Abstract
Planktonic copepods play a major role in the fluxes of matter and energy in the marine ecosystem, provide a biological pump of carbon into the deep ocean, and play a role in determining fish recruitment. Owing to such ecological considerations, it is essential to understand the role that climate might play in the interannual variability of these organisms and the mechanisms by which it could modify the ecosystem functioning. In this study, a causal chain of meteorological, hydrological and ecological processes linked to the North Atlantic Oscillation (NAO) was identified in the Ligurian Sea, Northwestern Mediterranean. The forcing by the NAO drives most of the hydro-climatic variability during winter and early spring. Subsequently, interannual and decadal changes of the dominant copepods Centropages typicus and Temora stylifera were significantly correlated to the state of the hydro-climatic signal and tightly coupled to the NAO. Direct and indirect effects whose influence promoted phenological changes in the two copepod populations drove the species’ responses to climatic forcing. Opposite responses of the analysed species were also highlighted by these results. While years characterized by the positive phase of the NAO leads to enhancement of the strength and the forward move of the C. typicus peak, they act negatively on the annual cycle of T. stylifera, the abundance of which drops twofold and the annual peak appears delayed in time. In contrast, low NAO years lead to high abundance of T. stylifera and a forward timing of its peak, and acts in turn negatively on the C. typicus annual cycle in both abundance (low) and timing (delayed). Owing to the synchronism between hydro-climatic conditions and the NAO, and the major role of these species in the pelagic ecosystem of the studied area, these results provide key elements for interpreting and forecasting decadal changes of planktonic populations in the Ligurian Sea.
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Agnew D, Beddington J, Hill S (2002) The potential use of environmental information to manage squid stocks. Can J Fish Aquat Sci 59:1851–1857
Beaugrand G, Reid PC. (2002) Long-term changes in phytoplankton, zooplankton and salmon related to climate. Global Change Biol 9:1–17
Beaugrand G, Brander K, Lindley A, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664
Bethoux JP, Gentili B, Raunet J, Taillez D (1990) Warming trend in the Western Mediterranean deep water. Nature 397:660–662
Bethoux JP, Morin P, Ruiz-Pino D (2002) Temporal trends in nutrient ratios : chemical evidence of Mediterranean ecosystem changes driven by human activity. Deep-Sea Res II 49:2007–2016
Bustillos-Guzman J, Claustre H, Marty JC (1995) Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal northwestern Mediterranean Sea. Mar Ecol Prog Ser 124:247–258
Chelton DB (1984) Commentary : short term climatic variability in the Northeast Pacific Ocean. In: Pearcy WG (ed) The influence of Ocean conditions on the production of salmonids in the North Pacific. Oregon State University Press, Oregon, pp 87–99
Claustre H, Marty JC, Cassiani L (1989) Intraspecific differences in the biochemical composition of a diatom during a spring bloom in the Villefranche-sur-mer Bay, Mediterranean Sea. J Exp Mar Biol Ecol 129:17–32
Colebrook JM (1978) Continous plankton records : zooplankton and environment, north-east Atlantic and North Sea, 1948–1975. Oceanol Acta 1:9–23
Di Capua I, Mazzocci MG (2004) Population structure of the copepods Centropages typicus and Temora stylifera in different environmental conditions. ICES J Mar Sci 61: 632–644
Dippner J, Kroncke I (2003) Forecast of climate-induced change in macrozoobenthos in the southern North Sea in spring. Climate Res 25: 179–182
