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

Marine Biology

Volumn 159, Issue 3, 2012, Pages 583-599

  Urzúa, Ángel ^a,d   Paschke, Kurt ^b   Gebauer, Paulina ^c   Anger, Klaus ^d  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c UNIVERSIDAD DE LOS LAGOS   (Chile)

^d ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANNUAL VARIATION; BIOCHEMICAL COMPOSITION; BIOMASS; BREEDING SEASON; COMMERCIAL SPECIES; CRUSTACEAN; EGG; EGG SIZE; LIFE HISTORY TRAIT; PHENOTYPIC PLASTICITY; REPRODUCTIVE BIOLOGY; SEASONAL VARIATION; SEASONALITY;

CARIDEA; CRANGON CRANGON; DECAPODA (CRUSTACEA);

EID: 84857458715     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-011-1837-x     Document Type: Article

References (107)

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: 39-49.
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: 225-237.
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: 31-38.
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: 203-215.
5. Anger K (2001) The biology of decapod crustacean larvae. Crustacean issues, vol 14. Balkema, Lisse.
6. Anger K, Harms J (1990) Elemental (CHN) and proximate biochemical composition of decapod crustacean larvae. Comp Biochem Physiol B 97: 69-80.
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: 83-93.
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: 243-251.
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: 335-349.
10. Arthur W (2000) Intraspecific variation in developmental characters: the origin of evolutionary novelties. Am Zool 40: 811-818.
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: 1157-1164.
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: 225-237.
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: 1-12.
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: 151-162.
15. Bomirski A, Kle{ogonek}k E (1974) Action of eyestalks on ovary in Rhithropanopeus harrisii and Crangon crangon (Crustacea- Decapoda). Mar Biol 24: 329-337.
16. Botsford LW (1991) Crustacean egg production and fisheries management. In: Wenner A, Kuris A (eds) Crustacean egg production. Balkema, Rotterdam, pp 379-394.
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: 15-27.
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: 106-113.
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: 203-219.
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: 4297-4303.
21. Clarke A (1993) Reproductive trade-offs in caridean shrimps. Funct Ecol 7: 411-419.
22. Criales MM (1985) Untersuchungen zur Larvalentwicklung von Crangon crangon L. und Crangon allmanni Kinahan (Decapoda, Natantia, Caridea). Dissertation, University of Kiel, Germany.
23. Criales MM, Anger K (1986) Experimental studies on the larval development of the shrimps Crangon crangon and C. allmanni. Helgoländer Meeresunters 40: 241-265.
24. Díaz H (1980) The mole crab Emerita talpoida (Say): a case of changing life history pattern. Ecol Monogr 50: 437-456.
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: 585-601.
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: 157-164.
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: 193-202.
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: 497-509.
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: 103-112.
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 609-665.
31. Giménez L (2006) Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans. Integr Comp Biol 46: 615-622.
32. Giménez L (2010) Relationships between habitat conditions, larval traits, and juvenile performance in a marine invertebrate. Ecology 91: 1401-1413.
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: 570-580.
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: 275-305.
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: 747-753.
36. Hadfield M, Strathmann M (1996) Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanol Acta 19: 323-334.
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: 4-18.
38. Havinga B (1930) Der Granat (Crangon vulgaris Fabr.) in den hollandischen Gewassern. J Cons Int Explor Mer 5: 57-87.
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: 825-847.
40. Hines A (1986a) Larval patterns in the life histories of brachyuran crabs (Crustacea, Decapoda, Brachyura). Bull Mar Sci 39: 444-466.
41. Hines A (1986b) Larval problems and perspectives in life histories of marine invertebrates. Bull Mar Sci 39: 506-525.
42. Hufnagl M, Temming A, Dänhardt A (2010) Hermaphroditism in brown shrimp: lessons from field data and modelling. Mar Biol 157: 2097-2108.
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: 1-63.
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: 311-324.
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 49-78.
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: 365-376.
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: 1239-1259.
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: 103-110.
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: 61-74.
