Why does Calanus sinicus prosper in the shelf ecosystem of the Northwest Pacific Ocean?
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ICES Journal of Marine Science, 57: 1850–1855. 2000
doi:10.1006/jmsc.2000.0965, available online at http://www.idealibrary.com on
Why does Calanus sinicus prosper in the shelf ecosystem of the
Northwest Pacific Ocean?
S. Uye
Uye, S. 2000. Why does Calanus sinicus prosper in the shelf ecosystem of the
Northwest Pacific Ocean? – ICES Journal of Marine Science, 57: 1850–1855.
Across the continental shelf of the eastern Inland Sea of Japan and the adjacent Pacific
Ocean, the Calanus sinicus population is centred in the shelf waters and declines
inshore and offshore. The reasons why this species prospers in the shelf ecosystem are
discussed in terms of its biological attributes and pattern of water circulation. Offshore
in deep water, the surface temperature near the Kuroshio Current is lethally or
sublethally high for C. sinicus, and the food supply in the form of phytoplankton is
poor. Inshore in shallow water, C. sinicus is replaced by small species such as
Paracalanus sp., Acartia omorii, and Oithona davisae, although its reproductive
potential, represented by fecundity and development time, is comparable to or even
higher than theirs. Shallow water may enhance the rate of mortality of C. sinicus,
because its eggs tend to descend through the water column and die quickly when they
come into contact with bottom muds, and also because its older stages, particularly
CVs and adults, cannot perform a full-scale diel vertical migration to avoid visual
predators. In contrast, shelf waters may provide a suitable habitat for C. sinicus
because temperature, phytoplankton food supply, and depth are ideal.
2000 International Council for the Exploration of the Sea
Key words: Calanus sinicus, Inland Sea of Japan, northwest Pacific Ocean, population
maintenance mechanism, shelf ecosystem.
Received 27 August 1999; accepted 13 December 1999.
S. Uye: Faculty of Applied Biological Science, Hiroshima University, 4-4 Kagamiyama
1 Chome, Higashi-Hiroshima 739-8528, Japan [tel: +81 824 247940; fax: +81 824
227059; e-mail: suye@hiroshima-u.ac.jp]
Introduction istic of C. sinicus, because it is distributed over the shelf
waters of the South China Sea, the East China Sea, the
One of the major research objectives posed by the Yellow Sea, the Bohai Sea, and around Japan. Although
GLOBEC (Global Ocean Ecosystem Dynamics) project the other two species are also distributed in shelf waters,
is to understand the physical and biological processes their main habitat is spread over the subarctic North
that control the transport, retention, and loss of marine Pacific Ocean, including the Kuroshio Extension and
zooplankton, particularly over continental shelves, Transition Zone. In the shelf waters of the Inland Sea of
because such areas host most of the world’s commercial Japan and the adjacent Pacific Ocean, C. sinicus is
fisheries. Copepods of the genus Calanus are the major generally the dominant copepod and supports the pro-
macrozooplankton component in shelf ecosystems, duction of commercially important anchovy, sandeels,
except in tropical seas, and are the major food source to and sardines (Hashimoto et al., 1997; Uye and Shimazu,
fuel pelagic fish production. In typical coastal upwelling 1997; Uye et al., 1999). Although some biological
systems, such as in waters off Oregon, Peru/northern attributes (e.g. feeding, fecundity, development time,
Chile, northwestern and southwestern Africa, the inter- growth, diel vertical migration, spatio-temporal distri-
actions between water currents and the life cycle strate- bution, seasonal life cycle) of C. sinicus have been
gies of copepods, including the genus Calanus, have been demonstrated in previous field and laboratory investi-
reviewed by Peterson (1998). gations (Uye, 1988, 1994; Uye et al., 1990a, b, 1999;
Of three Calanus species (Calanus sinicus, C. pacificus, Huang et al., 1992, 1993a, b; Uye and Yamamoto, 1995;
and C. yashnovi) distributed in the Northwest Pacific Uye and Murase, 1997; Uye and Shimazu, 1997), little
Ocean (Brodskii, 1967, 1975; Hulsemann, 1994), close has been said about the maintenance mechanism of C.
association with the continental shelf is most character- sinicus populations in shelf waters.
