........

This papcr not to bc citcd without permission of the author.

PAPER

Intcrnational Council for theExploration of the Sea

ICES C.M. 1990!L:23Biological Occanography Committcc·

COMPARATIVE STABILITY OF ZOOPLANKTON COMMUNITIES OFTI-IE NORTHEAST V.S. SHELF ECOSYSTEM AND THE

NORTH SEA ECOSYSTEM IN RELATION TOCLIMATIC VARIABILITY

_by

Kcnncth Sherman, Jack Jossi, and Julicn Goulet

National Oceanic and Atmospheric AdministrationNational Marine Fisheries Service

Northeast Fisheries CenterNarragansett, Rhode Island 02882-1199, USA

INTRODUCflON

. Climate changes can cause significant effects on the prodllctivity cycles of marineecosystems (Gieskes and Kraay, 1977; Colebrook, 1986; Colcbrook and Robinson, 1986;Dickson et al., 1988; Colebrook, 1990). In the northern North Atlantie several marineecosystems are at risk from climatic warming. Expected changes in the oceanographicregime of the Scotian Shdf ecosystem have been· dcscribcd by \Vright ct al. (1986).Assessment of the impact of warming on the fishery resomces of the Scotian Shclfecosystem has been made by Frank ct al. (1988); cxpcctcd cffccts inclllde shifts in thcdistrihutions of grollndfish stocks at the limits of their ranges, carlier arrival times, and latcrdcparturcs for pelagic spccics undergoing feeding amI spawning migrations, ami redllctionof organic flllx from extcnded stratification periods.

Climate, throllgh its inflllence on the physical characteristics of the water colllmnplays an important role in determining prodllction levels within thc large marine ecosystemsacross the northern North Atlantic, including the Northeast Continental Shclf ecosystem,tllc Scotian Shelf ccosystcm, the \Vest Greenlnnd Sen ecosystem, the Enst Grccnlnnd Scaecosystem, the Icelandie Shclf ecosystem, the North Sea ecosystcm and the Norwcginn Scnecosystem. \Vhile there is some evidence for global warming (Kerr, 1990a,b), significant

1

. ,uncertainty remains abotJt the rates and the consequenccs ofthe warining. C1inlatc indiiccdwarming wOllld have dircct cffects on the metabolie rates ofthe plan~ton of lhe northernNorth Atlantic ccosystem. Effects are Iikely to be expressed at qle ecosystem level fromaltered growth arid prodllction rates of tlie plankton as feedback to changes in the timingof seasonal biological everits, resulting Jrom the altcred coupling of trophie levels, amIqualitative changes in the stmcture of the food chain (Frank et a1.; 1988).

Data col1ected under the NMFS ContinllOlis Planktori Recorder (CPR)program arebeing analyzed for both dircct andindirect indications of the Cffects of c1imate change onmarine ecosystems. Direct indications indude alterations of the annual pattern of watercoltimri temperature stmcture. Indirect changes are observed in the water COllllnr1 biology.Zooplankton prodllction retlects the state-of-thc-environmerit over a per.iod of wecks tomonths rathei" than short terrri (days-wecks) weather pertürbations.

Zooplankton can be used to assess trends in dimate. Zooplankton processessensitive to climate change iridtide the, tiIning of. events in the productiori eyde (e.g.,recruitment, growth, maturation), as weil as the actual abundarice levels and production"rates. Temperature has ancffcct on the sizeof zooplankters, with aniinals growing larger eat colder temperature (Marshall and Orr, 1955). Slight interannual changes in nieantemperature ean result in differences in the stage ofdevelopmerit of the cohort, and in thesize of the animals in the cohort on any given sampling date (Ellertsen et a1.; 1987; Dmbinand Durbin; in press).

