Marine Biology

, Volume 159, Issue 3, pp 583–599 | Cite as

Seasonal and interannual variations in size, biomass and chemical composition of the eggs of North Sea shrimp, Crangon crangon (Decapoda: Caridea)

  • Ángel Urzúa
  • Kurt Paschke
  • Paulina Gebauer
  • Klaus Anger
Original Paper


In the shrimp Crangon crangon, an important fishery resource and key species in the southern North Sea, we studied temporal variations in size, biomass (dry weight, W) and chemical composition (C, N, protein and lipid) of eggs in an initial embryonic stage. Data from 2 years, 1996 and 2009, consistently revealed that egg size and biomass varied seasonally, with maxima at the beginning of the reproductive season (January), decreasing values throughout spring, minima in June–July, and a slight increase thereafter. This cyclic pattern explains why “Winter eggs” are on average larger and heavier than “summer eggs”. Using a modelling approach, we estimated the duration of oogenesis in relation to seasonally changing seawater temperatures. According to an additive model of multiple explanatory variables, the C content per newly laid egg showed in both years a highly significant negative relationship with day length (r² = 0.38 and 0.40, respectively; P < 0.0001), a weak positive relationship with temperature (r² = 0.08 and 0.09; P < 0.05), and a weak negative relationship with phytoplankton biomass (r² = 0.11 and 0.12; P < 0.05) at the estimated time of beginning oogenesis. Phenotypic plasticity in initial egg size and biomass is interpreted as an adaptive reproductive trait that has evolved in regions with strong seasonality in plankton production and periods of larval food limitation. In contrast to biomass per egg, the percentage chemical composition remained similar throughout the reproductive period. Both the absolute and percentage values also showed significant interannual variations, which caution against generalizations based on short-term studies of reproductive traits of C. crangon and other species of shrimp.


Reproductive Season Reproductive Trait German Bight Ovigerous Female Female Body Size 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the crews of R.V. “Uthörn” and “Aade” for capture and transporting live shrimps to Helgoland, Uwe Nettelmann helped in the maintenance of the animals; Cornelia Püschel, Bettina Oppermann and Julia Haafke made elemental analyses. We also thank two anonymous reviewers for constructive criticism and helpful suggestions. AU and KP were financially supported by the Deutscher Akademischer Austauschdienst (DAAD, Bonn, Germany). AU also thanks the support of the Comisión Nacional de Ciencia y Tecnología, CONICYT (Santiago de Chile), funding this study as a part of his doctoral dissertation. The experiments comply with animal manipulation laws in Germany.


  1. Abelló P, Valladares FJ, Castellón A (1988) Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar Biol 98:39–49CrossRefGoogle Scholar
  2. Allen RM, Buckley YM, Marshall DJ (2008) Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. Am Nat 171:225–237CrossRefGoogle Scholar
  3. Andresen H, van der Meer J (2010) Brown shrimp (Crangon crangon, L.) functional response to density of different sized juvenile bivalves Macoma balthica (L.). J Exp Mar Biol Ecol 390:31–38CrossRefGoogle Scholar
  4. Anger K (1983) Temperature and the larval development of Hyas araneus L. (Decapoda: Majidae); extrapolation of laboratory data to field conditions. J Exp Mar Biol Ecol 69:203–215CrossRefGoogle Scholar
  5. Anger K (2001) The biology of decapod crustacean larvae. Crustacean issues, vol 14. Balkema, LisseGoogle Scholar
  6. Anger K, Harms J (1990) Elemental (CHN) and proximate biochemical composition of decapod crustacean larvae. Comp Biochem Physiol B 97:69–80CrossRefGoogle Scholar