50. Kuipers BR, Dapper R (1984) Nursery function of Wadden Sea tidal flats for the brown shrimp Crangon crangon. Mar Ecol Prog Ser 17: 171-181.
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: 7-14.
52. Lardies MA, Castilla JC (2001) Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodeschilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar Biol 139: 1125-1133.
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 1-48.
54. Linck BM (1995) Einfluß von Temperatur und Salzgehalt auf die Larven der Nordseegarnele Crangon crangon. Master thesis, University of Oldenburg, Germany.
55. Lowry D, Rosenberg N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
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: 203-250.
57. Meixner R (1969) Wachstum, Häutung und Fortpflanzung von Crangon crangon (L.) bei. Einzelaufzucht. Ber Dt Wiss Kommn Meerersforsch 20: 93-111.
58. Meredith SS (1952) A study of Crangon vulgaris in the Liverpool Bay area. Proc Trans Liverp Biol Soc 58: 75-109.
59. Meusy JJ, Payen GG (1988) Female reproduction in Malacostracan Crustacea. Zool Sci 5: 217-265.
60. Miller CB, Tande KS (1993) Stage duration estimation for Calanus populations, a modelling study. Mar Ecol Prog Ser 102: 15-34.
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: 165-173.
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: 226-242.
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 279-321.
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: 187-197.
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: 1-9.
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: 546-553.
67. Oh CW, Hartnoll RG (2004) Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Mar Biol 144: 303-316.
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: 718-733.
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: 211-223.
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: 241-251.
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: 481-495.
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: 31-46.
73. Paschke K (1998) Untersuchungen zum Energiestoffwechsel während der Embryonalentwicklung der Nordsee Garnele Crangon crangon (Linnaeus 1758) (Decapoda: Caridea). Dissertation, University of Hamburg, Germany.
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: 183-191.
75. Pechenik JA (2006) Larval experience and latent effects: metamorphosis is not a new beginning. Integr Comp Biol 46: 323-333.
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: 299-306.
77. Plagmann J (1939) Ernahrungsbiologie der Garnele (Crangon vulgaris Fabr.). Helgol Wiss Meeresunters 2: 113-162.
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: 45-63.
79. Salonen K, Sarvala J, Hakala I, Viljamen ML (1976) The relation of energy and organic carbon in aquatic invertebrates. Limnol Oceanogr 21: 724-730.
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 79-270.
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: 624-628.
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: 339-349.
83. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108: 499-506.
84. Sokal R, Rohlf J (1995) Biometry, 3rd edn. W. H. Freeman, New York.
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: 547-563.
86. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford.
87. Steele DH, Steele VJ (1975) Egg size and duration of embryonic development in crustacea. Int Rev ges Hydrobiol 60: 711-715.
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: 45-58.
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: 159-174.
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: 214-228.
91. Tiews K (1954) Die biologischen Grundlagen der Büsumer Garnelenfischerei. Ber Dtsch Wiss Komm Meeresforsch 13: 235-269.
92. Tiews K (1970) Synopsis of biological data on the common shrimp Crangon crangon (Linnaeus, 1758). FAO Fish Rep 57: 1167-1224.
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: 209-224.
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 25-40.
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 183-200.
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: 451-460.
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: 745-762.
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: 67-75.
99. Wehrtmann IS (1991) How important are starvation periods in early larval development for survival of Crangon septemspinosa larvae? Mar Ecol Prog Ser 73: 183-190.
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: 413-422.
101. Wenner A, Kuris A (1991) Crustacean egg production. Crustacean issues, vol 7. Balkema, Lisse.
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: 1294-1302.
103. Winberg GG (1971) Methods for the estimation of production of aquatic animals. Academic Press, London.
104. Wood SN (2006) Generalized additive models. An introduction. R. Chapman and Hall/CRC, Boca Raton.
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: 94-100.
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: 545-561.
107. Zuur AF, Ieno EN, Graham SM (2007) Analysing ecological data (Statistics for Biology and Health). Springer, New York.