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Interannual variability of copepods in a Mediterranean coastal area (Saronikos Gulf, Aegean Sea)
Journal of Marine Systems 15 Ž1998. 523–532
Interannual variability of copepods in a Mediterranean coastal area ž 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 the eastern Mediterranean Sea ŽSaronikos 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 environmental parameters, almost all, exhibited pronounced annual cycles. Most copepods revealed repeated patterns and considerable interannual variability. Both salinity and abundance of total copepods, revealed a clear interannual increase from 1989 to 1993. Multiple regression models, based on stepwise variable selection, suggested that temperature and salinity were the most significant environmental parameters accounting for the variability of abundances. Simple regression models applied on mean annual values reveal the importance of salinity as the most significant factor affecting interannual variability of copepods. 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 on copepods are few and concern mainly the northwest regions ŽKouwenberg and Razouls, 1990; Mazzocchi and Ribera d’Alcala, 1995. and the Adriatic Sea ŽRegner, 1985; Baranovic et al., 1993.. Besides, the determination of factors driving interannual variability in marine zooplankton is an important issue. The comprehensive description of long-term temporal cycles of the biological communities and the environmental factors is fundamental in order to understand the overall range of this variability. Through this type 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 offshore waters often interact with complex dynamics on a wide range of temporal and spatial scales and fluctuations in ecological parameters can be quite complex. Copepods, characterized by extreme flexibility in adapting to a fluctuating environment and tending to maintain a stable standing stock even in the presence of variable food sources ŽMazzocchi and Ribera d’Alcala, 1995., seem to constitute a valuable tool for the study of long-term variability in coastal areas. In the present study, the patterns of abundance of the dominant copepods as well as that of the total copepods in the coastal area of the Saronikos Gulf ŽAegean Sea., are described, during a 5-year period. Their relationships with the environmental factors are also examined.
0924-7963r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 9 2 4 - 7 9 6 3 Ž 9 7 . 0 0 0 8 0 - 8
524
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 1. Temperature, salinity and chlorophyll-a averaged over the water column, Saronikos Gulf, January 1989–December 1993.
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
525
2. Materials and methods
3. Results
The results were based on 124 zooplankton samples collected biweekly during a 5-year period, from January 1989 through December 1993. Samples were collected by oblique hauls at a coastal station Ž12 m depth. in the eastern Saronikos Gulf ŽAegean Sea.. The station is typical of the coastal area of the Saronikos Gulf and considered representative for the larger area from which populations may be advected. A 200 mm net ŽWP2., equipped with a Hydrobios flowmeter, was used. The samples were preserved in 4% buffered formalin. Copepod adults and copepodids were identified to the speciesrgenus level. The abundances were expressed as number of individuals per cubic meter Žind. my3 .. Temperature, salinity and chlorophyll-a values were also determined from samples taken at 1, 5 and 10 m, using a 2 l Hydrobios water sampler equipped with a Hydrobios thermometer, and the mean values for the water column were estimated. The effect of the environmental factors on copepod abundance was examined using simple and multiple regression analysis, the latter based on stepwise variable selection, of log-transformed data. The time between two successive samplings ranged from 12 to 17 days Žmean s 14.4 days, SD s 1.5 days.. However, for the purposes of this study the sampling interval was considered constant Žs 14 days..
All environmental factors, exhibited pronounced annual cycles, except chlorophyll ŽFig. 1.. Salinity revealed a clear interannual increase from 1989 to 1993, but no such trend was evident for temperature. Pronounced annual cycles were also true for most copepod species but not for total copepods ŽFigs. 2 and 3.. Centropages spp. Žmainly C. ponticus ., Centropages typicus and Ctenocalanus Õanus were characterized by the strongest seasonal variability. Paracalanus parÕus, the only true perennial species, Clausocalanus spp. Žmainly C. furcatus . and Oithona spp. Žmainly O. similis and O. plumifera. were present all year round. Most copepods revealed repeated patterns and considerable interannual variability ŽFigs. 3 and 4.. The abundance of total copepods showed a strong increasing trend from 1989 to 1993 ŽFigs. 2 and 4.. Clausocalanus spp., Oithona spp., Acartia clausi and C. typicus, also showing a rather increasing trend, seem mostly to account for such an increase ŽFigs. 3 and 4.. All multiple regression models between biweekly abundances and environmental factors produced by stepwise variable selection, are summarized in Table 1. The R 2 values ranged from 0.03, for C. typicus adults, to 0.63, for T. stylifera copepodits. Temperature and salinity were the most significant environmental parameters accounting for the variability of
Fig. 2. Abundance of total copepods, Saronikos Gulf, January 1989–December 1993.
