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Partial decoupling from the temperature size rule by North Sea copepods

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Abstract

In temperate seas, multi-voltine copepods show a pronounced seasonal variability in body size, which affects both their reproductive capacity and their accessibility to size-selective predators. Here, we studied seasonal changes of female prosome length from six common copepods, Acartia clausi, Centropages hamatus, Centropages typicus, Paracalanus parvus, Pseudocalanus elongatus, and Temora longicornis between 2000 and 2005 at the time series station Helgoland Roads, southern North Sea. We observed no significant effect of food (measured as phytoplankton carbon content) with size of adult females. Moreover, in none of the species investigated was prosome length significantly correlated with temperature when considering the whole year. Instead, all species had a period of temperature-related size, but for the size distribution during the rest of the year we distinguished two groups of species. Group 1 (Acartia clausi, Centropages hamatus, and Pseudocalanus elongatus) had a resting phase with females of the same size persisting for > half a year, while in group 2 the time after the temperature-related phase was characterized by irregular size distributions. A female resting phase of Acartia clausi, Centropages hamatus, and Pseudocalanus elongatus has been hitherto unknown. Size distribution control after the temperature-related phase in group 2 is as yet not understood, but the awakening/hatching of resting eggs and/or copepodids may be found to be involved.

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References

  • Adler G, Jespersen P (1920) Variations saisonnières chez quelques copépodes planctoniques marins. Medd Komm Havundersøg Ser Plankton 2:1–46

    Google Scholar 

  • Ambler JW (1986) Formulation of an ingestion function for a population of Paracalanus feeding on mixtures of phytoplankton. J Plankton Res 8:957–972

    Article  Google Scholar 

  • Baumgartner MF, Tarrant AM (2017) The physiology and ecology of diapause in marine copepods. Annu Rev Mar Sci 9:387–411

    Article  Google Scholar 

  • Bellantoni DC, Peterson WT (1987) Temporal variability in egg production rates of Acartia tonsa Dana in Long Island Sound. J Exp Mar Biol Ecol 107:199–208

    Article  Google Scholar 

  • Boersma M, Spaak P, De Meester L (1998) Predator mediated plasticity in morphology, life-history and behavior of Daphnia: the uncoupling of responses. Am Nat 152:237–248

    CAS  PubMed  Google Scholar 

  • Boersma M, Wesche A, Hirche HJ (2014) Predation of calanoid copepods on their own and other copepod’s offspring. Mar Biol 161:733–743. https://doi.org/10.1007/s00227-013-2373-7

    Article  Google Scholar 

  • Boersma M, Wiltshire KH, Kong SM, Greve W, Renz J (2015) Long-term change in the copepod community in the southern German Bight. J Sea Res 101:41–50. https://doi.org/10.1016/j.seares.2014.12.004

    Article  Google Scholar 

  • Bonnet D, Harris R, Lopez-Urrutia A, Halsband-Lenk C, Greve W, Valdes L, Hirche H-J, Engel M, Alvarez-Ossorio MT, Wiltshire K (2007) Comparative seasonal dynamics of Centropages typicus at seven coastal monitoring stations in the North Sea, English Channel and Bay of Biscay. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2007.01.007

    Article  Google Scholar 

  • Boyer S, Bonnet D (2013) Triggers for hatching of Paracartia grani (Copepoda: Calanoida) resting eggs: an experimental approach. J Plankton Res 35:668–676. https://doi.org/10.1093/plankt/fbt020

    Article  Google Scholar 

  • Brooks JL (1968) The effects of prey size selection by lake planktivores. Syst Zool 17:272–291

    Article  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–45

    Article  CAS  PubMed  Google Scholar 

  • Carter JCH, Sprules WG, Dadswell MJ, Roff JC (1983) Factors governing geographical variation in body size of Diaptomus minutus (Copepoda, Calanoida). Can J Fish Aquat Sci 40:1303–1307

    Article  Google Scholar 

  • Castellani C, Altunbas Y (2006) Factors controlling the temporal dynamics of egg production in the copepod Temora longicornis. Mar Ecol Prog Ser 308:143–153

