interannual variations in abundance and body size in...

I N T RO D U C T I O N

Copepods are the dominant component of mostmetazoan plankton communities throughout the worldocean [cf. (Mauchline, 1998)]. Among them, Neocalanus

cristatus, Neocalanus plumchrus and Neocalanus flemingeri arelarge grazing copepods occurring across the entiresubarctic Pacific and in its marginal seas (Conover, 1988;Mackas and Tsuda, 1999). These three Neocalanus

copepods are characterized by an annual life cycle, duringwhich they undergo extensive ontogenetic vertical migra-tion down to 500 m or more following their rapid develop-ment in the surface layer during spring–summer (Miller et

al., 1984; Miller and Clemons, 1988; Kobari and Ikeda,1999, 2001a,b). Together with one other large grazingcopepod (Eucalanus bungii ), the three Neocalanus species

often account for 80–95% of the summer zooplanktonbiomass in the surface layer (Vinogradov, 1970; Vidal andSmith, 1986). They are an important diet component ofmesopelagic fish (Gordon et al., 1985; Beamish et al.,1999), salmon (LeBrasseur, 1972; Burgner, 1991), Pacificsaury (Odate, 1994), baleen whales (Kawamura, 1982)and seabirds (Hunt et al., 1993), and are therefore a vitallink between primary production and production athigher trophic levels in the subarctic North Pacific.

Recently, analysis of long-term variables of oceanicecosystems in response to the climatic ‘regime shift’ in theNorth Pacific has been of great interest among scientistsof North Pacific rim countries. Brodeur and Ware(Brodeur and Ware, 1992) demonstrated that zooplanktonbiomass in the 1980s was higher than in the 1950s and1960s in the eastern subarctic Pacific. Pelagic nekton

Journal of Plankton Research 25(5), © Oxford University Press; all rights reserved

Interannual variations in abundance andbody size in Neocalanus copepods in thecentral North PacificTORU KOBARI*, TSUTOMU IKEDA1, YASUJI KANNO1, NAONOBU SHIGA, SHOGO TAKAGI1 AND TOMONORI AZUMAYA2

AQUATIC RESOURCE SCIENCE LABORATORY, FACULTY OF FISHERIES, KAGOSHIMA UNIVERSITY, -- SHIMOARATA, KAGOSHIMA -,1BIODIVERSITY LABORATORY, FACULTY OF FISHERIES, HOKKAIDO UNIVERSITY, -- MINATO-MACHI, HAKODATE, HOKKAIDO - AND 2PELAGIC FISH

AND CEPHALOPOD BIOLOGY SECTION, HOKKAIDO NATIONAL FISHERIES RESEARCH INSTITUTE, KATSURAKOI, KUSHIRO, HOKKAIDO -, JAPAN

*CORRESPONDING AUTHOR: [email protected]

As the integral components of zooplankton in the subarctic North Pacific, the three Neocalanus species (N.

cristatus, N. plumchrus and N. flemingeri) are characterized by an annual life cycle and rapid development

in the surface layer during spring–summer. Patterns of interannual variation of abundance and body size

of these Neocalanus species were analyzed using the time-series data collected during the summers of

1979–1998 (20 years) at stations along the longitudinal transect line in the central North Pacific, crossing

five sub-areas (Alaska Current System, Subarctic Current System, Northern Transition Domain, Southern

Transition Domain and Subtropical Current System). In the southern sub-areas, quasi-decadal oscillation

was observed for the 3-year running mean of abundance and prosome length for copepodite stage 5 (C5)

of the three Neocalanus species. Although the oscillation signal diminished towards northern waters, it

showed a positive phase during the early 1980s and 1990s and a negative phase during the late 1980s.

In the northern waters, a biennial pattern was pronounced for anomalies of C5 prosome length for N. plum-

chrus and N. flemingeri, which was large in odd years and small in even years. Significantly positive covari-

ations among the three species were found for both abundance and prosome length around mid-latitude,

where they were abundant. In the correlation analysis, these observed yearly patterns showed a statistically

insignificant correlation with most environmental (integrated mean temperature in surface waters, water

column stability and chlorophyll a concentration) or climatological (North Pacific Index and Southern Oscil-

lation Index) variables. The regional difference of the oscillation signal and the synchronized covariation

among these species suggest that interannual variations of their abundance and body size are mediated by

common environmental force(s) with some spatial and temporal scales in the subarctic North Pacific.

JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒

02 Kobari fbg020 (to/d) 23/4/03 9:29 pm Page 483

populations, such as salmon and squids, also increasedduring the same period (Beamish and Bouillon, 1993;Francis and Hare, 1994; Brodeur and Ware, 1995).Intensified winter mixing mediated by the strengthenedatmospheric Aleutian Low after the mid-1970s has beenhypothesized as a cause for these long-term changes inabundance. In the western Pacific, zooplankton biomassdecreased in the subarctic regions, but increased in theOyashio–Kuroshio transition regions after the late 1970s(Odate, 1994). These changes were interpreted to be aresult of the intensified southward intrusion of theOyashio water (Tomosada and Odate, 1995). In thecentral subarctic Pacific, biennial cycles have been foundin zooplankton biomass (Sugimoto and Tadokoro, 1997;Shiomoto et al., 1997). Shiomoto et al. (Shiomoto et al.,1997) considered that the biennial cycle pattern inzooplankton biomass is possibly due to predation by pinksalmon, the stock size of which varies every other year [cf.(Ishida, 1995)]. Zooplankton are known to be the majordiet component of pink salmon (Fukataki, 1967).

In most previous analyses of long-term variability ofzooplankton in the subarctic Pacific, zooplankton weredealt with as a single entity, e.g. as biomass, whichcomprises a mixture of various metazoan species at diversetrophic levels. Because the effects of long-term climatechanges on a given zooplankton species population arelikely to be via species-specific ‘top-down’ and/or ‘bottom-up’ control through prey–predator relationships, analysisbased on individual species rather than biomass of totalmetazoan zooplankton is considered to be more sensitiveand the results more useful for understanding of pelagicecosystems. Thus, the species-based analysis of long-termvariabilities in response to climate changes has beenreported for copepods in the North Atlantic, such asCalanus finmarchicus and Calanus helgolandicus (Fromentin andPlanque, 1996; Planque and Fromentin, 1996; Reid et al.,1998), and Pseudocalanus elongatus and Acartia clausi

(Colebrook, 1985, 1986), but only a limited attempt hasbeen made on the copepods in the North Pacific (Mackas,1995; Mackas et al., 1998).

In the present study, we investigate interannual varia-tions in population sizes and body sizes of the threeNeocalanus copepods (N. cristatus, N. plumchrus and N. flemin-

geri ) using a 20-year data set (1979–1998) collected atstations along a longitudinal transect in the central NorthPacific. In addition, possible correlations of environ-mental attributes to these variations are explored.

M E T H O D

Zooplankton samplings were carried out at stationsbetween 37 and 51°N latitude along 180º longitudeduring T/S ‘Oshoro-Maru’ cruises during the summers

( June) of 1979–1998 (20 years) (Figure 1). The number ofstations was varied interannually and ranged from 15 to32. At each station, a vertical tow was made from 150 mdepth to the surface with NORPAC nets (45 cm mouthdiameter, 0.35 mm mesh size) equipped with a flowmeter.Sampling precisions of the single tows were estimated bycomparing the two simultaneous catches from twin-typeNORPAC nets in the summer of 1996. The difference incopepod numbers between the catches was ±55.0% (n =21) for N. cristatus, ±15.9% (n = 22) for N. plumchrus and±23.3% (n = 21) for N. flemingeri (±95% confidence inter-vals; T. Kobari, unpublished data). The within-daysampling time at each station was not standardizedthroughout this study. However, the effect of non-standardized sampling time on estimating abundance ofNeocalanus copepods would be minimal, as Neocalanus

copepods usually carry out little or no diel vertical migra-tions (Mackas et al., 1993; Tsuda and Sugisaki, 1994).After collection, zooplankton samples were preservedimmediately in 5% formalin–seawater buffered withborax.

