Journal of Oceanography, Vol. 60, pp. 149 to 162, 2004
Increased Stratification and Decreased Lower Trophic
Level Productivity in the Oyashio Region of the North
Pacific: A 30-Year Retrospective Study
S ANAE C HIBA1*, T SUNEO O NO2, K AZUAKI TADOKORO1, TAKASHI MIDORIKAWA3
and T OSHIRO S AINO1,4
1
Frontier Research System for Global Change,
Showa-machi, Kanazawa-ku, Yokohama, Kanagawa 236-0001, Japan
2
Hokkaido National Fisheries Research Institute, Katsurakoi, Kushiro, Hokkaido 085-0802, Japan
3
Japan Meteorological Agency, Otemachi, Chiyoda-ku, Tokyo 100-8122, Japan
4
Hydrospheric Atmospheric Research Center, Nagoya University,
Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan
(Received 11 August 2003; in revised form 28 October 2003; accepted 1 November 2003)
An analysis of the time series data sets collected from the 1960s to 1990s in the Oyashio
Water revealed signs of alteration in the physical, chemical and biological properties
of the water column in the western subarctic North Pacific. Wintertime salinity, phosphate concentration and apparent oxygen utilization (AOU) in the subsurface increased linearly over the 30 years. At the same time, salinity and phosphate in the
surface mixed layer decreased. An increase in the density gradient in the surface and
subsurface suggested that the water column stratification intensified, reducing the
vertical exchange of water properties during the period. The Net Community Production (NCP), estimated from the phosphate consumption from February through
August, also declined. Water column Chl a was approximately halved and diatoms
decreased by one order of magnitude in spring, consistent with the multi-decadal
decreasing trend of NCP. Zooplankton biomass was also nearly halved during the
same period. In contrast, wintertime Chl a increased by 63% and diatom abundance
doubled. Developmental timing became earlier in Neocalanus flemingeri, and spring
occurrence of N. plumchrus increased after the 1980s. Reduced vertical water exchange might have limited nutrient supply to the level, decreasing winter-summer
NCP for these three decades. It is speculated that, in the meantime, the earlier
stabilization of the surface layer might have enhanced wintertime diatom production
in the Oyashio’s light-limited environment. This condition could allow zooplankton
to effectively utilize diatoms from earlier timing, resulting in the apparent early developmental timing and abundance increase.
Keywords:
⋅ Oyashio,
⋅ western subarctic
North Pacific,
⋅ multi-decadal scale
change,
⋅ AOU,
⋅ stratification,
⋅ NCP,
⋅ diatom,
⋅ Neocalanus.
1976/77 (Trenberth, 1990; Miller et al., 1994) and 1988/
89 (Trenberth and Hurrell, 1994, 1995; Hare and Mantua,
2000), and regime-shift related climate indices such as
PDO (Pacific Decadal Oscillation, Mantua et al., 1997).
The most extensively studied were correlations between
climatic forcing and both fish stock and zooplankton abundance thanks to the existing long-term fisheries observation records (e.g. Kawasaki, 1989; Brodeur and Ware,
1992; McFarlane and Beamish, 1992; Mantua et al., 1997;
Beamish et al., 1999; Noto and Yasuda, 1999, 2002; Hare
and Mantua, 2000). However, those correlations did not
fully clarify the mechanisms underlying variation in the
lower trophic level environments and ecosystem. The least
1. Introduction
In recent years, an increasing number of studies have
been conducted on possible influences of decadal and
longer scale climatic variations on marine ecosystems in
various regions of the North Pacific (reviewed in Miller
and Schneider, 2000; Miller et al., 2004). Many studies
revealed variation patterns in biological components in
relation to physical environments such as water temperature anomaly associated with climatic regime shifts in
* Corresponding author. E-mail: [email protected]
Copyright © The Oceanographic Society of Japan.
149
Fig. 1. Sampling site in the Oyashio domain. Area in which
hydrographic data were collected is shaded. Black dots indicate the PH line stations at which biological data were
collected.
ronmental variables (Kubo, 1994; Odate, 1994; Tomosada
and Odate, 1995; Sugimoto and Tadokoro, 1997, 1998).
In the ESNP and central North Pacific, not only quantitative but also phenological changes were detected by detailed analysis of plankton community structure (species,
maturity stage and size composition) (Miller et al., 1992;
Mackas et al., 1998). Also, the shift in the community
structure gave us valuable insights into the mechanisms
underlying the observed variations (Karl et al., 2001;
Mackas et al., 2001; Batchelder and Powell, 2002), which
is indispensable in evaluating the ecological consequences
of climate change in terms of the biological carbon pump
function. With this background, we conducted this study
to clarify the mechanisms underlying the variation of a
lower trophic level ecosystem in the Oyashio, using the
30-year archival physical, chemical and biological data
sets and analyzing the plankton community in detail. Particular focus was on the multi-decadal scale trend that
we detected in this study.
2. Data Sources and Methods
observed is the chemical-biological link, in spite of the
fundamental importance of nutrient availability for primary production.