    Article  CAS  Google Scholar 

  • Checkley DM Jr (1980) The egg production of a marine planktonic copepod in relation to its food supply: laboratory studies. Limnol Oceanogr 25:430–446

    Article  CAS  Google Scholar 

  • Christou ED, Verriopoulos GC (1993) Length, weight and condition factor of Acartia clausi (Copepoda) in the eastern Mediterranean. J Mar Biol Assoc UK 73:343–353

    Article  Google Scholar 

  • Coker RE (1933) Influence of temperature on size of freshwater copepods (Cyclops). Int Rev Gesamten Hydrobiol 29:406–436

    Article  Google Scholar 

  • Corkett CJ, McLaren IA (1978) The biology of Pseudocalanus. Adv Mar Biol 15:1–231

    Google Scholar 

  • Davis CC (1976) Overwintering strategies of common planktonic copepods in some North Norway fjords and sounds. Astarte 9:37–42

    Google Scholar 

  • Deevey GB (1960) Relative effects of temperature and food on seasonal variations in length of marine copepods in eastern American and western European waters. Bull Bingham Oceanogr Coll 17:54–86

    Google Scholar 

  • Donnelly A, Yu R (2017) The rise of phenology with climate change: an evaluation of IJB publications. Int J Biometeorol 61:29–50. https://doi.org/10.1007/s00484-017-1371-8

    Article  PubMed  Google Scholar 

  • Durbin EG, Durbin AG (1978) Length and weight relationships of Acartia clausi from Narragansett Bay, R.I. Limnol Oceanogr 23:958–969

    Article  Google Scholar 

  • Durbin EG, Durbin AG (1992) Seasonal changes in size frequency distribution and estimated age in the marine copepod Acartia hudsonica during a winter–spring diatom bloom in Narragansett Bay. Limnol Oceanogr 37:379–392

    Article  Google Scholar 

  • Durbin EG, Durbin AG, Smayda TJ, Verity PG (1983) Food limitation of production by adult Acartia tonsa in Narragansett Bay, Rhode Island. Limnol Oceanogr 28:1199–1213

    Article  Google Scholar 

  • Durbin EG, Durbin AG, Campbell RG (1992) Body size and egg production in the marine copepod Acartia hudsonica during a winter–spring diatom bloom in Narragansett Bay. Limnol Oceanogr 37:342–360

    Article  Google Scholar 

  • Edwards ME, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884

    Article  CAS  PubMed  Google Scholar 

  • Edwards M, John AWG, Hunt HG, Lindley JA (1999) Exceptional influx of oceanic species into the North Sea late 1997. J Mar Biol Assoc UK 79:737–739

    Article  Google Scholar 

  • Engel M, Hirche HJ (2004) Seasonal variability and inter-specific differences in hatching of calanoid copepod resting eggs from sediments of the German Bight (North Sea). J Plankton Res 26:1083–1093

    Article  Google Scholar 

  • Evans F (1977) Seasonal density and production estimates of the commoner planktonic copepods of Northumberland coastal waters. Estuar Coast Mar Sci 5:223–241

    Article  Google Scholar 

  • Evans F (1981) An investigation into the relationship of sea temperature and food supply to the size of the planktonic copepod Temora longicornis in the North Sea. Estuar Coast Mar Sci 13:145–158

    Article  Google Scholar 

  • Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17(6):805–815

    Article  Google Scholar 

  • Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551

    Article  Google Scholar 

  • Fryd M, Haslund OH, Wohlgemut O (1991) Development, growth and egg production of the two copepod species Centropages hamatus and Centropages typicus in the laboratory. J Plankton Res 13:683–689

    Article  Google Scholar 

  • Furlan L, Umani SF, Specchi M (1983) Some correlations between hydrobiological parameters and the population of Acartia clausi in the Gulf of Trieste. Rap Procès-verbaux Comm Int Explor Scientif Mer Méditerranée 28:165–167

    Google Scholar 

  • Galbraith MG (1967) Size-selective predation of Daphnia by rainbow trout and yellow perch. Trans Am Fish Soc 96:1–10

    Article  Google Scholar 

  • Gaudy R (1971) Étude expérimentale de la ponte chez trois espéces de copépodes pélagiques (Centropages typicus, Acartia clausi et Temora stylifera). Mar Biol 9:65–70

