Journal of Plankton Research Vol.21 no.12 pp.2263–2283, 1999
Microplanktonic respiration off northern Chile during El Niño
1997–1998
Yoanna Eissler and Renato A.Quiñones
Departamento de Oceanografía, Universidad de Concepción, Casilla 160-C,
Concepción, Chile
Abstract. Microplanktonic respiration rates were estimated in waters off the coast of northern Chile
(Antofagasta, 23ºS) during El Niño and pre-El Niño conditions. Three cruises were conducted during
pre-El Niño summer (January/February 1997), El Niño winter (July 1997) and El Niño summer
(January 1998). Oxygen consumption was estimated by the Winkler method using a semi-automatic
photometric end-point detector. The ranges of microplanktonic respiration rates found were
0.11–21.15, 0.03–6.25 and 0.06–9.01 µmol O2 l–1 day–1 during pre-El Niño summer, El Niño winter and
El Niño summer, respectively. Significant differences were found between winter and summer respiration rates (non-integrated and integrated). The mean integrated respiration (mixed layer) for preEl Niño summer, El Niño winter and El Niño summer was 95 ± 51 (SD) mmol O2 m–2 day–1, 50 ± 23
(SD) mmol O2 m–2 day–1 and 63 ± 32 (SD) mmol O2 m–2 day–1, respectively. The strong seasonal signal
detected in microplanktonic integrated respiration in the area seems to be characteristic of the preEl Niño/El Niño 1997–98 period. The integrated respiration rates found off Antofagasta are similar
to reported values for the upwelling area off Peru despite methodological differences. A positive
significant correlation was found between respiration and water temperature (r = 0.76, P ≤ 0.001, preEl Niño summer; r = 0.61, P ≤ 0.001, El Niño winter), as well as between respiration and dissolved
oxygen concentration (r = 0.78, P ≤ 0.001, pre-El Niño summer; r = 0.23, P ≤ 0.02, El Niño winter).
The Humboldt Current System (HCS) presents an extensive oxygen minimum layer composed of
Equatorial Subsurface Water. Our results indicate that oxygen levels lower than 177.3 and 136.0 mmol
O2 m–3 acted as a physical barrier for aerobic respiration during pre- El Niño and El Niño conditions,
respectively.
Introduction
The 1997–1998 El Niño event was one of the strongest of the 20th century and
heavily influenced the coastal zone of the Southeastern Pacific. El Niño events
are characterized by the incoming of Subtropical Surface Water (SSW) from the
equator into the American coasts. The entrance of subtropical warm water is triggered by the propagation of coastal Kelvin waves producing, among other effects,
water column warming and the deepening of the thermocline. The ecosystem
changes due to El Niño generate both negative and positive effects on the marine
biota (e.g. Tomicic, 1985; Arntz and Fahrbach, 1996).
Planktonic respiration is a very significant carbon flux in the pelagic system
and, in many cases, can be even higher than primary production in oceanic and
coastal areas (e.g. Packard et al., 1971; Williams and Purdie, 1991; Williams, 1998).
Respiration is used by living organisms to yield, from the degradation of organic
matter, the energy needed for their survival strategy (Packard et al., 1984). Therefore, the total respiration of a pelagic community is equivalent to the energy
needed to maintain its organized living structure and function (Quiñones, 1994;
Quiñones et al., 1994). In the Southeastern Pacific, planktonic respiration is
a process scarcely documented. Some studies have been conducted in the
Humboldt Current System (HCS) off Peru reporting a high range of planktonic
respiration rates (Pomeroy and Johannes, 1968; Packard, 1969; Packard et al.,
© Oxford University Press 1999
2263
Y.Eissler and R.A.Quiñones
1971; Vinogradov and Shushkina, 1978; Setchell and Packard, 1979; Sorokin and
Kogelschatz, 1979; Hendrikson et al., 1982). However, with the exception of
Pomeroy and Johannes (1968), the previous estimates of in situ oxygen consumption in the HCS are indirect [e.g. the electron transport activity (ETS) technique,
allometric relationships, physiological efficiency]. Furthermore, the oxygen
consumption experiments of Pomeroy and Johannes (1968) were conducted by
concentrating the planktonic community prior to incubation, which may distort
the final estimates (de Souza Lima and Williams, 1978; Williams, 1984). In relation to the HCS off Chile, no information on in situ oxygen consumption of the
water column is available.
