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Strong maternal effects and extreme heterogeneity of progeny development in the caridean shrimp Sclerocrangon boreas (Crangonidae)

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Abstract

Sclerocrangon boreas is uncommon among marine coastal carideans in having a non-dispersing, abbreviated (2-stage) larval phase. We investigated the implications of this strategy in terms of fecundity, offspring provisioning and brood care in S. boreas from the St. Lawrence Gulf and Estuary in 2009–2010. Fecundity scaled positively to female body size but was low due to the production of large, lipid-rich eggs. Offspring size at all stages of development was positively related to female size. Larval traits and lipid dynamics indicate obligatory lecithotrophic development from hatching to juvenile. The larva becomes a juvenile on the mother and remains associated with her for sometime after. The co-occurrence of early egg stages among many juveniles in some clutches raises the possibility that maternal care of juveniles includes the provisioning of trophic eggs or eggs reclaimed from other females.

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Notes

  1. Progeny CL can be estimated for stage 2 larva by CL = 0.740 + 0.218 TL, r 2 = 0.39, F 1,211 = 135.68, P < 0.001; for juvenile by CL = −0.041 + 0.292 TL, r 2 = 0.56, F 1,242 = 303.08, P < 0.001.

  2. Cited diameters are the mean of egg width and length reported in each study; most studies did not indicate egg development stage and maternal size which both influence egg diameter.

References

  • Anger K (2001) The biology of decapod crustacean larvae. Crustacean issues 14. AA Balkema, Lisse

    Google Scholar 

  • Bauer RT (2004) Remarkable shrimps: adaptations and natural history of the Carideans. University of Oklahoma Press, Norman

    Google Scholar 

  • Birkely S-R, Gulliksen B (2003a) Population features of the caridean shrimp, Sclerocrangon boreas (Phipps, 1774) in Isfjorden, Spitsbergen. Crustaceana 76:87–101

    Article  Google Scholar 

  • Birkely S-R, Gulliksen B (2003b) Feeding ecology in five shrimp species (Decapoda, Caridea) from an Arctic fjord (Isfjorden, Svalbard), with emphasis on Sclerocrangon boreas (Phipps, 1774). Crustaceana 76:699–715

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brillon S, Lambert Y, Dodson J (2005) Egg survival, embryonic development, and larval characteristics of the northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions. Mar Biol 147:895–911

    Article  Google Scholar 

  • Bukin SD (1992) Distribution, abundance and biology of the northern bear shrimp (Sclerocrangon boreas) in the northwestern Bering Sea. In: Ivanov BG (ed) Promyslovo-biologisheskie Issledovaniya Morskikh Bespozvonochnykh, VINRO Publishing, Moscow, pp 68–77 (In Russian, translated to English in Can Transl Fish Aquat Sci 5670)

  • Caine EA (1991) Behavior and sexual dimorphism of a caprellid amphipod. J Crustac Biol 11:56–63

    Article  Google Scholar 

  • Chace FA Jr, Holthuis LB (1978) Psalidopus: the scissor-foot shrimps (Crustacea: Decapoda: Caridea). Smiths Contr Zool 277

  • Clarke A (1977) Lipid class and fatty acid composition of Chorismus antarcticus (Pfeffer) (Crustacea: Decapoda) at South Georgia. J Exp Mar Biol Ecol 28:297–314

    Article  CAS  Google Scholar 

  • Clarke A (1993a) Reproductive trade-offs in caridean shrimps. Funct Ecol 7:411–419

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Correa C, Thiel M (2003) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Rev Chil Hist Natur 76:187–203

    Google Scholar 

  • Cuesta JA, Palacios-Theil E, Drake P, Rodríguez A (2006) A new rare case of parental care in decapods. Crustaceana 79:1401–1405

    Article  Google Scholar 

  • Elgar MA, Crespi BJ (1992) Cannibalism. Ecology and evolution among diverse taxa. Oxford University Press, Oxford

