Interannual variability of copepods in a Mediterranean coastal area (Saronikos Gulf, Aegean Sea)

Ž .Journal of Marine Systems 15 1998 523–532

Interannual variability of copepods in a Mediterranean coastalž /area Saronikos Gulf, Aegean Sea

Epaminondas D. Christou )

National Centre for Marine Research, Agios Kosmas, Hellinikon, 166 04 Athens, Greece

Revised 7 May 1997; accepted 26 September 1997

Abstract

Patterns of abundance of the dominant copepods as well as that of the total copepods, are given for a coastal area of theŽ .eastern Mediterranean Sea Saronikos Gulf, Aegean Sea . The results were based on 124 zooplankton samples collected

biweekly during a 5-year period from January 1989 through December 1993. Copepod abundances and environmentalparameters, almost all, exhibited pronounced annual cycles. Most copepods revealed repeated patterns and considerableinterannual variability. Both salinity and abundance of total copepods, revealed a clear interannual increase from 1989 to1993. Multiple regression models, based on stepwise variable selection, suggested that temperature and salinity were themost significant environmental parameters accounting for the variability of abundances. Simple regression models applied onmean annual values reveal the importance of salinity as the most significant factor affecting interannual variability ofcopepods. q 1998 Elsevier Science B.V. All rights reserved.

Keywords: zooplankton; Copepoda; coastal areas; Mediterranean; time series

1. Introduction

In the Mediterranean, long-term time series oncopepods are few and concern mainly the northwest

Žregions Kouwenberg and Razouls, 1990; Mazzocchi.and Ribera d’Alcala, 1995 and the Adriatic Sea

Ž .Regner, 1985; Baranovic et al., 1993 . Besides, thedetermination of factors driving interannual variabil-ity in marine zooplankton is an important issue. Thecomprehensive description of long-term temporal cy-cles of the biological communities and the environ-mental factors is fundamental in order to understandthe overall range of this variability. Through thistype of information, global change may also eluci-

) Corresponding author. Fax: q30-1-9653522. E-mail:[email protected]

dated. In coastal areas, land run-off and offshorewaters often interact with complex dynamics on awide range of temporal and spatial scales and fluctu-ations in ecological parameters can be quite com-plex. Copepods, characterized by extreme flexibilityin adapting to a fluctuating environment and tendingto maintain a stable standing stock even in the

Žpresence of variable food sources Mazzocchi and.Ribera d’Alcala, 1995 , seem to constitute a valuable

tool for the study of long-term variability in coastalareas.

In the present study, the patterns of abundance ofthe dominant copepods as well as that of the totalcopepods in the coastal area of the Saronikos GulfŽ .Aegean Sea , are described, during a 5-year period.Their relationships with the environmental factorsare also examined.

0924-7963r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved.Ž .PII S0924-7963 97 00080-8

( )E.D. ChristourJournal of Marine Systems 15 1998 523–532524

Fig. 1. Temperature, salinity and chlorophyll-a averaged over the water column, Saronikos Gulf, January 1989–December 1993.

( )E.D. ChristourJournal of Marine Systems 15 1998 523–532 525

2. Materials and methods

The results were based on 124 zooplankton sam-ples collected biweekly during a 5-year period, fromJanuary 1989 through December 1993. Samples were

Žcollected by oblique hauls at a coastal station 12 m. Ž .depth in the eastern Saronikos Gulf Aegean Sea .

The station is typical of the coastal area of theSaronikos Gulf and considered representative for thelarger area from which populations may be advected.

Ž .A 200 mm net WP2 , equipped with a Hydrobiosflowmeter, was used. The samples were preserved in4% buffered formalin. Copepod adults and copepo-dids were identified to the speciesrgenus level. Theabundances were expressed as number of individuals

Ž y3 .per cubic meter ind. m .Temperature, salinity and chlorophyll-a values

were also determined from samples taken at 1, 5 and10 m, using a 2 l Hydrobios water sampler equippedwith a Hydrobios thermometer, and the mean valuesfor the water column were estimated.

The effect of the environmental factors on cope-pod abundance was examined using simple and mul-tiple regression analysis, the latter based on stepwisevariable selection, of log-transformed data. The timebetween two successive samplings ranged from 12 to

Ž .17 days means14.4 days, SDs1.5 days . How-ever, for the purposes of this study the sampling

Ž .interval was considered constant s14 days .