    Article  Google Scholar 

  • Gaudy R (1984) Structure et fonctionnement de l’écosystème zooplanctonique de l’interface terremer en Mediterranée Nord-Occidentale. Océanis 10:367–383

    Google Scholar 

  • Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34

    Article  CAS  Google Scholar 

  • Gilat E, Kane JE, Martin JC (1965) Study of an ecosystem in the coastal waters of the Ligurian Sea. Bull Inst Océanogr Monaco 65:1–56

    Google Scholar 

  • Grabbert S, Renz J, Hirche HJ, Bucklin A (2010) Species specific PCR discrimination of species of the calanoid copepod Pseudocalanus, P. acuspes and P. elongatus, in the Baltic and North Seas. Hydrobiologia 652:289–297. https://doi.org/10.1007/s10750-010-0360-2

    Article  Google Scholar 

  • Halsband C, Hirche HJ (2001) Reproductive cycles of dominant calanoid copepods in the North Sea. Mar Ecol Prog Ser 209:219–229

    Article  Google Scholar 

  • Halsband-Lenk C, Carlotti F, Greve W (2004) Life-history strategies of calanoid congeners under two different climate regimes: a comparison. ICES J Mar Sci 61:709–720

    Article  Google Scholar 

  • Harris RP, Paffenhofer GA (1976) Feeding, growth and reproduction of the marine planktonic copepod Temora longicornis Miller. J Mar Biol Assoc UK 56:675–690

    Article  Google Scholar 

  • Hickel W (1998) Temporal variability of micro- and nanoplankton in the German Bight in relation to hydrographic structure and nutrient changes. ICES J Mar Sci 55:600–609

    Article  Google Scholar 

  • Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Hirche HJ (1992) Egg production of Eurytemora affinis—effect of k-strategy. Estuar Coast Shelf Sci 35:395–407

    Article  Google Scholar 

  • Hirche HJ, Kattner G (1993) Egg production and lipid content of Calanus glacialis in spring—indication of a food dependent and food independent reproductive mode. Mar Biol 117:615–622

    Article  CAS  Google Scholar 

  • Hirche HJ, Niehoff B (1996) Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea—field and laboratory observations. Polar Biol 16:209–219

    Article  Google Scholar 

  • Holm MW, Kiørboe T, Brun P, Licandro P, Alameda LR, Hansen BW (2018) Resting eggs in free living marine and estuarine copepods. J Plankton Res 40:2–15

    Article  Google Scholar 

  • Horne CR, Hirst AG, Atkinson D, Neves A, Kiørboe T (2016) A global synthesis of seasonal temperature size responses in copepods. Glob Ecol Biogeogr 25:1–12. https://doi.org/10.1111/geb.12460

    Article  Google Scholar 

  • Hrbacek J (1962) Species composition and the amount of zooplankton in relation to the fish stock. Rozpr Cesk Akad Ved 72:1–116

    Google Scholar 

  • Ianora A, Buttino I (1990) Seasonal cycles in population abundances and egg production rates in the planktonic copepods Centropages typicus and Acartia clausi. J Plankton Res 12:473–481

    Article  Google Scholar 

  • Klein Breteler WCM (1980) Continuous breeding of marine pelagic copepods in the presence of heterotrophic dinoflagellates. Mar Ecol Prog Ser 2:229–233

    Article  Google Scholar 

  • Klein Breteler WCM, Gonzalez SR (1982) Influence of cultivation and food concentration on body length of calanoid copepods. Mar Biol 71:157–161

    Article  Google Scholar 

  • Klein Breteler WCM, Gonzalez SR (1984) Culture and development of Temora longicornis (Copepoda, Calanoida) at different conditions of temperature and food. Syllogeus 58:71–84

    Google Scholar 

  • Klein Breteler WCM, Schogt N (1994) Development of Acartia clausi (Copepoda, Calanoida) cultured at different conditions of temperature and food. Hydrobiologia 292–293(1):469–479

    Article  Google Scholar 

  • Klein Breteler WCM, Gonzalez SR, Schogt N (1995) Development of Pseudocalanus elongatus (Copepoda, Calanoida) cultured at different temperature and food conditions. Mar Ecol Prog Ser 119:99–110