  7. Anger K, Moreira GS, Ismael D (2002) Comparative size, biomass, elemental composition (C, H, N), and energy concentration of caridean shrimp eggs. Invertebr Reprod Dev 42:83–93CrossRefGoogle Scholar
  8. Anger K, Thatje S, Lovrich G, Calcagno J (2003) Larval and early juvenile development of Paralomis granulosa reared at different temperatures: tolerance of cold and food limitation in a lithotid crab from high latitudes. Mar Ecol Prog Ser 253:243–251CrossRefGoogle Scholar
  9. Arcos FG, Ibarra AM, Palacios E, Vazquez-Boucard C, Racotta IS (2003) Feasible predictive criteria for reproductive performance of white shrimp Litopenaeus vannamei: egg quality and female physiological condition. Aquaculture 228:335–349CrossRefGoogle Scholar
  10. Arthur W (2000) Intraspecific variation in developmental characters: the origin of evolutionary novelties. Am Zool 40:811–818CrossRefGoogle Scholar
  11. Attard J, Hudon C (1987) Embryonic development and energetic investment in egg production in relation to size of female lobster (Homarus americanus). Can J Fish Aquat Sci 44:1157–1164CrossRefGoogle Scholar
  12. Bas C, Spivak E, Anger K (2007) Seasonal and interpopulational variability in fecundity, egg size, and elemental composition (CHN) of eggs and larvae in a grapsoid crab, Chasmagnathus granulatus. Helgol Mar Res 61:225–237CrossRefGoogle Scholar
  13. Boddeke R (1971) The influence of strong 1969 and 1970 year-classes of cod on the stock of brown shrimp along the Netherlands coast in 1970 and 1971. ICES CM 1971/K:32:1–12Google Scholar
  14. Boddeke R (1982) The occurence of winter and summer eggs in the brown shrimp (Crangon crangon) and the pattern of recruitment. Neth J Sea Res 16:151–162CrossRefGoogle Scholar
  15. Bomirski A, Klęk E (1974) Action of eyestalks on ovary in Rhithropanopeus harrisii and Crangon crangon (Crustacea- Decapoda). Mar Biol 24:329–337CrossRefGoogle Scholar
  16. Botsford LW (1991) Crustacean egg production and fisheries management. In: Wenner A, Kuris A (eds) Crustacean egg production. Balkema, Rotterdam, pp 379–394Google Scholar
  17. Brante A, Cifuentes S, Pörtner H, Arntz W, Fernández M (2004) Latitudinal comparison of reproductive traits in five Brachyuran species along the Chilean coast. Rev Chil Hist Nat 77:15–27CrossRefGoogle Scholar
  18. Campos J, Van der Veer H, Freitas V, Kooijman S (2009) Contribution of different generations of the brown shrimp Crangon crangon (L.) in the Dutch Wadden Sea to commercial fisheries: a dynamic energy budget approach. J Sea Res 62:106–113CrossRefGoogle Scholar
  19. Campos J, Bio A, Cardoso JFMF, Dapper R, Witte JIJ, van der Veer HW (2010) Fluctuations of brown shrimp Crangon crangon abundance in the western Dutch Wadden Sea. Mar Ecol Prog Ser 405:203–219CrossRefGoogle Scholar
  20. Cequier-Sánchez E, Rodriguez C, Ravelo AG, Zarate R (2008) Dichloromethane as a solvent for lipid extraction and assessment of lipid classes and fatty acids from samples of different natures. J Agric Food Chem 56:4297–4303CrossRefGoogle Scholar
  21. Clarke A (1993) Reproductive trade-offs in caridean shrimps. Funct Ecol 7:411–419CrossRefGoogle Scholar
  22. Criales MM (1985) Untersuchungen zur Larvalentwicklung von Crangon crangon L. und Crangon allmanni Kinahan (Decapoda, Natantia, Caridea). Dissertation, University of Kiel, GermanyGoogle Scholar
  23. Criales MM, Anger K (1986) Experimental studies on the larval development of the shrimps Crangon crangon and C. allmanni. Helgoländer Meeresunters 40:241–265CrossRefGoogle Scholar
  24. Díaz H (1980) The mole crab Emerita talpoida (Say): a case of changing life history pattern. Ecol Monogr 50:437–456CrossRefGoogle Scholar
  25. Drake P, Arias AM, Rodríguez A (1998) Seasonal and tidal abundance patterns of decapods crustacean larvae in a shallow inlet (SW Spain). J Plankton Res 20:585–601CrossRefGoogle Scholar