The HCS is characterized by the presence of upwelling events and a permanent subsurface minimum oxygen layer (Brandhorst, 1971; Sievers and Silva,
1982; Silva, 1983). The oxygen minimum is associated with the Equatorial Subsurface Water (ESSW) carried by the Gunther Current poleward (Brandhorst, 1971;
Silva, 1983). The ESSW is generally the source of upwelled water playing an
important role in fertilizing the surface layer because of its high nutrient content
(Morales et al., 1996a). The oxygen minimum layer has an upper limit marked by
dissolved oxygen concentrations of ~44.66 mmol O2 m–3 (i.e. 1 ml O2 l–1) reaching depths shallower than 100 m in the coastal zone off northern Chile (Morales
et al., 1996b). Although it is known that the minimum oxygen layer of the HCS
affects the distribution of zooplankton (Longhurst, 1967; Sameoto, 1981) and
anchovy larvae (Morales, 1996b), its effect on carbon fluxes such as aerobic
respiration remains unknown.
Here, we analyze the vertical distribution of microplanktonic community
respiration during three oceanographic cruises carried out off northern Chile
(Antofagasta area, 23°S) with the objective of describing the levels and variation
of community respiration under El Niño conditions.
Method
Three cruises (Table I) were conducted in northern Chile (Antofagasta area;
Figure 1), on board the B/I ‘Abate Molina’, covering pre-El Niño (January/February 1997), El Niño winter (July 1997) and El Niño summer (January 1998). The
term ‘pre-El Niño’ refers to the transition period of the ecosystem towards full
El Niño conditions. It is characterized by physical or biological properties clearly
different from normal conditions according to time series of the zone, despite the
fact that El Niño global indexes do not define the time period as an El Niño event.
In the case of the marine ecosystem off Antofagasta, after a cold period, the sea
surface temperature gradually increased from October 1996 (Escribano and
McLaren, 1998). In January 1997, higher than normal sea surface temperature
and drastic changes in the taxonomic composition of the zooplankton community
were observed (González et al., 1998, 1999). Furthermore, January 1997 was
characterized by an anomalous decrement of the frequency and magnitude of
winds favorable to upwelling in the study area (González et al., 1998).
The term microplankton is used to define all organisms with a nominal size of
<200 µm. A total of 38 experiments were carried out to estimate microplanktonic
2264
Microplanktonic respiration during El Niño 1997–98
Table I. Integrated respiration and P/R ratios for the three cruises conducted in the Antofagasta area.
Primary production data (14C) were extracted from González et al. (1998)
Station Location Sampling
time
January 1997, pre-El Niño
3
C
14:12
10
C
15:48
22
C
02:13
22
C
14:12
24
C
21:32
24
C
14:47
1
C
16:14
27
C
04:20
15
C
22:17
15
C
11:11
15
C
19:08
7
O
23:14
7
O
11:04
19
O
13:57
19
O
03:00
19
O
15:00
Mean ± 1 SD
Minimum–maximum
July 1997, El Niño
3
C
04:16
15
C
20:41
15
C
13:02
15
C
10:14
27
C
11:49
32
C
17:50
32
C
14:42
10
C
22:03
2
C
06:52
7
O
17:54
19
O
10:39
19
O
22:32
19
O
09:38
19
O
18:13
31
O
01:12
200
O
10:49
Mean ± 1 SD
Minimum–maximum
January 1998, El Niño
33
C
09:26
34
C
09:19
35
C
09:42
Mean ± 1 SD
Minimum–maximum
Date
Respiration (mmol O2 m–2 day–1) ± 1 SE
P/R
————————————————————
Mixed
Depth
Oxycline
Depth
layer
(m)
(m)
1/11
1/13
1/15
1/25
1/18
1/20
1/22
1/26
1/28
1/30
1/31
1/12
1/23
1/16
1/25
1/27
66 ± 9
133 ± 14
45 ± 4
18 ± 7
189 ± 8
99 ± 6
125 ± 8
39 ± 7
132 ± 12
182 ± 5
127 ± 16
43 ± 5
72 ± 7
50 ± 10
82 ± 15
115 ± 15
95 ± 51
18–189
16
15
16
14
10
7
15
15
16
12
12
8
12
19
19
19
188 ± 59
251 ± 42
70 ± 26
100 ± 66
250 ± 43
117 ± 42
188 ± 34
114 ± 37
150 ± 18
264 ± 19
279 ± 54
111 ± 44
162 ± 55
95 ± 42
235 ± 37
256 ± 35
177 ± 71
70–279
100
100
60
84
60
60
32
80
44
32
48
96
72
100
100
100
7/1
7/2
7/9
7/10
7/4
7/11
7/12
7/19
7/20
7/1
7/3
7/5
7/6
7/18
7/5
7/16
33 ± 15
27 ± 6
43 ± 11
31 ± 7
58 ± 13
111 ± 8
37 ± 8
30 ± 20
68 ± 28
51 ± 12
25 ± 17
38 ± 14
70 ± 18
68 ± 13
69 ± 13
41 ± 22
50 ± 23
25–111
34
20
16
20
30
28
24
46
32
50
60
54
54
54
48
57
53 ± 30
89 ± 33
67 ± 48
39 ± 29
98 ± 28
147 ± 17
58 ± 17
48 ± 31
99 ± 52
53 ± 16
35 ± 30
46 ± 20
79 ± 39
71 ± 21
85 ± 19
68 ± 43
71 ± 29
35–147
95
78
64
78
84
64
64
92
79
76
100
100
100
88
94
100
1/26
1/27
1/28
66 ± 10
94 ± 15
30 ± 6
63 ± 32
30–94
20
24
8
141 ± 38
198 ± 75
114 ± 46
151 ± 43
114–198
100
88
100
0.2
0.8
1.2
2.4
1.1
3.3
0.7
0.6
0.2
1.2 ± 1.1
0.2–3.3
1.1
3.5
3.9
9.0
1.4
0.9
3.3 ± 3.1
0.9–9.0
P, primary production; R, integrated respiration (mixed layer and base of the oxycline); C, coastal
station; O, oceanic station.