In the land laboratory, copepodite stage 5 (C5) ofN. cristatus, N. plumchrus and N. flemingeri was sorted fromthe zooplankton samples and counted under a dissectingmicroscope. As an index of body size, the prosome lengthwas measured on 50 specimens arbitrarily selected at eachstations to the nearest 0.1 mm for N. cristatus and 0.05 mmfor N. plumchrus and N. flemingeri. In the present analysis,C5 was used for abundance and prosome length becausetheir life histories/ontogenetic vertical migration patternsare characterized by surface occurrence of C5 with theirlonger development time and status as the last feedingstage (Miller et al., 1984; Miller and Clemons, 1988;Kobari and Ikeda, 1999, 2001a,b).

Temperature and salinity were determined with reversing thermometers and Auto-Lab salinometers in1979–1983, and a CTD system in 1984–1998 at eachsampling location. Chlorophyll a concentration (mg m–3)was estimated indirectly from Secchi disc readings (Zd; m)using the equation proposed by Falkowski and Wilson(Falkowski and Wilson, 1992): Chl = 457 Zd

–2.37. Detailsof sampling data have been reported in the Data Recordsof Oceanographic Observation and Exploratory Fish-eries No. 23-42 (Hokkaido University, 1980–1999).

R E S U LT S

Environment

According to Favorite et al. (Favorite et al., 1976), theboundary between the Subarctic Current System (SA)and the Transition Domain is delineated by cold water(<4°C) below 100 m depth, a characteristic of the



Subarctic Current. The Subarctic Boundary between theTransition Domain and the Subtropical Current System(ST) is detected by the vertical isohaline of 34.0. TheTransition Domain is further divided into the Northernand Southern Transition Domains (TN and TS, respec-tively) by a frontal structure of salinity (33.6), called theTransition Front (Anma et al., 1990). In northern stations,an intrusion of low salinity water (<32.8) and a well devel-oped halocline in the epipelagic layer are indicative of theAlaska Current System (AS), which flows westerly fromthe Gulf of Alaska along the southern edge of theAleutian Islands (Favorite et al., 1976). We used thosecriteria to separate the entire longitudinal transect datainto five sub-areas in the following analysis. Over thestudy period, the position of the boundary between SAand TN was relatively stable (45°00�–47°30�N), whilepositions of the Transition Front and Subarctic Boundaryvaried (41°45�–45°30�N and 38°30�–43°00�N, respec-tively) (Figure 2). The Transition Domain (TN plus TS)expanded to the south in the late 1980s and 1990s due toa southward shift of the Transition Front and SubarcticBoundary.

As a climatological index, we used annual means of theNorth Pacific Index (NPI) (Trenberth and Hurrell, 1995)and Southern Oscillation Index (SOI) (Climate PredictCenter, http://www.cpc.ncep.noaa.gov). Although the

anomalies of both indexes were highly fluctuating, the 3-year running mean of SOI showed a quasi-decadaloscillation (Figure 3). This signal was a positive phaseduring the late 1980s and a negative phase during theearly 1980s and 1990s.

In each sub-area, station data for integrated meantemperatures from sea surface to 150 m depth (T0–150),vertical stability index (STBL = differences in tempera-tures between sea surface and 150 m depth) and estimatedchlorophyll a concentration (mg m–3) were pooled, andthen anomaly and its 3-year running mean werecomputed. Although no distinct pattern was found fortheir anomalies, a quasi-decadal oscillation was evidentfor their 3-year running means (Figure 4). The oscillationsignal was predominant in the southern sub-areas, anddiminished towards northern waters. The yearly patternsshowed a positive correlation with SOI which was statisti-cally significant (Kendall rank) in the TS and ST.

Abundance of Neocalanus copepods

C5 abundance of N. cristatus, N. plumchrus and N. flemingeri

showed a common north-to-south trend, which wascharacterized by a mid-latitude maximum around theTN, decreasing both northwards and southwards fromthe TN (Figure 5). Overall, the most and least abundantspecies were N. plumchrus and N. cristatus, respectively, with

T. KOBARI ET AL. INTERANNUAL VARIATIONS IN NEOCALANUS COPEPODS

Fig. 1. Schematic diagram of the surface current and gyre systems in the northern North Pacific (redrawn from Dodimead et al., 1963) and thetransect (180° longitude) at which zooplankton samplings were carried out on the ‘Oshoro-Maru’ cruises during the summers of 1979–1998.