  26. Fischer S, Thatje S (2008) Temperature-induced oviposition in the brachyuran crab Cancer setosus along a latitudinal cline: aquaria experiments and analysis of field data. J Exp Mar Biol Ecol 357:157–164CrossRefGoogle Scholar
  27. Fischer S, Thatje S, Brey T (2009) Early eggs traits in Cancer setosus (Decapoda, Brachyura): effects of temperature and female size. Mar Ecol Prog Ser 377:193–202CrossRefGoogle Scholar
  28. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  29. Gebauer P, Paschke K, Anger K (2010) Seasonal variation in the nutritional vulnerability of first-stage larval porcelain crab, Petrolisthes laevigatus (Anomura: Porcellanidae) in southern Chile. J Exp Mar Biol Ecol 386:103–112CrossRefGoogle Scholar
  30. Ghiselin M (1987) Evolutionary aspects of marine invertebrate reproduction. In: Giese A, Pearse J, Pearse V (eds) Reproduction of marine invertebrates, vol IX. Blackwell, California, pp 609–665Google Scholar
  31. Giménez L (2006) Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans. Integr Comp Biol 46:615–622CrossRefGoogle Scholar
  32. Giménez L (2010) Relationships between habitat conditions, larval traits, and juvenile performance in a marine invertebrate. Ecology 91:1401–1413CrossRefGoogle Scholar
  33. Giménez L, Anger K, Torres G (2004) Linking life history traits in successive phases of a complex life cycle: effects of larval biomass on early juvenile development in an estuarine crab, Chasmagnathus granulata. Oikos 104:570–580CrossRefGoogle Scholar
  34. González-Gordillo JI, dos Santos A, Rodríguez A (2001) Checklist and an annotated bibliography of decapod crustacea larvae from the southwestern European coast (Gibraltar Strait area). Scientia Marina 65:275–305CrossRefGoogle Scholar
  35. Gunnarsson B, Asgeirsson PH, Ingolfsson A (2007) The rapid colonization by Crangon crangon (Linnaeus, 1758) (Eucarida, Caridea, Crangonidae) of Icelandic coastal waters. Crustaceana 80:747–753CrossRefGoogle Scholar
  36. Hadfield M, Strathmann M (1996) Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanol Acta 19:323–334Google Scholar
  37. Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18CrossRefGoogle Scholar
  38. Havinga B (1930) Der Granat (Crangon vulgaris Fabr.) in den hollandischen Gewassern. J Cons Int Explor Mer 5:57–87Google Scholar
  39. Henderson PA, Holmes RHA (1987) On the population biology of the common shrimp Crangon crangon (L.) (Crustacea: Caridea) in the Severn Estuary and Bristol Channel. J Mar Biol Assoc UK 67:825–847CrossRefGoogle Scholar
  40. Hines A (1986a) Larval patterns in the life histories of brachyuran crabs (Crustacea, Decapoda, Brachyura). Bull Mar Sci 39:444–466Google Scholar
  41. Hines A (1986b) Larval problems and perspectives in life histories of marine invertebrates. Bull Mar Sci 39:506–525Google Scholar
  42. Hufnagl M, Temming A, Dänhardt A (2010) Hermaphroditism in brown shrimp: lessons from field data and modelling. Mar Biol 157:2097–2108CrossRefGoogle Scholar
  43. ICES (2009) Report of the Working Group on Crangon Fisheries and Life History (WGCRAN). 10–13 May 2009, Oostende, Belgium. ICES CM 2009/LRC:07 12:1–63Google Scholar
  44. Jacobs JR, Biesiot PM, Perry HM, Trigg C (2003) Biochemical composition of embryonic blue crabs Callinectes sapidus Rathbun 1896 (Crustacea: Decapoda) from the Gulf of Mexico. Bull Mar Sci 72:311–324Google Scholar
  45. Jaeckle WB (1995) Variation in the size, energy content and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 49–78Google Scholar
  46. Jalihal DR, Sankolli KN, Shenoy S (1993) Evolution of larval developmental patterns and the process of freshwaterization in the prawn genus Macrobrachium Bate, 1868 (Decapoda, Palaemonidae). Crustaceana 65:365–376CrossRefGoogle Scholar