Plankton biomass arid \vater. coltinln temperatllfe and strllcllii"e have been usedsuccessfully for detecting changes in the states of large marine ccosystems and their fisheriesyields (Shernlan arid Alexander, 1989). One of the most cost-cffective \vays of obtainingthe needed data is using .commcrcial ships to tO\V CPRs. The Institute for MarineEnvironmental Research (IMER), Plyrriollth, England, has sampled with CPRs fronl ships­of-opportunity in thenorthern North Atlantie since 1939, providing a survey of the planktonat the standard deptll of 10 m(Hardy, 1939; Glover, 1967). The data are used in ecologicalstlldies of the biogeography, annual cycles, and long term variation in the distribution,abundance, and composition of the planktori.

. . Lang-term trends sho\ving decIining zooplankton abundance have been reported forthe northeast North Atlantie (Garrod and Colebrook, 1978; Colebrook, 1982; Radach; e1982). In the northwest Atlantic, on the Northeast D.S. Shclf, MARMAP sürveys tisingbongo net tows, conducted from the 1970s through the mid-1980s showcd iio evidence ofa downward trend when compared to eadier plankton net-tow data (Sherman ct a1.; 1983).This .pnpcr examincs CPR, data collected from the V.S. Northeast Contiilerltal Shclfecosystem from 1961 throllgh 1989 (Fig. 1).

METI-IODS

Dnta Colleetion amI Processes

The dntn were processed \vith the same tcchriiques uscd by IMER (Colchrook, 1975,to compare. trends in plankton ahundance on both sides of the North Atlantic llasiil,1978) using the log tr~lI1sformed abimdance,of cachtaxonoillic grollp. The means of theseahundnnccs wcre cnlculntcd for cach month in each subarea. The iechniqtie used hy theßritish CPR siJrvey, conducted by IMER; was eillployed for interpolating valucs for rilOllths

2

(

I-.'.. •• ......._ ~ ..... _, " .• c " ." ......: -i v. ~. ~ ~". t • '.' ..

.' ...

•

with nl.issing meas.u~emerits. Its application was con~idercd separateiy for each taxonomiegroup In each region. The long-term monthly means were ealculated for each taxonomiegroup; those ~ix months \vi.th th.e highest meari abiJridanees were incllldcd in the annlysis.Ir three or more of these '11Igh-slx months were sampled in a year, then interpolntcd val liesfor missing months in that year. were caleulated follmving Colebrook (1978): (1) the thrceor more, monthly mean abundanees fro.":1 measurements in the year \vere summed; (2) thelong-term means from the. eorrespondmg months were summed; and (3) the ratio of the'year su?'ls to the long-terin sums was multiplied by the long-term mean of each missingmonth In timt year to produee the interpolated value. Ir less than three of the high-sixmonths were sampled in a year, no interpolation was performed.

The resulÜmt data set was averaged by year, and yearly series were standardizedaeeording to the IMER methodology by subtraeting the series mean and dividing by theseries standard deviation. The subareas and taxonomie grOlips eonsidered in the analysisare listed in Tables 1 and 2, respeetively.

The first five taxonomie groups in Table 2 are among the nine most abundant in theGulf of Maine. They are also among the 25 most abundant taxonomie grOlips in the NewYork Hight and in the northeast North Atlantie (Colebrook, 1978; Jossi and Goulet, 1990).

Principnl Component Annlyses

. 1\yo sets of principal .eoinponent analyses (PCAs) wcre, performed. The firstarialyzed thecoherence of staridardized yearly aburidances for eaeh taxonomie group amongsix of the subnreas (exeltiding the whole Gulf of Mnine and the whole New York Hight).The seeond annlyzed the coherenee of abundances arnong tnxononiie groups sepnratelywithin eaeh subnrea. '

In all the PCAs performed, the first iwo corriponents aceounted for 61--87% of ihetotal varianee., Following Colebrook (1978) \ve retained only the first two components.Since eaeh of these two principnl eonlponents are significantly eorrc1ated with a differentsubset of the arialyzed variables, the yearly principal eomponent scores were calculatedonly for those yenrs \vith rio missing yearly means for the appropriate subset of variables.

