Estuarine, Coastal and Shelf Science (1999) 48, 589–598
Article No. ecss.1999.0468, available online at http://www.idealibrary.com on
Phytoplankton Nitrogen Nutrition in the Western
Indian Ocean: Ecophysiological Adaptations of Neritic
and Oceanic Assemblages to Ammonium Supply
S. Mengesha, F. Dehairs, M. Elskens and L. Goeyensa
Laboratorium voor Analytische Chemie, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium
Received 2 October 1997 and accepted in revised form 18 January 1999
The nitrogen nutrition of the phytoplankton community in the neritic and oceanic waters of the western Indian Ocean
was investigated during the south-east monsoon (June–July) and intermonsoon periods (November–December). The
region is very oligotrophic, characterized by very low nutrient concentrations (surface NO3 <0·5 ìM), low phytoplankton
biomass (PON 0·85 ìmol l 1) and predominance of regenerated production (maximum f-ratio <0·47). Ammonium
was the major nitrogen substrate during the two seasons, supplying 53–99% of the phytoplankton’s nitrogen requirement.
Nevertheless, both the uptake of nitrate and its relative contribution to total nitrogen removal (f-ratio) were significantly
higher during the intermonsoon period than during the south-east monsoon period. While nutrient concentrations and
nitrate uptake rates varied little, ammonium uptake and regeneration rates as well as f-ratio values showed significant
spatial variability (i.e. between neritic and oceanic regions), which reflected the difference in the plankton assemblage and
its ecophysiology. The oceanic assemblage exhibited higher ammonium uptake capacity, tuned to the activity of an
efficient regenerating community that supplied about 68% of the daily nitrogen requirement of the phytoplankton.
Analysis of ammonium uptake in relation to seasonal changes in ammonium availability showed that the neritic and
oceanic assemblages had different uptake responses. While the ammonium uptake rates of the neritic assemblage varied
according to the ambient ammonium availability, the oceanic assemblage maintained a relatively high specific ammonium
uptake rate throughout the two seasons despite large variations in ammonium availability. Maintaining a relatively high
ammonium uptake rate in the oceanic stations is interpreted as a physiological adaptation to ammonium supply.
1999 Academic Press
Keywords: nitrogen uptake; ammonium; f-ratio, ecophysiological adaptations; monsoon; western Indian Ocean
Introduction
The seasonal migration of the Inter-Tropical
Convergence Zone (ITCZ) in the Indian Ocean leads
to two alternating cycles of monsoons: the southeast (SE) and north-east (NE) monsoons. These
monsoonal cycles cause a seasonal reversal of the
surface water circulation pattern. During the SE
monsoon (May–September) the westward-flowing
Southern Equatorial Current approaches the African
continent, splits and eventually forms the northwardmoving East African Coastal Current (EACC) and
the southward-moving Mozambique current. The
EACC, with an average velocity of >1 m s 1, causes
upwelling along the Somalia coast. During the NE
monsoon (November–March) the wind starts to blow
from the north-east leading to the weakening of the
EACC and the formation of the Somalia Current.
This south-westward-flowing Somalia Current pushes
a
To whom correspondence should be addressed. Tel: +32 2 629
3264; fax: +32 2 629 3274. E-mail: [email protected]
0272–7714/99/050589+10 $30.00/0
the EACC down to 3S, veers eastward and then
merges with the remaining EACC to feed the
Equatorial Counter Current [Figure 1(a)] (Düng
et al., 1980; McClanahan, 1988; Swallow et al., 1991;
Burkill et al., 1993).
Strong seasonal and spatial variability in primary
production characterizes the north-western Indian
Ocean. Regarding nitrogen cycling, the region is
diverse consisting of different biogeochemical
provinces (Burkill et al., 1993; Owens et al., 1993).