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E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3. Abundance of the eight dominant copepods, Saronikos Gulf, January 1989–December 1993.
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3 Žcontinued..
527
528
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3 Žcontinued..
copepod abundances. Temperature was found to be related with almost all copepods abundances. Salinity was related with the abundance of total copepods, P. parÕus, A. clausi, Oithona spp. and Centropages spp. Chlorophyll proved to be significant on only three occasions. The best multiple regression models were produced for T. stylifera Ž R 2 s 0.15–0.63., Centropages spp. Ž R 2 s 0.40–0.45. and Ctenocalanus Õanus Ž R 2 s 0.26–0.46. and the worst for Oithona spp. adults Ž R 2 s 0.07., Clausocalanus spp. Ž R 2 s 0.07–0.12. and A. clausi Ž R 2 s 0.07–0.15.. The estimated equations of simple regression models between the mean annual copepod abundances and the different environmental factors, are
presented in Table 2. The R 2 values ranged from 0.83, for P. parÕus, to 0.95, for T. stylifera. Salinity was proved the most significant environmental parameter related with the interannual variability of total copepods and Clausocalanus spp. Chlorophyll showed a strong negative correlation Ž R 2 s 0.95. with T. stylifera abundance.
4. Discussion The dominant copepods, examined in the present study, comprised on average 88% of the total numbers. P. parÕus and A. clausi predominated the
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
copepod community and represented 44% of the total number on average. The copepods P.parÕus, A. clausi, T. stylifera and C. typicus have been characterized as key species for the Gulf of Naples in the Mediterranean ŽMazzocchi and Ribera d’Alcala, 1995.. This is true in the present study, for the coastal area of the Saronikos Gulf. The above species never 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 occurrence. The copepods P. parÕus, Clausocalanus furcatus and T. stylifera have been also found to pre-
529
dominate the copepod community in the Saronikos Gulf during 1984–1985 ŽSiokou-Frangou, 1996.. Both Clausocalanus spp. and Oithona spp. abundances exhibited an increasing trend and comprised an important fraction of the total copepods. These copepods, known as dominant in all oceans, were found to be the most abundant genera in the coastal area of the northwestern Mediterranean ŽKouwenberg and Razouls, 1990. and the Aegean Sea ŽSiokou-Frangou et al., 1994.. Both genera have been found to show some similarities in life histories and dietary requirements, such as carrying of egg sacs, low reproduction rates, preference for animal
Fig. 4. Mean annual abundance of total copepods and the eight dominant copepods, Saronikos Gulf, 1989–1993.
530
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 4 Žcontinued..