community respiration. Stations were selected in an attempt to cover the broadest area possible within the study zone, and taking into consideration the limitations imposed by the basic track of the multidisciplinary cruises and the capacity
of our team to conduct as many respiration experiments as possible. At each
2265
Y.Eissler and R.A.Quiñones
Fig. 1. Location of the sampling stations during the three cruises conducted in the Antofagasta area,
Chile. d, coastal stations; j, oceanic stations.
station, microplankton samples were obtained from the first 100 m of the water
column using 5 l Niskin bottles.
Temperature, salinity, oxygen and fluorescence profiles were obtained using a
Neil Brown CTD-DO (Model MK3 B) provided with a sensor SEATECH
(Model FL3000). Irradiance was obtained with a Biospherical Irradiance Profiler
(Model QSP200L). The oxygen sensor was calibrated with in situ measurements
of dissolved oxygen (Winkler method; see below).
Six different depths were selected according to the physical structure of the water
column (temperature, salinity and oxygen) and the fluorescence level, covering the
mixed layer, the thermocline and below the main thermocline, when the thermocline was present. If there was no defined thermocline, the fluorescence and oxygen
profiles were used to select the sampling depths. From each sampling depth, 10
water samples were incubated on board in the dark in 125 ml borosilicate glass
bottles. The samples were incubated in two thermoregulated baths (precision
±0.3°C) and one water bath refrigerated with a constant flux of sea surface water.
The temperature of the incubators, and the distribution of the bottles among them,
were arranged to ensure that the samples were always incubated at in situ temperature or at no more than ±1.2°C from the in situ temperature. The samples were first
acclimatized during 30–45 min in the water baths to ensure a homogeneous
temperature at the fixation time (T0). After the acclimatization period, five replicates from each depth were fixed (T0). The remaining bottles (i.e. five replicates
per depth) were incubated during 18–24 h (Tf). Microplanktonic respiration is estimated as the difference in dissolved oxygen between T0 and Tf.
2266
Microplanktonic respiration during El Niño 1997–98
Occasionally, we conducted experiments to test the linear decay of oxygen
during the incubation period. Additional samples were taken from one depth
from the photic zone and 25 bottles were incubated as described above. Five replicates were fixed at 6, 12, 18 and 24 h of incubation. In all experiments conducted
(five), dissolved oxygen declined linearly during the whole incubation period.
Dissolved oxygen measurements were made using a semi-automatic version of
the Winkler method (Williams and Jenkinson, 1982) based on a photometric endpoint detector, a Dosimat 665 (Metrohom) and a chart recorder. The analytical
procedures were conducted as suggested by Knap et al. (1993). The coefficient of
variation of the measurements of dissolved oxygen in laboratory conditions was
0.08%, i.e. similar to that reported by Williams and Jenkinson (1982). The coefficient of variation of the dissolved oxygen estimation under onboard conditions
was, generally, 0.18% for the whole water column and 0.15% for the euphotic
zone. Integrated respiration rates of the mixed layer were calculated using the
trapezoid method.