For example, high primary production (up to
1·8 g C m 2 day 1) and enhanced export of organic
matter to the deep ocean ( f-ratio up to 0·92) are
reported to occur during the SE monsoon along the
Somalia coast and the south-eastern Arabian Sea due
to increased nutrient availability through deep mixing
(Smith & Codispoti, 1980; Nair et al., 1989; Owens
et al., 1993). The region immediately south of the
Somalia upwelling zone and the northern central
part of the Indian Ocean exhibit very low primary
production (0·3 g C m 2 day 1), however, with a
1999 Academic Press
590 S. Mengesha et al.
40°
50°
(a)
r
a Rive
Tan
f
lf o
Somalia
(b)
n
e
Ad
hi
op
(532)
7)
(52
132
127
128 130 131 133
(531) (533)
(528)
an
ny
Ke oast
C
So
m
ali
a
Et
10°
ia
Gu
200 m
121
ia
120
123 126
137
135 136
Et
hi
op
Tana
Sabaki River
(511)
111 115
117
(517)
108114 116
(508)
Ta
nz
an
ia
0°
2°
Lamu Kiwayu
118
119
(518)
(519)
Sabaki
0
100
Indian
Ocean
m
4°
Mombasa
10°
Gazi
101
103
(503)
105
104 (505)
40°
50°
39°
40°
3°
102
106
(506)
107
(507)
Gazi
41°
F 1. (a) Wind and surface water circulation patterns during the south-east (SE) monsoon (May–September) and
north-east (NE) monsoon (November–March) in the western Indian Ocean. Wind SE monsoon (– – – ), surface current SE
monsoon (— ), wind NE monsoon (==⇒) and surface current NE monsoon (— – –
) (adapted from McClanahan,
1988). (b) The positions of sampling stations during the SE monsoon (June–July, 1992) and intermonsoon (November–
December, 1992) periods; station numbers in parentheses pertain to the intermonsoon period.
preponderance of regenerated production ( f-ratio
0·12; Smith and Codispoti, 1980; Owens et al.,
1993).
One of the main objectives of the Netherlands
Indian Ocean Programme (NIOP) was to assess the
influence of monsoons on the productivity of the
pelagic ecosystem. As part of this programme, we
studied the nitrogen nutrition of phytoplankton during two cruises in the western Indian Ocean (Kenyan
coast), located south of the Somalia upwelling zone
(Figure 1). The specific objectives were to study the
seasonal (monsoonal) and spatial variations of
nitrogenous nutrients, their uptake rates, and the
ecophysiological adaptations of phytoplankton to
ammonium supply.
Materials and methods
Data were collected during two cruises on board RV
Tyro in the western Indian Ocean (Kenyan coastal
area, 2–4·5S, 39–42E) during the SE monsoon
(A1, June–July 1992) and intermonsoon (A2,
November– December 1992) periods [Figure 1(a)].
Although the latter cruise was meant to sample during
the NE monsoon period, the current meter data
indicated a transitional (intermonsoon) period (C.
Heip, pers. comm.). Twenty-four hydrographic
stations were occupied during the first cruise (A1)
along four transects [opposite to Gazi, Sabaki, Tana
and Kiwayu; Figure 1(b)], each with six stations
corresponding to bottom depths of 20, 50, 200, 500,
1000 and 2000 m, respectively. During the second
cruise (A2) only the Gazi, Sabaki and Kiwayu
transects were repeatedly investigated.
Water samples were taken using a CTD rosette
system, equipped with 12 litre ‘ Go-Flo ’ bottles.
Nitrate (NO3) and nitrite (NO2) were measured by
either a TRAACS 800 or Technicon AA II autoanalyser according to the diazotization method
(D’Elia, 1983). Ammonium (NH4) was determined in
duplicate with a Bausch and Lomb spectronic 21 spectrophotometer according to the indophenol blue
method of Koroleff (1969). Particulate matter was
collected on pre-combusted (450 C) Whatman glassfibre filters (GF/F) and analysed for particulate organic
carbon (POC) and nitrogen (PN) with a Carlo Erba
NA 1500 C/N Analyser. Prior to analysis, the filters
were held in a closed Pyrex container saturated with
HCl vapour for 1 h to eliminate the inorganic carbon.
Incubation experiments were done to quantify
nitrogen (NO3, NO2 and NH4) uptake by phytoplankton in the surface layer and NH4 regeneration
Nitrogen uptake in the western Indian Ocean 591
by heterotrophs in the subsurface layer, where NH4
accumulation was observed during the first cruise.
NO2 uptake rates were measured during the intermonsoon period only. For uptake experiments, water
samples were taken at a depth of 10 m, filled in
three 2·7 litre polycarbonate bottles and enriched with
labelled (99% 15N) 15NO3, 15NO2 or 15NH4. After
taking subsamples for the measurement of the
nutrient concentrations (before and after tracer
addition), the samples were incubated in a Plexiglass
on deck incubator with a surface sea water flowing
system. At the end of the incubation period (24 h),
the particulate matter from the uptake experiment
bottle was retained on a GF/F filter, dried and sealed
for later 15N analysis. NH4 production (regeneration)
rates were measured using the isotope dilution
method (Glibert et al., 1982). Water samples, taken
from the subsurface layer (75 m depth in offshore
stations and between 20 and 50 m in shallow
stations), were enriched with 0·05 ìM labelled NH4
(99% 15N) and incubated as above. At the end of the
incubation period, the 15N abundance in NH4 was
determined after recovering NH4 from the seawater
by an extraction technique (Roose, 1990), adapted
from earlier published diffusion methods (Blackburn,
1979; Kristiansen & Paasche, 1989). Also measured
was the original, initial (after 15NH4 addition) and
final NH4 concentrations. The 15N abundance in PN
(uptake experiments) and in NH4 (regeneration experiments) was determined by emission spectroscopy
after conversion of the bound nitrogen into N2
(Fiedler & Proksch, 1975). The 15N abundance was
calculated from the emission intensities of 14N15N
and 14N14N molecules, obtained with a Jasco 15N
Analyser (model NIA-1), and calibrated against
certified standards (Goeyens et al., 1985).
