Marine Biology

, 166:58 | Cite as

Partial decoupling from the temperature size rule by North Sea copepods

  • Hans-Jürgen HircheEmail author
  • Maarten Boersma
  • Karen H. Wiltshire
Original Paper


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.



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.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

227_2019_3503_MOESM1_ESM.pdf (2.5 mb)
Supplementary material 1 (PDF 2574 kb)


  1. Adler G, Jespersen P (1920) Variations saisonnières chez quelques copépodes planctoniques marins. Medd Komm Havundersøg Ser Plankton 2:1–46Google Scholar
  2. Ambler JW (1986) Formulation of an ingestion function for a population of Paracalanus feeding on mixtures of phytoplankton. J Plankton Res 8:957–972CrossRefGoogle Scholar
  3. Baumgartner MF, Tarrant AM (2017) The physiology and ecology of diapause in marine copepods. Annu Rev Mar Sci 9:387–411CrossRefGoogle Scholar
  4. Bellantoni DC, Peterson WT (1987) Temporal variability in egg production rates of Acartia tonsa Dana in Long Island Sound. J Exp Mar Biol Ecol 107:199–208CrossRefGoogle Scholar
  5. 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 152:237–248PubMedPubMedCentralGoogle Scholar
  6. Boersma M, Wesche A, Hirche HJ (2014) Predation of calanoid copepods on their own and other copepod’s offspring. Mar Biol 161:733–743. CrossRefGoogle Scholar
  7. 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. CrossRefGoogle Scholar
  8. 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. CrossRefGoogle Scholar
  9. Boyer S, Bonnet D (2013) Triggers for hatching of Paracartia grani (Copepoda: Calanoida) resting eggs: an experimental approach. J Plankton Res 35:668–676. CrossRefGoogle Scholar
  10. Brooks JL (1968) The effects of prey size selection by lake planktivores. Syst Zool 17:272–291CrossRefGoogle Scholar
  11. Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–45PubMedCrossRefPubMedCentralGoogle Scholar
  12. 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 40:1303–1307CrossRefGoogle Scholar
  13. Castellani C, Altunbas Y (2006) Factors controlling the temporal dynamics of egg production in the copepod Temora longicornis. Mar Ecol Prog Ser 308:143–153CrossRefGoogle Scholar
  14. Checkley DM Jr (1980) The egg production of a marine planktonic copepod in relation to its food supply: laboratory studies. Limnol Oceanogr 25:430–446CrossRefGoogle Scholar
  15. Christou ED, Verriopoulos GC (1993) Length, weight and condition factor of Acartia clausi (Copepoda) in the eastern Mediterranean. J Mar Biol Assoc UK 73:343–353CrossRefGoogle Scholar
  16. Coker RE (1933) Influence of temperature on size of freshwater copepods (Cyclops). Int Rev Gesamten Hydrobiol 29:406–436CrossRefGoogle Scholar
  17. Corkett CJ, McLaren IA (1978) The biology of Pseudocalanus. Adv Mar Biol 15:1–231Google Scholar
  18. Davis CC (1976) Overwintering strategies of common planktonic copepods in some North Norway fjords and sounds. Astarte 9:37–42Google Scholar
  19. 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 17:54–86Google Scholar
  20. Donnelly A, Yu R (2017) The rise of phenology with climate change: an evaluation of IJB publications. Int J Biometeorol 61:29–50. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Durbin EG, Durbin AG (1978) Length and weight relationships of Acartia clausi from Narragansett Bay, R.I. Limnol Oceanogr 23:958–969CrossRefGoogle Scholar
  22. 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 37:379–392CrossRefGoogle Scholar
  23. Durbin EG, Durbin AG, Smayda TJ, Verity PG (1983) Food limitation of production by adult Acartia tonsa in Narragansett Bay, Rhode Island. Limnol Oceanogr 28:1199–1213CrossRefGoogle Scholar
  24. 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 37:342–360CrossRefGoogle Scholar
  25. Edwards ME, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884PubMedCrossRefPubMedCentralGoogle Scholar
  26. 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 79:737–739CrossRefGoogle Scholar
  27. 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 26:1083–1093CrossRefGoogle Scholar