3. Results

All environmental factors, exhibited pronouncedŽ .annual cycles, except chlorophyll Fig. 1 . Salinity

revealed a clear interannual increase from 1989 to1993, but no such trend was evident for temperature.

Pronounced annual cycles were also true for mostŽcopepod species but not for total copepods Figs. 2

. Ž .and 3 . Centropages spp. mainly C. ponticus , Cen-tropages typicus and Ctenocalanus Õanus were char-acterized by the strongest seasonal variability. Para-calanus parÕus, the only true perennial species,

Ž .Clausocalanus spp. mainly C. furcatus and OithonaŽ .spp. mainly O. similis and O. plumifera were

present all year round. Most copepods revealed re-peated patterns and considerable interannual variabil-

Ž .ity Figs. 3 and 4 . The abundance of total copepodsshowed a strong increasing trend from 1989 to 1993Ž .Figs. 2 and 4 . Clausocalanus spp., Oithona spp.,Acartia clausi and C. typicus, also showing a ratherincreasing trend, seem mostly to account for such an

Ž .increase Figs. 3 and 4 .All multiple regression models between biweekly

abundances and environmental factors produced bystepwise variable selection, are summarized in Table1. The R2 values ranged from 0.03, for C. typicusadults, to 0.63, for T. stylifera copepodits. Tempera-ture and salinity were the most significant environ-mental parameters accounting for the variability of

Fig. 2. Abundance of total copepods, Saronikos Gulf, January 1989–December 1993.


Fig. 3. Abundance of the eight dominant copepods, Saronikos Gulf, January 1989–December 1993.


Ž .Fig. 3 continued .



copepod abundances. Temperature was found to berelated with almost all copepods abundances. Salin-ity was related with the abundance of total copepods,P. parÕus, A. clausi, Oithona spp. and Centropagesspp. Chlorophyll proved to be significant on onlythree occasions. The best multiple regression models

Ž 2 .were produced for T. stylifera R s0.15–0.63 ,Ž 2 .Centropages spp. R s 0.40–0.45 and Cteno-

Ž 2 .calanus Õanus R s0.26–0.46 and the worst forŽ 2 .Oithona spp. adults R s0.07 , Clausocalanus spp.

Ž 2 . Ž 2 .R s0.07–0.12 and A. clausi R s0.07–0.15 .The estimated equations of simple regression

models between the mean annual copepod abun-dances and the different environmental factors, are

presented in Table 2. The R2 values ranged from0.83, for P. parÕus, to 0.95, for T. stylifera. Salinitywas proved the most significant environmental pa-rameter related with the interannual variability oftotal copepods and Clausocalanus spp. Chlorophyll

Ž 2 .showed a strong negative correlation R s0.95with T. stylifera abundance.

4. Discussion

The dominant copepods, examined in the presentstudy, comprised on average 88% of the total num-bers. P. parÕus and A. clausi predominated the


copepod community and represented 44% of thetotal number on average. The copepods P.parÕus, A.clausi, T. stylifera and C. typicus have been charac-terized as key species for the Gulf of Naples in the

ŽMediterranean Mazzocchi and Ribera d’Alcala,.1995 . This is true in the present study, for the

coastal area of the Saronikos Gulf. The above speciesnever disappear completely from the Gulf of Naples.On the contrary, in the Saronikos Gulf, only P.parÕus seems to be continuously present, whereas C.typicus has a particularly limited seasonal occur-rence. The copepods P. parÕus, Clausocalanus fur-catus and T. stylifera have been also found to pre-

dominate the copepod community in the SaronikosŽ .Gulf during 1984–1985 Siokou-Frangou, 1996 .

