Variations in the distribution, abundance, and development of copepods in the southeastern Bering Sea in 1980 and 1981

ContinentalShelfResearch,Vol.5, Nos 1/2,pp. 215 to 239, 1986.

0278-4343/86$3.00+ 0.00 © 1985PergamonPressLtd.

Printedin GreatBritain.

V a r i a t i o n s in t h e distribution, a b u n d a n c e , a n d d e v e l o p m e n t o f c o p e p o d s in the s o u t h e a s t e r n Bering S e a in 1 9 8 0 a n d 1 9 8 1 SHARON L. SMITH* a n d JULIO VIDAL* t

(Receivedfor publication 28 January 1985) Abstraet--When a relatively warm year (1981) in the southeastern Bering Sea is compared with a cooler year (1980), the upper layer of both the middle shelf, and outer shelf warmed at a faster rate in the warmer year, but the spring bloom of phytoplankton took place at approximately the same time both years. The middle front near the 100 m isobath separated the two major communities of zooplankton both years. Offshore of the front, large calanoid copepods such as Neocalanus plumchrus, Neocalanus cristatus, Eucalanus bungii, and Metridia pacifica dominated, while inshore of that front Pseudocalanus spp., Acartia spp., and Calanus marshallae dominated. Over the outer shelf (Sta. 5) at the end of April, N. plumchrus, N. cristatus, E. bungii, and Pseudocalanus spp. were significantly more abundant in 1980 than in 1981, while over the middle shelf (Sta. 12) all stages of Pseudocalanus spp. and C. marshallae were more abundant in 1981 than in 1980. Gradients in abundance of N. plumchrus and N. cristatus across the outer shelf reversed after periods of wind favourable to subsurface onshore flow suggesting that the shelf population of large calanoids is derived from overwintering slope populations during spring and summer storms. N. plumchrus and C. marshallae, which were thought to reproduce once per year based on 1980 data, produced two cohorts at some stations in 1981, and both E. bungii and C. marshallae reproduced earlier in 1981 than in 1980. Survivorship of N. plumchrus and N. cristatus over the outer shelf (Sta. 5), where only one cohort was produced both years, was higher in 1981 than in 1980, suggesting that predation occurred later in 1981 than in 1980. The abundance of the chaetognath Sagitta elegans over the middle shelf was higher in 1980 than in 1981 suggesting that both increased temperature and reduced predation may account for the larger numbers of small copepods found over the middle shelf in the warmer year.

INTRODUCTION

THE annual cycles of atmospheric variation and sea-surface response in the southeastern Bering Sea have been analyzed for the period 1963 to 1981 (NxEnAUER, 1980, 1981, 1983), and the extremes in warming and cooling trends are apparent. The warmest period was 1966 to 1967 when sea-surface temperature was on average 3.6°C above the mean in April, and the coldest period was 1975 to 1976 when temperatures were 2.3oC below the mean in April (NIEBAUER, 1980, 1983). The coldest period also had above average ice-cover (15%) and above average winds from the north (NIEBAUE~ 1983). Because winter cloud cover and wind were correlated with year-to-year changes in sea-surface temperature, NIEBAUER(1981) concluded that atmospheric circulation in winter was the major factor determining temperature and ice conditions in the southeastern Bering Sea. Both 1980 and 1981 were in the intermediate to warm end (+ 1.0 and +1.8°C, respectively) of the range of mean sea-surface

* Oceanographic Sciences Division, Brookhaven National Laboratory, Upton, NY 11973, U.S.A. t Present address: 9 Block Blvd., Port Jefferson Station, NY 11776, U.S.A. 215

216

s.L. SMITHand J. VIDAL

temperatures (-2.3 to +3.6°C) observed in April (NIEBAUER, 1983). The contrast between 1980 and 198 l, however, should be sufficient to detect changes in the plankton that might be related to temperature since 1981 was similar to 1979, the last year of a 3-year period of warming (NIEBAUER,1983), and 1980 was on average at least 1°C cooler. A number of assessments of year-to-year variations in biological characteristics of the southeastern Bering Sea have led to conclusions that general cross-shelf patterns in chlorophyll a and seasonal succession in species of phytoplankton were similar, at least in 1978 and 1979 (IVERSONet al., 1979), and that species assemblages of zooplankton over the middle and outer portions of the shelf and shelf break were similar (MOTODAand MINODA, 1974; IVERSON et aL, 1979; COONEY, 1981). Biomass of zooplankton over the shelf break has been reported to vary between 0.02 g dry wt m -3 in May 1977 (CoONEY, 1981) to 0.24 g dry wt m -3 in May 1980 (VIDALand SMITH, 1985). Caution is necessary in drawing conclusions based on data collected in May, hawever, since it is a month of rapid change in biomass over the outer shelf and slope as the large calanoid species migrate out of the surface layer at this time. The range in biomass of large calanoids observed during May 1980 over the slope was 0.12 to 0.21 g dry wt m -3 (VIDAL and SMITH, 1985). In terms of the zooplankton of the southeastern Bering Sea, interannual differences in biomass, running in approximately 3-year cycles and with variations of 4-4096, have been observed (MoTODAand MINODA,1974). In an earlier paper we suggested that the weather prevailing over the continental slope and Aleutian Basin during February and March was critical to the absolute abundance and onshore gradients in the large-bodied copepods of the outer shelf and that over the middle shelf, abundances of some taxa were highly correlated with temperature (SMITH and VIDAL, 1985). Since our study of zooplankton in the southeastern Bering Sea included a relatively cold and stormy spring (1980) and a warmer, more stormfree spring (1981), we can evaluate the importance of these two climatic variables influencing the distribution, abundance, and life cycles of the dominant species of copepods. In this paper we will compare abundances and development of the dominant taxa of copepods over the middle shelf and outer shelf and slope in spring and summer of 1980 and 1981, relating any significant differences observed to variations between years in weather, temperature, and food availability. MATERIALS AND METHODS

Data used in this study were collected during the 1980 and 1981 field seasons of PROBES (Processes and Resources of the Bering Sea shelf), from 24 March to 6 June 1980, 11 April to 20 July 1981, and 3 to 15 October 1981. The standard PROBES' transect consisted of 19 stations spaced 22 km apart, extending from the slope (~1500 m) to the inner shelf (~50 m isobath). Stratified samples of zooplankton were collected at five standard stations (Fig. 1) using a multiple opening-closing net system in spring and summer (MOCNESS; WIEBEet al., 1976) and Puget Sound nets in October; both were fitted with 149 ttm mesh nets. The sampling intervals were 1200 to 600, 600 to 300, 300 to120, 120 to 80, 80 to 60, 60 to 40, 40 to 20, and 20 to 0. Collections were split at sea, with 50% preserved in 5% neutral formalin, and returned to the laboratory for analysis of species composition and age-structure. Remaining fractions were washed onto filters for dry weight (20%) or given to collaborating investigators (20 and 10%). In 1980, all copepodid and adult stages of the major herbivorous copepods that were captured quantitatively were counted (Neocalanus plumchrus, Neocalanus cristatus, Pseudocalanus spp., and Calanus marshallae); for other copepod

Distribution,abundance,and development of copepods in the SE BeringSea I

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species (Eucalanus bungii, Metridia pacifica, Acartia spp.), copepodid, adult males, and adult females were counted. In 1981, copepodid stages of all seven taxa were counted if they were captured quantitatively. Additional details as well as the results of the quantitative analyses of the samples were reported elsewhere (SMITH et al., 1982, 1983; VIDAL and SMITH, 1985). Approximately once each 3 weeks we occupied a 24-h station at each of the five main locations of sampling. Full sets of stratified samples were collected five times in a 24-h period, and each set was preceded and followed by a CTD cast. The local times of the collections were 0300, 0900, 1500, 1900, and 2300 h. Because sampling extended to within a few meters of the bottom, we use these sets of samples as replicates in estimating the mean abundance in the water column of various taxa of zooplankton. Statistical comparisons among abundances were made with log-transformed data, while mean abundances given are arithmetic (CASsm, 1968). Dry weights of specimens preserved in a 5% formalin-seawater solution were measured using a Cahn Microelectrobalance. Several individuals of a single species and particular stage of development were sorted from preserved samples, rinsed with distilled water, transferred to preweighed aluminium boats, and dried in a drying oven at 40 to 5 0 ° 0 for at least 24 h before