Polovina et al. (1995) demonstrated, both through
observation and modeling, the process by which large
scale climatic forcing could have different effects on lower
trophic level productivity in the central North Pacific
under nutrient-limited conditions, and the eastern
subarctic North Pacific (ESNP) under light-limited conditions. Furthermore, Chavez et al. (2003) synthesized
regional responses of physical, chemical and biological
components to multi-decadal scale climate change in the
whole North Pacific. To verify these scenarios and obtain a comprehensive view of the North Pacific ecosystem change, mechanisms have to be elucidated region by
region.
The Oyashio domain is located along the western
edge of the North Pacific subarctic circulation. Wintertime vertical mixing supplies rich nutrients to the surface
layer, and an extensive spring bloom occurs when the
surface water warms to form a stable mixed layer
(Taniguchi, 1999). The biological drawdown of atmospheric CO2 (Takahashi et al., 2002) and the ratio of organic to inorganic carbon flux (Honda et al., 2002) in the
Oyashio and the adjacent region were reported to be
amongst the highest in the world’s oceans. Hence, a better understanding of the mechanisms and consequences
of long-term ecosystem change in this region will be crucial to global biogeochemical studies. Nevertheless, compared to other regions, the process of ecosystem change
has not been fully investigated in the Oyashio where most
of the past studies have been limited to describing total
biomass variation in relation to climate and other envi150
S. Chiba et al.
2.1 Hydrography
Hydrocast data taken in the area west of 155°E and
north of 36°N (Fig. 1) from 1968 to 1999 were collected
from the archival data sets of the Hakodate Marine Observatory of the Japan Meteorological Agency (JMA) (Japan Meteorological Agency, 1995–2000) and the Japan
Oceanographic Data Center (JODC) (http://
www.jodc.go.jp). We used temperature, salinity, dissolved
oxygen (DO) and phosphate data obtained at standard
depths. DO and phosphate were measured following the
standard methods of Carpenter (1965) and Murphy and
Riley (1961), respectively. We did not use macronutrient
data other than phosphate because observations of silicate, nitrate and nitrite were less frequent. From these
collections, data taken at stations that meet criterion for
the Oyashio Water, <5°C at 100 m (Kawai, 1972), were
selected for use. In addition, stations shallower than 500
m were eliminated to avoid confusion by coastal water
signals. Density was estimated from temperature and salinity. The bottom of the mixed layer (MLD) was defined
as the depth at which the density increased by 0.125σ θ
from the surface value (Levitus, 1982), and MLD was
estimated by linearly interpolating the density profile.
Mean phosphate concentration within a mixed layer
(MLP) was obtained by the trapezoidal approximation
method. Subsurface Apparent Oxygen Utilization (AOU)
of each profile was calculated from DO values which were
linearly interpolated and averaged on five isopycnals from
26.70 to 27.20σθ.
2.2 Net community production (NCP)
The minimum net phosphate consumption by the
mixed-layer biological community between month i and
month j (NPCmini–j) was estimated from monthly mean
MLP by the following equation,
NPCmini–j = (MLPi – MLPj)*MLDj,
where MLP i and MLPj were the mean MLP for a month i
and the next month j, and MLDj is the mean MLD in the
month j. MLDi is always larger than MLD j from February to August in the Oyashio Water. Annual net community production (NCP) (g C m–2) was estimated from the
NPCmini–j (mmolP m–2) assuming a constant C/P ratio of
106 (Redfield et al., 1963). The equation for NPCmin was
based on the shallowest MLD during the period, and assumes there was no phosphate influx from the mixed layer
bottom after winter and no production of a subsurface
phytoplankton community. The NPCmini–j obtained for
the periods therefore gives the minimum monthly phosphate consumption, and NCP estimated from total
NPCmin is the minimum estimation of primary production.
2.3 Biological data
We used biological data sets collected during seasonal observations along the line PH (Stas. 3, 4, 5 and 6)
by the Hakodate Marine Observatory of the Japan Meteorological Agency for 1972–1999 (Fig. 1). The temperature criterion for the Oyashio Water (see Subsection 2.1)
was also applied to the selected biological stations. Data
from wintertime observation (late-January to mid-February) and spring observation (mid-April to early May) were
analyzed in this study. The midpoint of the sampling was
Julian Day 41 (SD: ±5) for winter and Julian Day 114
(SD: ±4) for spring. There was no significant multidecadal scale trend in the sampling date. Water samples
were taken at discrete depths by Nansen bottles or Niskin
bottles, and Chlorophyll a was measured by the
fluorometric method (Yentsch and Menzel, 1963). Water
column integrated Chl a was estimated by the trapezoidal
approximation method.
Diatoms taken by surface water sampling were identified and counted by species with an optical microscope
to estimate numerical abundance (cell l–1). For a detailed
description of diatom analysis, refer to Chiba and Saino
(2002). Diatom species with mean abundance of >1% of
the total were defined as the major diatoms in each season. Among major diatoms, those whose mean abundances
were significantly higher in spring than other seasons were
defined as the Spring-type species (ANOVA, a = 0.05).
To detect the possible phenological change in diatom community, interannual occurrence of the Spring-type species in wintertime and springtime was compared.
Zooplankton were collected by a vertical haul of a
NORPAC net (dia.: 0.45 m, mesh size: 0.33 mm) from
150 m depth to the surface. Total wet weight was measured from 1972–1999; however, detailed microscopic
analysis of species composition was done only after 1980.