Dupuis H, Taylor PK, Weill A, Katsaros K (1997) The inertial dissipation method applied to derive turbulent fluxes over the ocean during the SOFIA/ASTEX and SEMAPHORE experiments with low to moderate speeds. J Geophys Res 102(C9):21.115–21.129
Durant J, Anker-Nielssen T, Hjermann D, Stenseth NC (2004) Regime shifts in the breeding of an Atlantic puffin population. Ecol Lett 7:388–394
Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884
Edwards M, Beaugrand G, Reid C, Rowden A, Jones M (2002) Ocean climate anomalies and the ecology of the North Sea. Mar Ecol Prog Ser 239: 1–10
Fernandez de Puelles M, Valencia P, Vicente L (2004) Zooplankton variability and climatic anomalies from 1994 to 2001 in the Balearic Sea. ICES J Mar Sci 61:492–500
Fromentin J, Planque B (1996) Calanus and environment in the eastern North Atlantic. II. Influence of the North Atlantic Oscillation on C. finmarchicus and C. helgolandicus. Mar Ecol Prog Ser 134:111–118
Gaudy R (1984) Biological cycle of Centropages typicus in the North-western Mediterranean neritic waters. Crustaceana 7:200–213
Gerten D, Adrian R (2000) Climate-driven changes in spring plankton dynamics and the sensitivity of shallow polimictic lakes to the North Atlantic Oscillation. Limnol Oceanogr 45:1058–1066
Goffart A, Hecq JH, Legendre L (2002) Changes in the development of the winter-spring phytoplankton bloom in the Bay of Calvi (Northwestern Mediterranean) over the last two decades: a response to the changing climate ? Mar Ecol Prog Ser 235: 387–399
Gomez F, Gorsky G (2003) Microoplankton cycle in the Northwestern Mediterranean. J Plankton Res 25:323–329
Halsband-Lenk C, Nival S, Carlotti F, Hirche H-J (2001) Seasonal cycles of egg production of two planktonic copepods, Centropages typicus and Temora stylifera, in the north-western Mediterranean Sea. J Plankton Res 23:597–609
Halsband-Lenk C, Cartlotti F, Greve W (2004) Life-history strategies of calanoid congeneres under two different climate regimes: a comparison. ICES J Mar Sci 61:709–720
Hirst A, Bunker AJ (2003) Growth of marine planktonic copepods: global rates and patterns in relation to chlorophyll a, temperature, and body weight. Limnol Oceanogr 48:1988–2010
Huntley ME, Lopez DG, (1992) Temperature dependent production of marine copepods: a global synthesis. Am Nat 140:201–242
Hurrel JW (1995) Decadal trends in the North Atlantic Oscillation : regional temperature and precipitation. Science 269:1997
Ianora A (1998) Copepod life history traits in subtemperate regions. J Mar Syst 15:337–349
Ibanez F, Boucher J, (1987) Anisotropie des populations zooplanctoniques dans la zone frontale de Mer Ligure. Oceanol Acta 10(2):205–216
Ibanez F, Etienne M (1992) Le filtrage des séries chronologiques par l’analyse en composant principales de processus (ACPP). J de Recherches Océanographiques 16:66–72
Ibanez F, Fromentin JM, Castel J (1993) Application of the cumulated function to the processing of chronological data in oceanography. Comptes rendus de l’Académie des Sciences Série 3, Sciences de la vie/Life sciences 318:745–748
Kiorboe T (1998) Population regulation and role of mesozooplankton in shaping pelagic food webs. Hydrobiologia 363:13–27
Landry MR (1975) Seasonal temperature effects and predicting development rates of marine copepods eggs. Limnol Oceanogr 28:614–624
Lindley JA and Reid PC (2002) Variations in the abundance of Centropages typicus and Calanus helgolandcus in the North Sea: deviations from close relationships with temperature. Mar Biol 141:153–165
Lloret J, Lleonart J, Sole I, Fromentin JM (2001) Fluctuations of landings and environmental conditions in the north-western Mediterranean Sea. Fish Oceanogr 10:33–50
Marshall J et al (2001) North Atlantic climate variability: phenomena, impacts and mechanisms. Int J Climatol 21:1863–1998
Mazzocchi MG, 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 IA, Corckett CJ, Zillioux EJ (1969) Temperature adaptations of copepods eggs from the Arctic to the Tropics. Biol Bull Mar Biol 137:486–493