. The eigenveetors, or eorrclations between componerits and variables, of the first twoeomponents were plotted against each other. These show the strengths of the associatioribet\veeri the analyzed variables and the first two eomponents. The 0.05 mllltivariatesignificanee level for six variables and 29 observations is approximatc1y 0.55. Variables withvalues greater than 0.55 (or less than -0.55) are significantly correlritedwith the indicatedCoillponcnt arid thus have a commOllality which is mapped by the principal compOl1eiltscores. The time series of pdncipal component scores were plotted arid polynOlllialsmoothing furictions were superimposed. A sixth order polyriomial \vas used to sn100th thc29-year series of the Gulf of Maine subareas rind a fourth order polynon1ial was used forsnioothing the 14-yea'r series of the New York Hight.

RESULTS

The copepod Ca/allUS jilll1iarc!licus (copepodites 5 amI adults) showcd a positivetrend in all Gulf of Maine subareas exelusive of Massachusetts ßay. No consistent pattenl

3

arriong subareas eould be seen in the time series of any of the other taxononiic groups (Fig.2).

. 1l1eeoherence of a· taxonomie grütip's variations among the suhareas anaiyzed isshown by eigenveetors(Fig. 3) and principal component scores (Fig. 4). This eoherence iswithout regard to differences in mean aburidance or variance among the subareas becausethe annual series has· been standardized. The first principal eomponcnt for all sixtaxonomie groups is eorriprised of ihe standardized annllal abllndanees in the Glllf of Maineexclllsive of Massachllsetts Bay (Fig. 3). The annllal scores of these first principalcomponents (Fig. 4) show a positive trend for Cil[anlls jimnarclziclls and a variable patternfor Centropages t)'piCIiS arid Oi/hoila spp. (Table 3). 111e variable pattern is high in 1961­62 and 1973-83, and low in 1963-72 and 1984-89.

Principal eomponent änalyses by subareas, to examine the coherence of a siJbarea;svariations among taxonomie groups, werc performed. 111ere were no consisterit patternsin either the eigenvectors ~r the time sefies of principal component scores;

111e Gulf of Maine average surfrice temperatüre obiairied on autumn groundfishsurveys (Mountain and Holzworth, 1990) ure superimposed on the first principal coniponeniscores of Ca/anlls jinll1arcllicllS, CeJltropages l)picus, Oi/I1Oiza spp., ami all other taxa inFigure 5. Mountain ,arid Holzwarth removed the seasonal eycle from the, surveytemperature data, both to remove the effects of timing of the survey eruises and to use thissingle season data, set as a proxy. for 'interannllal variability. Surface and bottomtemperatures from 1963 to 1987, show a ,cool period in the 1960s; a \varm period in theearly 1970s, followed by a moderatety cool period in the late 1970s and a moderately \varmperiod iri the late 1980s. \Ve are presently examining the relationships betweentemperature and zooplankton abllndrince. llms far, the correspondence seems weak. Irithe 1960s there is an apparent correspondence between slIbnorrnal temperatures rindCelltropages l)'PiCIiS poptllations. 1l1e correspondence breaks do\vri in the early 1970s anddoes not reappear. The positive trend in Ca/anlls jinmarc!liclls eompares witll a positivetrend in surfaee temperature anomaly only on a broad scale. The year-to-year varintionshave almost no eorresporidence. ßetween 1963 and 1970, there appears to be acorrespondenee between the first principal component ofCentropages l)'PiCIiS al1<1 the slirfacetempernture anonlaly.

DISCUSSION

Colcbrook (1978) reported consistent negative trends in principal component scoresfor npproximatety 25 taxa over nluch of fhe northeastern North Atlantic. More recently(Colcbrook, 1986) found a positive trend beginning in approximatcly 1979. \Ve found noeori1ll1Ori signal in the time series of priricipal component scores among ohr six taxonomiegroups. If a North Atlantic-widc c1imatic reginie were responsible for the coiisistency ofColcbrook's trends, we would expect a similar corisistency and timiilg in the pdncipalcomponcnt scores for the zooplankton in the V.S. Northeast Corltinental Shelf eeosystem.