Because Neocalanus copepods are reported as the dominant zooplankton, accounting for more than 70% of total
zooplankton biomass in the Oyashio Water (e.g. Kobari
et al., 2003), interannual variations of their wet weight
(mg m–3) and copepodite maturity stage composition were
further examined for the three species, N. cristatus, N.
flemingeri and N. plumchrus. The springtime Developmental Stage Index (DSI), which is the mean developmental stage in spring (mid-April to May) for each
Neocalanus sp. was estimated by the following equation,
DSI = (CIN*1 + CIIN*2 + CVN*5)/TotalN
where CI N –CV N is abundance (inds m –3 ) of each
copepodite stage and Total N is abundance of all
copepodite stages. DSI was calculated based on
copepodite stages of CI–CV for N. cristatus, and CII–CV
for N. plumchrus and N. flemingeri, because CI of N.
plumchrus (also applicable to N. flemingeri) was reported
to escape through the 0.33 mm mesh (Miller et al., 1984).
Zooplankton sampling was done regardless of time
of day. However, we neglected the influence of diurnal
vertical migration of zooplankton on their abundance and
biomass because Neocalanus copepods, the major
zooplankton components, have little diel vertical migration during copepodite periods (Mackas et al., 1993).
3. Results
3.1 Hydrography
Maximum density of the winter mixed layer is about
26.55 in the wide area of the western subarctic North
Pacific (WSNP) (Levitus and Boyer, 1994). Wintertime
(January) salinity, phosphate and AOU were plotted on
five subsurface isopycnals from 26.7, 26.8, 26.9, 27.0 and
27.2σθ, each of which corresponds to ca. 190, 260, 340,
420 and 630 m isobaths (Fig. 2). Both phosphate and AOU
linearly increased from 1968 to 1998 by 0.005 ± 0.003
µmol kg–1yr–1 and 0.9 ± 0.5 µmol kg–1y–1 on average,
respectively. (Note: hereafter the error bars for the respective linear regression represent the 95% confidence
level.) Salinity increased slightly with slopes of
0.0007~0.0011 psu y –1 for all isopycnals except the shallowest (26.7σθ). The corresponding warming trend on the
isopycnals was 0.007 ± 0.004°C y–1. In addition to the
linear trend, the AOU time series showed a bi-decadal
oscillation pattern superimposed on the linear increase
on all isopycnals. The wintertime salinity and density at
10 m depth decreased linearly for these three decades by
–0.003 psu y–1 and –0.004σθ y–1, respectively (Fig. 3).
The 5-year running mean of the density gradient between
Multi-Decadal Scale Ecosystem Change in the Oyashio
151
Fig. 2. a) Time series of wintertime salinity (psu) along the subsurface isopycnals 26.7, 26.8, 26.9, 27.0 and 27.2σθ. Approximate
depth of each isopycnal is 190, 260, 340, 420 and 630 m. Slope of regression lines (dash-dotted line) varied between –0.0001
psu y –1 (26.7σθ) and 0.0011 psu y–1 (27.0σ θ). b) As a) but for phosphate concentration (µ mol kg–1). Slope of regression lines
is 0.007 µ mol kg–1y –1on average. c) As a) but for AOU ( µmol kg–1). Slope of regression lines is 0.9 µmol kg–1y–1on average.
Besides the linear regression line, a non-linear-fit curve is shown (broken line). Average amplitude and cycle of the fitting
curves are 13 µ mol kg–1 and 20 yr, respectively (redrawn from Ono et al., 2001).
Fig. 3. Time series of wintertime salinity (psu) (black circle)
and density ( σθ) (open circle) at 10 m depth. Slope of regression line (dash-dotted line) is –0.003 psu y –1 for salinity and –0.004 σθ y–1 for density (redrawn from Ono et al.,
2001).
the surface and 250 m depth increased slightly but significantly both in winter and spring (Fig. 4). The density
gradient between the MLD and 250 m also showed a
gradual increase at a rate of 5% per century (data not
shown). Despite the changes in the T-S, the depth of each
isopycnal showed only a little shoaling trend (–0.5 m y–1
152
S. Chiba et al.
Fig. 4. Time series of density gradient (∆σt) between the surface and 250 m in winter a) and spring b). Thick line indicates 5-year running mean. Slope of regression line (broken line) is 0.003 ∆σ t y–1 for a), and 0.005 ∆σ t y –1 for b).
in average). The MLD shoaled by –0.3 m y –1, although
the trend was not significant due to large variation.
3.2 Net Community Production (NCP)
The 5-year running mean of MLP for February, July
Fig. 5. a) 5-year running mean of monthly mean phosphate
concentration within a mixed layer (MLP) ( µmol l–1) for
February, April, May, July and August. Slope of regression
line is (broken line) is –0.008 µ mol l–1y –1 for February,
–0.019 µmol l–1y–1 for July, and –0.008 µmol l –1y –1 for August. Regressions for other months are not statistically significant (a = 0.05). b) 5-year running mean of minimum net
phosphate consumption within a mixed layer (NPCmin)
(mmol P m–2) between the months: February to April, April
to May, May to July, July to August and the total (February
to August). Slope of regression line is –0.43 mmol P
m–2y–1 for February to April, 0.16 mmol P m–2y –1 for May
to July, and –0.40 mmol P m–2y –1 for February to August.