In order to calculate the gross primary production to community respiration
ratios (P/R), oxygen consumption measurements were transformed into carbon
equivalents, assuming a respiratory quotient (RQ) of 1.0. There is no consensus
about what is the best RQ to use (e.g. 0.7–1.1; Lampert, 1984) and values higher
than those that could be accounted for by the stoichiometry of organic metabolism have been found (Robinson and Williams, 1999). An RQ of 1 has been
commonly used in the literature for microplankton species assemblages (e.g.
Biddanda et al., 1994; Aristegui and Montero, 1995; del Giorgio et al., 1998).
The primary production data available (i.e. González et al., 1998) were vertically
integrated from the surface to the depth corresponding to 2% of incident light at
the surface. Consequently, the respiration rates used to calculate P/R ratios were
vertically integrated to the same depth as the primary production data.
The standard error of the respiration rates was calculated according to Zar
(1996, p. 125), as follows:
SS0 + SSf
s2p = —————
n0 + n f
and
ST0 – Tf =
√
s2p
s2p
—— + ——
nf
n0
(1)
(2)
where s2p is the pooled variance, SS0 and SSf are the sum of squares at T0 and Tf,
n0 and nf are the degrees of freedom at T0 and Tf, n0 and nf are the number of
replicates at T0 and Tf, and ST0 – Tf is the standard error of the difference between
the means at T0 and Tf.
A Spearman rank correlation analysis (Zar, 1996) was used to examine the
association between respiration rates and oceanographic variables (temperature,
salinity, oxygen, fluorescence, irradiance). A Mann–Whitney U-test was conducted to test differences in the respiration rate: (i) of coastal versus oceanic
stations, (ii) of stations located in upwelling versus non-upwelling areas and (iii)
between cruises. The statistical analyses were carried out using STATISTICA®.
2267
Y.Eissler and R.A.Quiñones
Fig. 2. Vertical distribution of microplanktonic respiration during pre-El Niño summer (January/
February 1997) in the Antofagasta area. Each symbol is characterized by station (Sta.) number and
date. Bars indicate SE.
Results
Vertical distribution of microplanktonic respiration
During pre-El Niño summer conditions, the vertical distribution of community
respiration showed a subsurface maximum located between 5 and 30 m deep
(Figure 2). The respiration rates ranged from ≤0.11 (station 15) to 21.15 µmol O2
l–1 day–1 (station 24) with an average value of 3.23 ± 4.44 (SD) µmol O2 l–1 day–1
and quickly diminished below the subsurface maximum (Figure 2).
The subsurface respiration maximum was generally found within the mixed
2268
Microplanktonic respiration during El Niño 1997–98
Fig. 3. Selected examples of vertical profiles of temperature, salinity, oxygen and chlorophyll a during
pre-El Niño summer (January/February 1997) in the Antofagasta area. Each symbol is characterized
by station (Sta.) number and date.
layer, which during the pre-El Niño conditions was always located above 20 m
deep (Figure 3). The shapes of the respiration profiles are usually related to the
position of the oxycline and to the presence of the subsurface chlorophyll
maximum (Figures 2 and 3).
2269
Y.Eissler and R.A.Quiñones
Fig. 4. Vertical distribution of microplanktonic respiration during El Niño winter (July 1997) in the
Antofagasta area. Each symbol is characterized by station (Sta.) number and date. Bars indicate SE.
During the El Niño winter, the vertical distribution of microplanktonic respiration through the water column did not show a conspicuous subsurface
maximum, with the exception of station 32 (Figure 4). Respiration values ranged
from ≤0.03 µmol O2 l–1 day–1 (station 7) to 6.25 µmol O2 l–1 day–1 (station 32) with
an average value of 1.00 ± 1.02 (SD) µmol O2 l–1 day–1 (Figure 4).
The water column mixing was more pronounced during El Niño winter in
comparison to pre-El Niño conditions (Figures 3 and 5). The mixed layer reached
a maximum depth of 60 m (station 19, 3 July) and 20 m (station 19, 25 January)
in El Niño winter and pre-El Niño conditions, respectively. The oxycline was
usually less pronounced in El Niño winter, and the respiration profiles tended to
follow the same trend as the oxygen profile (Figures 4 and 5).
In El Niño summer, respiration values ranged from ≤0.06 to 9.01 µmol O2 l–1
day–1 with an average of 2.78 ± 2.37 (SD) µmol O2 l–1 day–1 (Figures 6 and 7).
The Mann–Whitney test showed that respiration rates were significantly
2270
Microplanktonic respiration during El Niño 1997–98
Fig. 5. Selected examples of vertical profiles of temperature, salinity, oxygen and chlorophyll a during
El Niño winter (July 1997) in the Antofagasta area. Each symbol is characterized by station (Sta.)
number and date.