    Article  Google Scholar 

  • Klok CJ, Harrison JF (2013) The temperature size rule in arthropods: independent of macro-environmental variables but size dependent. ICB 53:557–570

    Google Scholar 

  • Krause M, Dippner JW, Beil J (1995) A review of hydrographic controls on the distribution of zooplankton biomass and species in the North Sea with particular reference to a survey conducted in January–March 1987. Prog Oceanogr 35:81–152

    Article  Google Scholar 

  • Laakmann S, Gerdts G, Erler R, Knebelsberger P, Martínez Arbizu P, Raupach MJ (2013) Comparison of molecular species identification for North Sea calanoid copepods (Crustacea) using proteome fingerprints and DNA sequences. Mol Ecol Res 13:862–876

    Article  CAS  Google Scholar 

  • Le Ruyet-Person J, Razouls C, Razouls S (1975) Biologie comparée entre espèces vicariantes et communes de copépodes dans un écosystème néritique en Méditerranée et en Manche. Vie Milieu 25:283–312

    Google Scholar 

  • Lee HW, Ban S, Ikeda T, Matsuishi T (2003) Effect of temperature on development, growth and reproduction in the marine copepod Pseudocalanus newmani at satiating food condition. J Plankton Res 25:261–271

    Article  CAS  Google Scholar 

  • Lindley JA (1986) Dormant eggs of calanoid copepods in sea-bed sediments of the English Channel and southern North Sea. J Plankton Res 8(2):399–400

    Article  Google Scholar 

  • Lindley JA (1990) Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern. Br Mar Biol 104:209–217

    Article  Google Scholar 

  • Lindley JA, Batten SD (2002) Long-term variability in the diversity of North Sea zooplankton. J Mar Biol Assoc UK 82:31–40

    Article  Google Scholar 

  • Lock AR, McLaren IA (1970) The effect of varying and constant temperatures on the size of a marine copepod. Limnol Oceanogr 15:638–640

    Article  Google Scholar 

  • Marshall SM (1949) On the biology of the small copepods in Loch Striven. J Mar Biol Assoc UK 28:45–122

    Article  Google Scholar 

  • Mclaren IA (1965) Some relationships between temperature and egg size, body size, development rate, and fecundity of the copepod Pseudocalanus. Limnol Oceanogr 10:528–538

    Article  Google Scholar 

  • McLaren IA (1978) Generation lengths of some temperate marine copepods: estimation, prediction, and implications. J Fish Res Board Can 35(10):1330–1342

    Article  Google Scholar 

  • Myers RA, Runge JA (1983) Predictions of seasonal natural mortality rates in a copepod population using life-history theory. Mar Ecol Prog Ser 11:189–219

    Article  Google Scholar 

  • Næss T (1991) Marine calanoid resting eggs in Norway: abundance and distribution of two copepod species in the sediment of an enclosed marine basin. Mar Biol 110(2):261–266

    Article  Google Scholar 

  • Næss T, Nilssen JP (1991) Diapausing fertilized adults. A new pattern of copepod life cycle. Oecologia (Berl) 86:368–371

    Article  Google Scholar 

  • Norrbin MF (1994) Seasonal patterns in gonad maturation, sex ratio and size in some small, high latitude copepods: implications for overwintering tactics. J Plankton Res 16:115–131

    Article  Google Scholar 

  • Norrbin MF (2001) Ultra-structural changes in the reproductive system of overwintering females of Acartia longiremis. Mar Biol 139:697–704

    Article  Google Scholar 

  • O’Brien WJ (1979) The predator–prey interaction of planktivorous fish and zooplankton. Am Sci 67:572–581

    Google Scholar 

  • O’Brien TD, Wiebe P, Falkenhaug T (eds) (2013) ICES zooplankton status report 2010/20121. ICES Coop Res Rep 318:1–212

  • Pertzova NM (1974) Life cycle and ecology of a thermophilous copepod Centropages hamatus in the White Sea. Zool Zh 53:1013–1022