218

S.L. SMITHand J. VIDAL

the dry weight determinations. A mean loss of 40% of dry weight because of preservation in formalin has been assumed (VIOAL and Sin'H, 1985). Profiles of salinity and temperature were obtained at all stations using a Neff Brown Mark III C T D surrounded by a small rosette sampler, and the data were processed according to COACHMAN and CHARNELL (1979) and reported by NIEBAOER et aL (1982a, b). Mean temperature over the upper 20 m was estimated by trapezoidal integration. Chlorophyll a was measured by extracted fluorescence (STRICKLANDand PARSONS, 1972) on samples collected by the small rosette during the upcast of the CTD; samples were filtered through Gelman G F / A glass fiber filters and processed immediately. The results have been reported elsewhere (NIEBAUER el aL, 1982c). Samples for analyses of nutrients were collected by the rosette also, and taken from the same bottles as for Chl a. Methods (WHITLEDGEet al., 1981) and results (NIEBAUER et al., 1982a, b) were reported elsewhere. RESULTS Hydrography

The regressions relating mean temperature in the upper 20 m (I'0-2o) and time for the 1980 data showed that the rates of warming of the upper layer over the middle shelf and outer shelf were identical, but that the intercepts differed due to the subzero temperatures at Sta. 16 in March (Table l). In 1981, however, the upper layer of the middle shelf warmed at a faster rate than that of the outer shelf and slope (Table 1). Over the middle shelf, the slopes were significantly different (t59 = 16.394; P ~< 0.01) between years, suggesting that in 1981 the upper layer at Stas 12 and 16 warmed at a faster rate than in 1980. The intercepts were also significantiy different (t59 = 9.426; P ~< 0.01). When all of the data at Stas 1 and 5 are analyzed in a similar manner, the slopes are significantly different (t56 = 9.566; P x< 0.01) between years, with the rate of warming in the upper layer in 1981 faster than that in 1980. Thus, over both the outer shelf and slope and the middle shelf, the rate at which the upper layer warmed in 1981 was significantly faster than the warming rate in 1980. When we plotted To-20 against time, it was clear that the early subzero temperatures at Sta. 16 in 1980 were very important in determining the slope of the regression. We recomputed the regressions for both domains in 1980 and 1981 using only the interval in which 1"0-20 data were collected in both years (10 April to 4 June). The differences in the slopes of the regressions between years were significant in both the middle shelf (t23 = 2.161; P ~< 0.05) and outer shelf and slope domains (t33 = 3.400; P < 0.01). In both domains the slopes were greater in 1981 compared with 1980, Table 1. Regressions of mean temperature in the upper 20 m against time

Year

Location

Regression

N

r2

Comment

1980 Middleshelf

1"o-2o= 0.03 (Julian Day) - - 1.576

63

0.801 All data

1980 1981 1981 1980

Outershelf and slope Middleshelf and slope Outershelf and slope Middleshelf and slope

~'o-,2o= 0.03 (Julian Day) To_2o = 0.08 (Julian Day)-- 6.308 To_2o = 0.06 (Julian Day)-- 2.692 TO_2O= 0,06 (Julian Day) - - 5.192

51 61 58 50

0.808 0.956 0.936 0.851

1980 Outer shelfand slope 1981 Middleshelfand,slope

_To-2o= 0.04 (Julian Day) - - 1.174 To_2o= 0.07 (Julian Day) - - 5.010

41 25

0.867 10 April-4 June 0.803 10 April--4June

1981 Outershelf and slope

7"o-2o= 0.05 (Julian Day) - - 1.496

35

0.752 10 April--4June

All data All data All data 10 April--4June

Distribution, abundance, and development of copepodsin the SE BeringSea

219

indicating that the upper layer in April to June warmed at a faster rate in 1981. The intercepts of the regressions for the 10 April to 4 June period were not significantly different between years in either domain. We also compared the slopes of the regression for the middle shelf in 1981 with that of the outer shelf and slope. The rate of warming of the surface layer over the middle shelf in 1981 (l I April to 20 July) was significantly faster than that over the outer shelf and slope in the same time interval (t59 ~ 6.936; P ~< 0.01). In 1980 however, the slopes of the regression for each domain were the same (0.03), indicating rates of warming of the surface layer were identical in the two domains in 1980. The onset of the spring bloom of phytoplankton over the middle shelf (Stas 12 and 16) was later in 1981 than in 1980, and because the bloom terminated at essentially the same time both years, the duration of the bloom was shorter in 1981 (Table 2; details of the development of the spring bloom at Sta. 12 can be found in SAMBRoa-ro et al., 1986). Over the outer shelf (Sta. 5) the timing and duration of the spring bloom was similar in 1980 and 1981 (Table 2). In 1980 over the slope (Sta. 1) there was a suggestion of two blooms, which in 1981 clearly occurred, with the first peak of Chl a in 1981 lasting only about half as long as the first peak in 1980 (Table 2). In both 1980 and 1981 the bloom had its longest duration at Sta. 8 where it showed the earliest onset (Table 2). Station 8, at the 112 m isobath, is in an area of the shelf where mixing between two water masses is taking place. Water originating from the outer shelf and slope spreads over the bottom, while the upper part of the water column arises from the middle shelf (S~irrn and VIDAL, 1985). This mixing may prolong the spring bloom in the vicinity of this station. Over the middle shelf, the spring bloom was not dependent on temperature since in 1980 the peak in Chl a was at approximately ~ro_2o= 2°C while in 1981 the peak was observed at To-20 --- 4.5 °C. Over the outer shelf (Sta. 5), the bloom reached similar concentrations of Chl a (,~10 mg m -a) in 1980 and 1981, while over the middle shelf mean standing stocks during the bloom in 1980 were nearly twice those of 1981 (Table 3). A comparison of mean temperature, nitrate, and Chl a in the upper 20 m during the interval sampled in both years suggests that the bloom may have been more intense in 1980 compared with 1981 (Table 3; see also CODISPOTXet al., 1986). Over both the middle shelf and the outer shelf, nitrate concentrations at the surface in late April (prior to the bloom) were higher in 1980 than in 1981 (Table 3). During the bloom there were no significant differences in nitrate or Chl a between Table 2. Dates of onset and termination of the spring bloom of phytoplankton in 1980and 1981

1980

Station

Bloomonset

Bloomtermination

Duration

l

16April 29May 26April 10April 25April 30April

20May ? 28May 28May 28May 25May

34 ? 32 48 33 25

2~ April 26 June 20 April 18 April 5 May l0 May

I l May 17 July 28 May 30 May 29 May 30 May

18 2l 38 42 24 20

5 8 12 16 1981

! 5 8 12 16

220

S.L. SMITHand J. VIDAL

Table 3. Mean concentrations of nitrate and chlorophyll a in the upper 20 m of the middle shelf and outer shelf in 1980 and 1981 1980 Middle shelf, prior to bloom Temperature, 0-20 m, °C Nitrate, 0-20 m, laM Chl a, 0.20 m, mg m-3 Middle shelf, during bloom Temperature, 0-20 m, °C Nitrate, 0.20 m, ~tM Chl a, 0-20 m, mg m-3 Outer shelf, prior to bloom Temperature, 0-20 m, °C Nitrate, 0.20 m, BM Chl a, 0-20 m, mg m-3 Outer shelf, daring bloom Temperature, 0-20 m, °C Nitrate, 0-20 m, p.M Chl a, 0-20 m, mg m-3