Specific (í, h 1) and absolute (ñ, ìM day 1) uptake rates of NO3, NO2 and NH4 were calculated
according to Dugdale and Wilkerson (1986). Because
nutrient concentrations were often close to the detection limit (0·03 ìM), 0·05 ìM of each labelled
nutrient was added as suggested by Glibert et al.
(1982). This addition occasionally exceeded the conventional (10%) enrichment and might have induced
overestimation of the uptake rates. Assuming saturation uptake kinetics, the uptake rate at ambient
nutrient concentration ñA is a function of the
measured uptake rate (ñT, at enhanced concentration), the ambient (A) and enhanced (T) nutrient
concentrations and the half-saturation constant KN
(Elskens et al., 1997):
ñA =ñT
[A].([T]+KN)
[T].([A]+KN)
Application of this formula demonstrates that the
measured uptake rate, corresponding to a nutrient
concentration which equals the analytical detection
limit and a KN value of 0·1 ìM, amounts to about two
times the real uptake rate. A half-saturation constant
of 0·1 ìM is very plausible for oligotrophic marine
ecosystems (Harrison et al., 1996); moreover, lower
values reduce the overestimation. On the contrary,
extremely low nutrient concentrations (<0·03 ìM)
lead to increased overestimation.
Our NH4 uptake rates are not corrected for isotope dilution and must, therefore, be considered as
minimal estimates. Assuming similar NH4 regeneration rates (ìM day 1) in subsurface (20–50 m) and
surface (10 m) waters, we calculated that underestimation ranges from a factor of 1·5 to 2·5, when using
the model of Glibert et al. (1982).
f-ratios, i.e. the relative contributions of new production to total primary production, were calculated
according to Eppley and Peterson (1979).
Results
Nutrient signature
In general, surface nutrient concentrations were very
low; NO3 ranged from <0·1 (undetectable) to
0·41 ìM, NO2 from 0·07 to 0·1 ìM and NH4 from
0·03 (undetectable) to 0·51 ìM (Table 1). Vertical
profiles indicated that the state of nutrient impoverishment in the surface layer extended to the whole
upper mixed layer (UML) (Figure 2). Although not
evident from Figure 2, the UML was shallower during
the intermonsoon (mean=57 m) period than during
the SE monsoon (mean=85 m). Seasonal variations in
NO3 concentration were small despite seasonal differences in UML depth (Figure 2; Table 1). On the
contrary, surface NH4 concentrations were significantly higher during the SE monsoon than during the
intermonsoon period (Table 1; Figure 2). NO2 profiles showed a subsurface maximum but the depth of
the NO2 maximum was shallower during the intermonsoon (75 m) than during the SE monsoon
period (100 m; Figure 2). This is concurrent with
the shoaling of the UML during the second cruise.
On the whole, NH4 was the major inorganic nitrogenous nutrient during the two sampling seasons,
representing on average 72% of the total DIN concentrations, followed by NO3 (21% ) and NO2 (7%).
Spatially, variations of nutrient concentrations
between the neritic stations (bottom depth <200 m)
and oceanic stations (>200 m) were small. However,
slightly higher concentrations were observed in very
shallow stations (e.g. station 127, NO3 =0·41 ìM)