The standardized ablllHlances of Calanllsjinll1arclliclis iri the GlIlf of Maine, exclllsiveof Massachllsetts ßay showed a positive trend in abmidance in the first priilcipalcomponcnt. \Ve also obtaincd a common pattern for t\vo of the remaining taxonomiegrollP's first principal component. That commorl pattern is a variable signal wiih highs in

,4

..e

.' ~.-, ' ,.1.. ~ •

1961-62 and 1973-83, and lows in 1963-72 and 1984-89. Based on the principal componentanalyses, it does not appear that the zooplankton of northeast North AtJantie amI the V.S.

. Northeast Continenial Shelf are responding to the same climatie signals... ';>-:". ": ~. ')0, ,; ;' .:. '", ":. .',~ •• ," ~.;' ". •

\Ve used t1~e analyses designed by IMER for CPR data (CoJcbrook, 1975, 1978)specifically for our initial comparisons with pubJished reports of the decIining trends inzooplankton for waters of the Northeast AtJantie. In the relatively smaller areas of the'Northeastern D.S. Continental Shelf and the western Nova Scotian Shelf sampJcd duringthe present investigation, more information can be obtained from time series of aetualabundanee levels of the zooplankton than their seasonal variations. \Ve share with Radaeh(1982) reservations eoneerning the utiJity of principal component analyses of standardizedannual abundances for studying climate effects on eeosystem proeesses. Othercontemporary studies by the plankton group at NMFS/NOAA show considerableinterannual variabiJity in zooplankton volumes for a 10-year series based on bongo net towson the Northeast Shdf (Kane and Green, 1990) and signifieant variability in abundance ofphytoplankton, and zooplankton at seales less than 100 km and 60 days (Jossi and Smith1990).

The patterris and trends extracted by more detailed analyses will serve as a guidcinthe continuing study ofclimate-scale signals in the zooplankton, physical oceanographic, andmeteorologie records. Focus on seasonal and interannlJaI variabiJity, as weil as smnll-scaletime-space variability, in zooplankton abundance should allow for significant progress inunderstanding cIimate cffects on eeosystems proeesses.

ACKNO\VLEDGMENT

\Ve thank Jane Allen for the data proccssing support she so chccrfully provided, amiDan Smith for providing taxonomie identifications.

LITERATURE CITED

Colebrook, J. M. 1975. Continuous plankton recorder survey: Automatie datn proccssingmethods. Bull. Mar. Ecol. 8:123-142.

Colebrook, J. M. 1978.. Continuous plankton rccords: Zooplankton ami environment,North-East AtJantie and North Sea, 1948-1975. OceanoJ. Acta 1:9-23.

Colebrook, J. M. 1982. Continuous plankton records: Phytoplankton, zooplankton andenvironment, north-east Atlantic and North Sea, 1958-1980. Oeeanol. Acta 5:473-480. .

CoJcbrook, J. M. 1986. Environmental infiuences on long-term viuiahility in 'marineplankton. Hydrobiologia 142:309-325.

Colcbrook, J. M. 1990. Continuolls Plankton Rceords: Global warmillg and the planktonof the North Sea and North-East Atlantic. (in prep.)

5

Colebrook, J. M., and G. A. Robinson. 1986. The Continuous Plankton Recorder Survey.IOC Tech. Sero Time Series of Ocean Measurements 3:33-42.

Dickson, R. R., P. M. KeIly, J. M. Co1cbrook, \V. S. \Vooster, and D. H. Clishing. 1988.North winds and prodllction in the eastern North Atlantic. J. Plank. Res. 10:151-169. .