1981

0.97 _+0.37 (19)* 15.22 _+0.90 (19) 2.87 + 1.37 (19)

3.04 _+0.42 (15)t 11.42 + 0.99 (15)t 1.37 _+0.49 (15)

2.22 + 0.97 (30) 4.17 _+4,59 (30) 9.51 + 5.70 (30)

5.06 + 1.05 (10)f 2.21 + 2.19 (10) 5.71 + 5,92 (9)

3.41 + 0.11 (12) 21.12 + 0.47 (12) 0.96 + 0.79 (12)

4.00 _+0.13 (2)t 12.51 _+ 1.85 (2) 0.87 _+0.11 (2)

4.59 + 0.72 (14) 3.18 + 4.88 (12) 6.27 _+3.21 (12)

4.71 + 0.71 (21) 6.79 + 3.74 (20) 6.55 + 2.04 (20)

* N is in parentheses. f Significant difference between years at P = 0.01.

years implying that whatever additional production was realized due to higher initial nitrate concentrations in 1980, it was not observed as increases in the standing stock of phytoplankton in either the outer shelf or the middle shelf domain.

Distribution and abundance o f zooplankton Sampling o f the five main stations for zooplankton in 1981 was more even than in 1980, and although the main features o f population structure found in 1980 were repeated in 1981, the patterns o f abundance and distribution for some species differed substantially between the two years. We found that in 1980 Oithona spp. was rather evenly distributed across the shelf while in a similar period of time in 1981, i.e., April to early June, Oithona spp. was observed in elevated abundance more frequently at Stas 1 and 5 (Fig. 2). Chaetognaths, which had two peaks in abundance in 1980, were observed at high concentrations primarily at Stas 1 and 12 in 1981 and were not found to exceed 1 0 m -a at Stas 5, 8, and 16 in the spring to early summer period (Fig. 2). Stages CV and C I I + C I I I of Pseudocalanus spp., which occurred most frequently in elevated abundance at Sta. 5 in 1980, followed by Stas 8 and 12, showed two distinct peaks in 1981 centering on Stas 5 and 12 in 1981 (Fig. 2). The distributions o f t h e large-bodied taxa of the outer shelf, N. plumchrus, N. cristatus, and E. bungii, in March to June 1980 were similar to those of April to early June 1981 (Fig. 3) in that these taxa were restricted to the outer shelf and slope (Stas 1, 5, and 8). However, in 1980 stage CV of N. plumchrus and N. cristatus occurred more frequently in elevated abundance at Stas 5 and 8 while in 1981 N. plumchrus CV was most frequently found in high abundance at Sta. 5, and the peak in frequency o f N . cristatus was at Sta. 1 (Fig. 3). Copepodids o f E . bungii occurred most frequently in elevated abundance at Sta. 1 in both years, and the frequency distributions of copepodids of M. pacifica showed the highest frequency at Sta. 5 in both years (Fig. 3). o n e o f the most striking differences between 1980 and 1981 was in the distribution of C. marshallae. In 1980 stages CIV and CV of this species were found primarily over the

I

5

8

I2

I6

1980#=125 198lN=47 0; thona spp >5OO/m3

STATIONS

0

80

I 5 8

I2

1980 N = 50 1981 N = I4 Choetoam _ >IO/mJ

16

l980N = 50 198lN =69 Pseudocalonuh C2+C3 >50/m3 I

. - ._ -- - . - _ .^

-

-

I

5

C > IO/m3

81216

0

80

STATIONS

1980 N = 147

M. pocifico

1980 N = 86 1981 N=37

c

l-l

20

40

‘;; 6 80

spp. > 20/m3 N= 58 N=IO

N. plumchrus Cl! > IO/m3

1980 1981

Acortio

1981

1980

_

I

CE + Cp >5/m3

I

5

8

I2

I6

q

l980N =55 1981 N I2

E. bunqii C > l/m3

N. cristotus CP >I /m3

r-7

C. morsholloe

-

._I . - -. _ ._ _.

--

----..

Fig. 3. Frequency of collection of various taxa at specified levels of abundance in 1980 and 1981. The level of abundance is indicative of the relative abundance of the taxa, and the number of samples gives a general impression of overall abundance between years.

. - -- ._ -. _

Fig. 2. Frequency of collection of various taxa at specified levels of abundance in 1980 and 1981. The level of abundance is indicative of the relative abundance of the taxa, and the number of samples gives a general impression of overall abundance between years.

E40

;f

z

>50/m3

1980N=40 1981 N =43 Pseudocolonut spp Cy

0

40

80

C2

m

._

222

s.L. SMITH and J. VIDAL

middle shelf (Stas 12 and 16) while in the same period of 1981 they were found at all stations (Fig. 3).

Zooplankton over the outer shelf and slope Abundance. At the onset of the spring bloom over the outer shelf, Sta. 5 was occupied five times in 24 h on 18 to 19 April 1980 and 25 to 26 April 1981. Mean abundances of the life stages of numerically dominant species of copepod in the 2 years have been compared, and when significant differences occurred, all taxa except adult Acartia spp. were significantly more abundant in 1980 (Table 4). The abundances of N. plumchrus, N. cristatus, E. bungii, and Pseudocalanus spp. were greater in 1980, while abundance of M. pacifica was not significantly different between years. Peaks in the abundance ofN. plumchrus, N. cristatus, and Pseudocalanus spp. were observed in April 1980, while in 1981 the peak in Pseudocalanus spp. was observed in June (Fig. 4). In both years peaks in abundance of M. pacifica > 200 per cubic meter were observed in May, and in 1981 also in June. The pattern in abundance of the large-bodied hervibore N. plumchrus in the upper 120 m over the slope (Sta. 1) in spring 1981 was similar to spring 1980. On 21 April of both years abundance was between 135 and 155 m -a, and by early June of both years abundance was reduced to 20 to 30m -3. The peak abundances in the upper 120m over the slope (,~24,000 m -2) are similar to those observed in the upper 100 m of the subarctic North Pacific (--,28,000 m-:), but they were observed about one month earlier (April) in the Bering Sea compared with the North Pacific (May; MILLERet al., 1984). The extended sampling in 1981 showed a second peak in abundance in June (Fig. 5) which was composed of all copepodid stages (Fig. 6). Our sampling over the slope in October 1981 revealed that copepodid stage I Table 4.

Mean abundances o f selected taxa collected in the upper 120 m at Sta. 5 in late April o f 1980 and 1981

Taxon Acartia spp. C* A cartia spp. AMF Pseudocalanus spp. CII+III Pseudocalanus spp. CIV Pseudocalanus spp. CV Pseudocalanus spp. ~ 9 Neocalanus plumchrus CI Neocalanus plumchrus CII Neocalanusplumchrus CIII Neocalanus plumchrus CIV Neocalanus plumchrus C V Neocalanus cristatus CI Neocalanus cristatus CII Neocalanus cristatus CIII Neocalanus cristatus CIV Neocalanus eristatus CV Eucalanus bungii C Metridia paeifica C Oithona spp.

1980 abundance (number m -3)

1981 abundance (number m-3 )

t (6 d.f.)

5.4 0 175.2 86.3 72.9 44.6 93.1 69.0 93.1 61.0 4.0 0 2.8 10.8 4.7 O. 1 0.2 104.6 1055.6

1.9 0.9 32.6 20.2 29.5 20.2 8.9 9.4 18.2 23.8 1.2 0. I 0 0.3 0.3 0 O. 1 109.7 506.0

0.945 5.261 "l" 2.888t 2.791 t 1.872 1.960 4.619t 4.036t 3.35 I t 1.801 1.008 0.973 3.784t 5.861 f 0.002 2.526t 2.621 t 0.801 !.917

* Notations are: C, all copepodids combined; AMF, adult males and females combined; CI, copepodid stage I; CII, copepodid stage II, and so forth. t Difference is significant at P ~< 0.05.