  28. Evans F (1977) Seasonal density and production estimates of the commoner planktonic copepods of Northumberland coastal waters. Estuar Coast Mar Sci 5:223–241CrossRefGoogle Scholar
  29. 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 13:145–158CrossRefGoogle Scholar
  30. 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):805–815CrossRefGoogle Scholar
  31. Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551CrossRefGoogle Scholar
  32. 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 13:683–689CrossRefGoogle Scholar
  33. 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 28:165–167Google Scholar
  34. Galbraith MG (1967) Size-selective predation of Daphnia by rainbow trout and yellow perch. Trans Am Fish Soc 96:1–10CrossRefGoogle Scholar
  35. Gaudy R (1971) Étude expérimentale de la ponte chez trois espéces de copépodes pélagiques (Centropages typicus, Acartia clausi et Temora stylifera). Mar Biol 9:65–70CrossRefGoogle Scholar
  36. Gaudy R (1984) Structure et fonctionnement de l’écosystème zooplanctonique de l’interface terremer en Mediterranée Nord-Occidentale. Océanis 10:367–383Google Scholar
  37. 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 106:1–34CrossRefGoogle Scholar
  38. Gilat E, Kane JE, Martin JC (1965) Study of an ecosystem in the coastal waters of the Ligurian Sea. Bull Inst Océanogr Monaco 65:1–56Google Scholar
  39. 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. CrossRefGoogle Scholar
  40. Halsband C, Hirche HJ (2001) Reproductive cycles of dominant calanoid copepods in the North Sea. Mar Ecol Prog Ser 209:219–229CrossRefGoogle Scholar
  41. 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 61:709–720CrossRefGoogle Scholar
  42. Harris RP, Paffenhofer GA (1976) Feeding, growth and reproduction of the marine planktonic copepod Temora longicornis Miller. J Mar Biol Assoc UK 56:675–690CrossRefGoogle Scholar
  43. 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 55:600–609CrossRefGoogle Scholar
  44. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  45. Hirche HJ (1992) Egg production of Eurytemora affinis—effect of k-strategy. Estuar Coast Shelf Sci 35:395–407CrossRefGoogle Scholar
  46. 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 117:615–622CrossRefGoogle Scholar
  47. Hirche HJ, Niehoff B (1996) Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea—field and laboratory observations. Polar Biol 16:209–219CrossRefGoogle Scholar
  48. 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 40:2–15CrossRefGoogle Scholar
  49. 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. CrossRefGoogle Scholar
  50. Hrbacek J (1962) Species composition and the amount of zooplankton in relation to the fish stock. Rozpr Cesk Akad Ved 72:1–116Google Scholar
  51. 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 12:473–481CrossRefGoogle Scholar
  52. Klein Breteler WCM (1980) Continuous breeding of marine pelagic copepods in the presence of heterotrophic dinoflagellates. Mar Ecol Prog Ser 2:229–233CrossRefGoogle Scholar
  53. Klein Breteler WCM, Gonzalez SR (1982) Influence of cultivation and food concentration on body length of calanoid copepods. Mar Biol 71:157–161CrossRefGoogle Scholar
  54. Klein Breteler WCM, Gonzalez SR (1984) Culture and development of Temora longicornis (Copepoda, Calanoida) at different conditions of temperature and food. Syllogeus 58:71–84Google Scholar
  55. Klein Breteler WCM, Schogt N (1994) Development of Acartia clausi (Copepoda, Calanoida) cultured at different conditions of temperature and food. Hydrobiologia 292–293(1):469–479CrossRefGoogle Scholar
  56. 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 119:99–110CrossRefGoogle Scholar
  57. Klok CJ, Harrison JF (2013) The temperature size rule in arthropods: independent of macro-environmental variables but size dependent. ICB 53:557–570Google Scholar
  58. 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 35:81–152CrossRefGoogle Scholar
  59. 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 13:862–876CrossRefGoogle Scholar
  60. 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 25:283–312Google Scholar
  61. 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 25:261–271CrossRefGoogle Scholar