130˚ E 140˚ E 150˚ E 160˚ E 170˚ E 180˚ 170˚ W 160˚ W 150˚ W 140˚ W 130˚ W

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N. flemingeri being intermediate. The coefficient of vari-ation in the yearly abundance at each station was high inthe AS and ST where their abundance was low. Two-wayANOVA was performed to quantify the relative import-ance between year-to-year and station-to-station varia-tions to the observed total variations in thelog-transformed abundance data of the three species ineach sub-area (Table I). Station-to-station variations werea more important source of the total variations than year-to-year variations in the sub-areas with low abundance.

Anomaly and its 3-year running mean computed fromthe log-transformed C5 abundance of the three speciesshowed a regional difference of interannual variationpatterns (Figure 6). Anomaly showed positive correlationsamong the three species in the SA and TN where C5abundance was high. Decreasing trend was evident foranomaly of N. plumchrus in the TN (Kendall rank, P <0.05). A quasi-decadal oscillation was observed for 3-yearrunning means of the three species in the southern sub-areas. Its negative phase was found during the late 1980swhen T0–150 were positive phase (Figure 4). The oscilla-tion signals diminished towards northern waters.

Body size of Neocalanus copepods

C5 prosome length of N. cristatus, N. plumchrus and N. flemingeri decreased consistently from northern to


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Fig. 3. Interannual variations in anomaly of the North Pacific Index(NPI) and Southern Oscillation Index (SOI) from 1979 to 1998. Solidlines show 3-year running mean.

Fig. 2. Interannual variations in the locations of the Alaska Current System (AS), Subarctic Current System (SA), Northern Transition Domain(TN), Southern Transition Domain (TS) and Subtropical Current System (ST) of the northern North Pacific during the summers of 1979–1998.Closed circles represent the stations where both hydrographic observations and zooplankton samplings were made, open circles represent hydro-graphic observations only, and open triangles represent zooplankton samplings only.

02 Kobari fbg020 (to/d) 23/4/03 9:29 pm 86

southern sub-areas (Figure 7). No latitudinal patterns wereevident for coefficients of variation in their yearly abun-dance at each station. Analysis of variance (two-wayANOVA) was also performed for the log-transformedprosome length data for the three species in each sub-area(Table II). Year-to-year variations were significant amongthe three Neocalanus species in most sub-areas, and were themost important source of the total variations. The onlyexception in which station-to-station variation exceededyear-to-year variation was observed for N. cristatus in the SA.

Anomaly was positively correlated among the threespecies in the mid-latitude (Figure 4). For their 3-yearrunning means, a weak quasi-decadal oscillation waspronounced in the southern sub-areas. Its negative phase wasduring the late 1980s when T0–150 were positive phase(Figure 3). In the SA, a biennial pattern was observed foranomaly and 3-year running means of N. plumchrus and

N. flemingeri (Run-test, P < 0.05). The biennial pattern meantlarger specimens in odd years and smaller ones in even years.

Correlation analysis with environmentalvariables

Correlation coefficients (Kendall rank) of log-trans-formed C5 abundance and prosome length of eachNeocalanus species with environmental or climatologicalvariables are summarized in Tables III and IV. Inter-annual variation patterns of their abundance were nega-tively correlated with T0–150 in the southern sub-areaswhere abundance was low. Although correlation of theirabundance was statistically significant with some vari-ables, most correlations were weak. Significant correlationof C5 prosome length with those variables was observedfor only two cases. Most correlations were statisticallyinsignificant.


Fig. 4. Interannual variations in anomaly of integrated mean temperature above 150 m depth (T0–150), vertical stability index (STBL) and esti-mated Chl a concentration (CHL) in the five sub-areas along 180° longitude during the summers of 1979–1998. Anomaly was computed from log-transformed data. Solid lines show 3-year running mean.