Distribution, abundance,and development of copepods in the SE Bering Sea

223

1981

1980

500 o Metridia pacifica • Pseudocalonus spp.

x Eucolonus bun~

400

A Neocaianus plumchrus Neocolanus cristatus

0. 300

z 200 W

IOO

--/!

-IAPff, L I MAY I

"[ ~AY I 0o7~ I ~o1¥

STATION 5

Fig. 4,

Mean (_+ 1 S.D.) abundance of the five taxa that dominated the biomass of zooplankton over the outer shelf (Sta. 5) in 1980 and 1981.

o 1980 • 1981

200I

='=" ,ooI z= oL Fig. 5.

Abundance of Neocalanus plumchrus in the upper 120 m over the slope (Sta. 1) in 1980 and 1981.

of N. plumchrus was still present in the upper 120 m, as were all other copepodid stages, but all adult males and females and more than 78% of all stage CV were below 300 m. At Sta. 5 over the outer shelf, where the population of N. plumchrus showed no sign of additional reproduction in June and July (Figs 4 and 6), the N. plumchrus population in October was small (]¢ = 4 m -3, N = 4) and was primarly copepodid stages III and IV (63%). Another large-bodied, primarily herbivorous copepod, N. cristatus, showed the same patterns as N. plumchrus. At Sta. 1 over the slope a second peak in abundance was observed in June and July. The October sampling at Sta. 1 over the slope showed virtually no copepodids of N. cristatus younger than stage IV in the upper 120 m; more than 88% of the population was stage CV. In October over the outer shelf(Sta. 5) there was an occasional N. cristatus in the water column, but mean abundance of all stages was 0.2 m -3 (N = 4). Growth and development. The development of N. plumehrus at Sta. 1 began earlier in 1980 than in 1981. In 1980 at Sta. 1 the population was 5096 stage CIII on approximately 15

224

s.L. SMITH and J. VIDAL

iO0

>. 8 0

1980 J 3

20

STATION I

STATION 5

STATION 8

1981

STATION I

Fig. 6.

STATION 5

STATION 8

Age-structure of Neocalanusplumchrus over the slope (Sta. 1) and outer shelf Stas (5 and 8) in 1980 and 1981.

April, while in 1981 the 50th percentile occurred on 23 April (Fig. 6). For stage CV, the 50th percentile was observed on 25 May 1980 and on 15 June 1981. The time that elapsed between peaks in abundance of stages CIV and CV was approximately 30 days both years. At Sta. 5, the population was 50% stage CIV on 26 April 1980 and on 1 May 1981, and 50% stage CV on 5 May 1980 and 14 May 1981 (Fig. 6). The time that elapsed between peaks in abundance of stages CIV and CV in 1980 and 1981 at Sta. 5 was approximately 35 days, or somewhat more than that at Sta. 1. In mid May of 1981, the abundance of stage CV o f N . plumchrus in the upper 300 m at Sta. 1 was 2978 m -2, and 3038 m -2 in the upper 1200 m; of the 0 to 1200 m population of stage CV, 65% were collected in the upper 40m. By 31 May 1981, the population in the upper 300 m was 2976 m -2, and over the upper 1200 m was 4026 m -2, with 81% of the population of CV's between 1200 and 600 m and 26% between 300 and 600 m. This shift in depth of the bulk of the stage CV's suggests a growth cycle ofN. plumchrus that was completed by late May, just as it was in 1980 (VIDAL and SMITH, 1985). Furthermore, males began to be collected below 120 m in late May, just as they had been in 1980. Until the end of May the life cycles ofN. plumchrus in 1980 and 1981 are similar to each other and to the chronologies described for this species by others (HEINRIC., 1962; FULTON, 1973; NAUMENKO, 1979). N. plumchrus was thought to have a single growth cycle per year which was completed by early June. However, in late June of 1981, 77% of the population of stage CV occurring between the surface and 1200 m at Sta. 1 were located in the upper 40 m (131 m-3), and adult males and adult females were collected in the upper 60 m as well as below 300 m. Whether this second period of reproduction by N. plumchrus over the slope is a

Distribution, abundance,and development of copepodsin the SE BeringSea

225

regular feature of the life cycle or was induced by the generally warm and calm conditions prevailing in 1981 is unknown. During spring the development of N. plumchrus over the slope in the Bering Sea is somewhat ahead of that of N. plumchrus in the subarctic North Pacific (I~LLER et al., 1984). While copepodid stages I, II, and III are most abundant in late April in the Bering Sea, they were most abundant in mid May in the North Pacific (MILLERet aL, 1984). In both areas, however, the spring pulse of copepodids have reached their maximum abundance as stage CV's, or completed their development, by late June. Although we observed a second group of copepodids in June and July in the Bering Sea (Figs 5 and 6), no similar second spawning in summer was observed in the North Pacific (MILLERet al., 1984). At the present time there is confusion concerning the identity of N. plumchrus in the North Pacific (C. B. I~LLER, personal communication). Based upon Miller's preliminary observations concerning the two potential species that may have been lumped as N. plumchrus, we have re-examined our samples from May, June, and July 1981 over the slope. The second group of copepodids observed in July are, as far as can be determined presently, properly called N. plumchrus. The development ofN. cristatus at Sta. 1 in 1980 was also earlier than in 1981. The population of N. cristatus was 50% stage CIII on 8 April 1980 and on 29 April 1981. For stage CIV, the 50th percentile was observed on 20 April 1980 and 17 May 1981. At Sta. 5, however, N. cristatus showed an age-structure in 1981 that was nearly identical to 1980. The population was 50% stage CIV on 27 April 1980 and 26 April 1981, and 50% stage CV on 22 May 1980 and 27 May 1981. In mid May of 1981, 41% of the stage CV's were between 120 and 300 m, a stratum where adult males were also collected. Since the average dry weight of these CV's was 5084 Bg (+206; N = 3) downward migration ofN. cristatus was underway in mid May. In late May 26% of the stage CV's were in the upper 40 m and 47% were still between 120 and 300 m, with adult males between 80 and 120 m. It was mid June before stage CV of N. cristatus was primarily (58%) near the surface, between 20 and 60 m. N. cristatus was rarely collected in the upper 20 m. In 1981 N. cristatus also exhibited secondary peaks in overall abundance and early copepodids in mid June, but the peaks were less pronounced and of shorter duration than for N. plumchrus. A second reproduction may have taken place over the slope, in which case its link with temperature between years is also unknown. The presence of N. cristatus in the upper 120 m until later in the season both years is consistent with its slower growth and development. Although advection is a possible reason for the second peaks in abundance of N. plumchrus and N. eristatus in 1981, it is less likely than additional reproduction. Water movement in mid June of 1981, when the additional peaks were observed, was similar to that of early June 1980 when no additional copepodids were seen. If advection were the primary cause of variation in N. plumchrus and N. eristatus at Sta. 1, it should have acted in the same way both years, which it did not. The greatest differences in the development ofN. plumehrus and N. eristatus between years was observed at Sta. 1, the presumed source of the population over the outer shelf. Development was completed somewhat earlier in the cold year of 1980, although the duration of stage CIV was similar both years. Therefore, the difference in the dates at which various stages were observed in the upper layer over the slope is probably a function of the time at which the earliest stages reached the surface in spring. In October early copepodids of N. plumchrus were in the upper water column, suggesting ongoing reproduction, while early copepodids of N. cristatus were not. The development of N, cristatus over the slope in the Bering Sea is at odds with the description of the life-cycle of N. cristatus in the North Pacific where a new