592 S. Mengesha et al.
T 1. Mean surface concentrations (0–25 m) of nutrients and particulate organic matter during
the intermonsoon (November–December 1992) and SE monsoon (June–July 1993) periods; ranges
are given between parentheses; neritic stations: bottom depth <200 m and oceanic stations: bottom
depth >200 m
Monsoon
Region
Intermonsoon
Neritic
NO3
(ìM)
0·03
(0·03–0·12)
SE monsoon
Neritic
0·09
(<0·03–0·41)
Intermonsoon Oceanic
0·04
(<0·03–0·13)
SE monsoon Oceanic
0·05
(0·03–0·15)
Intermonsoon
All
0·03
(<0·03–0·13)
SE monsoon
All
0·06
(<0·03–0·41)
(a)
22
0
23
Density (kg m–3)
24
25
NO2
(ìM)
<0·03
(<0·03–0·06)
0·03
(<0·03–0·07)
<0·03
0·12
(0·07–0·21)
0·24
(0·03–0·51)
0·08
(<0·03–0·14)
<0·03
0·21
(0·06–0·45)
<0·03
0·10
(<0·03–0·06) (<0·03–0·21)
<0·03
0·22
(<0·03–0·07) (0·03–0·51)
(b)
26
0
27
Depth (m)
100
150
250
250
Nitrite concentration (µM)
0.05
0.1
0.15
(d)
0.2
0
1·08
(0·33–0·78)
1·19
(0·49–2·15)
0·56
(0·60–1·30)
0·50
(0·33–0·66)
0·75
(0·60–1·30)
0·82
(0·33–2·15)
Nitrate concentration (µM)
5
10
15
20
Ammonium concentration (µM)
0.05
0.1
0.15
0.2
50
Depth (m)
50
Depth (m)
9·2
(6·81–12·59)
11·7
(9·09–20·67)
6·1
(5·0–8·66)
6·2
(3·91–6·76)
7·2
(5·00–12·59)
8·7
(3·91–20·67)
150
200
0
PN
(ìmol l 1)
100
200
(c)
POC
(ìmol l 1)
50
50
Depth (m)
NH4
(ìM)
100
150
200
100
150
200
250
250
3
F 2. Vertical profiles of (a) density (óè in kg m ), (b) nitrate concentration (ìM), (c) nitrite concentration (ìM) and
(d) ammonium concentration (ìM) at station 131 (0200S, 4126E) during the SE monsoon (black diamonds) and the
intermonsoon (open circles) periods.
and/or in stations close to the mouth of large rivers
(e.g. station 108, Sabaki river, NO3 =0·21 ìM). In
contrast to our expectation, we found the influence of
large rivers, such as the Sabaki and Tana, on nutrient
distribution to be very small.
Phytoplankton biomass
Phytoplankton biomass was low throughout; POC
concentrations ranged from 3·9 to 20·7 ìmol litre 1
and PN concentrations from 0·3 to 2·2 ìmol litre 1
(Table 1). Seasonal variations were small; for
example, PN concentrations during the SE and
the intermonsoon periods were 0·80·5 and
0·80·3 ìmol litre 1, respectively. Spatially, however, POC and PN concentrations were significantly
higher in the neritic stations than in the oceanic
stations (Table 1). For example, PN concentrations
in the neritic and oceanic stations were, respectively, 1·10·2 and 0·60·2 ìmol litre 1 during
Nitrogen uptake in the western Indian Ocean 593
T 2. Absolute nitrogen uptake rates (ñN) and f-ratio values in surface water (10 m) during the intermonsoon and
SE monsoon periods in the western Indian Ocean: ND=no data; f-ratio =ñNO3/(ñNO3 +ñNH4) and *f-ratio=ñNO3/
(ñNO3 +ñNO2 +ñNH4)
Monsoon
Transect
Region
ñNO3
(ìM day 1)
ñNH4
(ìM day 1)
ñNO2
(ìM day 1)
f-ratio
*f-ratio
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
Intermonsoon
SE Monsoon
SE Monsoon
SE Monsoon
SE Monsoon
SE Monsoon
SE Monsoon
SE Monsoon
Kiwayu
Kiwayu
Kiwayu
Kiwayu
Kiwayu
Sabaki
Sabaki
Sabaki
Sabaki
Sabaki
Gazi
Gazi
Gazi
Gazi
Kiwayu
Kiwayu
Kiwayu
Tana
Sabaki
Sabaki
Sabaki
Neritic
Neritic
Oceanic
Oceanic
Oceanic
Neritic
Neritic
Oceanic
Oceanic
Oceanic
Neritic
Oceanic
Oceanic
Oceanic
Neritic
Neritic
Oceanic
Neritic
Neritic
Neritic
Oceanic
0·0272
0·0366
0·0451
0·0169
0·0483
0·0900
0·0276
0·0178
0·0128
0·0241
0·0397
0·0459
0·0309
0·0166
0·0087
0·0007
0·0015
0·0016
0·0049
0·0001
0·0006
0·0918
0·0423
0·3733
0·0690
0·1926
0·1019
0·0462
0·0755
0·0921
0·1581
0·1053
0·1575
0·0952
0·0670
1·0834
0·4914
0·1597
0·2361
0·1849
0·2395
0·0563
0·0105
0·0275
ND
0·0143
0·0353
0·0650
0·0335
0·0157
0·0100
ND
0·0288
0·0251
ND
0·0193
ND
ND
ND
ND
ND
ND
ND
0·23
0·46
0·11
0·20
0·20
0·47
0·37
0·19
0·12
0·13
0·27
0·23
0·24
0·20
0·01
<0·01
0·01
0·01
0·03
<0·01
0·01
0·21
0·34
ND
0·17
0·18
0·35
0·26
0·16
0·11
ND
0·23
0·20
ND
0·16
ND
ND
ND
ND
ND
ND
ND
Nitrogen uptake and ammonium regeneration rates
Table 2 shows nitrogen uptake rates for the two
sampling periods. NO3 uptake rates (ñNO3) during
the SE monsoon period (0·0030·003 ìM day 1)
were an order of magnitude less than during the
intermonsoon period (0·0340·020 ìM day 1). On
the contrary, NH4 uptake rates during the two monsoon periods (barring very shallow stations such as
127 and 128) were rather similar (Table 2). During
both sampling periods the NH4 uptake rates exceeded
the corresponding NO3 uptake rates, a common feature of oligotrophic systems (Smith & Codispoti,
1980; Owens et al., 1993). Spatial variation for NO3
uptake rates was very small (Figure 3). On the contrary, NH4 uptake rates showed large spatial variations
and the variations were particularly more pronounced
during the intermonsoon period (Figure 3; Table 2).