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D I S C U S S I O N

The best known examples of long-term changes in abun-dance of copepods are those derived from ContinuousPlankton Recorder (CPR) data analysis in the NorthAtlantic and North Sea. There have been consistentdeclines over the 1950s–1990s in C. finmarchicus (Cole-brook, 1985; Fromentin and Planque, 1996; Planque andFromentin, 1996; Reid et al., 1998) and P. elongatus (Cole-brook, 1985, 1986), and steady increases of C. helgolandi-

cus during the same period (Fromentin and Planque,1996; Planque and Fromentin, 1996). These long-termchanges in abundance have been shown to be correlatedwith climatological variables such as North Atlantic Oscil-lation [NAO; basin-scale atmospheric alternation of thepressure field between the Azores High and the IcelandicLow (Mann and Lazier, 1991)] and Gulf Stream Index[GSI, the latitudinal position of the north wall of the GulfStream; (Taylor, 1995)]. Positive NAO results in thehigher sea surface temperature (SST), large advectioninto the North Sea and decline and delay of the springphytoplankton production (Dickson et al., 1988; Planqueand Taylor, 1998), all of which create unfavorableconditions for survival of C. finmarchicus and P. elongatus, but


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N. flemingeri

Table I: The summary results for two-way

ANOVA in the log-transformed C5

abundance of the Neocalanus species

Species Sub-area Source of d.f. SS F value

variation

N. cristatus AS Station 7 0.695 2.566*

Year 11 0.586 1.376

Residual 28 1.083

SA Station 11 0.699 1.210

Year 19 4.123 4.133***

Residual 85 4.463

TN Station 11 0.903 1.177

Year 18 7.203 5.732***

Residual 57 3.979

TS Station 12 0.672 0.646

Year 19 3.296 2.000*

Residual 58 5.029

ST Station 11 1.008 5.013***

Year 19 0.786 2.263**

Residual 99 1.810

N. plumchrus AS Station 7 0.498 0.465

Year 10 4.978 3.255*

Residual 23 3.517

SA Station 11 7.349 2.553**

Year 18 5.148 1.093

Residual 81 21.196

TN Station 11 1.129 0.882

Year 17 5.739 2.903**

Residual 56 6.513

TS Station 12 0.639 0.442

Year 18 5.178 2.389**

Residual 53 6.382

ST Station 11 8.104 3.323***

Year 18 8.249 2.067*

Residual 89 19.730

N. flemingeri AS Station 5 0.238 0.606

Year 9 0.954 1.347

Residual 23 1.810

SA Station 11 3.752 4.658***

Year 17 5.237 4.279***

Residual 79 5.784

TN Station 10 0.518 0.996

Year 16 10.007 12.018***

Residual 49 2.550

TS Station 12 1.336 1.727

Year 17 5.802 5.294***

Residual 50 3.223

ST Station 11 0.052 7.058***

Year 17 0.031 2.722**

Residual 84 0.057

SS, sum of squares; d.f., degrees of freedom; *P < 0.05; **P < 0.01;***P < 0.001.

Fig. 5. Latitudinal changes in abundance of copepodite stage 5 (C5)for N. cristatus, N. plumchrus and N. flemingeri along 180° longitude duringthe summers of 1979–1998. Bars show 1 SD. Broken lines are coefficientof variation (CV %). Open circles denote no occurrence.


favorable conditions for survival and advective supply ofC. helgolandicus populations.

In this study, the time-series data sets of the threeNeocalanus species were analyzed in the hydrographicallydefined sub-areas. In the central North Pacific, weobserved significant interannual variation patterns fortheir abundance. These patterns were characterized by aquasi-decadal signal which was in a positive phase duringthe early 1980s and 1990s and a negative phase duringthe late 1980s (Figure 6). According to the results ofMinobe (Minobe, 2000), a similar quasi-decadal oscilla-tion signal was found for the Pacific Decadal OscillationIndex (PDOI). Positive PDOI means higher sea surfacetemperature in the northern waters of 20°N in the NorthPacific. Its phase was positive during the late 1980s andnegative during the early 1980s and 1990s. Similar quasi-decadal signals were evident for 3-year running means of