food and ability to survive under a wide range of environmental conditions ŽSazhina, 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. The type of correlation, either positive or negative, rely on the species ecological habits Žmaxima occurred during the warm or cold period.. During a study of the annual variability of mesozooplankton metabolism at the same area, temperature was found to be the most significant factor driving this variability ŽChristou and Moraitou-Apostolopoulou, 1995.. Temperature was also reported to be related with the
seasonal evolution of zooplankton in the Saronikos Gulf ŽSiokou-Frangou, 1996.. Zooplankton interannual variability has been linked, in the North Sea and Northeast Atlantic, to climatic factors, such as changes in the North Atlantic current and localized wind events Že.g. Colebrook, 1985, 1986.. Other experimental studies have indicated that variability in plankton abundance and productivity may be influenced by environmental conditions, such as vertical structure of water column ŽMullin et al., 1985; Alcaraz et al., 1988., temperature ŽMcLaren, 1963; Davis, 1987. and water mass exchange ŽKiorboe et al., 1988; Lindahl and Hernroth, 1988.. Long-term changes of many copepod
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
531
Table 1 Stepwise variable selection wlog y s aŽ"SE. q bŽ"SE.log x x between copepod abundance and environmental factors as independent variables, January 1989–December 1993 Multiple regression
R2
F
log COPs y74.88 Ž"18.24. q 1.78ŽŽ"0.31.log T q 47.49Ž"11.41.log S logŽPPad q 1. s y83.16Ž"36.26. q 4.26Ž"0.62.log T q 49.86Ž"22.70.log S log PPco s y1.35Ž"0.56. q 2.49Ž"0.44.log T log PP s y1.74Ž"0.58. q 2.94Ž"0.46.log T logŽAC ad q 1. s y134.31Ž"42.51. q 85.38 Ž"26.77.log S logŽAC co q 1. s y135.65Ž"40.45. y 1.72Ž"0.69.log T q 87.57Ž"25.32.log S logŽAC q 1. s y151.80Ž"41.88. q 96.58Ž"26.37.log S logŽCSad q 1. s y1.51Ž"0.66. q 2.19Ž"0.52.log T logŽCSco q 1. s y0.50Ž"0.69. q 1.72Ž"0.54.log T logŽCS q 1. s y0.48Ž"0.67. q 1.83Ž"0.52.log T logŽOSad q 1. s y87.36Ž"26.90. q 55.75Ž"16.94.log S logŽTS ad q 1. s y1.74Ž"0.41. q 1.55Ž"0.32.log T logŽTSco q 1. s y7.07Ž"0.57. q 6.46Ž"0.45.log T logŽTS q 1. s y7.01Ž"0.58. q 6.43Ž"0.45.log T logŽCPad q 1. s y4.26Ž"0.50. q 3.65Ž"0.39.log T q 0.20Ž"0.10.log C logŽCPco q 1. s y65.21Ž"29.39. q 4.53Ž"0.50.log T q 37.70Ž"18.40.log S logŽCP q 1. s y5.93Ž"0.64. q 5.05Ž"0.50.log T logŽCTad q 1. s 1.01Ž"0.42. y 0.68Ž"0.33.log T logŽCTco q 1. s 4.64Ž"0.70. y 3.30Ž"0.55.log T logŽCT q 1. s 4.94Ž"0.71. y 3.50Ž"0.56.log T logŽCVad q 1. s 2.47Ž"0.35. y 1.78Ž"0.27.log T logŽCVco q 1. s 5.72Ž"0.54. y 4.01Ž"0.43.log T q 0.34Ž"0.11.log C logŽCV q 1. s 6.07Ž"0.57. y 4.26Ž"0.44.log T q 0.33Ž"0.11.log C
0.24 0.27 0.20 0.25 0.07 ) 0.15 0.09 0.12 0.07 ) 0.08 0.07 ) 0.15 0.63 0.62 0.42 0.40 0.45 0.03 ) ) 0.22 0.24 0.26 0.45 0.46
20.21 23.99 32.04 41.39 10.17 12.28 13.41 18.04 10.20 12.24 10.83 23.32 206.34 203.43 46.77 41.28 101.23 4.23 36.12 39.36 42.55 50.64 53.63
COP s total copepods; PP s Paracalanus parÕus; AC s Acartia clausi; CS s Clausocalanus spp.; OS s Oithona spp.; TS s Temora stylifera; CP s Centropages spp.; CT s Centropages typicus; CV s Ctenocalanus Õanus; ad s adults; co s copepodits. T s temperature; S s salinity; C s chlorophyll. For all regressions n s 124, p - 0.001, except ) p - 0.01, ) ) p - 0.05.