Despite similar ambient NH4 concentrations (Table
1), specific NH4 uptake rates (íNH4) in oceanic
stations were 3·4 times those in neritic regions
(Figure 3).
NH4 regeneration rates at subsurface depths during
the intermonsoon period ranged from 0·04 to
0·36 ìM day 1, (mean=0·11 ìM day 1, Table 3).
On average, NH4 regeneration accounted for 59%
(31–85%) of the total N uptake and for 90%
(74–98%) of the NH4 uptake in the surface layer,
indicating a close coupling between uptake and regeneration processes. Spatially, NH4 regeneration
rates were significantly higher in oceanic stations
(0·20·1 ìM day 1) than in neritic stations
(0·070·02 ìM day 1). Additionally, the relative
contribution of NH4 regeneration to the uptake of
Specific uptake rate
the intermonsoon period and 1·10·6 and
0·50·1 ìmol litre 1 during the SE monsoon.
0.025
0.020
0.015
0.010
0.005
0.000
20
50
1000
500
Station bottom depth (m)
2000
F 3. Specific uptake rates of nitrate (íNO3, clear
columns) and ammonium (íNH4, dark columns) during the
intermonsoon period (November–December, 1992) vs
station bottom depths: neritic stations are characterized by
bottom depths <200 m and oceanic stations by bottom
depths >200 m.
594 S. Mengesha et al.
T 3. Ammonium regeneration rates by heterotrophs at
subsurface-layer depths during the intermonsoon period
1.00
Kiwayu
Kiwayu
Kiwayu
Kiwayu
Kiwayu
Sabaki
Sabaki
Sabaki
Sabaki
Sabaki
Gazi
Neritic
Neritic
Oceanic
Oceanic
Oceanic
Neritic
Neritic
Oceanic
Oceanic
Oceanic
Neritic
20
50
75
75
75
20
50
75
75
75
50
0·087
0·038
0·359
0·066
0·189
0·080
0·042
0·073
0·081
0·141
0·078
Station
Average NH4 regeneration rate
(ìM day 1)
Neritic
Oceanic
All
0·0650·023
0·1510·112
0·1120·092
NH4 as well as total N was higher in oceanic stations
than in neritic stations; for example, the mean
contribution of NH4 regeneration to total N uptake
in oceanic and neritic stations amounted to 68%
(43·2–85·6%) and 43% (31·0–67·0%), respectively
(Tables 2 and 3).
Although NO2 concentrations in surface water were
small (Table 1), its uptake rates were comparable to
those of NO3 (ñNO2 =0·030·02 ìM day 1 and
ñNO3 =0·030·02 ìM day 1; Table 2). NO2 in the
water column can be produced by oxidation of NH4
as well as by reduction of NO3 (McCarthy, 1980). As
far as the sources of nitrogen for primary production
(i.e. new vs regenerated production) are concerned,
these processes occur within the euphotic zone and
hence, represent autochthonous sources. Thus, NO2
uptake was considered as regenerated production.
In general, f-ratio values during the two monsoon
periods were low (<0·01–0·47; Table 2), indicating that the phytoplankton were largely based on
ammonium (regenerated production). Since NO2
uptake data are available only for one cruise, it was
calculated f-ratio values with and without NO2
contribution (Table 2). For comparison of seasonal
variations, f-ratios without the NO2 contribution are
considered. Seasonally, f-ratios were significantly
higher during the intermonsoon period (0·240·12)
than during the SE monsoon (0·010·01; Table 2).
