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Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions

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Abstract

Laboratory experiments on ovigerous females of northern shrimp (Pandalus borealis) were used to assess the effects of temperature and food ration on female condition during incubation and examine how combined effects of temperature and female condition influenced egg survival, embryonic development, and larval characteristics. Ovigerous females were maintained at 2°C, 5°C, and 8°C and fed on a low (three times/week; 2–2.7% W/W) or high ration (five times/week at satiation). The increase in temperature accelerated the developmental time of the eggs but their survival at 8°C was reduced. Conversion efficiency of yolk reserves in developing embryos was significantly reduced at elevated temperatures and larvae hatching at 2°C and 5°C were significantly larger and heavier than those hatching at 8°C. The experimental design did not result in any effect of food ration on the energetic condition of females or on egg characteristics and their biochemical composition. However, lower energy reserves were observed for females held at 8°C.

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References

  • Allen JA (1959) On the biology of the Pandalus borealis Kroyer, with reference to a population off the Northumberland coast. J Mar Biol Assoc UK 38:189–220

    Google Scholar 

  • Anderson PJ (1999) Pandalid shrimp as indicator of ocean climate regime shift. NAFO SCR Doc. 99/80

  • Anderson PJ, Piatt JF (1999) Community reorganization in the Gulf of Alaska following ocean climate regime shift. Mar Ecol Prog Ser 189:117–123

    Google Scholar 

  • Apollonio S, Stevenson DK, Dunton EEJ (1986) Effects of temperature on the biology of the Northern Shrimp, Pandalus borealis, in the Gulf of Maine. NOAA Tech Rep NMFS 42

  • 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

    Google Scholar 

  • Baeza JA, Fernandez M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Funct Ecol 16:241–251

    Article  Google Scholar 

  • Balasundaram C, Pandian TJ (1982) Egg loss during incubation in Macrobrachium nobilii (Henderson and Mathai). J Exp Mar Biol Ecol 59:289–299

    Article  Google Scholar 

  • Berejikian BA, Mathews SB, Quinn TP (1996) Effects of hatchery and wild ancestry and rearing environments on the development of agonistic behaviour in steelhead trout (Oncorhynchus mykiss) fry. Can J Fish Aquat Sci 53:2004–2014

    Article  Google Scholar 

  • Berenboim BI, Sheveleva GK (1989) Data on the deepwater shrimp (Pandalus borealis Koeyer) fecundity in the Barents Sea. ICES C.M. 1989/K:16

  • Bergström BI (1991) Reproductive cycle and the effect of temperature on oogenesis of Pandalus borealis Kroyer, 1838. J Shellfish Res 10:327–331

    Google Scholar 

  • Bergström BI (2000) The biology of Pandalus. Adv Mar Biol 38:55–245

    Google Scholar 

  • Biesiot PM, Perry HM (1995) Biochemical composition of the deep-sea red crab Chaceon quinquedens (Geryonidae): organic reserves of developing embryos and adults. Mar Biol 124:407–416

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  PubMed  Google Scholar 

  • Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34:171–182

    Google Scholar 

  • Branford JR (1978) Incubation period for the lobster Homarus gammarus at various temperatures. Mar Biol 47:363–368

    Article  Google Scholar 

  • Braum E (1967) The survival of fish larvae with reference to their feeding behaviour and food supply. In: Gerking SD (ed) The biological basis of freshwater fish production. Blackwell, Oxford, pp, 113–131

  • Burukovsky RN, Sudnik SA (1997) On realized fecundity of northern shrimp (Pandalus borealis) at Flemish Cap during spring–summer 1996. NAFO SCR Doc 97/94

  • Carr RS, Neff J (1984) Quantitative semi-automated enzymatic assay for tissue glycogen. Comp Biochem Physiol B 77:447–449

    Article  CAS  PubMed  Google Scholar 

  • Chaffee C, Strathmann RR (1984) Constraints on egg masses. I. Retarded development within thick egg masses. J Exp Mar Biol Ecol 84:73–83

    Article  Google Scholar 

  • Clarke A (1982) Lipid synthesis and reproduction in the Polar Shrimp Chorismus antarcticus. Mar Ecol Prog Ser 9:81–90

    CAS  Google Scholar 

  • Clarke A (1993) Egg size and egg composition in polar shrimps (Caridea; Decapoda). J Exp Mar Biol Ecol 168:189–203

    Article  Google Scholar 

  • Clarke A, Gore DJ (1992) Egg size and composition in Ceratoserolis (Crustacea: Isopoda) from the Weddell Sea. Polar Biol 12:129–134