Regressions for other periods are not statistically significant (a = 0.05). Error bar represents 95% confidence limit
of each average and is calculated from the original values
rather than 5-year running mean (redrawn from Ono et al.,
2002).
and August showed a significant multi-decadal decreasing trend with a slope of –0.008 ± 0.003 µmol l–1y–1,
–0.019 ± 0.005 µ mol l–1y –1 and –0.008 ± 0.006 µ mol
l–1y–1, respectively (Fig. 5a). There was no significant
multi-decadal decreasing trend in MLP for April and May.
Consequently, the NPCmin between February and April
decreased significantly by –0.43 ± 0.11 mmol P m–2y–1,
and contributed greatly to the multi-decadal decrease of
total NPCmin from February to August (Fig. 5b). In contrast, the NPCmin between May and July showed a slight
increasing trend of 0.16 ± 0.05 mmol P m –2y –1 . The
NPCmin between July and August was low after 1983.
The observed decrease in total NPCmin (February to
August) of –0.40 ± 0.07 mmol P m–2y–1 was estimated as
equivalent to –0.51 ± 0.09 g C m–2y–1 decrease in NCP.
The NCP estimated from total NPCmin in the 1990s (45
mmol P m–2 on average, Fig. 5b) was 57 g C m–2, equiva-
Fig. 6. Time series of water column integrated Chl a (mg m–2)
in winter a) and spring b). Thick line indicates 5-year running mean. Slope of regression line (broken line) is 0.96
mg m –2y –1 for a) and 11.52 for mg m–2y–1 for b).
lent to 39% of the recent observation of annual primary
production in the Oyashio (146 g C m–2y–1) (Kasai, 2000).
Hence, it is obvious that the NCP in this study accounted
for the minimum estimation of water column primary production.
3.3 Phytoplankton
The mean value of water column integrated Chl a
for 1972–1999 was 371.9 mg m–2 (SD: ±217.4) in spring,
and 51.5 mg m–2 (SD: ±16.9) in winter. Springtime Chl a
showed a significant decreasing trend of –11.52 ± 5.30
mg m–2y–1 for these years (Fig. 6). In contrast, winter Chl
a showed an increasing trend of 0.96 ± 0.40 mg m –2y–1.
These values correspond to a 45% decrease in spring and
a 63% increase in winter for the 26 years, although Chl a
stock was more than four times larger in spring even in
the late 1990s.
The mean abundance of diatoms for 1973–1999 was
358120 cells l–1 (SD: ±301750) in spring and 2898 cells
l–1 (SD: ±2502) in winter. Wintertime diatoms increased
significantly by 0.018 ± 0.007 log10 (cell+1) l–1y–1 for
1973–1999, while springtime diatom decreased by –0.031
log10 (cell+1) l–1y–1 although the trend was not significant (Fig. 7a). 20 diatom species were defined as Springtype species (Table 1). Abundance of the Spring-type species increased significantly by 0.016 ± 0.007 log10 (cell+1)
l–1y–1 in winter, and decreased by –0.048 ± 0.016 log10
(cell+1) l–1y–1 in spring (Fig. 7b). These values correspond
to a doubling in wintertime abundance and a decrease of
more than one order of magnitude in springtime abunMulti-Decadal Scale Ecosystem Change in the Oyashio
153
Table 1. List of the Spring-type species that are major diatom
species (>1.0% of total) with abundances significantly
higher in spring that in other seasons (ANOVA, a = 0.05).
Species are in order of high mean in abundance. % is the
mean relative abundance to the total spring diatom cell
number.
Species
Fig. 7. a) Time series of diatom abundance {log10 (cell l –1+1)}
in winter (black circle) and spring (open circle) for total
diatoms. Thick line indicates 5-year running mean. Slope
of regression line (broken line) is 0.018 {log10 (cell l–1+1)}
y –1 for winter. Regression is not statistically significant for
spring (a = 0.05). b) As a) but for the Spring-type species.
Slope of regression line is 0.016 {log 10 (cell l–1+1)} y–1 for
winter, and –0.048 {log10 (cell l –1+1)} y–1 for spring.
Fig. 8. Time series of relative abundance of the Spring-type
diatom species (see Table 1) to the total diatoms in spring.
Thick line indicates 5-year running mean. Slope of regression line (broken line) is –2.156% y–1.
dance. The Spring-type species varied in a similar manner as Chl a for the period on a logarithmic scale, implying that the observed multi-decadal scale trend in Chl a
was mainly due to the change in abundance of these species. The relative occurrence of the Spring-type species
in spring decreased significantly by –2.156 ± 0.434% y –1
for the period. In particular, it dropped below 40% after
1990 (Fig. 8). There was no significant trend in relative
abundance of the Spring-type species in winter.
154
S. Chiba et al.
Thalassiosira nordenskieoldii
Nitzschia grunowii
T. angulata
Odontella aurita
Neodenticula seminae
T. gravida
Chaetoceros debilis
C. socialis
C. radicans
C. diadema
C. compressus
Porosira glacialis
C. curvisetus
T. hyalina
T. anguste-lineata
C. convolutus
Thalassionema nitzschioides
Asterionella kariana
Detonula confervacea
C. furcellatus
Mean abundance
(cell l – 1 )
%
74281
20204
19825
17883
15518
12457
11988
11079
8578
6518
6373
6148
6036
4106
3802
2364
2243
2161
2153
1999
30.0
8.2
8.0
7.2
6.3
5.0
4.8
4.5
3.5
2.6
2.6
2.5
2.4
1.7
1.5
1.0
1.0
1.0
1.0
1.0
3.4 Zooplankton
Mean total zooplankton biomass (wet weight) in
spring was 152.9 mg m–3 (SD: ±73.8) for 1972–1999.