species and other zooplankton groups have been also found to be related with changes in temperature and salinity ŽViitasalo et al., 1990; Meise-Munns et al., 1990; Baranovic et al., 1993.. In the Mediterranean, a decline of zooplankton abundance from 1984 to 1990 was observed in the Gulf of Naples ŽMazzocchi and Ribera d’Alcala, 1995., whereas an increasing trend of zooplankton abundance from 1960 to 1982 was related to eutrophication, in the Adriatic Sea ŽBaranovic et al., 1993.. In the present study, salinity was significantly related with interannual variability of copepods. The observed relations of salinity with the fluctuations in copepod abundance probably reflect changes in the proportions of different water masses. The parallel strong long-term increasing trend detected in both salinity and total copepods, may indicate that most copepods respond to a possible change in the hydrological regime of the area. Such a change could be the intrusion of more saline water from the South
Aegean Sea into the gulf. Note that the Aegean Sea is the main water source for the Saronikos Gulf, providing waters masses either from the northern part Žless saline. or from the southern part Žmore saline., depending on the circulation regime in the area ŽS. Christianidis, pers. commun., 1991.. It is
Table 2 Statistically significant regressions w log y s aŽ"SE . q bŽ"SE.log x x between copepod mean annual abundance and environmental factors as independent variables, 1989–1993 Regression
R2
F
log COPsy82.67Ž"16.77.q53.91Ž"10.56.log S log CSsy104.46Ž"27.22.q67.14Ž"17.14.log S log PPsy27.16Ž"7.34.q22.97Ž"5.72.log T log TSs1.74Ž"0.02.y0.94Ž"0.13.log C
0.90 0.84 0.83 0.95
26.07 15.34 16.12 53.56
COP s total copepods; CS s Clausocalanus spp.; PP s Paracalanus parÕus; TSsTemora stylifera. T s temperature; S ssalinity; C s chlorophyll. For all regressions ns 5, p- 0.01.
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E.D. Christour Journal of Marine Systems 15 (1998) 523–532
also worth mentioning that Kouwenberg and Razouls Ž1990. related the considerable increase of Clausocalanus spp. in the northwestern Mediterranean during the 1986–1988 period with an increase in salinity. In the present study, a parallel increase of salinity and Clausocalanus spp., confirmed by the regression models ŽTable 2., was also evident. Chlorophyll values exhibited a strong negative correlation with interannual variability of T. stylifera. This could indicate that in the study area, this copepod showed some preference for food other than phytoplankton, such as small flagellates, microzooplankton, other suspended material or a combination of all. Food other than phytoplankton has been indicated that may be important for zooplankton populations in the area ŽChristou and Moraitou-Apostolopoulou, 1995.. This situation is expected especially during the periods of food limitation in the area ŽChristou and Verriopoulos, 1993.. The ability of copepods to adapt their feeding strategies responding to food environment has been recently reviewed by Kleppel Ž1993.. With a 5-year time series of data, interannual variability is difficult to elucidate and only pronounced relationships can be identified, such as the importance of salinity. The specific mechanisms driving the observed relationships between environmental factors and copepod populations need to be addressed by extending the time series and employing additional in situ and laboratory studies.
References Alcaraz, M., Saiz, E., Marrasse, C., Vague, D., 1988. Effects of turbulence on the development of phytoplankton biomass and copepod populations in marine microcosms. Mar. Ecol. Prog. Ser. 49, 117–125. Baranovic, A., Solic, M., Vucetic, T., Krstulovic, N., 1993. Temporal fluctuations of zooplankton and bacteria in the middle Adriatic Sea. Mar. Ecol. Prog. Ser. 92, 65–75. Christou, E.D., Moraitou-Apostolopoulou, M., 1995. Metabolism and feeding of mesozooplankton at the eastern Mediterranean ŽHellenic coastal waters.. Mar. Ecol. Prog. Ser. 126, 39–48. Christou, E.D., Verriopoulos, G.C., 1993. Analysis of the biological cycle of Acartia clausi ŽCopepoda. in a meso-oligotrophic