    Google Scholar 

  • Peterson WT (2001) Patterns in stage duration and development among marine and freshwater calanoid and cyclopoid copepods: a review of rules, physiological constraints, and evolutionary significance. Hydrobiologia 453(454):91–105

    Article  Google Scholar 

  • Razouls S (1975) Fécondité, maturité sexuelle et differenciation de l’appareil génital des femelles de deux copépodes planctoniques: Centropages typicus et Temora stylifera. Publ Stazione Zoologica Napoli 39:297–306

    Google Scholar 

  • Riccardi N, Mariotto L (2000) Seasonal variations in copepod body length: a comparison between different species in the Lagoon of Venice. Aquat Ecol 34:243–252

    Article  CAS  Google Scholar 

  • Sander F, Moore EA (1983) Physioecology of tropical marine copepods. I. Size variations. Crustaceana 44:83–93

    Article  Google Scholar 

  • Smith SL, Lane PVZ (1987) On the life history of Centropages typicus: responses to a fall diatom bloom in the New York Bight. Mar Biol 95:305–313

    Article  Google Scholar 

  • Sun X, Liang Z, Zou J, Wang L (2013) Seasonal variation in community structure and body length of dominant copepods around artificial reefs in Xiaoshi Island, China. Chin J Oceanol Limnol 31:282–289

    Article  Google Scholar 

  • Thompson BM (1982) Growth and development of Pseudocalanus elongatus and Calanus sp. in the laboratory. J Mar Biol Assoc UK 62:359–372

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Biol Sci 272:2561–2569. https://doi.org/10.1098/rspb.2005.3356

    Article  PubMed  PubMed Central  Google Scholar 

  • Warren GJ, Evans MS, Jude DJ, Ayers JC (1986) Seasonal variations in copepod size: effects of temperature, food abundance, and vertebrate predation. J Plankton Res 8:841–853

    Article  Google Scholar 

  • Wells L (1970) Effects of alewife predation on zooplankton populations in Lake Michigan. Limnol Oceanogr 15:556–565

    Article  Google Scholar 

  • Wiltshire KH, Dürselen CD (2004) Revision and quality analyses of the Helgoland Reede long-term phytoplankton data archive. Helgol Mar Res 58:252–268

    Article  Google Scholar 

  • Wiltshire KH, Malzahn AM, Wirtz K, Greve W, Janisch S, Mangelsdorf P, Manly BFJ, Boersma M (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnol Oceanogr 53:1294–1302

    Article  Google Scholar 

  • Wiltshire KH, Kraberg A, Bartsch I, Boersma M, Franke H-D, Freund J, Gebühr C, Gerdts G, Stockmann K, Wichels A (2010) Helgoland Roads, North Sea: 45 years of change. Estuar Coasts 33:295–310

    Article  CAS  Google Scholar 

  • Wiltshire KH, Boersma M, Carstens K, Kraberg AC, Peters S, Scharfe M (2015) Control of phytoplankton in a shelf sea: determination of the main drivers based on the Helgoland Roads Time Series. J Sea Res 105:42–52

    Article  Google Scholar 

  • Zaret TG (1980) Predation and freshwater communities. Yale University Press, New Haven

    Google Scholar 

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Acknowledgements

We thank the personnel of the Biologische Anstalt Helgoland for collection and delivery of the samples, especially the crew and captain of the research vessel “Aade”. This study was possible only by the tireless und conscientious assistance of Ulrike Holtz.

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Authors and Affiliations

  1. Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Am Alten Hafen, 27468, Bremerhaven, Germany

    Hans-Jürgen Hirche

  2. Biologische Anstalt Helgoland, Kurpromenade, 27498, Helgoland, Germany

    Maarten Boersma

  3. FB2, University of Bremen, Bremen, Germany

    Maarten Boersma

  4. Wattenmeerstation, Hafenstraße 43, 25992, List/Sylt, Germany

    Karen H. Wiltshire

  5. University of Kiel, Kiel, Germany

    Karen H. Wiltshire

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  1. Hans-Jürgen Hirche
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Hirche, HJ., Boersma, M. & Wiltshire, K.H. Partial decoupling from the temperature size rule by North Sea copepods. Mar Biol 166, 58 (2019). https://doi.org/10.1007/s00227-019-3503-7

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