

Phytoplankton

Macroalgae
Freshw. angiosperms
.._ Seagrasses

10

Nitrogen concentration

12

14

16

(9 dry wt )

4000
.-0
3

3000

.-si

2000

1000

--iiPhosphorus

concentration

(% dry wt )

Fig. 6. Arithmetic relationships between C : N and

C : P ratios and N and P concentrations, respectively,
of aquatic plants. The lines represent regressions fitted
for each plant group (Table 1) and the arrows indicate
the approximate
nutrient concentration
at which
C : nutrient ratios become stable against further increments in nutrient concentration (i.e. the asymptotic
C : nutrient ratio).

C : nutrient = nutrient-l),
because the decrease in C : N and C : P ratios with increasing N and P concentrations, respectively,
was slower than expected (i.e. C : nutrient
M nutrient-0.75; Table 1). The observed deviation from the expected inverse relationship is attributable to the tendency of C concentration to increase with increasing N and
P concentrations (Fig. 4).
The relationship between C : nutrient ratios and nutrient concentrations
differed
among plant groups (ANCOVA, P < 0.00 1;
Fig. 5). Aquatic angiosperms had greater
C : N ratios than nonvascular aquatic plants
with similar concentrations of N (t-test, P
< 0.0 1; Fig. 5; Table l), and the rate of
decline in C : N ratio with increasing N con-

centration was much smaller for phytoplankton than for macrophytes (t-test, P <
0.0 1; Fig. 5; Table 1). Similarly, freshwater
angiosperms tended to have greater C : P ratios than other plants with similar P concentrations (t-test, P < 0.01; Fig. 5; Table
l), and the rate of decline in C : P ratio with
increasing concentration of P was also much
smaller for phytoplankton
than for macrophytes (t-test, P < 0.01; Fig. 5; Table 1).
Despite these differences, the relationships
described reflected a common pattern of
change (Fig. 5), involving a steep decline in
C : N and C : P ratios as N and P concentrations in the plant tissues increased to = 4%
dry wt N and 0.3% dry wt P, respectivelyC : N and C : P ratios remaining relatively
constant at ~9 and 200 (by atoms) against
further increments in nutrient concentrations (Fig. 6).
The close association between the concentrations of N and P (Fig. 4; Table 1) also
involves a tendency of plants with tissues
depleted in N relative to C to have tissues
depleted in P relative to C (i.e. a positive
relationship between C : N and C : P ratios;
Table 1). Similarly, the concentration of N
relative to that of P (i.e. N : P ratio) is closely
associated to the P concentration
of the
plants, as reflected in the tendency for the
N : P ratio to decrease as the - l/2 power of
the P concentration (Table 1).
The results presented demonstrate the existence of strong patterns in the nutrient
concentration of aquatic plants, despite significant differences in nutrient concentrations across aquatic plant groups. Phytoplankton tended to be enriched in N and P
relative to C compared to macrophytes, particularly macroalgae, which often showed
nutrient, particularly P, concentrations below the critical concentration for maximum
growth (Figs. 2-3), suggesting that natural
macrophyte communities often experience
P and N limitation of growth. Because most
phytoplankton
populations examined here
were grown in the laboratory, their high nutrient concentrations are not conclusive as
to the extent of nutrient limitation in nature.
However, the chemical composition
of
many natural plankton communities is similar to that found here (i.e. the Redfield ra-

Notes

889

trient availability, and the concept of relative

growth rate in marine phytoplankton ecology, p.
179-194. In Primary productivity in the sea.
Brookhaven Symp. Biol. 3 1. Plenum.
J.J. MCCARTHY, AND D. G. PEAVEY. 1979.
Carlos M. Duarte -,
Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature
Centro de Estudios Avanzados de Blanes
279: 210-215.
Camino de Santa Bkrbara
HECKY, R. E., AND P. KILHAM. 1988. Nutrient lim17300 Blanes, Gerona, Spain
itation of phytoplankton in freshwater and marine
environments: A review of recent evidence on the
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