  47. Jónasdóttir SH, Trung NH, Hansen F (2005) Egg production and hatching success of the Calanoid copepods Calanus helgolandicus and Calanus finmarchicus in the North Sea from March to September 2001. J Plankton Res 27:1239–1259CrossRefGoogle Scholar
  48. Kattner G, Wehrtmann IS, Merck T (1994) Interannual variations of lipids and fatty acids during larval development of Crangon spp. in the German Bight, North Sea. Comp Biochem Physiol 107B:103–110Google Scholar
  49. Kattner G, Graeve M, Calcagno JA, Lovrich GA, Thatje S, Anger K (2003) Lipid, fatty acid and protein utilization during lecithotrophic larval development of Lithodes santolla (Molina) and Paralomis granulosa (Jacquinot). J Exp Mar Biol Ecol 292:61–74CrossRefGoogle Scholar
  50. Kuipers BR, Dapper R (1984) Nursery function of Wadden Sea tidal flats for the brown shrimp Crangon crangon. Mar Ecol Prog Ser 17:171–181CrossRefGoogle Scholar
  51. Laptikhovsky V (2006) Latitudinal and bathymetric trends in egg size variation: a new look at Thorson’s and Rass’s rules. Mar Ecol 27:7–14CrossRefGoogle Scholar
  52. Lardies MA, Castilla JC (2001) Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar Biol 139:1125–1133CrossRefGoogle Scholar
  53. Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 1–48Google Scholar
  54. Linck BM (1995) Einfluß von Temperatur und Salzgehalt auf die Larven der Nordseegarnele Crangon crangon. Master thesis, University of Oldenburg, GermanyGoogle Scholar
  55. Lowry D, Rosenberg N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  56. Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. Oceanogr Mar Bio Annu Rev 46:203–250CrossRefGoogle Scholar
  57. Meixner R (1969) Wachstum, Häutung und Fortpflanzung von Crangon crangon (L.) bei. Einzelaufzucht. Ber Dt Wiss Kommn Meerersforsch 20:93–111Google Scholar
  58. Meredith SS (1952) A study of Crangon vulgaris in the Liverpool Bay area. Proc Trans Liverp Biol Soc 58:75–109Google Scholar
  59. Meusy JJ, Payen GG (1988) Female reproduction in Malacostracan Crustacea. Zool Sci 5:217–265Google Scholar
  60. Miller CB, Tande KS (1993) Stage duration estimation for Calanus populations, a modelling study. Mar Ecol Prog Ser 102:15–34CrossRefGoogle Scholar
  61. Moland E, Moland OE, Stenseth NC (2010) Maternal influences on offspring size variation and viability in wild European lobster Homarus gammarus. Mar Ecol Prog Ser 400:165–173CrossRefGoogle Scholar
  62. Moran AL, McAlister JS (2009) Egg Size as a life history character of marine invertebrates: is it all it’s cracked up to be? Biol Bull 216:226–242Google Scholar
  63. Morgan SG (1995) Life and death in the plankton: larval mortality and adaptation. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 279–321Google Scholar
  64. Murphy NP, Austin CM (2005) Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development. Zool Script 34:187–197CrossRefGoogle Scholar
  65. Neudecker T, Damm U (1992) Seasonality of egg-bearing shrimp (Crangon crangon L.) in coastal waters of the German Bight. ICES CM K 28:1–9Google Scholar
  66. O’Leary Amsler M, George R (1984) Seasonal variation in the biochemical composition of the embryos of Callinectes sapidus Rathbun. J Crustac Biol 4:546–553CrossRefGoogle Scholar
  67. Oh CW, Hartnoll RG (2004) Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Mar Biol 144:303–316CrossRefGoogle Scholar
  68. Oh CW, Hartnoll RG, Nash RDM (1999) Population dynamics of the common shrimp Crangon crangon (L.), in Port Erin Bay, Isle of Man, Irish Sea. Ices J Mar Sci 56:718–733CrossRefGoogle Scholar
  69. Oh CW, Hartnoll RG, Nash RDM (2001) Feeding ecology of the common shrimp Crangon crangon in Port Erin Bay, Isle of Man, Irish Sea. Mar Ecol Prog Ser 214:211–223CrossRefGoogle Scholar