1054–3139/00/061850+06 $35.00/0 2000 International Council for the Exploration of the SeaCalanus sinicus in the Pacific shelf ecosystem 1851
134° 30' 135°E Harima Nada (a)
30' 600
Harima-nada 20
20
400
(Mean: 116)
200
Kii
HONSHU
Channel
0
34°
SHIKOKU 600 Kii Channel (b)
50
100
Abundance (individuals m )
400
–3
(Mean: 172)
200
200
1000 30'
0
100
Coastal Pacific (c)
Inland Sea of 75
Japan
50 (Mean: 35.9)
Pacific 33°N
Ocean 25
0
Figure 1. Location of sampling stations of Calanus sinicus
across the continental shelf in the eastern Inland Sea of Japan 100
and adjacent Pacific Ocean. The area is divided into four Offshore Pacific (d)
subareas, Harima Nada, the Kii Channel, the coastal Pacific 75
with depths 200 m (modified from Huang et al., 1993a). 50 (Mean: 10.3)
25
0
In this paper, I integrate published and unpublished A M J J A S O N D J F M
information on the biological attributes of C. sinicus Month
with environmental factors to pose a hypothesis explain- Figure 2. Monthly change in mean abundance of copepodites
ing why it prospers in the shelf ecosystem of the North- and adults of Calanus sinicus in (a) Harima Nada, (b) the Kii
Channel, (c) the coastal Pacific, and (d) the offshore Pacific.
west Pacific Ocean.
Annual mean abundance is given in parenthesis. Note differ-
ence in abundance scales between panels (a)–(b) and (c)–(d) –
modified from Huang et al. (1993a).
Geographical and seasonal distribution
across the continental shelf
The population was centred in the Kii Channel (aver-
The geographical distribution of C. sinicus was investi- age depth about 50 m) and declined both inshore and
gated monthly during one year (April 1987 through offshore. The monthly patterns of mean abundance
March 1988) over the relatively narrow (distance differed among the four subareas delineated (Harima
between the innermost station and 200 m isobath, Nada, the Kii Channel, the coastal Pacific, and the
c. 100 km) continental shelf of the eastern Inland Sea of offshore Pacific; see Figure 1), most notably inshore
Japan and the adjacent Pacific Ocean, where the depth (Figure 2). It was highest in early summer and declined
varies from about 30 m in Harima Nada to more than to a minimum in autumn in Harima Nada and the Kii
1000 m in the Pacific Ocean (Figure 1; Huang et al., Channel. The population barely continued to exist in
1993b). C. sinicus (copepodites and adults) were col- Harima Nada, where the summer temperature (>25C)
lected at 60 stations by hauling a plankton net vertically apparently exceeded the upper thermal tolerance of the
from the bottom (or from 150 m where the bottom species (see below). Analysis of the monthly proportions
is deeper) to the surface. Because of the coarseness of of the various copepodite stages revealed that all stages
the mesh (320 m), it was likely that some of the CIs occurred continuously, indicating that reproduction of
and CIIs might have passed through the net. Further, the species takes place throughout the year. No diapaus-
the population in deep (>150 m) water was not ing CVs were found in the study area (Huang et al.,
sampled. 1993a).1852 S. Uye
150 where it is found only in winter and spring, disappearing
Temperature (°C) (a) in June when the temperature warms to 24C (Lin and
Li, 1984). Salinity may be unimportant, at least over the
100
range examined, because C. sinicus is capable of repro-
ducing in the laboratory at 26 (unpublished data), and
50 its occurrence in the plankton has been confirmed at
salinities as low as 15 (Imabayashi and Endo, 1986). A
0 tolerance to lower salinity is also indicated by its con-
5 10 15 20 23 25 30
? tinuous presence in the Bohai Sea, China, where the
Hatching salinity seasonally decreases to 5 m as a food
the depth at the sampling stations. Data were accumulated source for egg production in the Inland Sea of Japan.