some variables in the present study, especially for T0–150.These phases showed an opposite pattern to the abun-dance of Neocalanus copepods (Figures 3, 4 and 6). Thepresent correlation analysis, in which the environmentalvariables were taken into account, showed T0–150 wasnegatively correlated with the abundance of all Neocalanus

species in the southern waters (Table III). These resultsindicate that the yearly patterns of their abundance aredue to the influence of colder water. According toprevious knowledge (Miller et al., 1984; Miller andClemons, 1988; Kobari and Ikeda, 1999, 2001a,b), theirsurface occurrence was limited during the colder season.Considering that among the three species, N. flemingeri wasmost adapted to cold water, our hypothesis could also besupported both by the results of no occurrence in thesouthernmost stations (Figure 5) and by the significantnegative correlation with temperature (Table III).


Fig. 6. Interannual variations in anomaly of abundance of copepodite stage 5 (C5) for N. cristatus, N. plumchrus and N. flemingeri in the five sub-areasalong 180° longitude during the summers of 1979–1998. Anomaly was computed from log-transformed data. Solid lines are 3-year running mean.Open circles denote no occurrence. Species abbreviations (NC, NP, NF) show significant correlation of abundance between the species.

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In the subarctic North Pacific, a biennial signal was alsofound for interannual variations in phytoplankton andzooplankton biomass which were negatively correlated(Shiomoto et al., 1997; Sugimoto and Tadokoro, 1997).Shiomoto et al. (Shiomoto et al., 1997) pointed out that thenegative correlation resulted from the top-down effectfrom pink salmon with biennial patterns of standingstock. Although we could not observe a distinct biennialsignal in the abundance of all Neocalanus species, a statisti-cally negative correlation of abundance with Chl wasfound only for N. plumchrus in the SA. Mackas et al.(Mackas et al., 1998) reported that N. plumchrus made upabout half the mesozooplankton biomass in the AlaskanGyre. Neocalanus copepods were grazing on phytoplankton(T. Kobari et al., unpublished) and important foodresources for pink salmon (Fukataki, 1967). The negativecorrelation might be partly associated with the top-downeffect through trophic cascade from pink salmon.

From a methodological point of view, our abundancedata may have some time-series noises. In the easternsubarctic North Pacific, Mackas et al. (Mackas et al., 1998)showed a yearly shift of seasonal timing (within 60 days)in the annual maximum of zooplankton biomass, whichwas made up largely of N. plumchrus. They suggested thatthe shift resulted from the fluctuation of not only


Table II: The summary results for two-

way ANOVA in the log-transformed C5

prosome length of the Neocalanus species

Species Sub-area Source of d.f. SS F value

variation

N. cristatus AS Station 7 <0.001 1.232

Year 11 0.003 7.353***

Residual 23 0.001

SA Station 11 0.006 9.089***

Year 19 0.008 7.937***

Residual 82 0.005

TN Station 11 0.003 3.187**

Year 18 0.009 7.230***

Residual 54 0.004

TS Station 12 <0.001 0.740

Year 19 0.002 2.707**

Residual 56 0.003

ST Station 11 <0.001 0.507

Year 16 0.003 2.883**

Residual 40 0.003

N. plumchrus AS Station 7 <0.001 0.692

Year 6 0.001 2.724

Residual 14 0.001

SA Station 10 0.001 1.356

Year 19 0.007 8.777***

Residual 74 0.003

TN Station 11 <0.001 1.079

Year 18 0.008 20.614***

Residual 57 0.001

TS Station 12 0.001 2.563**

Year 19 0.004 13.518***

Residual 58 0.001

ST Station 11 0.001 0.720

Year 18 0.005 2.540**

Residual 54 0.006

N. flemingeri AS Station 7 0.001 2.663*

Year 11 0.003 4.860***

Residual 28 0.002

SA Station 11 0.001 0.712

Year 19 0.010 7.800***

Residual 86 0.006

TN Station 11 0.001 2.239*

Year 18 0.009 14.284***

Residual 57 0.002

TS Station 10 0.001 2.068*

Year 18 0.003 3.841***

Residual 48 0.002

ST Station – – –

Year – – –

Residual – – –

SS, sum of squares; d.f., degrees of freedom; –, no data; *P < 0.05;**P < 0.01; ***P < 0.001.