Durbin, A. G., and E. G. Durbin. In press. Seasonal change in size frequency distributionand estimated age iri the copepod Acartia hudsollica during a winter/spring hloom.Limnol. Oceanogr.

Ellertsen, 0., P. Fossum, P~ Solemdal, and S. Sundby. 1987. The effectof biological andphysical factors on ·the survival of Arcto-Norwegian cod and the inflllence onrecruitment variability. Contribution to the 3rd Soviet/Norwegian Symposium inMurmansk, 26-30 May 1986: The effect of oceanographie conditions on distributionand population dynamies of commercial fish stocks in the Barents Sea. 29 pp.

Frank, K. T., R. I. Perry, K. F. Drinkwater, and W. H. Lear. 1988. Changes in the fisheriesof Atlantic Canada associated with global increases in atmospherie carbon dioxide:A preliminary repori. Can. Tech. Rep. Fish. Aquat. Sci. 1952:v + 52 p.

Gareod, D. J., and J. M. Colebrook. 1978. Biological cffects of variability in the NorthAtlantie Ocean. Rapp. P.-v. Reun. Cons. int. Explor. Mer 173:128-144.

Gieskes, \V. \V. C., and G. \V. Kraay. 1977. Continuous Plankton Records: Changes inthe plankton of the North Sea and:its eutrophie Southern Bight from 1948 to 1975.Neth. J. Sea Res. 11:334-364.

Glover, R. S. 1967. The contimious plankton recorder survey of the North Atlantie. Symp.Zool. Soe. Lond. 19:189-210.

i

Hardy, A. C. 1939. Ecological investigations with the continuous plankton recorder.Objee, plan, and methods. Hall. Bull. Mar. EcoI. 1:1-57.

Jossi, J. \V., and J. R. Goulet. 1990. Zooplankton community abundance, coherence, and •stability of the Nortlieast Shelf Ecosystem. ICES C.M. 1990/L:93. .

Jossi, J. \V., amI D. E. Smith. 1990. Continuous plankton records: Massachusetts to CapeSable, N.S., and New York to the Gulf Stream, 1989. NAFO Scr. Doc. 90/66:1-11.

Kane, J. and J. Green. 1990. Zooplankton biomass on Georges Bank 1977-86. ICES C.M.1990/L:22.

Kerr, R. A. 1990a. Global warming continues in 1989. Science 247:521.

Kerr, R. A. 1990b. New greenhollsc rcport puts down dissenters. Scicnce 249:481-482.

MarshalI, S. M., amI A. P. Orr. 1955. The biology of a copepod. Oliver and Boyd,London. 195 pp.

6

Mountain, D. G., and T. J. Holzwarth. 1990. Surfaee and bottom tcmpcr<lturc andtempcraturc anomaly time scrics from thc Northcast Fishcrics Ccntcr spring ancl fallbottom trawl survcy program, 1963-1989. NAFO Sero Doe. 90/13:1-20.

Radaeh, G. 1982. Variations of the plankton in rclation to c1imatc. lCES C.M.1982/Gen:S, Mini-Symposium, 21 pp.

Sherman, K., and Alexandcr (Editors). 1989. Biomass yiclds and gcography of largemarine eeosystems. AAAS Sclceted Symposium 111, Wcstview Press, Bouldcr. 493pp.

Shcrman, K., J. R. Green, J. R. Goulet, and L Ejsymont. 1983. Cohcrcnce in zooplanktonof a large Northeast Atlantic ecosystcm. Fish. BulI., V.S. 81:855-862.

Wright, D. G., R. M. Hcndry, J. W. Loder, and F. W. Dobson. 1986. Occanic ehangesassociated with global increases in atmosphcric earbon dioxidc: A prc1iminary rcportfor the Atlantic eoast of Canada. Can. Teeh. Rcp. Fish. Aqual. Sei. 1426:vii + 78p.

7

Table 1. Geographical subareas off the Northeast V.S. Shelf sampled with the ContinuousPlankton Recorder.