2271
Y.Eissler and R.A.Quiñones
Fig. 6. Vertical distribution of microplanktonic respiration during El Niño summer (January 1998) in
the Antofagasta area. Each symbol is characterized by station (Sta.) number and date. Bars indicate
SE.
Table II. Correlation analyses between microplanktonic respiration (µmol O2 l–1 day–1) and
oceanographic variables (temperature, salinity, oxygen, chlorophyll and irradiance). Values in bold
are those with P ≤ 0.05
Temperature
(ºC)
Salinity
(p.s.u.)
Oxygen
(µmol O2 l–1)
Chlorophyll
(mg m–3)
Irradiance
(µW cm–2)
Respiration
January/February 1997
r
0.76
n
93
P
(P ≤ 0.001)
–0.07
93
(P ≥ 0.5)
0.78
93
(P ≤ 0.001)
–0.01
93
(P ≥ 0.9)
0.22
54
(P ≥ 0.1)
Respiration
July 1997
r
n
P
0.61
96
(P ≤ 0.001)
0.62
96
(P ≤ 0.001)
0.23
96
(P ≤ 0.02)
0.70
96
(P ≤ 0.001)
0.33
96
(P ≤ 0.01)
Respiration
January 1998
r
n
P
0.77
21
(P ≤ 0.001)
0.75
21
(P ≤ 0.001)
0.26
21
(P ≥ 0.25)
0.19
21
(P ≥ 0.4)
0.86
21
(P ≤ 0.001)
Respiration
Total
r
n
P
0.63
210
(P ≤ 0.001)
0.15
210
(P ≥ 0.29)
0.59
210
(P ≤ 0.001)
0.13
210
(P ≥ 0.05)
0.37
171
(P ≤ 0.001)
r, Spearman correlation coefficient; n, number of observations.
different between El Niño winter and both pre-El Niño summer (P ≤ 0.006) and
El Niño summer (P ≤ 0.008). On the other hand, no significant differences were
detected between respiration rates measured during El Niño summer and pre-El
Niño summer (P ≥ 0.65). The latter is also valid when comparing only the coastal
stations (P ≥ 0.58).
2272
Microplanktonic respiration during El Niño 1997–98
Fig. 7. Selected examples of vertical profiles of temperature, salinity, oxygen and chlorophyll a during
El Niño summer (January 1998) in the Antofagasta area. Each symbol is characterized by station
(Sta.) number and date.
Microplanktonic respiration was positively correlated with temperature both
during El Niño and pre-El Niño conditions (Table II). During El Niño, there was
also a positive correlation between respiration and the variables salinity, chlorophyll and irradiance, which was not observed during pre-El Niño conditions.
Furthermore, a strong correlation was found between respiration and dissolved
oxygen concentration during pre-El Niño conditions, an association which
remained weakly during El Niño conditions (Table II).
The hypoxic zone of the upper portion of the Gunther Current was a clear
physical barrier for aerobic respiration. In pre-El Niño conditions, aerobic respiration was usually not detected at oxygen concentrations below 177.3 mmol O2
m–3 (Figure 8). In contrast, during El Niño winter, the average minimum oxygen
concentration at which respiration was detected was 136 mmol O2 m–3 (Figure 8).
The average depth of low-oxygen waters (44.66 mmol O2 m–3) in the coastal and
offshore zone during pre-El Niño summer was 45 and 89 m, respectively (Figure
9). In contrast, during El Niño winter, a deepening of the low-oxygen waters was
observed (average coastal zone 84 m; average offshore zone 126 m).
2273
Y.Eissler and R.A.Quiñones
Fig. 8. Relationship between the concentration of dissolved oxygen and microplanktonic respiration
rates found during pre-El Niño summer (January/February 1997) and El Niño winter (July 1997). The
vertical line indicates the average level of dissolved oxygen at which respiration was not detectable.
Integrated respiration in the water column
During pre-El Niño summer, integrated respiration values for the mixed layer
ranged from 18 (station 22) to 189 mmol O2 m–2 day–1 (station 24) with an average
of 95 ± 51 (SD) mmol O2 m–2 day–1 (Table I). On the other hand, integrated respiration (mixed layer) values between 30 and 94 mmol O2 m–2 day–1 (Table I) were
observed during El Niño summer. In the course of El Niño winter, the integrated
respiration for the mixed layer ranged from 25 (station 19) to 111 mmol O2 m–2
day–1 (station 32), with an average of 50 ± 23 (SD) mmol O2 m–2 day–1 (Table I).