Fig. 7. Latitudinal changes in prosome length of copepodite stage 5(C5) for N. cristatus, N. plumchrus and N. flemingeri along 180° longitudeduring the summers of 1979–1998. Bars show 1 SD. Broken lines denotecoefficient of variation (CV %).

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aria

tion

(%)

3

3.5

4

4.5

Pro

som

e le

ngth

(m

m)

N. plumchrus

0

5

10

15

5

6

7

8

N. cristatus


development rate but also survival rate for N. plumchrus

during surface occurrence. Moreover, seasonal descend-ing into deep waters occurs at C5 [e.g. (Kobari and Ikeda,2000)]. Thus, surface C5 abundance could change withdevelopmental timing and mortality. In this study, therewas no significant correlation of their abundance withmost environmental variables. These results may showthat our time-series data have such time-series noisesdependent on their life history. Unfortunately, we cannotevaluate their possible interannual fluctuations becauseour sampling was carried out once a year.

We also observed two signals that were quasi-decadalin the southern sub-areas and biennial in the SA from theyearly patterns of prosome length (Figure 8). The quasi-decadal signal was opposite to the 3-year running meanof T0–150. On the other hand, the biennial cycle showeda positive correlation with surface Chl a concentrationsreported by Shiomoto et al. (Shiomoto et al., 1997).However, we found no significant correlation coefficientof their prosome length with environmental variables,except for N. cristatus in SA and N. flemingeri in TS. It has

been well documented that temperature and food supplyare important factors affecting the body size of marinecopepods from laboratory experiments (Corkett andMcLaren, 1978; Escribano and McLaren, 1992) and fromseasonal field data analysis (Deevey, 1960; Viitasalo et al.,1995). Actually, it was confirmed that temperature wasthe most important factor affecting the geographical vari-ations in prosome length for Neocalanus copepods (Kobariet al., 2002). Miller et al. (Miller et al., 1992) analyzed inter-annual variations in the prosome length of N. plumchrus

and N. flemingeri in the Gulf of Alaska based on 20-yearrecords (1956–1980). According to their results, a biennialpattern that was in good agreement with ours was evidentfor time-series data of prosome length. However, therewas no significant correlation of prosome length withmost variables. Comparing the different results of thespatial or temporal variations of habitat temperature, therange of the interannual variations was narrower (4°C)than that of the geographical variations (7°C) (Kobariet al., 2002) in the North Pacific. No significant correlationsuggests that the range of variations of these two factorswas too narrow to affect the interannual size variations.

From the present results of both abundance and bodysize for Neocalanus copepods, it was evident that the


Table III: Correlation coefficients (Kendall

rank) between anomalies of C5 abundance

of each Neocalanus species and

environmental or climatological variables in

different sub-areas

Sub-area Species T0–150 STBL CHL NPI SOI

AS NC –0.091 –0.455 –0.061 0.667*** 0.121

NP 0.091 0.152 –0.242 0.061 –0.182

NF –0.182 0.121 –0.091 0.030 0.030

SA NC –0.137 –0.136 –0.074 –0.137 –0.147

NP 0.074 –0.084 –0.621*** 0.011 –0.232

NF –0.200 –0.168 –0.242 –0.242 –0.105

TN NC –0.193 –0.029 0.216 –0.041 –0.088

NP –0.240 0.041 –0.205 –0.205 –0.041

NF –0.287 0.111 –0.158 –0.439** –0.135

TS NC 0.221 –0.074 0.032 0.221 –0.189

NP 0.158 0.368* –0.137 0.053 –0.105

NF –0.516** –0.074 –0.284 –0.179 –0.232

ST NC –0.440** 0.239 –0.164 0.027 –0.101

NP –0.505** 0.274 –0.032 <0.001 –0.095

NF –0.343** 0.165 –0.096 –0.137 0.137

AS, Alaska Current System; SA, Subarctic Current System; TN, NorthernTransition Domain; TS, Southern Transition Domain; ST, SubtropicalCurrent System. NC, N. cristatus; NP, N. plumchrus; NF, N. flemingeri;T0–150, integrated mean temperature above 150 m depth; STBL, verticalstability index; CHL, chlorophyll a concentration estimated from Secchidepth; NPI, North Pacific Index; SOI, Southern Oscillation Index. Asterisksshow significant correlation coefficients: *P < 0.05; **P < 0.01; ***P <0.001.