Molinero JC, Buecher E, Ibanez F, Nival P, Souissi S (2004) Large scale climate control on oceanographic and ecological changes in the Ligurian Sea, NW Mediterranean. In: Proceedings comm. int. Mer Medit. CIESM, vol. 37, pp 403
Molinero JC, Ibanez F, Nival P, Buecher E, Souissi S (2005) The North Atlantic climate and Northwestern Mediterranean plankton variability. Limnol Oceanogr 50:1213–1220
Nival P, Corre MC (1976) Variation annuelle des caractéristiques hydrologiques de surface dans la Rade de Villefranche-sur-Mer. Ann. Inst. Océanogr. Monaco 52:57–78
Ohman MD, Hirche HJ (2001) Density-dependent mortality in an oceanic copepod population. Nature 412:638–641
Ottersen G, Planque B, Belgrano A, Post E, Reid C, Stenseth N (2001) Ecological effects of the North Atlantic Oscillation. Oecologia 128:1–14
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impact across natural systems. Nature 421:37–42
Pyper BJ, Peterman RM (1998) Comparison of methods to account for autocorrelation in correlation analysis of fish data. Can J Fish Aquat Sci 55:2127–2140
Razouls C, (1974) Variations annuelles quantitatives de deux espèces dominantes de copépodes planctoniques Centropages typicus et Temora stylifera de la région de Banyuls : Cycles biologiques et estimations de la production. III.- Dynamique des populations et calcul de leur production. Cahiers de Biologie Marine XV: 51–88
Razouls S (1982) Etude experimental de la ponte de deux copepodes pelagiques Temora stylifera et Centropages typicus. II. Dynamique des pontes. Vie et Milieu 32:11–20
Reid PC, Holliday N, Smith T (2001) Pulses in the eastern margin current with higher temperatures and North Sea ecosystem changes. Mar Ecol Prog Ser 215:283–287
Send U, Font J, Krahmann G, Millot C, Rhein M, Tintore J (1999) Recent advances in observing the physical oceanography of the western Mediterranean Sea. Prog Oceanogr 44:37–64
Souissi S, Seuront L, Schmitt F, Ginot V (2005) Describing space-time patterns in aquatic ecology using IBMs and scaling and multiscaling approaches. Nonlinear analysis: real world applications 6:705–730
Straile D (2002) North Atlantic Oscillation synchronizes food-web interactions in central European lakes. Proc Roy Soc Lond Ser B Bio 269:391–395
Trigo I, Davies T, Bigg G (2000) Decline in Mediterranean rainfall caused by weakening of Mediterranean cyclones. Geophys Res Lett 27:2913–2916
Vignudelli S, Gasparini GP, Astraldi M, Schiano ME (1999) A possible influence of the North Atlantic Oscillation on the circulation of the Western Mediterranean Sea. Geophys Res Lett 26:623–626
Walther GR, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395
Winder M, Schindler D (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106
Xoplaki E (2002) Climate variability over the Mediterranean. Ph. D. thesis. University of Thessaloniki, Greece
Acknowledgements
We wish to thank Serge Dallot and the staff of the Laboratory of Oceanography of Villefranche, whose commitment in sampling and technical support have made possible the long-term survey used in this study. We gratefully thank Oliver Beck for contribution in C. typicus counts. This study was conducted as a part of the JCM’s PhD dissertation and supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT, México). We thank Prof. J. Dippner and an anonymous reviewer for constructive comments on the manuscript. This work is a contribution to the French IFB ‘Biodiversité et Changement Global’ programme.
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Molinero, J.C., Ibanez, F., Souissi, S. et al. Phenological changes in the Northwestern Mediterranean copepods Centropages typicus and Temora stylifera linked to climate forcing. Oecologia 145, 640–649 (2005). https://doi.org/10.1007/s00442-005-0130-4
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DOI: https://doi.org/10.1007/s00442-005-0130-4