Significant differences were found between integrated respiration for the
2274
Microplanktonic respiration during El Niño 1997–98
Fig. 9. Vertical distribution of dissolved oxygen (mmol O2 m–3) in a transect from station 15 to station
19 during pre-El Niño summer (January/February 1997) and El Niño winter (July 1997).
whole study area between pre-El Niño summer and El Niño winter (P ≤ 0.01).
Owing to the coastal location of the stations sampled during El Niño summer
(Figure 1; stations 33, 34 and 35), statistical comparisons with El Niño winter and
pre-El Niño summer are not valid for the whole study area.
No significant differences (P ≥ 0.2) were noticed between the integrated respiration (mixed layer) of coastal and oceanic stations during pre-El Niño as well as
during El Niño conditions (P ≥ 0.4) (Figure 10). Similarly, no significant differences were detected when comparing: (i) the integrated respiration rates
2275
Y.Eissler and R.A.Quiñones
Fig. 10. Longitudinal distribution of integrated respiration during the three cruises conducted in the
Antofagasta area (d, January/February 1997; s, July 1997; h, January 1998).
measured in the coastal zone of the study area during pre-El Niño summer (1997)
with those of El Niño summer (1998; P ≥ 0.2), as well as (ii) the integrated respiration rates measured in the coastal zone of the study area during El Niño winter
with those of El Niño summer (P ≥ 0.5).
Similar results were found when the base of the oxycline is used as a criterion
for integrating respiration (Table I).
Upwelling areas
The Antofagasta area is known to be an upwelling zone (Fonseca and Farías,
1987; Fonseca, 1989). The upwelling events take place all year around (Fonseca
and Farías, 1987) and are important in supporting high rates of primary production in the nearshore areas (Rodríguez et al., 1991; Marín et al., 1993). However,
during the El Niño winter, only an extremely weak upwelling located nearshore
was detected in the area (González et al., 1998).
On the other hand, during the pre-El Niño summer, an upwelling zone with a
filament shape was described for the study area (Sobarzo and Figueroa, 1999).
The integrated respiration rates of the mixed layer of those stations located in
(stations 1, 15, 24 and 27; 18–31 January 1997) and out of the upwelling areas were
not significantly different (P ≥ 0.2).
Discussion
Considerable differences in winter and summer respiration rates were observed
in the Antofagasta area under the influence of El Niño. It is important to note
2276
Microplanktonic respiration during El Niño 1997–98
that during non-El Niño conditions the seasonal signal in the Antofagasta area
is distinct in the coastal zone, but is weak offshore. For example, in Mejillones
Bay (23°059S), there are seasonal trends in phytoplankton abundance
(Rodríguez et al., 1986) presenting a certain degree of interannual variability in
the dominance of diatoms or dinoflagellates (Rodríguez et al., 1999). Chlorophyll a and primary production also show a seasonal trend in Mejillones Bay
(Rodríguez et al., 1986) with higher values of chlorophyll a at the end of spring
(8 mg m–3) and summer (24.8 mg m–3), and lower values during the rest of the
year (0.6 mg m–3) (Rodríguez et al., 1991). On the other hand, Rodríguez (1987)
has reported seasonal succession patterns of phytoplankton species in San Jorge
Bay (23°429S).
Offshore, the seasonal signal in the Antofagasta area is weak in comparison to
other zones of the HCS. Morales et al. (1996a) reported that no significant differences were found in the chlorophyll a surface concentration (maximum values
> 10 mg m–3) in the Arica (18°289S) to Antofagasta area between winter (<5 mg
m–2, upper 25 m layer) and spring (highest values 10–20 mg m–3) 1993. However,
integrated chlorophyll a was significantly lower in winter (53 mg m–2, 0–100 m)
than in spring (141 mg m–2, 0–100 m) and copepod density was significantly higher
in winter compared to spring of 1993 (Morales et al., 1996a). Avaria and Muñoz
(1983), studying the offshore area in Northern Chile from Arica to Chañaral
(26°209S), reported similarity in the species composition of phytoplankton
between spring 1980 and autumn 1981, although they noticed changes in the
dominant species between the two seasons. These authors also observed slightly
higher biomass and cell density of phytoplankton during spring in comparison to
autumn. Based on monthly composite satellite images from 1978 to 1986, Thomas
et al. (1994) indicate that along northern Chile (18–30°S) pigment concentrations
of <0.3 mg m–3 persist throughout the year, with slightly higher concentrations in
winter–spring. Thomas et al. (1994) also conclude that interannual pigment variability in northern Chile is low.