Table IV: Correlation coefficients (Kendall

rank) between anomalies of C5 prosome

length of each Neocalanus species and

environmental or climatological variables in

different sub-areas

Sub-area Species T0–150 STBL CHL NPI SOI

AS NC –0.091 –0.152 0.364 –0.121 0.182

NP –0.056 0.278 –0.111 –0.111 0.278

NF 0.091 –0.091 –0.121 –0.121 0.182

SA NC –0.158 0.211 0.326* –0.137 0.111

NP –0.021 0.221 0.168 –0.126 0.074

NF –0.021 0.095 0.274 –0.126 –0.011

TN NC –0.228 0.170 0.088 –0.029 0.088

NP –0.158 0.240 –0.029 –0.146 0.088

NF 0.006 0.076 0.064 0.064 –0.029

TS NC –0.221 0.011 0.011 0.116 –0.168

NP 0.074 –0.137 0.158 0.053 <0.001

NF –0.427* –0.146 0.263 0.205 –0.064

ST NC –0.206 –0.015 0.162 –0.015 0.235

NP –0.053 0.240 –0.240 0.076 –0.099

NF – – – – –

Abbreviations as in Table III. Asterisks show significant correlationcoefficients: *P < 0.05; **P < 0.01; ***P < 0.001. –, no data.


quasi-decadal signal was predominant in the southernsub-areas and became weak towards northern sub-areas(Figures 6 and 8). Corresponding to the latitudinalpatterns, a biennial signal appeared for body size in thenorthern waters. Although there were the regional differ-ences of the predominant signal, significant covariationsamong the three species were found for yearly patterns oftheir abundance and body size around mid-latitude,where Neocalanus copepods were abundant. In general,they have identical ecological properties, which are anannual life cycle with a large ontogenetic vertical migra-tion (Miller et al., 1984; Miller and Clemons, 1988), anoverlapped surface growing phase during the cold waterseason (Kobari and Ikeda, 1999, 2001a,b) and accumu-lation of a large amount of lipid (Evanson et al., 2000;Tsuda et al., 2001). These results suggest that yearlypatterns of their abundance and body size are mediated

by common environmental force(s) with some spatial andtemporal scales in the North Pacific.

AC K N OW L E D G E M E N T S

We thank K. Tadokoro for providing us with time-seriesdata. We are grateful to D. Mackas for reviewing earlydrafts. Thanks are extended to the captain, crew andcadet students of T/S ‘Oshoro-Maru’ for their help infield samplings over 20 years.

R E F E R E N C E SAnma, G., Masuda, K., Kobayashi, G., Yamaguchi, H., Meguro, T.,

Sasaki, S. and Ohtani, K. (1990) Oceanographic structure andchanges around the transition domain along 180° longitude, duringJune 1979–1988. Bull. Fac. Fish. Hokkaido Univ., 41, 73–88.


-0.04

0

0.04

N. cristatus N. flemingeriN. plumchrus

-0.04

0

0.04SA

-0.04

0

0.04

An

om

aly

TN

-0.04

0

0.04TS

-0.04

0

0.04

19

76

19

80

19

84

19

88

19

92

19

96

20

00

ST

19

76

19

80

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84

19

88

19

92

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96

20

00

Year

19

76

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88

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00

AS

NC, NPNP, NF

NC, NF

NC, NP

NP

NP, NF NC, NF

NC, NF

NP

Fig. 8. Interannual variations in anomaly of prosome length of copepodite stage 5 (C5) for N. cristatus, N. plumchrus and N. flemingeri in the five sub-areas along 180° longitude during the summers of 1979–1998. Anomaly was computed from log-transformed data. Solid lines denote 3-year runningmean. Species abbreviations (NC, NP, NF) show significant correlation of prosome length between the species.


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Received on July 15, 2001; accepted on December 30, 2002



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