There was a significant multi-decadal decreasing trend
with a slope of –3.822 ± 1.592 mg m–3y–1 although it remained rather constant after the late 1970s (Fig. 9). Consequently, the biomass nearly halved during these 27
years. The sum of the wet weight of Neocalanus cristatus,
N. flemingeri and N. plumchrus accounted for 43.9% (SD:
±21.4) of total spring zooplankton biomass on average
and up to over 90% at maximum for 1980–1999. This
value was smaller than annual mean of 71.6% in the
Oyashio water reported by Kobari et al., (2003), and than
the spring record of 50–60% in the Gulf of Alaska (Miller
et al., 1984; Mackas et al., 1998). Even so, it is still reasonable to consider that Neocalanus species were the
major zooplankton components in this study.
The mean spring numerical abundance was 10.8 inds.
m–3 (SD: ±6.4), 30.0 inds. m–3 (SD: ±14.6) and 10.9 inds.
m–3 (SD: ±13.4) for N. cristatus, N. flemingeri, and N.
plumchrus, respectively, for 1980–1999. Neocalanus
plumchrus showed a significant increasing trend on a logarithmic scale by 0.079 ± 0.013 log10 (inds.+1) m–3y–1 (Fig.
10). Neocalanus plumchrus appeared only in a small
Fig. 9. Time series of total zooplankton biomass (wet weight)
(mg m–3 ) in spring. Thick line indicates 5-year running
mean. Slope of regression line (broken line) is –3.822 mg
m–3y –1.
Fig. 11. Time series of spring Developmental Stage Index (DSI)
of Neocalanus cristatus a), N. flemingeri b) and N.
plumchrus c). Thick line indicates 5-year running mean.
Slope of the regression line (broken line) is 0.022 y–1 for
b). Regressions for a) and c) are not statistically significant
(a = 0.05).
(SD: ±0.2) for N. cristatus, N. flemingeri and N. plumchrus
respectively. Only N. flemingeri showed a significant
trend by 0.022 ± 0.009 y–1, that corresponds to DSI increase by 0.3 for the 19 years (Fig. 11). This implies that
development timing of N. flemingeri might have become
earlier.
4. Discussion
Fig. 10. Time series of spring numerical abundance {log10 (inds.
m–3+1)} of Neocalanus cristatus a), N. flemingeri b) and
N. plumchrus c). Thick lines indicate 5-year running mean.
Slope of the regression line (broken line) is 0.079 {log10
(inds. m–3+1)} y–1 for c). Regressions for a) and b) are not
statistically significant (a = 0.05).
number in the early 1980s with “zero” abundance in 1980
and 1982, but reached more than 40 inds. m–3 in the late
1990s. However, there was no significant trend for other
two species.
Mean spring DSI (Developmental Stage Index) for
1980–1999 was 3.1 (SD: ±0.3), 3.4 (SD: ±0.3) and 2.4
4.1 Reduced vertical exchange of water properties
We have detected a multi-decadal increase in the gradient of density, salinity and phosphate between the surface and subsurface, as well as an increase in subsurface
AOU (Fig. 2) in the Oyashio. These changes indicate that
the vertical exchange of water properties was reduced for
these three decades. Although we found that the MLD
decrease rate of –0.3 m y–1 was not statistically significant, the observed surface water freshening suggested that
wintertime vertical mixing might be slightly attenuated
during the 30 yrs. In addition, the slight increase in the
density gradient below the MLD evidenced a gradual reduction in vertical eddy diffusivity. Ono et al. (2001) demonstrated that the subsurface salinity increase within the
Multi-Decadal Scale Ecosystem Change in the Oyashio
155
density range of 26.7 and 27.4 σθ of the Oyashio could
not be explained in terms of a change in the horizontal
water exchange with saline subtropical water or less saline Okhotsk water. An increase in the influx of subtropical water should have decreased subsurface phosphate,
while it actually increased. A decrease in the influx from
the Sea of Okhotsk should have resulted in an AOU decrease in the Okhotsk water by reduction of the mixing
rate of Oyashio water with high AOU value, while
Andreev and Kusakabe (2001) observed that AOU in the
Okhotsk water has also increased linearly for these 30
years. Moreover, the estimated AOU increase in the
Oyashio induced by decrease in the Okhotsk water influx
was too small compared to the actual observation. The
influence of biological production on the AOU increase
is unlikely, too, because the NCP decreased (Fig. 5).