226

s.L. SMITH and J. VIDAL

pulse of young copepodids appeared in autumn with a peak in mid winter (MILLER et aL, 1984). The dry weights of stage V copepodids of N. plumchrus captured in the upper 20 m over the slope (Sta. 1) during development of the first cohort in May were similar to those of individuals captured in the upper layer in late June (Table 5). The dry weights indicate that the N. plumchrus CV's captured over the slope in late June were a second cohort which was developing. If the cohort of stage CV's there in May was simply remaining at the surface adding oil during June, the average dry weight in June should have been much higher than it was. At Sta. 5, on the other hand, where no additional reproduction was apparent, stage CV of N. plumchrus was heavier by a factor of two in July compared with May (Table 5) suggesting the single cohort apparent there in April and May continued to add weight during June. Similarly, in July at Sta. 1, stage CV of N. cristatus weighed the same as CV's captured in May indicating additional spawning, while at Sta. 5 stage CV's in July weighed four times what they weighed in May (Table 5). The development of the annual cohort of E. bungii began approximately 2 weeks earlier in 1981 compared with 1980 ( Fig. 7). In late May of 1980 the population was 20 to 4096 adults that had developed from the overwintering stock while in late May of 1981 virtually no adults from the overwintering stock remained and the population was already 80% copepodid stages I and II (Fig. 7). E. bungii reached the surface over the slope later than N. plumchrus and N. cristatus in both years, and became abundant in the upper 120 m during the spring bloom. The peak in abundance observed over the slope in 1981 (200 m -a) was much higher than that in 1980 (15 m-3), perhaps indicating an enhancing effect of the warm year on reproduction and growth of this species. The abundacne of E. bungii in the upper 120 m on 5 June 1980 (12 m -3) was similar to that observed on 12 May 1981 (10 m-a), also an indication of earlier reproduction or accelerated growth in the warm year. Rates of development of M. pacifica in 1981 at Sta. 5 were similar to 1980; as total numbers increased in May and June (Fig. 4) the age-structure of the population did not change dramatically suggesting continuous reproduction and development during spring and early summer by this species (Fig. 7). The development ofPseudocalanus spp. was similar in 1980 and 1981 at Sta. 5, with the first cohort reaching adulthood in May both years (Fig. 7). The extending sampling in 1981 showed the development of a second cohort in late June and July.

Table 5.

1981 21 May 27 June 11 May 8 July 12 May 8 July 1 June 8 July

Dr), weights of selected taxa from the upper 120 m in the southeastern Bering Sea Station 1 1 5 5 1 1 5 5

* N is in parentheses.

Taxon

Neocalanus plumchrus CV Neocalanus plumchrus CV Neocalanusplumchrus CV Neocalanus plumchrus CV Neocalanus eristatus CV Neocalanus cristatus CV Neocalanus cristatus CV Neocalanus cristatus CV

Mean dry weight (~g individual-1 ) 582 (3)* 606 (3) 553 (3) 1091 (3) 3732 (3) 3850 (3) 1238 (3) 5253 (3)

Distribution, abundance, and development of copepodsin the SE BeringSea

227

STATION 5, 1981

STATION 5, 1980

'°° F

'°°r

CI-C3

OL-t/ Mettidia

Metridio

pacifico

pocifico

bJ

60

C4

,,

C2 8, C5 Pseudocalanus spa.

o '1

APR,L I

MAY

Eucolanui bungii

o

I

PseudocoJonus sPt).

0

I

APRIL Eucolonus bu.ngii

Fig. 7. Age-structure of some of the herbivorous copepods over the outer shelf (Sta. 5) in spring and summer of 1980 and i 981. The single cohort of E. bungii is in contrast to the other two species.

Zooplankton over the middle shelf Abundance. The middle shelf domain and its community of zooplankton are distinct from the outer shelf, kept separate by a front in the lower portion of the water column just inshore of the 100 m isobath (SMrrH and VIDAL, 1985). Over the middle shelf (Stas 12 and 16), Pseudocalanus spp. was more abundant in 1981 than in 1980 (Fig. 8). Comparison of mean abundances in late April (19 to 20 April 1980 and 24 April 1981) and late May (26 to 27 May 1980 and 25 May 1981) showed that all copepodid stages ofPseudocalanus spp. that were analyzed were significantly more abundant in 1981 than in 1980 over the middle shelf (Table 6). When late April and late May of 1980 at Sta. 12 are compared, all stages of Pseudocalanus spp. were significantly more abundant in May (Table 6). In 1981, however, the abundances of copepodid stages II to IV in late April and late May were not significantly different, while copepodid stage V and adult females were significantly more abundant in May (Table 6). By July of 1981, however, abundance ofPseudocalanus spp. was not much greater than it had been in April (Table 7). The numbers of adult females alone increased in July over abundances in previous months (Table 7). A steady increase in the numbers of Pseudocalanus

228

s.L. SMITH and J. VIDAL

2°°t

1980

o, "1 APR,L I MAY 800,

o

STATION 16

70(2 re LIJ

m :[

60(2

z

z

1981

50(2

i,i :[ 40C

30C

20C

I00

0 7//~ APRIL ] MAY

] JUNF" ] JULY

Fig. 8. Abundance of all stages of Pseudocalanus spp. combined over the middle shelf (Stas 12 and 16) in 1980 and 198 I. The period of the spring bloom of phytoplankton is indicated.

spp. females, from 14 m -3 in April 1981 to 105 m -3 in July is the dominant seasonal trend in this species over the middle shelf (Table 7), with the proportion of total numbers accounted for by adult females steadily increasing on average from 6% in April to 31% in July (Table 7). By October 1981 the population of Pseudocalanus spp. had reached 5032 m -3 over the middle shelf, or a 15-fold increase over July (Table 7). In the approximately 4 months of the spring and early summer (April to July), the population increased only 1.4-fold. A similar seasonal pattern in abundance was observed for Pseudoealanus elongatus in Loch Striven (MARSHALL, 1949). In a study extending from January to September, she found lowest abundances in March and some of the highest in September, when the population was primarily stages CIV and CV (~77%) with adults comprising ,--6%. Other taxa that were significantly more abundant in late April 1981 compared with late April 1980 were adult Acartia spp., all copepodid stages of C. marshallae, and copepodids of M. pacifica (Table 6). Comparing late May of 1980 with late May of 1981, all taxa except copepodids of Acartia spp. and Oithona spp. were significantly more abundant in the warmer year, 1981 (Table 6). The seasonal trends in abundance ofAcartia spp. and C. marshallae in spring and early summer are similar; both taxa showed an approximate 5-fold increase between April and July, with adults comprising a decreasing proportion of total numbers from

,,

,” ,,

8.7 12.1 120.6 36.1 35.7

11.0 0.8 0.7 0.8 0.6 0.7 3.3

169.1

5.4

5.1 0 0 0 0.01 0.4 0.4

465.5

April 198 1 abundance (number m-j)

12.6 1.8 3.8 3.6

April 1980 abundance (number me3)

3.012t

1.057 4.6937

2.837t 5.8937 6.2267 4.905t 5.367+

4.914f

0.979 2.772t 12.946j’ 4.458t

(5 L.)

20.3

233.4

1.6

269.6

106.8 0.5 1.5 3.5 4.8 0.8

56.5

8.5 2.8 113.6 31.6

May 1981 abundance (number m-‘)

19.4 7.3 9.7 9.0 5.7 0.1

18.6

18.9 9.4 30.3 14.8

May 1980 abundance (number m-))

Mean abundances of selected taxa collected at Sta. 12 in 1980 and 198 1

14.637t 5.356t 4.684t 5.3277 3.959t 10.371t 10.085t 0.385

5.584t

2.230 4.890t 6.512t 7.224t

(4 i.f.)

,,,

,,

* Notations are: C, all copepodids combined; AMF, adult males and females combined; CI, copepodid stage I; CII, copepodid stage II, and so forth. ‘I Difference signikant at P Q 0.05.