  62. 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):399–400CrossRefGoogle Scholar
  63. Lindley JA (1990) Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern. Br Mar Biol 104:209–217CrossRefGoogle Scholar
  64. Lindley JA, Batten SD (2002) Long-term variability in the diversity of North Sea zooplankton. J Mar Biol Assoc UK 82:31–40Google Scholar
  65. Lock AR, McLaren IA (1970) The effect of varying and constant temperatures on the size of a marine copepod. Limnol Oceanogr 15:638–640CrossRefGoogle Scholar
  66. Marshall SM (1949) On the biology of the small copepods in Loch Striven. J Mar Biol Assoc UK 28:45–122CrossRefGoogle Scholar
  67. Mclaren IA (1965) Some relationships between temperature and egg size, body size, development rate, and fecundity of the copepod Pseudocalanus. Limnol Oceanogr 10:528–538CrossRefGoogle Scholar
  68. McLaren IA (1978) Generation lengths of some temperate marine copepods: estimation, prediction, and implications. J Fish Res Board Can 35(10):1330–1342CrossRefGoogle Scholar
  69. Myers RA, Runge JA (1983) Predictions of seasonal natural mortality rates in a copepod population using life-history theory. Mar Ecol Prog Ser 11:189–219CrossRefGoogle Scholar
  70. 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):261–266CrossRefGoogle Scholar
  71. Næss T, Nilssen JP (1991) Diapausing fertilized adults. A new pattern of copepod life cycle. Oecologia (Berl) 86:368–371CrossRefGoogle Scholar
  72. 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 16:115–131CrossRefGoogle Scholar
  73. Norrbin MF (2001) Ultra-structural changes in the reproductive system of overwintering females of Acartia longiremis. Mar Biol 139:697–704CrossRefGoogle Scholar
  74. O’Brien WJ (1979) The predator–prey interaction of planktivorous fish and zooplankton. Am Sci 67:572–581Google Scholar
  75. O’Brien TD, Wiebe P, Falkenhaug T (eds) (2013) ICES zooplankton status report 2010/20121. ICES Coop Res Rep 318:1–212Google Scholar
  76. Pertzova NM (1974) Life cycle and ecology of a thermophilous copepod Centropages hamatus in the White Sea. Zool Zh 53:1013–1022Google Scholar
  77. 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):91–105CrossRefGoogle Scholar
  78. 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 39:297–306Google Scholar
  79. Riccardi N, Mariotto L (2000) Seasonal variations in copepod body length: a comparison between different species in the Lagoon of Venice. Aquat Ecol 34:243–252CrossRefGoogle Scholar
  80. Sander F, Moore EA (1983) Physioecology of tropical marine copepods. I. Size variations. Crustaceana 44:83–93CrossRefGoogle Scholar
  81. 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 95:305–313CrossRefGoogle Scholar
  82. 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 31:282–289CrossRefGoogle Scholar
  83. Thompson BM (1982) Growth and development of Pseudocalanus elongatus and Calanus sp. in the laboratory. J Mar Biol Assoc UK 62:359–372CrossRefGoogle Scholar
  84. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Biol Sci 272:2561–2569. CrossRefPubMedPubMedCentralGoogle Scholar
  85. 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 8:841–853CrossRefGoogle Scholar
  86. Wells L (1970) Effects of alewife predation on zooplankton populations in Lake Michigan. Limnol Oceanogr 15:556–565CrossRefGoogle Scholar
  87. Wiltshire KH, Dürselen CD (2004) Revision and quality analyses of the Helgoland Reede long-term phytoplankton data archive. Helgol Mar Res 58:252–268CrossRefGoogle Scholar
  88. 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 53:1294–1302CrossRefGoogle Scholar
  89. 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 33:295–310CrossRefGoogle Scholar
  90. 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 105:42–52CrossRefGoogle Scholar
  91. Zaret TG (1980) Predation and freshwater communities. Yale University Press, New HavenGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Alfred Wegener Institute, Helmholtz Centre for Polar and Marine ResearchBremerhavenGermany
  2. 2.Biologische Anstalt HelgolandHelgolandGermany
  3. 3.FB2University of BremenBremenGermany
  4. 4.WattenmeerstationList/SyltGermany
  5. 5.University of KielKielGermany

Personalised recommendations