Since similar trends in subsurface water properties
have been observed in other areas in the WSNP (Emerson
et al., 2001; Watanabe et al., 2001), it is plausible that
the multi-decadal scale change observed in the Oyashio
was not a local phenomenon but prevailed through the
wide areas of WSNP. Watanabe et al. (2001) pointed out
that AOU increase was well balanced by the increase in
the estimated residence time of subsurface water in the
WSNP after the 1980s, and concluded that formation of
subsurface water had been diminishing. This further supports the possibility of reduced vertical water exchange
for these decades. Meanwhile, in the Japan Sea, the socalled “Miniature Ocean” holding a subarctic gyre in its
semi-closed system, the formation of bottom water (Japan Sea Proper Water) had been hindered for the past several decades (Kim et al., 2001) (its formation was observed during 2000–2001 winter (Kim et al., 2002)). It is
noteworthy that these changes were recognized simultaneously in the Oyashio and the Japan Sea, in which the
water mass formation process was completely independent. This indicates the atmospheric forcing induced
changes in both regions.
Surface water freshening could be a factor in the
observed surface water density decrease, and might be
partly responsible for the reduction of vertical exchange
of water properties. No increasing trend was found in
surface temperature, consistent with the PDO signal indicating a “cold-phase” in the WSNP after the mid 1970s
(Mantua et al., 1997). Causes of freshening, however,
were not fully clarified. The southward shift of the
subarctic gyre associated with intensification of the Aleutian Low (AL) pressure system between the 1976/77 and
1988/89 regime shifts (Hanawa, 1995; Sekine, 1999)
might enhance the transport of less saline surface water
to the Oyashio domain. However, this study found no reversal of the freshening even after 1988/1989 (Fig. 3). A
multi-decadal freshening trend in the surface layer was
also observed in the western Bering Sea, besides bi-
156
S. Chiba et al.
decadal scale salinity changes in relation to the AL
(Andreev and Watanabe, 2002). Considering that the
freshening rate of –0.003 psu y–1 found in their study is
equivalent to our finding, the low salinity anomaly in the
western Bering Sea and Oyashio might have the same
source.
Intriguingly, surface density decline and subsequent
stratification increase for the last several decades have
also been reported in the eastern North Pacific
(Roemmich, 1992; Polovina et al., 1995; Roemmich and
McGowan, 1995; Freeland et al., 1997). In the eastern
subarctic, Freeland et al. (1997) ascribed the density decline to an increase in horizontal advection of northern
less saline water that was induced by a southward shift of
the center of the Alaskan Gyre. Polovina et al. (1995), on
the other hand, attributed the observed ML shoaling of
up to 30% to surface water warming that might be induced by an intensification of southerly wind with warmer
temperature anomaly (Miller and Schneider, 2000). Both
studies explained the observed stratification changes in
relation to the AL dynamics, but these trends lasted longer
than a decade. In the California Current System where a
surface water warming trend was prominent, a reduction
of surface heat loss resulting from atmospheric forcing
was important in the longer-time scale rather than the
horizontal advection of water temperature anomaly or
weakening of upwelling (Miller and Schneider, 2000). It
is quite plausible that compound effects of a large scale
climate forcing triggered the coincidental multi-decadal
increase of stratification in the wide area of the North
Pacific, although its teleconnection mechanisms are as
yet unknown.
4.2 Decrease in lower trophic level production
Stratification increase and subsequent decline in ML
nutrient availability negatively affected the lower trophic
level ecosystem in the Oyashio after the 1970s. The decrease in springtime Chl a and NCP, particularly from
February to April, obviously indicates that both the extent and magnitude of the spring bloom have diminished
(Figs. 5 and 6). This is presumably due to a decrease in
diatom production since diatoms dominate the spring
phytoplankton community in the WSNP (Shiomoto, 2000;
this study). On the other hand, the production increase
from May to July was likely caused by nano-plankton,
which are predominant in the post-bloom in the WSNP
(Odate, 1996; Shiomoto and Hashimoto, 2000). ML phosphate was not depleted in May (>0.6 µmol l –1), implying
that phosphate was not a factor in the spring production
decline. It is well known that silicate depletion could limit
diatom production (e.g. Treguer and Pondaven, 2000).
Although long-term data of other macronutrients were not
available, Saito et al. (2002) showed that both nitrate and
silicate remained replete in post-bloom at least through
the 1990s in the Oyashio, when wintertime ML phosphate
supply was observed to be at its lowest (Fig. 5). Hence,
we suppose silicate depletion was less likely to limit diatom production in the Oyashio. An increase in grazing
pressure was also unlikely because spring zooplankton
biomass was much smaller in the 1970s than the 1990s.
Given the fact that diatoms require a larger amount
of iron for nitrate utilization compared to smaller, nondiatom phytoplankton (Boyd et al., 1996), Ono et al.
(2002) suggested that iron depletion might be the cause
of NCP decline in the Oyashio. In the WSNP, atmospheric
iron influx was reported to be large compared to the ESNP
(Duce and Tindale, 1991), which is the well-known Highnitrate low-chlorophyll (HNLC) region (Harrison et al.,
1999). Indeed, the magnitude of the bloom is much greater
(Sugimoto and Tadokoro, 1997) and the relative abundance of diatoms is higher (Obayashi et al., 2001) in the
WSNP than in the ESNP. However, the HNLC condition
was also observed in the WSNP (Banse and English,
1999), and a recent iron enrichment experiment revealed
that iron regulation of phytoplankton stock was a relatively pandemic condition, even in the WSNP (Tsuda et
al., 2003). Concerning the iron supply to the ML, Ono et
al. (2002) hypothesized that variations in wintertime entrainment of dissolved iron from subsurface might be more
important to determine annual NCP rather than variations
in airborne iron supply, and there are some findings supporting their hypothesis, as follows. First, the dissolved
iron concentration within the ML is similar (ca. 0.2 nmol
l–1) in the WSNP and ESNP in post-bloom, while that just
below the MLD (0.4–0.6 nmol l–1) is several-fold higher
in the WSNP than the ESNP (Nishioka et al., 2003). As
the bioavailability of air born iron within a mixed layer
declines when it rapidly turns into suspended particulate
form (Nishioka et al., 2003), it is suggested that the
particulate iron might sink and accumulate in the deep
layer where it is reduced to a biologically available, dissolved form to be re-supplied to the ML. Second, we observed a little shoaling trend in the MLD, and reduction
of vertical exchange of water properties below the MLD.