On the other hand, González et al. (1998) showed marked differences between
January 1997 and July 1997 in the biomass and taxonomic composition of
zooplankton, as well as in the bacterial biomass and bacterial secondary production in the study area. Our results and those of González et al. (1998) allow us to
infer that the strong seasonal signal detected in the microplanktonic respiration
during this study is a characteristic of the 1997–1998 pre-El Niño/El Niño period.
Furthermore, no significant differences were found when comparing respiration
rates between El Niño summer and pre-El Niño summer, reinforcing the argument that January 1997 had biological characteristics in transition towards El
Niño conditions.
We did not detect any significant differences between the microplanktonic
respiration of the coastal and oceanic stations in any of the cruises, which is probably due to the lack of strong upwelling events during the study period (González
et al., 1998; Sobarzo and Figueroa, 1999). The only upwelling event detected took
place in pre-El Niño summer. It was extremely weak and most of the water
upwelled corresponded to SubAntarctic Waters (SAAW) (Sobarzo and Figueroa,
1999) which have lower fertilizing capacity than ESSW (Torres, 1995). In fact, the
2277
Y.Eissler and R.A.Quiñones
microplanktonic respiration both in and out of this upwelling zone did not show
significant differences.
The integrated respiration rates measured in our investigation are within the
same order of magnitude as those reported for the upwelling area of the HCS
off Peru (Pomeroy and Johannes, 1968; Packard, 1969; Packard et al., 1971;
Vinogradov and Shushkina, 1978; Setchell and Packard, 1979; Sorokin and
Kogelschatz, 1979; Hendrikson et al., 1982) and other upwelling regions such as
the Benguela system (Chapman et al., 1994). It is important to note, however, that
there is high variability in the respiration estimates observed in the HCS off Peru
(27.94–592 mmol O2 m–2 day–1; Packard, 1969; Packard et al., 1971) and in the
Benguela system (69–128 mmol O2 m–2 day–1; Chapman et al., 1994). Methodological considerations render our respiration measurements difficult to compare
with those mentioned above for the HCS off Peru. Packard (1969), Packard et al.
(1971), Setchell and Packard (1979), Hendrikson et al. (1982) and Chapman et al.
(1994) used the ETS which, despite certain controversy regarding the conversion
factors to be used when comparing with oxygen consumption methods (e.g.
Kenner and Ahmed, 1975; King and Packard, 1975; Bamstedt, 1979, 1980;
Packard, 1985; Relexans, 1996), provides an approximation of the in situ oxygen
consumption. On the other hand, based on some empirical measurements of
oxygen consumption, Vinogradov and Shushkina (1978) developed an indirect
allometric method. Sorokin and Kogelschatz (1979) estimated the respiration of
microheterotrophs from microbial production (14C) and an efficiency coefficient
for food assimilation of 0.3. Finally, the oxygen consumption measurements of
Pomeroy and Johannes (1968) were obtained by concentrating the plankton
before incubation, a procedure that distorts the final estimate (de Souza Lima
and Williams, 1978; Williams, 1984). Recently, Daneri et al. (1999) conducted a
series of surface primary production and respiration experiments in the HCS and
adjacent areas using the 14C and oxygen incubation method. The work of Daneri
et al. (1999) is the most comprehensive compilation of estimates of primary production of the HCS to date. However, their respiration estimates are not comparable to ours due to the fact that they represent a single measurement in the water
column. Therefore, until now, our measurements seem to be the most extensive
and reliable direct oxygen consumption estimates available from the HCS.
The positive correlation found between respiration and temperature (Table II)
indicates that community respiration rates increase with water temperature, an
effect observed in other ecosystems (Hopkinson, 1985; Kemp et al., 1992; Robinson and Williams, 1993; Sampou and Kemp, 1994). Consequently, it is likely that
specific respiration rates increased during the whole study period due to the positive sea surface temperature anomaly detected in the study area. Thus, lower
biomass or drastic changes in community composition can explain the decrease
in respiration rates observed during the El Niño winter. In fact González et al.
(1999), comparing the zooplankton community of the study area between pre-El
Niño summer and El Niño winter, concluded that a clear reduction of zooplankton biomass and a shift in the taxonomic composition took place. In addition,
González et al. (1998) also observed a change in the size distribution of phytoplankton communities during these time periods. During El Niño winter, the
2278
Microplanktonic respiration during El Niño 1997–98
pico- and nanoplankton fractions dominated both the coastal and oceanic areas
off Antofagasta, accounting for ~65% of primary production and 69% of phytoplanktonic biomass as chlorophyll a (González et al., 1998). In contrast, although
phytoplankton biomass during pre-El Niño summer was also dominated by
smaller size fractions (<23 µm), the microphytoplankton (>23 µm) size fraction
increased its relative contribution from oceanic to coastal stations, which seems
to be related to the upwelling filament observed nearshore (<15 nautical miles)
(González et al., 1998). In pre-El Niño summer, the bigger phytoplankton size
classes (>23 µm) accounted for 24 and 12% of primary production at the coastal
and oceanic stations, respectively (González et al., 1998).