coastal area of the eastern Mediterranean Sea using time-series analysis. Mar. Biol. 115, 643–651. Colebrook, J.M., 1985. Sea surface temperature and zooplankton, North Sea, 1948 to 1983. J. Cons. Int. Explor. Mer 42, 179–185. Colebrook, J.M., 1986. Environmental influences on long-term variability in marine plankton. Hydrobiologia 142, 309–325. Davis, C.S., 1987. Components of the zooplankton production cycle in the temperate ocean. J. Mar. Res. 45, 947–983. Kiorboe, T., Munk, P., Richardson, K., Christensen, V., Paulsen, H.K., 1988. Plankton dynamics and larval herring growth, drift and survival in a frontal area. Mar. Ecol. Prog. Ser. 44, 205–219. Kleppel, G.S., 1993. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 99, 183–195. Kleppel, G.S., Frazel, D., Pieper, R.E., Holliday, D.V., 1988. Natural diets of zooplankton off southern California. Mar. Ecol. Prog. Ser. 49, 231–241. Kouwenberg, J., Razouls, C., 1990. The incidence of environmental factors on the evolution of copepod populations in the ‘Golfe du Lion’ during the period 1986–88 in comparison with the period 1957–64. Bull. Soc. Zool. Fr. 115, 23–36. Lindahl, O., Hernroth, L., 1988. Large-scale and long-term variations in the zooplankton community of the Gullmar fjord, Sweden, in relation to advective processes. Mar. Ecol. Prog. Ser. 43, 161–171. Mazzocchi, M.G., Ribera d’Alcala, M., 1995. Recurrent patterns in zooplankton structure and succession in a variable coastal environment. ICES J. Mar. Sci. 52, 679–691. McLaren, I.A., 1963. Effects of temperature on growth of zooplankton and the adaptive value of vertical migration. J. Fish. Res. Bd. Can. 20, 685–727. Meise-Munns, C., Green, J., Ingham, M., Mountain, D., 1990. Interannual variability in the copepod populations of George Bank and the western Gulf of Maine. Mar. Ecol. Prog. Ser. 65, 225–232. Mullin, M.M., Brooks, E.R., Reid, F.M., Napp, J., Stewart, E.F., 1985. Vertical structure of nearshore plankton off Southern California: a storm and a larval fish food web. Fish. Bull. U.S. 83, 151–170. Regner, D., 1985. Seasonal and multiannual dynamics of copepods in the Middle Adriatic. Acta Adriat. 26, 11–99. Sazhina, L.I., 1982. The pattern of copepod production in the Atlantic Ocean. Ekol. Morya 11, 21–28. Siokou-Frangou, I., 1996. Zooplankton annual cycle in a Mediterranean coastal area. J. Plankton Res. 18, 203–223. Siokou-Frangou, I., Pancucci-Papadopoulou, M.A., Christou, E., 1994. Sur la repartition du zooplankton superficiel des mers entourant la Grece ŽPrintemps 1987.. Biol. Gallo-Hellen. 21, 313–330. Viitasalo, M., Vuorinen, I., Ranta, E., 1990. Changes in crustacean mesozooplankton and some environmental parameters in the Archipelago Sea ŽNorthern Baltic. in 1976–1984. Ophelia 31, 207–217.
Interannual variability of copepods in a Mediterranean coastal area ž 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 the eastern Mediterranean Sea ŽSaronikos 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 environmental parameters, almost all, exhibited pronounced annual cycles. Most copepods revealed repeated patterns and considerable interannual variability. Both salinity and abundance of total copepods, revealed a clear interannual increase from 1989 to 1993. Multiple regression models, based on stepwise variable selection, suggested that temperature and salinity were the most significant environmental parameters accounting for the variability of abundances. Simple regression models applied on mean annual values reveal the importance of salinity as the most significant factor affecting interannual variability of copepods. 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 on copepods are few and concern mainly the northwest regions ŽKouwenberg and Razouls, 1990; Mazzocchi and Ribera d’Alcala, 1995. and the Adriatic Sea ŽRegner, 1985; Baranovic et al., 1993.. Besides, the determination of factors driving interannual variability in marine zooplankton is an important issue. The comprehensive description of long-term temporal cycles of the biological communities and the environmental factors is fundamental in order to understand the overall range of this variability. Through this type 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 offshore waters often interact with complex dynamics on a wide range of temporal and spatial scales and fluctuations in ecological parameters can be quite complex. Copepods, characterized by extreme flexibility in adapting to a fluctuating environment and tending to maintain a stable standing stock even in the presence of variable food sources ŽMazzocchi and Ribera d’Alcala, 1995., seem to constitute a valuable tool for the study of long-term variability in coastal areas. In the present study, the patterns of abundance of the dominant copepods as well as that of the total copepods in the coastal area of the Saronikos Gulf ŽAegean Sea., are described, during a 5-year period. Their relationships with the environmental factors are also examined.
0924-7963r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 9 2 4 - 7 9 6 3 Ž 9 7 . 0 0 0 8 0 - 8
524
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 1. Temperature, salinity and chlorophyll-a averaged over the water column, Saronikos Gulf, January 1989–December 1993.