  70. Ouellet P, Allard J (2002) Seasonal and interannual variability in larval lobster Homarus americanus size, growth and condition in the Magdalen Islands, southern Gulf of St. Lawrence. Mar Ecol Prog Ser 230:241–251CrossRefGoogle Scholar
  71. Ouellet P, Plante F (2004) An investigation of the sources of variability in American lobster (Homarus americanus) eggs and larvae: female size and reproductive status, and interannual and interpopulation comparisons. J Crustac Biol 24:481–495CrossRefGoogle Scholar
  72. Pan M, Pierce G, Cunningham C, Hay S (2011) Spatiotemporal coupling/decoupling of planktonic larvae and benthic settlement in decapods in the Scottish east coast. Mar Biol 158:31–46CrossRefGoogle Scholar
  73. Paschke K (1998) Untersuchungen zum Energiestoffwechsel während der Embryonalentwicklung der Nordsee Garnele Crangon crangon (Linnaeus 1758) (Decapoda: Caridea). Dissertation, University of Hamburg, GermanyGoogle Scholar
  74. Paschke KA, Gebauer P, Buchholz F, Anger K (2004) Seasonal variation in starvation resistance of early larval North Sea shrimp Crangon crangon (Decapoda: Crangonidae). Mar Ecol Prog Ser 279:183–191CrossRefGoogle Scholar
  75. Pechenik JA (2006) Larval experience and latent effects: metamorphosis is not a new beginning. Integr Comp Biol 46:323–333CrossRefGoogle Scholar
  76. Petersen S, Anger K (1997) Chemical and physiological changes during the embryonic development of the spider crab, Hyas araneus L. (Decapoda: Majidae). Comp Biochem Physiol 117B:299–306Google Scholar
  77. Plagmann J (1939) Ernahrungsbiologie der Garnele (Crangon vulgaris Fabr.). Helgol Wiss Meeresunters 2:113–162CrossRefGoogle Scholar
  78. Pond DW, Harris RP, Head RN, Harbour D (1996) Environmental and nutritional factors determining seasonal variability in the fecundity and egg viability of Calanus helgolandicus in coastal waters off Plymouth. UK. Mar Ecol Prog Ser 143:45–63CrossRefGoogle Scholar
  79. Salonen K, Sarvala J, Hakala I, Viljamen ML (1976) The relation of energy and organic carbon in aquatic invertebrates. Limnol Oceanogr 21:724–730CrossRefGoogle Scholar
  80. Sastry AN (1983) Ecological aspects of reproduction. In: Vernberg FJ, Vernberg WB (eds) The biology of Crustacea; environmental adaptations. Academic Press, New York, pp 79–270Google Scholar
  81. Sato T, Suzuki N (2010) Female size as a determinant of larval size, weight, and survival period in the coconut crab, Birgus latro. J Crustac Biol 30:624–628CrossRefGoogle Scholar
  82. Siegel V, Damm U, Neudecker T (2008) Sex-ratio, seasonality and long-term variation in maturation and spawning of the brown shrimp Crangon crangon (L.) in the German Bight (North Sea). Helgol Mar Res 62:339–349CrossRefGoogle Scholar
  83. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506CrossRefGoogle Scholar
  84. Sokal R, Rohlf J (1995) Biometry, 3rd edn. W. H. Freeman, New YorkGoogle Scholar
  85. Spaargaren DH (2000) Seasonal, annual variations in the catches of Crangon crangon (L., 1758(Decapoda, Natantia) near the coast of texel, The Netherlands. Crustaceana 73:547–563CrossRefGoogle Scholar
  86. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  87. Steele DH, Steele VJ (1975) Egg size and duration of embryonic development in crustacea. Int Rev ges Hydrobiol 60:711–715CrossRefGoogle Scholar
  88. Temming A, Damm U (2002) Life cycle of Crangon crangon in the North Sea: a simulation of the timing of recruitment as a function of the seasonal temperature signal. Fish Oceanogr 11:45–58CrossRefGoogle Scholar
  89. Thatje S, Lovrich G, Torres G, Hagen W, Anger K (2004) Changes in biomass, lipid, fatty acid and elemental composition during the abbreviated larval development of the subantartic shrimp Campylonotus vagans. J Exp Mar Biol Ecol 301:159–174CrossRefGoogle Scholar
  90. Tian T, Merico A, Su J, Staneva J, Wiltshire K, Wirtz K (2009) Importance of resuspended sediment dynamics for the phytoplankton spring bloom in a coastal marine ecosystem. J Sea Res 62:214–228CrossRefGoogle Scholar