Table I shows the P/R ratios calculated by combining primary productivity
measurements (González et al., 1998) undertaken simultaneously with our
respiration experiments. There is a wide range of P/R ratios in El Niño and preEl Niño conditions, reflecting an uncoupling between photosynthesis and respiration. This uncoupling is produced because production and respiration, and their
relationship, are dependent on physical and biological processes and, consequently, are strongly influenced by the physical–biological variability of the
ocean. The physical variability occurs over a wide variety of space and time
scales, and there is a continuous interaction among the processes operating at
the various scales (Stommel, 1963). Consequently, in most time and space scales,
respiration and photosynthesis are not in balance (e.g. del Giorgio et al., 1998;
Duarte and Agustí, 1998; Williams, 1998). In general, higher P/R ratios were
detected during El Niño winter conditions (Table I), where on one occasion
primary production was 9-fold greater than microplanktonic respiration in the
photic zone. The P/R ratios indicate that, in comparison to pre-El Niño summer,
under El Niño winter conditions a lower percentage of the primary production
was dissipated as heat by the microplanktonic community and, accordingly, a
higher percentage of the fixed carbon was available for higher trophic levels
and/or export production.
Our results show that the ESSW is an important physical barrier for aerobic
respiration, and that community respiration and oxygen concentration in the
water column are significantly correlated except in El Niño summer (Table II).
It is known that the HCS presents an extensive oxygen minimum layer associated
with the ESSW carried by the Gunther Current (Sievers and Silva, 1982; Silva,
1983). The Gunther Current has oxygen levels of 4.46 and 44.66 mmol O2 m–3 (i.e.
0.1 and 1 ml O2 l–1) in its center and upper boundary, respectively. Moreover, in
northern Chile, some of the iso-oxylines of low oxygen commonly bend upwards
to the surface in the nearshore zone in association with coastal upwelling events
(Morales et al., 1996a). The mentioned characteristics of the HCS make oxygen
levels a critical factor for the pelagic biota (Boyd et al., 1980; Jarre et al., 1991;
Morales et al., 1996b).
During El Niño winter and El Niño summer, the minimum oxygen layer was
deeper in comparison to pre-El Niño summer (Figure 9), allowing the aerobic
respiration to take place at deeper depths. In addition, in El Niño winter, the
microplanktonic community was able to respire aerobically at lower oxygen
levels than that of the pre-El Niño summer (Figure 8). The importance of the
2279
Y.Eissler and R.A.Quiñones
upper limit of the oxygen minimum layer becomes more evident when comparisons between periods are conducted using the base of the oxycline instead of the
mixed layer as the vertical limit for the integration of the respiration rates (Table
I). The difference between pre-El Niño summer and El Niño winter is higher
using the oxycline (P < 0.00002) than the mixed layer (P < 0.01). The effect of
higher temperatures on integrated respiration rates during El Niño could be more
drastic if the oxycline does not deepen.
The observed positive correlation between respiration and oxygen concentration in the water column becomes weaker under El Niño conditions during
July 1997, which could be due to the deepening of the oxycline. It is evident that
the oxycline plays a critical role in limiting aerobic respiration in the HCS off
Chile. Since the HCS off northern Chile presents a permanent minimum oxygen
layer in the surface 200 m, the oxycline is fundamental to defining the pathways
of matter and energy in the upper water column. There is an obvious need to
increase our understanding of the adaptations of the biota to live under hypoxic
and anoxic conditions in the HCS.
Acknowledgements
We wish to thank Mr Marcelo Gutiérrez, Hernán Reyes and Rodrigo González
for their help in the field work and computer support. Dante Figueroa and
Humberto González provided the CTD and chlorophyll data, respectively. We
also acknowledge the captain of the B/I ‘Abate Molina’, Mr Arturo Nakanishi,
and the crew for their assistance. The comments and suggestions of two anonymous reviewers were very important in improving the original manuscript. R.Roa
provided useful advice regarding statistical analysis. This research was funded
by the Grant Sectorial FONDECYT 5960002-96 (CONICYT, Chile) and the
FONDAP-Humboldt Program (CONICYT, Chile).
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Received on September 29, 1998; accepted on June 30, 1999
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