from cruises in the Inland Sea of Japan conducted during the At lower concentrations of phytoplankton offshore
past two decades (n=374). Horizontal lines denote the thermal
range for embryonic development and the salinity range for (chlorophyll a concentrationCalanus sinicus in the Pacific shelf ecosystem 1853
(a) (b)
Egg Production Rate Clutch Size
80 80
day )
–1
( ) ( )
(eggs clutch )
–1
60 60
–1
(eggs female
40 40
20 (r = 0.78) 20 (r = 0.82)
–0.8P –2.3P
E = 3.0 + 66.4 (1 – e ) C = 1.1 + 46.6 (1 – e )
0 0
(c) (d)
Specific Egg Production Rate Spawning Frequency
day )
–1
0.15 1.5
( )
–1
( )
(clutches female
(day )
0.1 1
–1
0.05 0.5 –2.6P
(r = 0.83) F = 0.1 + 0.9 (1 – e )
–1.0P
Es = 0.003 + 0.139 (1 – e ) (r = 0.62)
0 0.5 1 1.5 2 11.5 0 0.5 1 1.5 2 11.5
–1
Chlorophyll (> 5 µm, µg l )
Figure 4. Relationships between fecundity parameters (a) rate of egg production, (b) clutch size, (c) specific rate of egg production,
and (d) spawning frequency of Calanus sinicus and >5 m chlorophyll a concentration in the Inland Sea of Japan (modified from
Uye and Murase, 1997).
the population is lost between the egg and stage NII, through diel vertical migration to avoid visual predators
probably at the egg stage. (Uye et al., 1990b; Huang et al., 1992, 1993b). Hence,
C. sinicus eggs sink at a velocity of some 70 m d 1 they may be subjected to greater predation than the
(Uye et al., 1990b). Therefore, in shallow water, a population in deep water.
considerable proportion of the eggs may sink to the
bottom before they hatch as nauplii. Most of those eggs
would probably die, based on the following laboratory Appropriate conditions in shelf water
experiment. Some 20–30 freshly spawned eggs of C.
sinicus were introduced into glass test tubes containing Figure 7 shows schematically the topographical features,
filtered (Whatman GF/C) seawater and allowed to settle water movement, and distribution of C. sinicus across
to the bottom. There, silty bottom mud, taken from the the continental shelf of the Inland Sea of Japan and the
central part of the Inland Sea of Japan, was added adjacent Pacific Ocean. The Inland Sea of Japan proper
gently to cover the eggs in a layer about 5 mm thick. The is separated from open shelf waters by a narrow strait in
same mud was introduced into other tubes and centri- which the tidal current is much stronger than in adjacent
fuged to the bottom before eggs were added and allowed waters. Offshore, the warm Kuroshio Current moves
to settle on it. All these tubes and other control tubes slowly, and temperature is always highest farther
without mud were incubated at 18C and the number of offshore. In summer, as a result of solar heating,
nauplii hatching counted on day 2. The eggs covered in temperature is higher inshore than over the shelf.
the 5-mm thick layer of mud were recovered and those Owing to nutrient-loading from the shore, phyto-
that looked viable were incubated as in the control. Only plankton concentration is always highest inshore; the
28% of the eggs that had settled on top of the mud average concentration of chlorophyll a is usually >2 g
hatched, although 94% of the eggs in the control hatched l 1 (Uye et al., 1990a, 1999; Uye, 1994). Cool, nutrient-
(Figure 6). Of the eggs buried in the mud, most had died rich water flows onshore along the bottom and is mixed
by day 2 and none remained viable to day 4. by the strong tidal current near the strait, so that
Not only the eggs, but also older stages, particularly nutrients from the bottom as well as from the shore are
CVs and adults, may suffer greater mortality in shallow available for phytoplankton production over the shelf
water, because they cannot descend deep enough (Fujiwara et al., 1997). Phytoplankton concentration is1854 S. Uye
60 Control On mud In mud
(a)
94%
day )
100
Hatching success (%)
–1
50 80
–1
Egg production rate (eggs female
60
40
Calanus sinicus
40
28%
30 Paracalanus sp.
20
3%
0%
0
20 2 days 2 days 2 days 4 days
Acartia omorii
Figure 6. Effects of mud on the survival of Calanus sinicus eggs
in the laboratory.