Region

Gulf of Maine as a whole

Massachusetts Bay

Wilkinson Basin

Gulf of Maine Ledges

Crowell Basin

Western Scotian Shelf

New York Bight (NYB) as a whole

Continental Shelf portion of NYB

8

DUTation

1961-present

1961-present

1961-present

1961-present

1961-present

1961-present

1976-present

1976-present

Table 2. Taxonomie groups examined for zooplankton community coherence.

Taxonomie Group

Calanus finmarchicus

Pseudocalanus spp.

Centropages typicus

Oithona spp.

Metridia lucens

All Other Taxa

Zooplankton Life Stage

copepodite 5 and adult

adults

all stages

all stages

copepodite 5 and adult stages

all stages including remaining stages of Calanus finmarchicus,Pseudocalanus and Metridia lucens

9

Table 3. Significance levels and R-square values for a linear trend and indepenclently fora two-phase function for the first principal components of subareas far each taxonomiegroup. Meuidea lucens is not included because its principal component time series is shart.

Taxonomie Group

Ca/anus jinmarchicus

Pseudocalanus spp.

Centropages typicus

Oi/hona spp.

All other taxa

Linear Trend Two PhaseSig. R sq. Sig. R sq.

< .005 .55 .26 .06

.23 .07 .67 .01

.41 .03 < .005 .41

.76 .00 < .005 .37

.30 .05 .10 .13

10

MARMAP ROUTE Me 1961 - 1990

44 .

43

42

71

o

70 69 68

MARMAP ROUTE MB 197167

1990

66

•

42

40

38

36 ----r-L...o..----r----.,:-----,.------y-----r---.....76 74 72 70 68 66

Figure 1. Sampling coverage within the Gulf of Maine (MC) and New York Bight (MB)polygons, with standard reference distances and major subareas of the NortheastContinental Shelf Ecosystem.

11

.....N

GULF OF MAINE

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

WILKINSON 8ASIN

3

2

1

0

-1

-2

-360 65 70 75 80 85 90.

MASSACHUSETTS 8AY

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

GOM LEDGES

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

Figure 2. Calanus finmarchicus in the whole Gulf of Maine, Massachusetts Bay, Wilkinson Basin, and the Gulf of MaineLed.ge~. The values plotted are the anlallogarithmic mean abundances, standa~ed to a zero mean and a unit standarddeviatIOn. •.

CROWELL BASIN

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

'e

WESTERN SCOTIAN SHELF

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

....w

NEW YORK BIGHT NYB CONTINENTAL SHELF3 3

2 2

1 1

0 0

-1 -1

-2 -2

-3 -360 65 70 75 80 85 90 60 65 70 75 80 85 90'.

Figure 2 (continued). Calanus jinmarchicus in Crowell Basin, thc Western Scotian Shelf, the whole New York Hight, and thcNew York Bight Continental Shelf. Tbc values plotted are thc annuallogarithmic mean abundances, standardized to a zeromean and a unit standard deviation.

CALANUS FINMAACHICUS PSEUDOCALANUS

1

o

o

········ ....... . ':' ... .. .. . .s .···········... .. . .. ..... . .· .······

1

O.J----;...---f---+--­+A

-1 L....._-.;...-_-+.__;..-._....

-1

6'~

uQ)>'0CouQ)cn

1

e :·.............. ,·; Ä

o

·.... ............

·... .... ... .. .... .

1

O+---+----f---+--,.,.• A~

·......."' .

-1 L.-_-w--_-+-_---;._--,

-1

L-o~

uQ)>'0Cou(l)cn

first vector first vector

CENTROPAGES TYPICUS OITHONA

e: A-P

..· .

....... : • .. : .. ·Ä· ..

· .· .· .· .· .· .o ~--i.i----+---+.--

..................................· .· .· .