Both Clausocalanus spp. and Oithona spp. abun-dances exhibited an increasing trend and comprisedan important fraction of the total copepods. Thesecopepods, known as dominant in all oceans, werefound to be the most abundant genera in the coastal

Žarea of the northwestern Mediterranean Kouwen-.berg and Razouls, 1990 and the Aegean Sea

Ž .Siokou-Frangou et al., 1994 . Both genera havebeen found to show some similarities in life historiesand dietary requirements, such as carrying of eggsacs, low reproduction rates, preference for animal

Fig. 4. Mean annual abundance of total copepods and the eight dominant copepods, Saronikos Gulf, 1989–1993.



food and ability to survive under a wide range ofŽenvironmental conditions Sazhina, 1982; Kleppel et

.al., 1988; Mazzocchi and Ribera d’Alcala, 1995 .Temperature was found to be related, with almost

all copepods. This is presumably, at least partly,related to the timing of their seasonal cycles. Thetype of correlation, either positive or negative, rely

Žon the species ecological habits maxima occurred.during the warm or cold period . During a study of

the annual variability of mesozooplanktonmetabolism at the same area, temperature was foundto be the most significant factor driving this variabil-

Ž .ity Christou and Moraitou-Apostolopoulou, 1995 .Temperature was also reported to be related with the

seasonal evolution of zooplankton in the SaronikosŽ .Gulf Siokou-Frangou, 1996 .

Zooplankton interannual variability has beenlinked, in the North Sea and Northeast Atlantic, toclimatic factors, such as changes in the North At-

Žlantic current and localized wind events e.g. Cole-.brook, 1985, 1986 . Other experimental studies have

indicated that variability in plankton abundance andproductivity may be influenced by environmentalconditions, such as vertical structure of water columnŽ .Mullin et al., 1985; Alcaraz et al., 1988 , tempera-

Ž .ture McLaren, 1963; Davis, 1987 and water massŽexchange Kiorboe et al., 1988; Lindahl and Hern-.roth, 1988 . Long-term changes of many copepod


Table 1w Ž . Ž . xStepwise variable selection log ysa "SE qb "SE log x between copepod abundance and environmental factors as independent

variables, January 1989–December 19932Multiple regression R F

Ž . ŽŽ . Ž .log COPsy74.88 "18.24 q1.78 "0.31 log Tq47.49 "11.41 log S 0.24 20.21Ž . Ž . Ž . Ž .log PPadq1 sy83.16 "36.26 q4.26 "0.62 log Tq49.86 "22.70 log S 0.27 23.99

Ž . Ž .log PPcosy1.35 "0.56 q2.49 "0.44 log T 0.20 32.04Ž . Ž .log PPsy1.74 "0.58 q2.94 "0.46 log T 0.25 41.39

)Ž . Ž . Ž .log AC adq1 sy134.31 "42.51 q85.38 "26.77 log S 0.07 10.17Ž . Ž . Ž . Ž .log ACcoq1 sy135.65 "40.45 y1.72 "0.69 log Tq87.57 "25.32 log S 0.15 12.28Ž . Ž . Ž .log ACq1 sy151.80 "41.88 q96.58 "26.37 log S 0.09 13.41Ž . Ž . Ž .log CSadq1 sy1.51 "0.66 q2.19 "0.52 log T 0.12 18.04

)Ž . Ž . Ž .log CScoq1 sy0.50 "0.69 q1.72 "0.54 log T 0.07 10.20Ž . Ž . Ž .log CSq1 sy0.48 "0.67 q1.83 "0.52 log T 0.08 12.24

)Ž . Ž . Ž .log OSadq1 sy87.36 "26.90 q55.75 "16.94 log S 0.07 10.83Ž . Ž . Ž .log TSadq1 sy1.74 "0.41 q1.55 "0.32 log T 0.15 23.32Ž . Ž . Ž .log TScoq1 sy7.07 "0.57 q6.46 "0.45 log T 0.63 206.34Ž . Ž . Ž .log TSq1 sy7.01 "0.58 q6.43 "0.45 log T 0.62 203.43Ž . Ž . Ž . Ž .log CPadq1 sy4.26 "0.50 q3.65 "0.39 log Tq0.20 "0.10 log C 0.42 46.77Ž . Ž . Ž . Ž .log CPcoq1 sy65.21 "29.39 q4.53 "0.50 log Tq37.70 "18.40 log S 0.40 41.28Ž . Ž . Ž .log CPq1 sy5.93 "0.64 q5.05 "0.50 log T 0.45 101.23