    Article  Google Scholar 

  • Fernandez M, Bock C, Poertner H (2000) The cost of being a caring mother: the ignored factor in the reproduction of marine invertebrates. Ecol Lett 3:487–494

    Article  Google Scholar 

  • Galois R (1987) Les lipides neutres chez les crustacés décapodes: métabolismes et besoins. Oceanis 13:197–215

    CAS  Google Scholar 

  • Gardner C (2001) Composition of eggs in relation to embryonic development and female size in giant crabs [Pseudocarcinus gigas (Lamarck)]. Mar Freshw Res 52:333–338

    Article  Google Scholar 

  • Gimenez L, Anger K (2001) Relationships among salinity, egg size, embryonic development, and larval biomass in the estuarine crab Chasmagnathus granulata Dana, 1851. J Exp Mar Biol Ecol 260:241–257

    Article  PubMed  Google Scholar 

  • Grant SM, Brown JA (1999) Variation in condition of coastal Newfoundland 0-group Atlantic cod (Gadus morhua): field and laboratory studies using simple condition indices. Mar Biol 133:611–620

    Article  Google Scholar 

  • Hartman KJ, Brandt SB (1995) Estimating energy density of fish. Trans Am Fish Soc 124:347–355

    Article  Google Scholar 

  • Harvey M, St-Pierre JF, Gagne A, Beaulieu MF, Gagnon Y (2003) Conditions océanographiques dans l’estuaire et le golf du Saint-Laurent en 2002: zooplancton. Sécretariat canadien de recherche scientifique. Document de recherche 2003/077

  • Hawkes CR, Meyers TR, Shirley TC (1986) Length-weight relationships of blue, Paralithodes platypus, and golden, Lithodes aequispina, king crabs parasitized by the rhizocephalan, Briarosaccus callosus Boschma. Fish Bull 84:327–332

    Google Scholar 

  • Haynes EB, Wigley RL (1969) Biology of the Northern Shrimp, Pandalus borealis, in the Gulf of Maine. Trans Am Fish Soc 98:60–76

    Google Scholar 

  • Heming TA (1982) Effects of temperature on utilization of yolk by Chinook Salmon (Oncorhynchus tshawytscha ) eggs and alevins. Can J Fish Aquat Sci 39:184–190

    Google Scholar 

  • Holdway DA, Beamish FWH (1984) Specific growth rate and proximate body composition of Atlantic cod (Gadus morhua L.). J Exp Mar Biol Ecol 81:147–170

    Article  Google Scholar 

  • Holland DL, Gabbott PA (1971) A micro-analytical scheme for the determination of protein, carbohydrate, lipid and RNA levels in marine invertebrate larvae. J Mar Biol Assoc UK 5:659–668

    Google Scholar 

  • Jeckel WH, Aizpun de Moreno JE, and Moreno VJ (1990) Changes in biochemical composition and lipids of the digestive gland in females of the shrimp Pleoticus muelleri (Bate) during the molting cycle. Comp Biochem Physiol B 96:521–525

    Article  Google Scholar 

  • Knutsen GM, Tilseth S (1985) Growth, development, and feeding success of Atlantic cod larvae Gadus morhua related to egg size. Trans Am Fish Soc 114:507–511

    Article  Google Scholar 

  • Koeller PA (2000) Relative importance of abiotic and biotic factors to the management of the northern shrimp (Pandalus borealis) fishery on the Scotian Shelf. J North Atl Fish Sci 27:21–33

    Google Scholar 

  • Kunisch M, Anger K (1984) Variation in development and growth rates of larval and juvenile spider crabs Hyas areneus reared in the laboratory. Mar Ecol Prog Ser 15:293–301

    Google Scholar 

  • Lambert Y, Dutil JD (1997 a) Can simple condition indices be used to monitor and quantify seasonal changes in the energy reserves of Atlantic cod (Gadus morhua)? Can J Fish Aquat Sci 54:104–112

    Article  Google Scholar 

  • Lambert Y, Dutil JD (1997 b) Condition and energy reserves of Atlantic cod (Gadus morhua) during the collapse of the northern Gulf of St. Lawrence stock. Can J Fish Aquat Sci 54:2388–2400

    Article  Google Scholar 

  • Lysy A, Dvinina EA (1991) On relation of the deep sea shrimp stock size with oceanographic conditions in the Barents Sea. ICES C.M. 1991/K:52

  • MacKenzie BR (1988) Assessment of temperature effects on interrelationships between stage durations, mortality, and growth in laboratory-reared Homarus americanus Milne Edwards larvae. J Exp Mar Biol Ecol 116:87–98