Acartia spp. C* Acartia spp.AMF Pseudocalanus spp. CII+III Pseudocalanus spp.CIV Pseudocalanus spp.CV Pseudocalanus spp. 0 0 Calanus marshallae CI Calanus marshallae CII Calanus marshallae CIII Calanus marshallae CIV+V Calanus marshallae Q Q Metridia pacifca C Oithona spp.

Taxon

Table 6.

21 20 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10

1.01 3.00 13.3 1.5 14.8 11.4 6.4 6.5 5.4 29.1 0 0 0 0.2 1.7 1.9 513.1

27 27 20 20 20 20 20 20 20 20 20 20 20 20 20 20 20

2.38 9.48 23.2 8.5 31.7 15.9 11.4 14.6 14.1 56.0 22.5 21.2 21.3 4.4 0.4 15.8 430.0

X

N

N

X

May 1980

April 1980

12 12 I 1 7 1 7 I 7 7 7 7 I 7 I 7 7

N 3.03 1.29 8.2 10.0 18.2 142.4 45.0 41.2 14.1 242.7 0.8 0.7 0.7 0.5 0.6 3.3 182.4

X

April 198 1

11 11 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5

N 4.53 8.28 6.6 3.0 9.6 100.1 45.4 68.1 52.1 266.9 1.7 1.3 1.2 2.0 0.3 6.5 110.8

X

May 1981

11 23 16 16 16 16 16 16 16 16 16 16 16 16 16 16 16

N 8.29 0.84 25.5 11.9 31.4 77.4 40.1 40.4 53.9 211.8 0.6 1.2 2.8 9.1 0.7 14.4 205.8

X

June 1981

14 14 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10

N

9.7 1.69 77.0 11.2 88.3 109.6 48.6 70.8 104.8 333.9 3.8 1.5 0.5 10.3 0.6 16.7 219.8

X

July 1981

Mean abundances of selected taxa over the middle shevin 1980 and 1981

4 4 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5

N

7.64 1.80 111.7 638.5 1356.2 3034.4 082.5 308.2 601.2 5032.3 0 0 0 13.7 0 13.7 2074.8

X

Oct. 1981

* Notations are: C, all copepodids combined; AMF, adult males and females combined; CI, copepodid stage I; CII, copepodid stage II, and so forth.

Calanus marshallae CI Calanus marshallae CII Calanus marshallae Cl11 Calanus marshallae CIV+V Calanus marshallae Q Q Total Calanus marshallae Oithona spp.

Sea-surface temperature (“C) Surface Chl a (mg me3) Acartia spp. C* Acartia spp. AMF Total Acartia spp. Pseudocalanus spp. CII+III Pseudocalanus spp. CIV Pseudocalanus spp. CV Pseudocalanus spp. Q Q Total Pseudocalanus spp.

Variable

Table I.

Distribution, abundance, and development of copepodsin the SE Bering Sea

231

month to month (Table 7). Between July and October, however, Acartia spp. showed a strong increase in abundance (15-fold) similar to that of Pseudocalanus spp. while numbers of C. marshallae did not change (Table 7). Growth and development. The age-structure of Acartia spp., C. marshallae, and Pseudocalanus spp. at Sta. 12 show differences that may be attributable to the general difference in temperature (,,03°C) between 1980 and 1981 over the middle shelf. In the relatively cold year (1980) the population ofAcartia spp. at Sta. 12 was largely copepodids (~77%) during the spring bloom of phytoplankton, while during the bloom in the warmer year (1981) the population was only ,,~37% copepodids (Fig. 9). In both years, however, proportions of copepodids and adults fluctuated among samplings in a manner suggesting cohorts were probably not produced. Pseudocalanus spp. produced less distinct cohorts in the warmer year, 1981, and during the spring bloom in May of 1981 showed a declining proportion of stages CII and CIII (Fig. 9). In May of 1980 the proportion of stages CII and CIII increased with time suggesting reproduction during the bloom at Sta. 12 (Fig. 9). Because of the large numbers of Pseudocalanus spp. collected in the warm year 1981, the overwintering stock of stage CV's probably had molted and reproduced well before our sampling began in April. The steadily increasing proportion of adult females throughout spring and summer indicates reproduction and maturation continuing after the spring bloom (Table 7). In October the proportion of adult females in the population had declined to 12%, and the bulk of the individuals were copepodid stages II to IV (82% of total numbers; Table 7) indicating reproduction had been sustained throughout August and September. The copepodids present in October would form the overwintering population of 1981. The large number of copepodid stages II and III collected in October (60% of total numbers) are in contrast with the development cycle of Pseudocalanus spp. in Ogac Lake and Loch Striven where by late September the population was almost completely the overwintering individuals, stages CIV and CV (MARSHALL,1949; MCLAREN, 1969). Thus, the seasonal cycle ofPseudocalanus spp. over the middle shelf in the Bering Sea, at least during a warm year, is prolonged by a month or more over that of Pseudocalanus spp. in other areas. In 1980 the copepod that dominated the biomass and community growth over the middle shelf was C. marshallae, which reproduced and became abundant during the spring bloom (SMITH and VIOAL, 1985). In the warmer year, 1981, reproduction began before the spring bloom, so that during the bloom (May) the population was primarily copepodid stages II to IV (Fig. 9). The average number of females present in April, prior to the bloom, was similar both years (Table 6). A second period of reproduction took place in June (a peak in numbers of stage CI was observed in mid July), suggesting that in warm years, and possibly every year, C. marshallae produces two cohorts, an observation consistent with that of NAUMENKO (1979; however he calls C. marshallae by the name Calanus glaeialis) for this area of the Bering Sea. The relative stability in total numbers of C. marshallae at Sta. 12 between July and October (Table 7), in a period when the age-structure changed from 37% stage CI's to 98% stage CV's, suggests that losses of C. marshallae to natural mortality or predation over the middle shelf were small in late summer and autumn of 1981. The mean concentrations of Chl a observed at the surface of Stas 12 and 16 in May of 1980 and 1981 were similar, 9.5 and 8.3 mg m -3, respectively (Table 7). Thus, although there were relatively large numbers of herbivorous copepods such as Pseudoealanus spp., C. marshallae, and M. paeifiea over the middle shelf in 1981 compared with 1980 (Table 7), the general timing, seasonal pattern, and magnitude of chlorophyll concentration in the spring

232

S.L. SMITHand J. VIDAL

I00

80

60 40 20 i pp t I00 80

o

60

u.

40 s~

20

0c u~

I00

I00

,-

Pseudoccllanu$ spp.

o

80

80 60

6O

I

40 ,..

20

2O

0

_, ~

/

STATION J980

12

~ ~ ~,~,>.',7.

.=-,,,~2,:,

.: .,. ~;s;.z.~Z~,~, ~:.,, ,.//,4,'., ,.,'~, STATION 12

1981

Fig. 9. Age-structure of three copepods of the middle shelf(Sta. 12) of the southeasternBering Sea in 1980 and 1981. bloom was unchanged from that of 1980. The spring bloom of phytoplankton over the middle shelf, therefore, seemed to have little influence on the abundance and reproduction of the herbivorous copepods, nor did fluctuations in their abundance seem to affect the bloom in any measurable way. Although the spring bloom preceded the increase in certain taxa over the middle shelf in both years, temperature, and not chlorophyll, was the most important variable influencing the timing of reproduction by most of the species of copepod. Even though reproduction seems to begin somewhat earlier or later from year to year depending upon