1

.e :

o

1 ····...... . .:. .. .. . .. . +:' .· .· .· .· .· .· .· .o ~---:'i----I---+'-....-; . t. Z• 0·· .

•••••• • ,'I •••• ••• • •••••• -. ••• I •••· .· .· .· .· .· .· .-1 L..-_-:.:--_-I-_....;..._---,

-1

6~

uQ)>"0Cou(l)cn

+ Mass8ay

Ä Wilkinson8asin

o GOMLedges

+ Crowell8asin

A Scotlan91eff

• NYBShelf

1

+

o

1

-1-1

L-o+JUQ)>

"UCou(l)cn

first vector first vector

Figure 3. Scatter diagram of the first eigenvector versus the second eigenvector far the principal component analysis ofstandardized abundances in each reg~ for Calanus finmarchicus, Pseudocalanu~p., Centropages typicus, and Oithona spp.The dashed lines are at approximat.he 0.05 significance level.. .

METRIDEA LUCENS ALL OTHER TAXA1 . + Mass 1 ··Bay ·... ·· +L- · ....L-

A Wilkinson 0 · ..•....:. .......0 ............................ .. '" ............ .............................+J ·+J

Basin 0 ·0 . · · +Cl> ·Cl> · + ·· > ·> · 0 GOM· n00 Ledges "0 ·"0 · ·· A C · 0

C · ·· + Crowell 0 ·0 + ·0 . :. Basin 0 ....•..; ..A...•Q) ................. ................. Q) ........ ~........Cf) · ·~ Cf) · ·• Scotian · ·(JJ

· ·· · ·Shelf ·-1 -10 1 • NYB -1 0 1-1

Shelf

first vector first vector

Figure 3 (continucd). Scatter diagram of the first eigcnvcctor vcrsus thc second eigcnvector for the principal componentanalysis of standardized abundances in each region for Metlidea lucens and AII Other Taxa. The dashed lincs are atapproximately the 0.05 significance level.

......0'1

CALANUS FINMARCHICUS

3

2

1

0

-1

-2

-360 65 70 75 80 85 90

PSEUDOCALANUS"3

2

1

0

-1

-2

-360 65 70 75 80 85 90

CENTROPAGES TYPICUS OITHONA

3 3

2 2

1 1

0 0

-1 -1

-2 -2

-3 -360 65 70 75 eO .85 90 60 65 70 75 80 85 90

. .Figure 4. AnnuaI scores of thc first principaI component among aII regions for Calanus jinmarchicus, Pseudocalanus spp.,Centropages typicus, and Oithona spp. e e

pu

•

•

METRIDEA LUCENS ALL OTHER TAXA

90

3

2

1

0

-1

-2

-360 65 70 75 80 85908580757065

3

2

o~-------------\\---t"?-:;-

-2

-3 L...,-T"""I""~~"""""""""''''''''''I''''''T""T''"'I'""'''''''''''''T'""T'~-r-r''''''''''''''''''r-TI

60

.... -1"'-J

Figurc 4 (continucd). Annual scores of thc first principal componcnt among all regions for Metridea lucens and AU Othcr Taxa.

......Cl:)

CALANUS FINMARCHICUS

3

2

1

-1

-2

-3 L...,---,....--,....--,---,---y--.,.--..,..---

60 64 68 72 76 80 84 88

OITHONA

3

2

1

-1

-2

-3 L-,...---r----r---,--.,.--..,..--...---y---

60 64 68 72 76 8,0 84 88

CENTROPAGES TYPICUS

3

2

1

O+---hrrnrrnrlTTl:rUrlltT"~r-n...."n"t""""''""'''-rrt-­

-1

-2

-3 L-,--~-~---,---,---r---,--...,---

60/, 64 68 72 76 BO B4 BB

Figure 5. Autumn surface temperature anomalies (bars) from Mountain and Holzwarth (1990) superimposed on the firstprincipal component scores of Calanus jinmarchicus, Centropages typicus, and Oithona spp.

e e•

•