    Article  Google Scholar 

  • Marsh E (1986) Effects of egg size on offspring fitness and maternal fecundity in the orangethroat darter, Etheostoma spectabile (Pisces: Percidae). Copeia 1:18–30

    Google Scholar 

  • Meyer E, Walther A (1988) Methods for the estimation of protein, lipid, carbohydrate and chitin levels in fresh water invertebrates. Arch Hydrobiol 113:161–177

    CAS  Google Scholar 

  • Morais S, Narciso L, Calado R, Nunes ML, Rosa R (2002) Lipid dynamics during the embryonic development of Plesionika martia martia (Decapoda;Pandalidae), Palaemon serratus and Palaemon elegans (Decapoda;Palaemonidae): relation to metabolic consumption. Mar Ecol Prog Ser 242:195–204

    CAS  Google Scholar 

  • MPO (2001) Les conditions océanographiques dans le golfe du Saint-Laurent en 2001. MPO—Sciences, Rapport sur l’état des stocks G4–01

  • Narciso L, Morais S (2001) Fatty acid profile of Palaemon serratus (Palaemonidae) eggs and larvae during embryonic and larval development using different live diets. J Crustac Biol 21:566–574

    Google Scholar 

  • Nates SF, McKenney CL Jr (2000) Ontogenetic changes in biochemical composition during larval and early postlarval development of Lepidophthalmus louisianensis, a ghost shrimp with abbreviated development. Comp Biochem Physiol B 127:459–468

    Article  CAS  PubMed  Google Scholar 

  • Nunes P (1984) Reproductive and larval biology of northern shrimp Pandalus borealis (Krøyer) in relation to temperature. PhD thesis, University of Alaska, Fairbanks, Alaska

  • Nunes P, Nishiyama T (1984) Effects of temperature and food availability on the survival and growth of larvae of the northern pink shrimp Pandalus borealis Kroyer. J Shellfish Res 1:96–97

    Google Scholar 

  • Ouellet P, Taggart CT, Frank KT (1992) Lipid condition and survival in shrimp (Pandalus borealis ) larvae. Can J Fish Aquat Sci 49:368–378

    Google Scholar 

  • Palacios E, Ibarra AM, Ramirez JL, Portillo G, Racotta IS (1998) Biochemical composition of eggs and nauplii in white Pacific shrimp, Penaeus vannamei (Boone), in relation to the physiological condition of spawners in a commercial hatchery. Aquacult Res 29:183–189

    Article  Google Scholar 

  • Pandian TJ (1970a) Ecophysiological studies on the developing eggs and embryos of the European lobster Homarus gammarus. Mar Biol 5:154–167

    Article  Google Scholar 

  • Pandian TJ (1970b) Yolk utilization and hatching time in the Canadian lobster, Homarus americanus. Mar Biol 7:249–254

    Article  Google Scholar 

  • Parsons DG, Tucker GE (1986) Fecundity of northern shrimp, Pandalus borealis, (Crustacea, Decapoda) in areas of the Northwest Atlantic. Fish Bull 84:549–558

    Google Scholar 

  • Perkins HC (1972) Developmental rates at various temperatures of embryos of the northern lobster (Homarus americanus Milne-Edwards). Fish Bull 70:95–99

    Google Scholar 

  • 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 B 117:299–306

    Article  Google Scholar 

  • Rasmussen B (1953) On the geographical variation in growth and sexual development of deep sea prawn (Pandalus borealis Kr.). Fiskeridir Skr (Havunders.) Rep Norw Fish Invest 10:1–160

  • Rasmussen T (1992) Temperature dependent growth in larvae of the deep water prawn, Pandalus borealis Kroyer, reared in the laboratory. ICES C.M. 1992/K:17

  • Rasmussen T, Tande K (1995) Temperature-dependent development, growth and mortality in larvae of the deep-water prawn Pandalus borealis reared in the laboratory. Mar Ecol Prog Ser 118:149–157

    Google Scholar 

  • Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Can J Fish Aquat Sci 43:2311–2319

    CAS  Google Scholar 

  • Shirley SM, Shirley TC, Rice SD (1987) Latitudinal variation in the Dungeness crab, Cancer magister, zoeal morphology explained by incubation temperature. Mar Biol 95:371–376

    Article  Google Scholar 

  • Shumway SE, Perkins HC, Schick DF, Stickney AP (1985) Synopsis of biological data on the pink shrimp, Pandalus borealis Krøyer, 1838. FAO Fisheries Synopsis No. 144

  • Sibert V, Ouellet P, Brêthes JC (2004) Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle. Mar Biol 144:1075–1086