If we do a simple calculation using the value of 0.5 nmol
l–1 iron at the bottom of MLD, following Nishioka et al.
(2003) and assuming a C:Fe ratio of 105:1 (mol:mol), only
a subtle change in the vertical water exchange rate would
be required to reduce the ML iron to the level to match
the estimated decrease of annual NCP of –0.51 g C m–2
(0.0425 mol C m–2) reported in this study (C. Measures,
personal communication). Furthermore, if atmospheric
influx is the major determinant of annual ML iron supply, the observed intensification of stratification should
have increased the ML iron availability and primary production for these three decades in the Oyashio as Freeland
et al. (1997) suggested for the ESNP. In conclusion, air
born iron flux is assuredly the major source of oceanic
iron in the WSNP, but wintertime entrainment could be
the important process by which dissolved iron is supplied
to the ML. Air born iron flux might be more responsible
for the sporadic formation and extent of local blooms (Ono
et al., 2002), although this argument is nothing more than
speculation in the absence of long-term iron data.
The decrease in the NCP apparently had a negative
influence on secondary production in the Oyashio through
the bottom-up control, as springtime total zooplankton
biomass declined for these decades (Fig. 9). Even so, we
must consider the possibility of other mechanisms because
zooplankton biomass and production were determined by
compound processes derived by (1) both bottom-up and
top-down controls, (2) the influence of physical environmental changes on physiological rate of organisms, and
(3) match-mismatch effects as a result of these two effects (Cushing, 1972). This complexity sometimes makes
the link between long-term variations in primary production and secondary production less clear. In the ESNP,
for example, a decrease in annual mean Chl a (Brodeur
et al., 1996) and net primary production (Whitney and
Freeland, 1999) were also reported in the Alaskan Gyre
for these decades during which nutrient entrainments (nitrate) to the surface layer decreased, associated with a
stratification increase (Freeland et al., 1997). Nevertheless, the biomass of zooplankton increased markedly
(Brodeur et al., 1996), unlike the case in the Oyashio.
Intensive monitoring of physical, chemical and biological components will be indispensable to elucidate the
detailed mechanisms.
4.3 Phenological change in plankton community
We found not only quantitative but also phenological changes in the lower trophic level ecosystem on a
multi-decadal scale. In relation to phytoplankton, we observed that total spring diatom abundance was fairly constant while the Spring-type diatoms and Chl a decreased
(Figs. 7 and 8), suggesting both absolute and relative increases in presumably small, non-Spring-type diatoms
with lower individual Chl a contents. Chiba and Saino
(2002) reported that, in the Japan Sea, smaller, summertype diatom species markedly increased to dominate the
spring diatom community in years of low-Chl a and lownutrient conditions. Moreover, iron deficiency could suppress the production of fast-growing, large diatom species, hence regulating the magnitude of the spring bloom
in the WSNP (Tsuda et al., 2003). These results imply
that the spring diatom community in the Oyashio have
gradually shifted from the highly productive bloom community to the post-bloom community as overall ML iron
availability decreased over these 30 years. At the same
time, the doubling of wintertime diatom abundance suggests that optimal conditions for phytoplankton growth
might be appearing earlier in response to the increased
Multi-Decadal Scale Ecosystem Change in the Oyashio
157
Fig. 12. Schematic diagram of ontogenetic vertical migration
pattern of Neocalanus cristatus, N. flemingeri and N.
plumchrus (modified from Kobari and Ikeda, 2000).
stratification. This can be explained by the critical depth
theory (Sverdrup, 1953), which shows that early
stabilization of the surface mixed layer should be optimal to enhance phytoplankton production in the light-limited, high-latitude regions such as the Oyashio (Obata et
al., 1996). The increase in wintertime diatoms offset only
a small fraction of the decrease in its springtime stock
(Figs. 6 and 7), resulting in a decline of annual NCP (Fig.
5).
As diatoms are major food sources for Neocalanus
copepods in spring in the Oyashio (Kobari et al., 2003),
the decline of zooplankton biomass in recent years compared to the 1970s seems reasonable at a first glance (Fig.
9). Tadokoro et al. (2003) also demonstrated that decline
in diatom food availability in one season could reduce
egg production and recruitment of Neocalanus spp. in the
following year. In this study, however, the negative influence of diatom decrease on Neocalanus spp., the major herbivorous copepods, was less clear after the 1980s
considering the following facts: (1) spring abundance of
N. plumchrus increased (Fig. 10), and (2) developmental
timing of N. flemingeri became earlier (Fig. 11).