Distribution, abundance, and development of copepods in the SE Bering Sea

233

temperature, much of the growth of copepodids took place during the spring bloom both years. Except for C. marshallae, survivorship is difficult to assess for the copepods of the middle shelf which have several, variable generations per year. Potential differences in predation over the middle shelf between years can be evaluated by the numbers of the chaetognath Sagitta elegans that were coflected. If we consider the period of time sampled in both years, 21 April to 5 June, we find that in 1980 the mean numbers of S. elegans per cubic meter in the water column at Stas 12 and 16 were 4.1 _+ 1.0 (N = 10) and 4.5 _+ 0.8 (N = 12), respectively. In 1981, however, the mean numbers ofS. elgans at Stas 12 and 16 were 1.5 + 0.5 (N= 10) and 2.2 _+ 0.6 (N = 5), respectively. Those differences between years are significant for Sta. 12 (tEE : 3.112; P < 0.05) but not for Sta. 16 (t15 : 1.976;p ~< 0.05). The above observations lead to some conclusive statements. These are: 1. The upper layer of both the middle shelf and outer shelf were warmer at any given time and showed faster increase in temperature in 1981 than in 1980. The spring bloom of phytoplankton began approximately l0 days later in 1981 compared with 1980, but the standing stocks observed during the bloom were similar. 2. The middle front at approximately the 100 m isobath separated the two major communities of zooplankton both years. Offshore of the front, large calanoids such as N. plumchrus, N. cristatus, E. bungii, and M. pacifica dominated, while inshore of that front Pseudocalanus spp., Acartia spp., and Calanus marshallae dominated. 3. Over the outer shelf (Sta. 5) in April, N. plumchrus, N. cristatus, E. bungii, and Pseudocalanus spp. were significantly more abundant in 1980, a relatively cold year, than in 1981, a relatively warm year, while over the middle shelf (Sta. 12) all stages of Pseudocalanus spp. and C. marshallae were more abundant in 1981 than in 1980. 4. Both N. plumchrus and C. marshallae, which were thought to reproduce once per year based on 1980 data, produced two cohorts at some stations in 1981, and both E. bungii and C. marshallae reproduced earlier in 1981 than in 1980. DISCUSSION

The year-to-year differences in the abundance of dominant, herbivorous copepods in the southeastern Bering Sea present a contradiction. Why were herbivorous copepods over the outer shelf significantly more abundant in 1980 while over the middle shelf the major herbivorous copepods were more abundant in 1981 ? The species are different owing to the water masses and circulation of this area which result in a front in the bottom of the water column near the 100 m isobath. Exchange of species across this front generally does not occur, a feature of the southeastern Bering Sea that has been documented previously (CooNEV and COYLE, 1982; IKEDA and MOTODA, 1978; MOTODA and MINODA, 1974; SMITH and VIDAL, 1985). The dominant herbivores of the outer shelf are eopepods whose life cycle includes a period of diapause at depths >500 m over the slope. Thus, the shelf population must be derived from the slope population which requires advection with speeds that exceed the observed currents (1 cm s-l; COACHMANand CHARNELL, 1979) and a direction, onshore, that is not the observed mean flow (alongshore). Over the middle shelf, the copepods dominant in the spring must have overwintered successfully in situ in an area that is often ice-covered and have reproduced at the temperatures and concentrations of food available. It is clear there are substantial differences between the two areas of the shelf, with the copepods of the middle shelf unable to escape

234

S.L. SMITHand J. VIDAL

year-to-year variations in the winter conditions which are felt over the entire water column. Since development in small-bodied copepods is more temperature-dependent than fooddependent (VIDAL, 1980), winter conditions and warming in spring should be variables that strongly influence abundance in spring. Because the outer shelf populations are derived from overwintering, deep populations from the slope, they are not exposed to winter conditions of the surface layer but are dependent upon spring storms of other advective events to transport them onto the shelf. The quite different winter conditions to which the populations of the middle and outer shelf are exposed, one relatively stable, the other quite variable year-to-year, and the dependence of the outer shelf on storms, could lead to opposite interannual variations such as we observed in 1980 and 1981. Large populations on the outer shelf would arise from storms in spring regardless of temperature, and 1980 was stormier and colder than 1981. Large populations over the middle shelf must arise from reproduction by the local population, which would be favored by warm years regardless of storms, and 1981 was warmer than 1980.

The outer shelf The mechanism by which the large, herbivorous copepods that overwinter at depth over the slope become part of the community of the outer shelf is probably an onshore flow at 50 to 80 m associated with storms having winds that blow parallel to the shelf break from the north and northwest (COACHMANand CHARNELL,1977; SCHUMACHERand KINDER, 1983). There are more storms over the outer shelf than over the middle shelf (ScHUMACHER and IQNDER, 1983), propagating along the Aleutian Islands and into the Bering Sea primarily in summer (OVERLAND, 1981). The 1981 data are particularly good for examining the relationship between wind speed and direction of the slope (Sta. 1) and the onshore gradients in abundance ofN. plumchrus, N. cristatus, and E. bungii over the outer shelf. The wind velocity recorded from the ship over the slope in 1981 had four peaks when wind speed was in excess of 15 kn, on 16 and 30 April, 15 June, and 18 July. Wind direction was from the north and northwest, paralleling the shelf break, during all observations from 13 May to 27 June, a period that contained one observation of wind in excess of 15 kn. Sections extending from the slope to Sta. 8 near the middle front, in which abundances of the slope species were measured, were completed in four 2-day periods, 21 to 22 April, 31 May to 1 June, 27 to 28 June, and 17 to 18 July. The first section was prior to the period of strong winds favorable for onshore movement of subsurface water and the last two were after presumed onshore flow associated with 15 kn winds from the north-northwest. The offshore-onshore gradient in total numbers of N. plumchrus in the water column between Stas 5 and 8 prior to the wind was -0.17 copepods km -l, and between Stas 1 and 8 was -0.73 copepod km -1 . That is, the abundance of N. plumchrus in the upper 120 m over the slope was greater than that at Sta. 8, and the abundance at Sta. 5 was also greater than at Sta. 8 (Table 8). Subsequent to the north--northwest winds (27 to 28 June), however, these gradients became positive, because mean abundance of N. plumchrus at Sta. 8 was greater that that at Stas 5 or 1 (Table 8). We take this reversal in gradients of abundance following prolonged winds favorable to inshore flow to mean that subsurface portions of the slope and outer shelf populations were moved toward shore where they accumulated at the area of convergence in the lower layer associated with the middle front near the 100 m isobath (COACHMAN,1982). The gradients in abundance of N. cristatus in the upper 120 m between Stas 1 and 8 and between Stas 5 and 8 were also positive only on 27 to 28 June following the peak in winds from the north-northwest. Gradients for E. bungii between Stas 1 and 8 were generally

Distribution, abundance, and development of copepods in the SE Bering Sea

235

Table 8. Abundance of slope taxa over the outer shelf in 1981 Station

1981)

Taxon

1

5

8

N.plumchrus N. cristatus E. bungii

153 7.1 5.8

52 0.5 0

41 0.3 0

31 M a y - l June N.plumchrus N. cristatus E. bungii

22 3.7 171

68 5.2 21

20 0.9 21

27-28 June

N. plumchrus N. cristatus E. bungii

70 2.5 76

87 2.4 25

117 l 1.4 77

17-18 July

N.plumchrus N. cristatus E. bungii

ll 0.5 38

23 0.5 20

14 0.4 26

21-22 April

_,ooOio 60

1980

o N. plumchrus x N. cristotus

o

MARCH I A R,L I

I STATION 5

,oIO[6o8O 40

,,~ 20 0

1981

x MARCH

I APRIL [

MAY

I

JUNE I

JULY

Fig. 10. Survivorship of Neocalanus plumchrus and Neocalanus cristatus in the water column of the outer shelf (Sta. 5) in 1980 and 1981. The calculation of frequency assumes that the earliest two samplings each year represent 100% of the population that will be present over the outer shelf in that year.