    Article  CAS  Google Scholar 

  • Simard Y, Savard L (1990) Variability, spatial patterns and scales of similarity in size-frequency distributions of the northern shrimp (Pandalus borealis ) and its migrations in the Gulf of St. Lawrence. Can J Fish Aquat Sci 47:794–804

    Google Scholar 

  • Skuladottir U, Jonsson E, Hallgrimsson I (1978) Testing for heterogeneity of Pandalus borealis populations at Iceland. ICES C.M. 1978/K:27

  • Smith GG, Ritar AJ, Dunstan GA (2003) An activity test to evaluate larval competency in spiny lobsters (Jasus edwardsii) from wild and captive ovigerous broodstock held under different environmental conditions. Aquaculture 218:1–4

    Article  Google Scholar 

  • Smith GG, Ritar AJ, Thompson PA, Dunstan GA, Brown MR (2002) The effect of embryo incubation temperature on indicators of larval viability in Stage I phyllosoma of the spiny lobster, Jasus edwardsii. Aquaculture 209:1–4

    Article  Google Scholar 

  • Starr M, St-Amand L, Berard-Therriault L (2002) Etat de phytoplancton dans l’estuaire et le golfe du Saint-Laurent en 2001. Sécretariat canadien de recherche scientifique. Document de recherche 2002/067

  • Stickney AP (1981) Laboratory studies on the development and survival of Pandalus borealis eggs in the Gulf of Maine. In: Frady T (ed) Proceedings of the International Pandalid Shrimp Symposium. February 13–15, 1979. Univ Alaska Sea Grant Rep 81–3, Kodiak, Alaska, pp, 395–405

  • Stickney AP, Perkins HC (1977) Environmental physiology of commercial shrimp, Pandalus borealis. Project 3-202-R Completion Report, February 1, 1974 to January 31, 1977. Dept Mar Resour, W Boothbay Harbor, Maine

  • Stickney AP, Perkins HC (1981) Observations on the food of the larvae of the Northern Shrimp, Pandalus borealis Kroeyer (Decapoda, Caridea). Crustaceana 40:36–49

    Google Scholar 

  • Strathmann RR, Strathmann MF (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428

    Google Scholar 

  • Tande KS, Rasmussen T, Pedersen G (1994) Thermal increase enhancement: a possible link between recruitment and climate in high latitude environments. ICES Mar Sci Symp 198:502–509

    Google Scholar 

  • Tessier AJ, Consolatti NL (1989) Variation in offspring size in Daphnia and consequences for individual fitness. Oikos 56:269–276

    Google Scholar 

  • Tong LJ, Moss GA, Pickering TD, Paewai MP (2000) Temperature effects on embryo and early larval development of the spiny lobster Jasus edwardsii, and description of a method to predict larval hatch times. Mar Freshw Res 51:243–248

    Google Scholar 

  • Wehrtmann IS, Graeve M (1998) Lipid composition and utilization in developing eggs of two tropical marine caridean shrimps (Decapoda: Caridea: Alpheidae, Palaemonidae). Comp Biochem Physiol B 121:457–463

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Wienberg R (1982) Studies on the influence of temperature, salinity, light, and feeding rate on laboratory reared larvae of deep sea shrimp, Pandalus borealis Kroyer 1838. Meeresforsch Rep Mar Res 29:136–153

    Google Scholar 

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Acknowledgements

Special thanks to Mario Peloquin for the construction and maintenance of the experimental set-up. We also thank Louise Savard for helpful discussions on the biology of northern shrimp and for the collection of wild shrimp samples and live shrimp specimens for the experiments. We are grateful to Brigitte Desrosiers for her assistance with the biochemical analysis and to Gaétan Daigle for his assistance with the statistics. Gilles Gauthier and two anonymous reviewers provided helpful comments on earlier versions of the manuscript. This study was made possible through funds provided by the Department of Fisheries and Oceans under the Science Strategic Fund program on Growth and Recruitment of Northern Shrimp and by the shrimp fisherman associations of Québec and New-Brunswick under the DFO—Group B Fishermen comanagement agreement. Sophie Brillon was supported by a FCAR postgraduate scholarship (fond québécois pour la Formation de Chercheurs et l’Aide à la Recherche). All experiments were conducted in compliance with the current laws of Canada.

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Correspondence to Yvan Lambert.

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Communicated by R.J. Thompson, St. John’s

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Brillon, S., Lambert, Y. & Dodson, J. Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions. Marine Biology 147, 895–911 (2005). https://doi.org/10.1007/s00227-005-1633-6

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