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
525
2. Materials and methods
3. Results
The results were based on 124 zooplankton samples collected biweekly during a 5-year period, from January 1989 through December 1993. Samples were collected by oblique hauls at a coastal station Ž12 m depth. in the eastern Saronikos Gulf ŽAegean Sea.. The station is typical of the coastal area of the Saronikos Gulf and considered representative for the larger area from which populations may be advected. A 200 mm net ŽWP2., equipped with a Hydrobios flowmeter, was used. The samples were preserved in 4% buffered formalin. Copepod adults and copepodids were identified to the speciesrgenus level. The abundances were expressed as number of individuals per cubic meter Žind. my3 .. Temperature, salinity and chlorophyll-a values were also determined from samples taken at 1, 5 and 10 m, using a 2 l Hydrobios water sampler equipped with a Hydrobios thermometer, and the mean values for the water column were estimated. The effect of the environmental factors on copepod abundance was examined using simple and multiple regression analysis, the latter based on stepwise variable selection, of log-transformed data. The time between two successive samplings ranged from 12 to 17 days Žmean s 14.4 days, SD s 1.5 days.. However, for the purposes of this study the sampling interval was considered constant Žs 14 days..
All environmental factors, exhibited pronounced annual cycles, except chlorophyll ŽFig. 1.. Salinity revealed a clear interannual increase from 1989 to 1993, but no such trend was evident for temperature. Pronounced annual cycles were also true for most copepod species but not for total copepods ŽFigs. 2 and 3.. Centropages spp. Žmainly C. ponticus ., Centropages typicus and Ctenocalanus Õanus were characterized by the strongest seasonal variability. Paracalanus parÕus, the only true perennial species, Clausocalanus spp. Žmainly C. furcatus . and Oithona spp. Žmainly O. similis and O. plumifera. were present all year round. Most copepods revealed repeated patterns and considerable interannual variability ŽFigs. 3 and 4.. The abundance of total copepods showed a strong increasing trend from 1989 to 1993 ŽFigs. 2 and 4.. Clausocalanus spp., Oithona spp., Acartia clausi and C. typicus, also showing a rather increasing trend, seem mostly to account for such an increase ŽFigs. 3 and 4.. All multiple regression models between biweekly abundances and environmental factors produced by stepwise variable selection, are summarized in Table 1. The R 2 values ranged from 0.03, for C. typicus adults, to 0.63, for T. stylifera copepodits. Temperature and salinity were the most significant environmental parameters accounting for the variability of
Fig. 2. Abundance of total copepods, Saronikos Gulf, January 1989–December 1993.
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E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3. Abundance of the eight dominant copepods, Saronikos Gulf, January 1989–December 1993.
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3 Žcontinued..
527
528
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 3 Žcontinued..
copepod abundances. Temperature was found to be related with almost all copepods abundances. Salinity was related with the abundance of total copepods, P. parÕus, A. clausi, Oithona spp. and Centropages spp. Chlorophyll proved to be significant on only three occasions. The best multiple regression models were produced for T. stylifera Ž R 2 s 0.15–0.63., Centropages spp. Ž R 2 s 0.40–0.45. and Ctenocalanus Õanus Ž R 2 s 0.26–0.46. and the worst for Oithona spp. adults Ž R 2 s 0.07., Clausocalanus spp. Ž R 2 s 0.07–0.12. and A. clausi Ž R 2 s 0.07–0.15.. The estimated equations of simple regression models between the mean annual copepod abundances and the different environmental factors, are
presented in Table 2. The R 2 values ranged from 0.83, for P. parÕus, to 0.95, for T. stylifera. Salinity was proved the most significant environmental parameter related with the interannual variability of total copepods and Clausocalanus spp. Chlorophyll showed a strong negative correlation Ž R 2 s 0.95. with T. stylifera abundance.
4. Discussion The dominant copepods, examined in the present study, comprised on average 88% of the total numbers. P. parÕus and A. clausi predominated the
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
copepod community and represented 44% of the total number on average. The copepods P.parÕus, A. clausi, T. stylifera and C. typicus have been characterized as key species for the Gulf of Naples in the Mediterranean ŽMazzocchi and Ribera d’Alcala, 1995.. This is true in the present study, for the coastal area of the Saronikos Gulf. The above species never 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 occurrence. The copepods P. parÕus, Clausocalanus furcatus and T. stylifera have been also found to pre-
529
dominate the copepod community in the Saronikos Gulf during 1984–1985 ŽSiokou-Frangou, 1996.. Both Clausocalanus spp. and Oithona spp. abundances exhibited an increasing trend and comprised an important fraction of the total copepods. These copepods, known as dominant in all oceans, were found to be the most abundant genera in the coastal area of the northwestern Mediterranean ŽKouwenberg and Razouls, 1990. and the Aegean Sea ŽSiokou-Frangou et al., 1994.. Both genera have been found to show some similarities in life histories and dietary requirements, such as carrying of egg sacs, low reproduction rates, preference for animal
Fig. 4. Mean annual abundance of total copepods and the eight dominant copepods, Saronikos Gulf, 1989–1993.