This was mainly due to large seasonal differences in
NO3 uptake rate (Table 2). Spatial variations in f-ratio
f-ratio
0.75
Sampling depth NH4 regeneration rate
Transect Region
(m)
(ìM day 1)
0.50
0.25
0.00
20
50
500
1000
Station bottom depth (m)
2000
F 4. f-ratio vs bottom depth during the intermonsoon
period: neritic stations are characterized by bottom depths
<200 m and oceanic stations by bottom depths >200 m.
were particularly greatest during the intermonsoon
period, when the f-ratio in the neritic stations
(0·360·11) was significantly higher than in the
oceanic stations (0·180·05; Figure 4; Table 2).
Since the phytoplankton in the neritic and oceanic
stations had similar NO3 uptake rates, the large spatial
variation in f-ratio mainly reflects differences in NH4
uptake rate (Figures 3 and 4).
Discussion
Seasonal variation
Both the nutrient distribution and uptake data indicate that the region is very oligotrophic. Very low
nutrient availability persisted throughout the two
seasons (NO3 c0·41 ìM; Table 1) and led the region
to depend largely on regenerated production (f-ratio
c0·47, Tables 2 and 4). The current uptake data
represent rates typical of tropical oligotrophic systems.
For example, results obtained from the Sargasso Sea
amount to ñNO3 =0·031 ìM day 1 and ñNH4 =
0·137 ìM day 1 (Dugdale & Goering, 1967) and to
ñNO3 =0·031 ìM day 1 and ñNH4 =0·232 ìM
day 1 (Glibert & McCarthy, 1984), respectively.
Data from the oligotrophic western Pacific Ocean
(Kanda et al., 1988) agree well with our results too
(ñNH4 =0·096 ìM day 1; Table 4). Moreover, our
data match the earlier obtained results from the oligotrophic northern central Indian Ocean (Owens et al.,
1993). The oligotrophic conditions in our study area
and in the northern central Indian Ocean contrast
with the seasonally very productive provinces of the
Indian Ocean (e.g. the Somalia upwelling or southeastern Arabian Sea) and this further corroborates the
spatially heterogeneous nature of the Indian Ocean in
terms of nitrogen dynamics (Burkill et al., 1993;
Owens et al., 1993).
Our results show significant seasonal variations.
During the SE monsoon wind stress was stronger
Nitrogen uptake in the western Indian Ocean 595
T 4. Summary (mean values and standard deviations) of nitrogen uptake rates and f-ratios in the surface water of the
western Indian Ocean
Monsoon
íNO3
íNH4
íNO2
ñNO3
Region (10 3 h 1) (10 3 h 1) (10 3 h 1) (ìM day 1)
Intermonsoon
SE monsoon
Intermonsoon
SE monsoon
Intermonsoon
SE monsoon
Neritic
Neritic
Oceanic
Oceanic
All
All
1·70·8
0·10·1
2·10·7
0·10
2·00·7
0·10·1
3·01·1
16·411·9
10·25·1
10·84·1
7·65·4
14·09·2
1·30·7
ND
1·60·4
ND
1·50·6
ND
0·0440·026
0·0040·004
0·0290·014
0·0010·001
0·0340·020
0·0030·003
ñNH4
(ìM day 1)
ñNO2
(ìM day 1)
f-ratio
0·0770·031 0·0330·020 0·360·11
0·4990·412
ND
0·010·01
0·1420·098 0·0200·0009 0·180·05
0·1520·092
ND
0·010·01
0·11990·085 0·0260·016 0·240·12
0·3500·349
ND
0·010·01
ND=no data.
(hence deeper UML), NH4 concentrations were significantly higher, NO3 uptake rates were lower by an
order of magnitude and inherently, f-ratio values were
significantly lower than during the intermonsoon
period (Tables 1 and 4). Stability of the water column
is very important for the phytoplankton to adapt to a
particular light and nutrient regime (Vincent, 1992).
Moreover, adaptation to light is particularly important
to NO3 as its uptake rate is light dependent. Despite
slightly higher NO3 concentrations during the SE
monsoon, NO3 uptake rates and f-ratio values were
extremely low (mean ñNO3 =0·003 ìM day 1 and
f-ratio=0·01; Table 4).
Three factors are likely to have contributed. First,
the increase in ambient NH4 concentration during
this period (Table 1; Figure 2) might have suppressed
the NO3 uptake rate. Although direct kinetic evidence
is lacking, inhibition by NH4 is likely considering the
prevailing nutrient regime and the type of phytoplankton assemblage. Phytoplankton cells in tropical
oligotrophic oceans are often very small in size
(nano- and pico-sized cells), ambient water temperature is high and nutrients are scarce (for example, the
concentrations of NO3 and NH4 were <0·6 ìM).