  91. Tiews K (1954) Die biologischen Grundlagen der Büsumer Garnelenfischerei. Ber Dtsch Wiss Komm Meeresforsch 13:235–269Google Scholar
  92. Tiews K (1970) Synopsis of biological data on the common shrimp Crangon crangon (Linnaeus, 1758). FAO Fish Rep 57:1167–1224Google Scholar
  93. Torres G, Giménez L, Anger K (2007) Effects of osmotic stress on crustacean larval growth and protein and lipid levels are related to life-histories: The genus Armases as a model. Comp Biochem Physiol B 148:209–224CrossRefGoogle Scholar
  94. Turner RL, Lawrence JM (1979) Volume and composition of echinoderm eggs: implications for the use of egg size in life history models. In: Stancyk SE (ed) Reproductive ecology of marine invertebrates. University of South Carolina Press, Columbia, pp 25–40Google Scholar
  95. Underwood AJ, Keough MJ (2001) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Bertness DM, Gaines SD, Hay EM (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 183–200Google Scholar
  96. Viegas I, Martinho F, Neto J, Pardal M (2007) Population dynamics, distribution and secondary production of the brown shrimp Crangon crangon (L.) in a Southern European Estuary. Latitudinal variations. Scientia Marina 71:451–460CrossRefGoogle Scholar
  97. Wear RG (1974) Incubation in British decapod crustacea, and the effects of temperature on the rate and success of embryonic development. J Mar Biol Ass UK 54:745–762CrossRefGoogle Scholar
  98. Webb JB, Eckert GL, Shirley TC, Tamone SL (2007) Changes in embryonic development and hatching in Chionoecetes opilio (Snow Crab) with variation in incubation temperature. Biol Bull 213:67–75CrossRefGoogle Scholar
  99. Wehrtmann IS (1991) How important are starvation periods in early larval development for survival of Crangon septemspinosa larvae? Mar Ecol Prog Ser 73:183–190CrossRefGoogle Scholar
  100. Wehrtmann IS, Kattner G (1998) Changes in volume, biomass, and fatty acids of developing eggs in Nauticaris magellanica (Decapoda: Caridea): a latitudinal comparison. J Crustac Biol 18:413–422CrossRefGoogle Scholar
  101. Wenner A, Kuris A (1991) Crustacean egg production. Crustacean issues, vol 7. Balkema, LisseGoogle Scholar
  102. Wiltshire KH, Malzahn AM, Greve W, Wirtz K, Janisch S, Mangelsdorf P, Manly B, Boersma M (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnol Ocean 53:1294–1302CrossRefGoogle Scholar
  103. Winberg GG (1971) Methods for the estimation of production of aquatic animals. Academic Press, LondonGoogle Scholar
  104. Wood SN (2006) Generalized additive models. An introduction. R. Chapman and Hall/CRC, Boca RatonGoogle Scholar
  105. Wu X, Cheng Y, Zeng C, Wang C, Cui Z (2010) Reproductive performance and offspring quality of the first and the second brood of female swimming crab, Portunus trituberculatus. Aquaculture 303:94–100CrossRefGoogle Scholar
  106. Zöllner N, Kirsch K (1962) Über die quantitative Bestimmung von Lipoiden (Mikromethode) mittels der vielen natürlichen Lipoiden (allen bekannten Plasmalipoide) gemeinsamen Sulphophosphovanillin-Reaktion. Z Gesamte Exp Med 135:545–561CrossRefGoogle Scholar
  107. Zuur AF, Ieno EN, Graham SM (2007) Analysing ecological data (Statistics for Biology and Health). Springer, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ángel Urzúa
    • 1
    • 4
  • Kurt Paschke
    • 2
  • Paulina Gebauer
    • 3
  • Klaus Anger
    • 4
  1. 1.Christian-Albrechts-Universität zu KielKielGermany
  2. 2.Instituto de AcuiculturaUniversidad Austral de ChilePuerto MonttChile
  3. 3.Centro de Investigaciones I-MARUniversidad de Los LagosPuerto MonttChile
  4. 4.Biologische Anstalt Helgoland, Alfred-Wegener-Institut für Polar und MeeresforschungHelgolandGermany

Personalised recommendations