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E.D. Christour Journal of Marine Systems 15 (1998) 523–532
Fig. 4 Žcontinued..
food and ability to survive under a wide range of environmental conditions ŽSazhina, 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. The type of correlation, either positive or negative, rely on the species ecological habits Žmaxima occurred during the warm or cold period.. During a study of the annual variability of mesozooplankton metabolism at the same area, temperature was found to be the most significant factor driving this variability ŽChristou and Moraitou-Apostolopoulou, 1995.. Temperature was also reported to be related with the
seasonal evolution of zooplankton in the Saronikos Gulf ŽSiokou-Frangou, 1996.. Zooplankton interannual variability has been linked, in the North Sea and Northeast Atlantic, to climatic factors, such as changes in the North Atlantic current and localized wind events Že.g. Colebrook, 1985, 1986.. Other experimental studies have indicated that variability in plankton abundance and productivity may be influenced by environmental conditions, such as vertical structure of water column ŽMullin et al., 1985; Alcaraz et al., 1988., temperature ŽMcLaren, 1963; Davis, 1987. and water mass exchange ŽKiorboe et al., 1988; Lindahl and Hernroth, 1988.. Long-term changes of many copepod
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
531
Table 1 Stepwise variable selection wlog y s aŽ"SE. q bŽ"SE.log x x between copepod abundance and environmental factors as independent variables, January 1989–December 1993 Multiple regression
R2
F
log COPs y74.88 Ž"18.24. q 1.78ŽŽ"0.31.log T q 47.49Ž"11.41.log S logŽPPad q 1. s y83.16Ž"36.26. q 4.26Ž"0.62.log T q 49.86Ž"22.70.log S log PPco s y1.35Ž"0.56. q 2.49Ž"0.44.log T log PP s y1.74Ž"0.58. q 2.94Ž"0.46.log T logŽAC ad q 1. s y134.31Ž"42.51. q 85.38 Ž"26.77.log S logŽAC co q 1. s y135.65Ž"40.45. y 1.72Ž"0.69.log T q 87.57Ž"25.32.log S logŽAC q 1. s y151.80Ž"41.88. q 96.58Ž"26.37.log S logŽCSad q 1. s y1.51Ž"0.66. q 2.19Ž"0.52.log T logŽCSco q 1. s y0.50Ž"0.69. q 1.72Ž"0.54.log T logŽCS q 1. s y0.48Ž"0.67. q 1.83Ž"0.52.log T logŽOSad q 1. s y87.36Ž"26.90. q 55.75Ž"16.94.log S logŽTS ad q 1. s y1.74Ž"0.41. q 1.55Ž"0.32.log T logŽTSco q 1. s y7.07Ž"0.57. q 6.46Ž"0.45.log T logŽTS q 1. s y7.01Ž"0.58. q 6.43Ž"0.45.log T logŽCPad q 1. s y4.26Ž"0.50. q 3.65Ž"0.39.log T q 0.20Ž"0.10.log C logŽCPco q 1. s y65.21Ž"29.39. q 4.53Ž"0.50.log T q 37.70Ž"18.40.log S logŽCP q 1. s y5.93Ž"0.64. q 5.05Ž"0.50.log T logŽCTad q 1. s 1.01Ž"0.42. y 0.68Ž"0.33.log T logŽCTco q 1. s 4.64Ž"0.70. y 3.30Ž"0.55.log T logŽCT q 1. s 4.94Ž"0.71. y 3.50Ž"0.56.log T logŽCVad q 1. s 2.47Ž"0.35. y 1.78Ž"0.27.log T logŽCVco q 1. s 5.72Ž"0.54. y 4.01Ž"0.43.log T q 0.34Ž"0.11.log C logŽCV q 1. s 6.07Ž"0.57. y 4.26Ž"0.44.log T q 0.33Ž"0.11.log C
0.24 0.27 0.20 0.25 0.07 ) 0.15 0.09 0.12 0.07 ) 0.08 0.07 ) 0.15 0.63 0.62 0.42 0.40 0.45 0.03 ) ) 0.22 0.24 0.26 0.45 0.46
20.21 23.99 32.04 41.39 10.17 12.28 13.41 18.04 10.20 12.24 10.83 23.32 206.34 203.43 46.77 41.28 101.23 4.23 36.12 39.36 42.55 50.64 53.63
COP s total copepods; PP s Paracalanus parÕus; AC s Acartia clausi; CS s Clausocalanus spp.; OS s Oithona spp.; TS s Temora stylifera; CP s Centropages spp.; CT s Centropages typicus; CV s Ctenocalanus Õanus; ad s adults; co s copepodits. T s temperature; S s salinity; C s chlorophyll. For all regressions n s 124, p - 0.001, except ) p - 0.01, ) ) p - 0.05.