These conditions led to high NH4 affinity (low Ks),
which enhances the inhibition of NO3 uptake by
NH4 at low ambient concentrations (Wheeler &
Kokkinakis, 1990; Parker, 1993). This has also been
documented by Harrison et al. (1996), who showed
that, over the whole range of nitrogen concentrations,
NH4 is utilized preferentially over NO3 and that the
inhibition of NO3 uptake by NH4 can occur at
nanomolar level of NH4. In certain cases the effect of
inhibition can be of considerable importance. Elskens
et al. (1997) estimated that inhibition of NO3 uptake
in a mesotrophic environment of the north-eastern
Atlantic Ocean increased from 8 to 50% for ambient
NH4 concentrations ranging from <0·05 to 0·56 ìM.
Second, the phytoplankton community was largely
dominated by picophytoplankton (Kromkamp et al.,
1997). Small cells exhibit greater preference for NH4
(Owens et al., 1991) and attain higher growth rates
than large cells (Stolte, 1996). For example, Owens
et al. (1993) reported that over 75% of the total
nitrogen assimilation in the oligotrophic northern
central Indian Ocean was due to the <5 ìm size
fraction.
Third, an unfavourable light regime (due to
reduced water column stability) during the SE
monsoon period, coupled with a significant increase in
the preferred nitrogen source might have contributed
to the diminished contribution of NO3 and greater
importance of NH4. According to Dortch (1990)
both the phytoplankton preference for NH4 and its
inhibitory effect on NO3 uptake rate become greater
at low light conditions. Therefore, in such a nutrientimpoverished ecosystem the preferential assimilation
and the greater importance of NH4 is not surprising
given the fact that NH4 is frequently available, locally
produced and energetically profitable (Syrett, 1981).
Although the region was extremely oligotrophic and
was characterized by the predominance of regenerated
production, a localized bloom of N2 fixing cyanobacteria (Trichodesmium sp.) was observed during the
intermonsoon period (Kromkamp et al., 1997). The
bloom of this phytoplankter, which depends on
allochthonous nitrogen supply (i.e. atmospheric nitrogen), results in greater new production or f-ratios
exceeding the ones based on NO3 and NH4 uptake
rates. As this species entirely depends on atmospheric
nitrogen, increased stability of the water column
must have been the most important environmental
factor that led to the bloom condition (Carpenter &
McCarthy, 1975).
Spatial variation
Oceanic and neritic regions showed marked differences in NH4 uptake rate, NH4 regeneration rate and
f-ratio (Figures 3 and 4; Table 4). These variations
596 S. Mengesha et al.
were most pronounced during the intermonsoon
period. Note that, while nutrient concentrations and
NO3 uptake rates were similar in the oceanic and
neritic regions, the NH4 uptake capacity (i.e. the
specific NH4 uptake rate) was selectively enhanced
and its rate closely coupled with regenerative processes only in the oceanic region (Figure 3; Table 1).
For example, in oceanic stations, íNH4 was about
3·4 times greater and the regeneration rates were
about 2·3 times greater than in the neritic stations.
Laboratory experiments have shown that cells reduce
their NO3 uptake rate and enhance their NH4 uptake
capacity when they become nitrogen deficient (Dortch
et al., 1982). If cells were nitrogen deficient, enhanced
NH4 uptake rates would be expected in the oceanic as
well as the neritic regions since both regions had very
low ambient NO3 and NH4 concentrations (Table 1).
Therefore, nitrogen deficiency was not the main factor
for the spatial variation in NH4 uptake rates.
Variation in the relative proportion of detrital nitrogen in PN between the neritic and oceanic regions can
also lead to differences in specific uptake rates, as íN
is the quotient of the absolute uptake rate ñN divided
by PN (Dugdale & Wilkerson, 1991). Since detrital
nitrogen underestimates both the NO3 and NH4
specific uptake rates in a similar way, the effect
cancels out when the quotient of ammonium to
nitrate uptake rate (íNH4/íNO3) is taken. Thus,
the large difference in uptake ratio between neritic
(íNH4/íNO3 =2·00·9) and oceanic stations (íNH4/
íNO3 =5·01·9) precludes detrital nitrogen as a
possible factor. On the contary, the above-mentioned
differences between the two regions reflect the difference in plankton assemblage and their ecophysiology.
A high NH4 uptake capacity coupled with an efficient
regenerating community characterized the oceanic
assemblage.
Although NH4 was the predominant nitrogen
source both in the oceanic and neritic regions, the
uptake responses of the oceanic and neritic assemblages to seasonal variations in ambient NH4 availability were markedly different. Both in the neritic and
oceanic regions the transition from the intermonsoon
to the SE monsoon period was accompanied by a
significant increase in NH4 concentration (Table 1).