) )Ž . Ž . Ž .log CTadq1 s1.01 "0.42 y0.68 "0.33 log T 0.03 4.23Ž . Ž . Ž .log CTcoq1 s4.64 "0.70 y3.30 "0.55 log T 0.22 36.12Ž . Ž . Ž .log CTq1 s4.94 "0.71 y3.50 "0.56 log T 0.24 39.36Ž . Ž . Ž .log CVadq1 s2.47 "0.35 y1.78 "0.27 log T 0.26 42.55Ž . Ž . Ž . Ž .log CVcoq1 s5.72 "0.54 y4.01 "0.43 log Tq0.34 "0.11 log C 0.45 50.64Ž . Ž . Ž . Ž .log CVq1 s6.07 "0.57 y4.26 "0.44 log Tq0.33 "0.11 log C 0.46 53.63

COPs total copepods; PPsParacalanus parÕus; ACsAcartia clausi; CSsClausocalanus spp.; OSsOithona spp.; TSsTemorastylifera; CPsCentropages spp.; CTsCentropages typicus; CVsCtenocalanus Õanus; adsadults; coscopepodits. Ts temperature;Sssalinity; Cschlorophyll. For all regressions ns124, p-0.001, except ) p-0.01, ) ) p-0.05.

species and other zooplankton groups have been alsofound to be related with changes in temperature and

Žsalinity Viitasalo et al., 1990; Meise-Munns et al.,.1990; Baranovic et al., 1993 . In the Mediterranean,

a decline of zooplankton abundance from 1984 toŽ1990 was observed in the Gulf of Naples Mazzocchi

.and Ribera d’Alcala, 1995 , whereas an increasingtrend of zooplankton abundance from 1960 to 1982was related to eutrophication, in the Adriatic SeaŽ .Baranovic et al., 1993 . In the present study, salinitywas significantly related with interannual variabilityof copepods.

The observed relations of salinity with the fluctua-tions in copepod abundance probably reflect changesin the proportions of different water masses. Theparallel strong long-term increasing trend detected inboth salinity and total copepods, may indicate thatmost copepods respond to a possible change in thehydrological regime of the area. Such a change couldbe the intrusion of more saline water from the South

Aegean Sea into the gulf. Note that the Aegean Seais the main water source for the Saronikos Gulf,providing waters masses either from the northern

Ž . Žpart less saline or from the southern part more.saline , depending on the circulation regime in theŽ .area S. Christianidis, pers. commun., 1991 . It is

Table 2w Ž .Statistically significant regressions log y s a "SE q

Ž . xb "SE log x between copepod mean annual abundance andenvironmental factors as independent variables, 1989–1993

2Regression R F

Ž . Ž .logCOPsy82.67 "16.77 q53.91 "10.56 log S 0.90 26.07Ž . Ž .logCSsy104.46 "27.22 q67.14 "17.14 log S 0.84 15.34

Ž . Ž .logPPsy27.16 "7.34 q22.97 "5.72 log T 0.83 16.12Ž . Ž .logTSs1.74 "0.02 y0.94 "0.13 log C 0.95 53.56

COP s total copepods; CS s Clausocalanus spp.; PP sParacalanus parÕus; TSsTemora stylifera. T s temperature; Sssalinity; Cschlorophyll. For all regressions ns5, p-0.01.


also worth mentioning that Kouwenberg and RazoulsŽ .1990 related the considerable increase of Clauso-calanus spp. in the northwestern Mediterranean dur-ing the 1986–1988 period with an increase in salin-ity. In the present study, a parallel increase of salin-ity and Clausocalanus spp., confirmed by the regres-

Ž .sion models Table 2 , was also evident.Chlorophyll values exhibited a strong negative

correlation with interannual variability of T. stylif-era. This could indicate that in the study area, thiscopepod showed some preference for food other thanphytoplankton, such as small flagellates, microzoo-plankton, other suspended material or a combinationof all. Food other than phytoplankton has been indi-cated that may be important for zooplankton popula-

Žtions in the area Christou and Moraitou-Apos-.tolopoulou, 1995 . This situation is expected espe-

cially during the periods of food limitation in theŽ .area Christou and Verriopoulos, 1993 . The ability

of copepods to adapt their feeding strategies respond-ing to food environment has been recently reviewed

Ž .by Kleppel 1993 .With a 5-year time series of data, interannual

variability is difficult to elucidate and only pro-nounced relationships can be identified, such as theimportance of salinity. The specific mechanismsdriving the observed relationships between environ-mental factors and copepod populations need to beaddressed by extending the time series and employ-ing additional in situ and laboratory studies.

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Interannual variability of copepods in a Mediterranean coastal area (Saronikos Gulf, Aegean Sea)