species and other zooplankton groups have been also found to be related with changes in temperature and salinity ŽViitasalo et al., 1990; Meise-Munns et al., 1990; Baranovic et al., 1993.. In the Mediterranean, a decline of zooplankton abundance from 1984 to 1990 was observed in the Gulf of Naples ŽMazzocchi and Ribera d’Alcala, 1995., whereas an increasing trend of zooplankton abundance from 1960 to 1982 was related to eutrophication, in the Adriatic Sea ŽBaranovic et al., 1993.. In the present study, salinity was significantly related with interannual variability of copepods. The observed relations of salinity with the fluctuations in copepod abundance probably reflect changes in the proportions of different water masses. The parallel strong long-term increasing trend detected in both salinity and total copepods, may indicate that most copepods respond to a possible change in the hydrological regime of the area. Such a change could be the intrusion of more saline water from the South
Aegean Sea into the gulf. Note that the Aegean Sea is the main water source for the Saronikos Gulf, providing waters masses either from the northern part Žless saline. or from the southern part Žmore saline., depending on the circulation regime in the area ŽS. Christianidis, pers. commun., 1991.. It is
Table 2 Statistically significant regressions w log y s aŽ"SE . q bŽ"SE.log x x between copepod mean annual abundance and environmental factors as independent variables, 1989–1993 Regression
R2
F
log COPsy82.67Ž"16.77.q53.91Ž"10.56.log S log CSsy104.46Ž"27.22.q67.14Ž"17.14.log S log PPsy27.16Ž"7.34.q22.97Ž"5.72.log T log TSs1.74Ž"0.02.y0.94Ž"0.13.log C
0.90 0.84 0.83 0.95
26.07 15.34 16.12 53.56
COP s total copepods; CS s Clausocalanus spp.; PP s Paracalanus parÕus; TSsTemora stylifera. T s temperature; S ssalinity; C s chlorophyll. For all regressions ns 5, p- 0.01.
532
E.D. Christour Journal of Marine Systems 15 (1998) 523–532
also worth mentioning that Kouwenberg and Razouls Ž1990. related the considerable increase of Clausocalanus spp. in the northwestern Mediterranean during the 1986–1988 period with an increase in salinity. In the present study, a parallel increase of salinity and Clausocalanus spp., confirmed by the regression models ŽTable 2., was also evident. Chlorophyll values exhibited a strong negative correlation with interannual variability of T. stylifera. This could indicate that in the study area, this copepod showed some preference for food other than phytoplankton, such as small flagellates, microzooplankton, other suspended material or a combination of all. Food other than phytoplankton has been indicated that may be important for zooplankton populations in the area ŽChristou and Moraitou-Apostolopoulou, 1995.. This situation is expected especially during the periods of food limitation in the area ŽChristou and Verriopoulos, 1993.. The ability of copepods to adapt their feeding strategies responding to food environment has been recently reviewed by Kleppel Ž1993.. With a 5-year time series of data, interannual variability is difficult to elucidate and only pronounced relationships can be identified, such as the importance of salinity. The specific mechanisms driving the observed relationships between environmental factors and copepod populations need to be addressed by extending the time series and employing additional in situ and laboratory studies.
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