negative except on 27 to 28 June when abundances at Stas 1 and 8 were roughly equivalent (Table 8). The peak in wind speed (28 kn) on 30 April at Sta. 1 was not followed by any increases in abundance of N. plumchrus, N. cristatus, or E. bungii at either Sta. 5 or 8, because the wind direction was south-southwest (~200°C) and therefore not favorable for onshore flow. The abundances of N. plumchrus, N. cristatus, and E. bungii at Sta. 1 were not correlated with wind since the slope is the source of these populations for the shelf. In 1980, wind speeds at Sta. 1 often exceeded 15 kn (60% of the observations) but the direction favorable for onshore

236

s.L. SMITHand J. VIDAL

flow was seen only twice and with relatively brief duration, 25 March for 4 days and 27 April for 6 days. In both cases the numbers of N. plumchrus and N. cristatus subsequently increased at Stas 5 and 8 but E. bungii did not. The lag was approximately 24 days. The periods of wind at Sta. 1 favorable for onshore flow in 1980 occurred prior to the end of April, a time when E. bungii had not yet come into the upper 120 m to reproduce (HEINRICH, 1962; HEINRICH,1968; SEKIGUCHI,1975; NAUMENKO,1979; KRAUSEand LEWIS,1979; VIDAL and SMITH, 1985). Predation on N. plumchrus and N. cristatus at Sta. 5 in 1981 was low until early June, while in 1980, predation on these two species at Sta. 5 began in late April, about 40 days earlier than in 1981 (Fig. 10). In both years, the population of N. plumehrus, which was collected nearer the surface than N. cristatus, was primarily stage CV (91% in 1980; 87% in 1981) when survivorship began to be <100%. Only 2 to 3% of the numbers of these two species present in mid-April were captured at Sta. 5 in October. Because sampling extended to the bottom, these losses between April and October represent potential removal by predators and suggest seasonality and interannual variation in the timing of predatory pressure over the outer shelf. In terms of carbon taken by birds over the outer shelf, where surface-feeding forms such as fulmars and gulls predominate, the annual estimates for 1980 and 1981 were similar (0.2 and 0.3 gC m-2 y-l, respectively; SCHNEIDERet al., 1986). Most of this annual estimated flux must occur in May to August when the large, herbivorous copepods are abundant at the surface.

The middle shelf The copepods comprising the community of the middle shelf, Acartia spp. (largely A. longiremis), Oithona spp. (largely O. similis), C. marshallae and Pseudocalanus sp., are common, cold-water, neritic species found in the upper 20 to 100 m of the water column from the Bering Sea (HEINRICH, 1962; MINODA,1971; MINODA,1972; IKEDAand MOTODA,1978; NAUMENKO,1979; COONEY and COYLE,1982; SMITHand VIDAL,1985) to the central Oregon coast (PETERSONand MILLER, 1977; PETERSON et al., 1979). Although reproduction and the seasonal cycle in abundance of Pseudocalanus sp. and Oithona similis have been characterized as being primarily dependent on the spring bloom of phytoplankton in some areas (MARSHALL,1949; MCLAREN, 1969), the timing of seasonal increases in Pseudocalanus sp. in Ogac Lake, Baffin Island, was influenced by temperature (MCLAREN, 1969). In warm years, the first brood appeared earlier in spring and the time between broods was reduced (MCLAREN, 1969), which by accumulating over the spring and summer seasons should lead to increased abundance in autumn. Additionally, the development rate of Pseudoealanus sp. is temperature-dependent (VIDAL, 1980) in such a way that in relatively cold years abundance should be reduced compared with warm years. The abundance of Pseudoealanus sp. over the middle shelf prior to the spring bloom in 1980 and 1981 is consistent with the hypothesis that temperature is the most important variable in the seasonal cycle of this species in the southeastern Bering Sea. In the month prior to the bloom (April), Pseudocalanus sp. in the warmer year (1981) was eight times more abundant than in the colder year (1980). Thus, the warmer temperatures of 1981 seem to have promoted earlier maturation and reproduction and possibly faster development of Pseudocalanus sp., resulting in a substantial population over the middle shelf prior to the spring diatom burst in May. Aeartia longiremis and O. similis responded differently than Pseudoealanus sp. to the

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temperature differences between years. O. similis was more abundant before the bloom in the colder year (1980) than in the warmer year (1981) and A. longiremis showed similar abundances both years. O. similis seems not to increase in numbers until July, well after the spring bloom in May, and a pattern similar to that observed in Loch Striven (MARSHALL, 1949) and Ogac Lake (MCLAREN, 1969). A. longiremis also seems not to increase substantially until July. Abundances of all these taxa continued to increase over the summer of 1981 after the bloom, and by October abundances were 5 to 71 times what they had been in April. Although the diatom bloom ends by 1 June over the middle shelf, total grazing, growth, and reproduction by the dominant herbivorous copepods clearly continues to increase until at least October. In terms of the food chain dynamics, the spring bloom of phytoplankton is more efficiently used in a warm year when considerable numbers of Pseudocalanus spp. are in the water column prior to the bloom. The largest herbivorous copepod of the middle shelf, C. marshallae, is abundant off Oregon when upwelling is underway and temperatures are cool; at other times (October to January) it is presumed to be in diapause (PETERSON, 1979). Its life cycle and vertical movements seem to 'match' the circulation in such a way that fast-growing juveniles are retained in the bloom of phytoplankton (PETERSON et al., 1979) with the result that abundance and population growth are predator-limited (PETERSON, 1979). In the Bering Sea, the life cycle of C. marshallae has been described as including diapause during winter and two periods of reproduction, the main period (February) being well in advance of the spring bloom of diatoms (NAUMENKO, 1979). Our results suggest the first spawning is in March, and approximately 2 weeks earlier in the warmer year (1981) than in the cold year. Most of the copepodid growth both years took place during the spring diatom bloom, and although there was a second spawning period in June 1981, abundance over the middle shelf was unchanged from June to October with the population almost entirely stage CV in October. The life-cycle of C. marshallae seems timed in such a way that most of the copepodid growth takes place during the sprint bloom even though low temperatures may delay reproduction somewhat. Such a strategy uses the spring bloom efficiently, and combined with the low mortality once copepodid stages are achieved following the spring bloom, should result in a more stable population from year to year than is possible with the strategy of Pseudocalanus spp. Our results indicate this is the case over the middle shelf. Predation on copepods over the middle shelf seems to be slight. The birds are subsurface feeders and ingest larger prey such as euphasiids and fish (SCHNEIDERet al., 1986) and larvae of the dominant fish species, Theragra chalcogramma, also seem to exert a small predatory impact (DAGG et al., 1985). However, the abundance of chaetognaths did vary significantly between years. The larger number of chaetognaths over the middle shelf during the spring bloom in 1980 suggests a greater loss of small-bodied copepods such as Pseudocalanus spp., Oithona spp., and nauplii of C. marshallae to predation in 1980 than in 1981. Increased temperature and lower predation by chaetognaths both acted to enhance the numbers of herbivores over the middle shelf in 1981 compared with 1980. Perhaps the presence of more herbivores over the middle shelf (Sta. 12) in 1981 compared with 1980 explains the lower standing stock of Chl a observed in the upper 20 m and at the surface in 1981.

Acknowledgements--This research was fundedby the Divisionof Polar Programsof the National ScienceFoundation under Grant DPP76-23340. The field work was completedwith help from our colleaguesin PROBES and the crew of the R.V. Thomas G. Thompson. We are gratefulto P. V. Z. Lane, J. C. Dugas, B. A. Plonski, L. Incze,J. Judson, M. Rochet, and C. Smith for assistance at sea. The laboratory analyseswere done by P. V. Z. Lane, J. C.

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Dugas, B.A. Plonski, and E. M. Schwarting; D. G. Smith assisted in data reduction. Chlorophyll a data were supplied by R. L. lverson and J. J. Goering, and T. E. Whitledge provided the nutrient data. Discussions with our PROBES colleagues substantially improved our understanding of this sea, and the advice of anonymous reviewers is gratefully acknowledged.

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