Neocalanus species are known to perform ontogenetic
vertical migration (Fig. 12): they develop from CI to CV
in the surface layer from late winter to summer, then descend to the meso-pelagic layer to diapause and spawn
(e.g. Miller et al., 1984; Kobari and Ikeda, 2000). Our
observation of the rare occurrence of N. plumchrus in
spring in the early 1980s was consistent with the previous report that in the WSNP it is a summer species which
appears in the surface layer only for a short period in the
post-bloom season (June to August) (Kobari and Ikeda,
2001). In the late 1990s, however, N. plumchrus even
numerically dominated over two other spring species, with
the result that average spring DSI of N. plumchrus (2.4)
did not change during these 20 years (Fig. 11). A possible explanation for its abundance increase is the improvement in survival chance of early ascending individuals
158
S. Chiba et al.
with the increase in wintertime food availability. The
spawning period of N. plumchrus is reported as being
prolonged from October to April in the Oyashio region,
despite the fact that its surface layer appearance is limited in summer (Kobari and Ikeda, 2001). The absence of
lipid storage and the rapid growth rate of N. plumchrus
copepodite (Tsuda et al., 2001) suggest that this species
might have an opportunistic feeding strategy, with which
they could grow by effectively utilizing diatoms whenever they are abundant and otherwise rely on other food
resources including micro-zooplankton (Gifford, 1993).
These facts all support the hypothesis that their survival
rate could be improved by an increase in temporal food
availability. Intriguingly, a possible improvement in survival of an early copepodite cohort of N. plumchrus was
also reported in the ESNP after the 1970s (Mackas et al.,
1998), although they attributed the change to a spring ML
temperature anomaly.
Neocalanus flemingeri occurs in the surface layer
from March to June (Kobari and Ikeda, 2000), the period
of high diatom abundance. Considering springtime surface water warming after the late 1980s in the Oyashio
(Tadokoro et al., 2003), temperature could be a factor
underlying the observed advance of its developmental timing (DSI 3.2 to 3.5). This temperature effect might also
compensate the negative influence of a decline in food
availability. However, it is still unclear why the overall
diatom stock decrease did not reduce the abundance of
N. flemingeri, a diatom feeder. In contrast to N. plumchrus,
the copepodite of N. flemingeri possesses a high lipid
content and grows slowly, and is thus considered tolerant
to temporal fluctuation in the ambient food availability
within a season (Tsuda et al., 2001). At the same time,
this suggests that N. flemingeri might have less behavioral
plasticity to utilize non-diatom food presented when diatoms are less available, and thus its production is likely
to be susceptible to total diatom availability through the
developmental period. In conclusion, observed diatom
abundance might never have dropped to the level limiting Neocalanus growth and production, even in the late
1990s. Daily primary production during the peak spring
bloom is reported to be approximately ten times larger
than the food requirement of these three Neocalanus spp.
in the Oyashio (Tadokoro et al., 2003). Moreover, recent
satellite observation has revealed that period of peak
bloom lasted only up to a few weeks in the subarctic region (Murata et al., 2002; Sasaoka et al., 2002; Yamada
et al., 2003) while the developmental period of
Neocalanus spp. extends from a few to several months.
The prolonged supply of a moderate amount of food derived by early water column stabilization rather than eventual, extensive spring bloom might therefore be favorable
for the growth and production of Neocalanus copepods,
at least to some extent.
Fig. 13. Hypothetical scenario describing mechanisms of lower trophic level ecosystem change for 1970s–1990s with physical,
chemical and biological processes from winter to spring.
5. Concluding Remark
A hypothetical scenario for the observed multidecadal changes in the Oyashio is summarized in Fig. 13.
This study was conducted based on time series of a limited number of variables; for example, we had no information on micronutrients, micro-zooplankton and
phytoplankton other than diatoms. Furthermore, we did
not successfully determine mechanisms underlying
change in physical properties and a possible climatephysical link. Nevertheless, this study has demonstrated
that a retrospective approach coupled with detailed plankton community analysis is useful to reveal mechanisms
of long-term change in lower-trophic level environments
and ecosystems.
In addition to a linear tend, we recognized a bidecadal oscillation pattern in subsurface AOU corresponding to the two well-documented two regime shifts in 1976/
77 and 1989. Considering the fact that a similar oscillation pattern superimposed on a linear trend of AOU was
also reported in the western Bering Sea (Andreev and
Watanabe, 2002), the linear trend in hydrographic properties might be independent of the bi-decadal oscillation
related to the AL dynamics, but correspond to longer-term
processes such as pentadecadal oscillation (Minobe, 1997)
or anthropogenic warming. Nevertheless, we could not
detect clear regime-shift-related changes in biological
properties, except in total zooplankton abundance, which
dropped markedly after the late 1970s. We have analyzed
only a 30 yr data set, and investigation of longer time
series would be required to distinguish whether the multi-
decadal scale trend we observed was related to the mechanism that caused the regime shifts.
Acknowledgements
We are grateful to the captains and crew of the R/V
Kofu-Maru and staff of the Oceanographic Division of
the Hakodate Marine Observatory for collection, measurement and management of the long-term data. We also
thank Dr. C. Measures for his insightful comments on our
iron entrainment scenario.
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