10
Oithona davisae 100 m
50 m 200 m
0 500 m
20 m
50
(b)
Calanus sinicus
Development time (egg to adult, days)
40 Paracalanus sp.
Acartia omorii
Oithona davisae
30
DVM
50 m
20
100 m
10
150 m
0
5 10 15 20 25
Temperature (°C) Figure 7. Schematic representation of (a) topographical fea-
Figure 5. Comparison of temperature and (a) rate of egg tures and (b) water movements and distribution of the Calanus
production and (b) development time to adult in Calanus sinicus population across the continental shelf of the Inland Sea
sinicus (from Uye, 1988, unpublished data), Paracalanus sp. of Japan and the adjacent Pacific Ocean. Arrows in (a) denote
(from Uye, 1991; Uye and Shibuno, 1992), Acartia omorii (from the relative strength of the tidal current, except for the most
Uye, 1980, 1981), and Oithona davisae (from Uye and Sano, offshore one, which shows the flow of the Kuroshio Current.
1995, 1998). Arrows in the bottom panel denote the tidal residual current,
except for the thick one (labelled DVM), which shows the diel
vertical migration of C. sinicus. Darker shading indicates a
denser population of C. sinicus.
of course lowest offshore, where the average concen-
tration of chlorophyll a never exceeds 0.5 g l 1 (Uye et
al., 1990a, 1999; Uye, 1994).
The patterns of water flow predominant in shelf upwelling systems. The work of Peterson (1998) on
waters are characterized by a typically estuarine circu- life-cycle strategies of copepods in coastal upwelling
lation. Fujiwara et al. (1997) examined the vertical areas revealed that combinations of water flow pattern
profiles of residual flow by means of an ADCP through with the copepod’s diel and/or ontogenetic vertical
a cross-section in the narrows of the Kii Channel in migration are mainly responsible for the maintenance of
August (depth 80 m). They found that surface water such populations in shelf waters. Moderate temperature,
(Calanus sinicus in the Pacific shelf ecosystem 1855
generalization may also be applicable to other species of in relation to salinity. Bulletin of the Plankton Society of
Calanus distributed across other shelf ecosystems. Japan, 33: 113–123.
Lin, Y., and Li, S. 1984. A preliminary study on the life cycle
of Calanus sinicus Brodsky in Xiamen Harbor. Journal of
Xiamen University (Natural Sciences), 23: 111–117 (in
Acknowledgements Chinese with English abstract).
I thank my colleagues and former students at the Peterson, W. T. 1998. Life cycle strategies of copepods in
coastal upwelling zones. Journal of Marine Systems, 15:
Laboratory of Biological Oceanography, Hiroshima 313–326.
University, many of whom contributed to this study. Uye, S. 1980. Development of neritic copepods Acartia clausi
Field assistance by the captain and crew of T&RV and A. steueri. 2. Isochronal larval development at various
‘‘Toyoshio Maru’’, Hiroshima University, and RV temperatures. Bulletin of the Plankton Society of Japan, 27:
11–18.
‘‘Tokushima’’, Tokushima Prefectural Fisheries Exper-
Uye, S. 1981. Fecundity studies on neritic calanoid copepods
imental Station, is also acknowledged. Comments and Acartia clausi Giesbrecht and A. steueri Smirnov: a simple
suggestions by anonymous referees and the editors, empirical model of daily egg production. Journal of Exper-
Charlie Miller and Kurt Tande, were most valuable. imental Marine Biology and Ecology, 50: 255–271.
Uye, S. 1988. Temperature-dependent development and growth
of Calanus sinicus (Copepoda: Calanoida) in the laboratory.
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