In neritic stations this seasonal increase in NH4 concentration was accompanied by a significant increase
in NH4 uptake rate (0·003 h 1 cíNH4 c0·017 h 1;
Table 4). In contrast herewith, NH4 uptake rates in
oceanic stations were already high and despite
elevated increase in NH4 concentration, íNH4
remained rather constant (0·0102 h 1cíNH4c
0·0108 h 1; Table 4). Thus, while the NH4 uptake
rate of the neritic assemblage varied according to the
ambient NH4 availability, the oceanic assemblage
maintained a relatively high uptake rate all the time
and assimilated NH4 irrespective of its availability.
Recall that the oceanic assemblage had also high NH4
supply (regeneration) that almost balanced (87·9–
98·1%) NH4 consumption by autotrophs (Tables 2
and 3). Apparently, in oceanic stations, high NH4
uptake and regeneration rates under low ambient
NH4 concentrations indicate a state of dynamic equilibrium between NH4 uptake and supply. Thus, the
high NH4 uptake rate in the oceanic stations appears
to be an uptake response to high NH4 supply by
heterotrophs and this represents an ecophysiological
adaptation to NH4 supply. By maintaining high NH4
uptake rates the opportunistic oceanic assemblage
could exploit temporally short events of high NH4
concentration. This has been described in other similar oligotrophic tropical oceanic systems (Glibert
& Goldman, 1981; Jackson, 1980; Dortch et al., 1982;
Glibert & McCarthy, 1984). However, our results
demonstrate the presence of different uptake
responses and physiological adaptations of two assemblages residing in adjacent coastal and oceanic ecosystems that had similar nutrient levels but different
sources of supply.
NH4 in the neritic region is supplied by rivers and
sediments as well as by bacterial regeneration and
zooplankton excretion. In the oceanic region the latter
processes are the major sources. Thus, the time and
space scales over which high NH4 levels persist in the
system, as well as the frequency of exposure to high
NH4 supply, are very different in the oceanic and
neritic regions. Therefore, for the neritic phytoplankton assemblage, it is of little physiological advantage to maintain high NH4 uptake rates in an area
where a relatively high NH4 concentration can persist
over a large area, for example after increased river
discharge. In contrast, in oceanic stations, due to
the random nature of NH4 supply by zooplankton
excretion and bacterial regeneration, the phytoplankton assemblage had developed a high NH4
uptake strategy that suits the irregular frequency of
supply and patchy distribution pattern of NH4 in
the environment. Results suggest that, despite a similar degree of oligotrophy and the overwhelming
importance of NH4 as a nitrogen source, the physiological uptake adaptations of phytoplankton to the
mode of NH4 supply were different in the oceanic and
neritic regions.
It is worth mentioning that the more pronounced
spatial differences between the oceanic and neritic
assemblages occurred during the intermonsoon
period. This can be partly explained by differences in
horizontal exchange (advection) between the oceanic
Nitrogen uptake in the western Indian Ocean 597
and neritic waters associated with the seasonal variation of surface circulation pattern during the two
sampling seasons. During the SE monsoon the EACC
is strong and flows towards the coast, thus advecting
the oceanic waters into the neritic region [Figure
1(a)]. This causes more intensive mixing between the
oceanic and neritic species leading to small horizontal
(spatial) variations. In contrast, during the intermonsoon period, both the Somalia Current and the
EACC flow in the opposite direction and the advected
neritic species are diluted in the open ocean. These
lead to a small horizontal exchange between the
oceanic and neritic species and, hence, large spatial
variations in NH4 uptake, regeneration and f-ratio.
Conclusions
The seasonal change in monsoon regime affected the
nitrogen nutrition of phytoplankton. The study area
was very oligotrophic and NH4 was the major nitrogenous nutrient used by phytoplankton throughout
the whole period. Despite the predominance of regenerated (NH4 based) production, new production and
its relative contribution (f-ratio) showed clear seasonal
(monsoonal) variations. The neritic and oceanic
regions exhibited marked differences in NH4 uptake
rate, regeneration rate and f-ratio. This reflects the
difference in plankton assemblage and their
ecophysiological uptake adaptations to NH4 supply.
Acknowledgements
The authors thank the captain and crew members of
the RV Tyro. We are grateful to C. Heip, J. Stel and J.
Kromkamp for inviting us on board as well as for their
kind assistance. We also thank J. Sinke and J. Van
Ooijen for nutrient analyses and J. P. Clement for his
technical assistance. This research was supported by
a grant from the Belgian National Foundation of
Science (Contract No. 2.0083.92) and by The
Netherlands Science Foundation (SOZ). The authors
appreciated the valuable comments of three anonymous reviewers. F. Dehairs is a research associate at
the National Fund for Scientific Research.
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