    Google Scholar 

  • Erdman RB, Blake NJ (1987) Population dynamics of the sponge-dwelling alpheid Synalpheus longicarpus, with observations on S. brooksi and S. pectiniger, in shallow-water assemblages of the eastern Gulf of Mexico. J Crustac Biol 7:328–337

    Article  Google Scholar 

  • Felder DL (1982) Reproduction of the snapping shrimps Synalpheus fritzmuelleri and S. apioceros (Crustacea: Decapoda: Alpheidae) on a sublittoral reef off Texas. J Crustac Biol 2:535–543

    Article  Google Scholar 

  • Fernández M, Ruiz-Tagle N, Cifuentes S, Pörtner HO, Arntz W (2003) Oxygen-dependent asynchrony of embryonic development in embryo masses of brachyuran crabs. Mar Biol 142:559–565

    Google Scholar 

  • Figueiredo J, Penha-Lopes G, Anto J, Narciso L, Lin J (2008) Potential fertility and egg development (volume, water, lipid, and fatty acid content) through embryogenesis of Uca rapax (Decapoda: Brachyura: Ocypodidae). J Crustac Biol 28:528–533

    Article  Google Scholar 

  • Fontaine B (1977) Fixation d’une ponte de gastéropode sur les crevettes de la famille des crangonidées. Rev Trav Inst Pêches Marit 41:301–307

    Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Ann Rev Entomol 45:341–369

    Article  CAS  Google Scholar 

  • Graeve M, Wehrtmann IS (2003) Lipid and fatty acid composition of Antarctic shrimp eggs (Decapoda: Caridea). Polar Biol 26:55–61

    Google Scholar 

  • Haynes EB (1985) Morphological development, identification, and biology of larvae of Pandalidae, Hippolytidae, and Crangonidae (Crustacea, Decapoda) of the northern north Pacific Ocean. Fish Bull US 83:253–288

    Google Scholar 

  • Heras H, Gonzalez-Baró MR, Pollero RJ (2000) Lipid and fatty acid composition and energy partitioning during embryo development in the shrimp Macrobrachium borellii. Lipids 35:645–651

    Article  CAS  Google Scholar 

  • Herring PJ (1974) Size, density and lipid content of some decapod eggs. Deep Sea Res 21:91–94

    Google Scholar 

  • Hines AH (1982) Allometric constraints and variables of reproductive effort in brachyuran crabs. Mar Biol 69:309–320

    Article  Google Scholar 

  • Huguet D, García Muñoz JE, García Rasto JEG, Cuesta JA (2011) Extended parental care in the freshwater shrimp genus Dugastella Bouvier, 1912 (Decapoda, Atyidae, Paratyinae). Crustaceana 84:251–255

    Article  Google Scholar 

  • Ingram MP (1979) On the biology and larval development of Sclerocrangon boreas (Phipps) and the mariculture of certain Crustacea. PhD thesis, University of Liverpool, Liverpool

  • Klekowski RZ, Węsławski JM (1991) Atlas of the marine fauna of southern Spitsbergen, 2, Invertebrates (1). Polish Academy of Science, Gdansk

    Google Scholar 

  • Kuris A (1991) A review of patterns and causes of crustacean brood mortality. In: Wenner A, Kuris A (eds) Crustacean egg production. Proceedings of the conference on crustacean egg production, Annual meeting of the American society of zoologists, Santa Barabara, 1987. Crustac Issues 7, AA Balkema, Rotterdam, pp 117–142

  • Lacoursière-Roussel A, Sainte-Marie B (2009) Sexual system and female spawning frequency in the sculptured shrimp Sclerocrangon boreas (Decapoda: Caridea: Crangonidae). J Crustac Biol 29:192–200

    Article  Google Scholar 

  • Li HY, Hong SY, Jin ZH (2011) Fecundity and brood loss of sand shrimp, Crangon uritai (Decapoda: Crangonidae). J Crustac Biol 31:34–40

    Article  CAS  Google Scholar 

  • Makarov R (1968) On the larval development of the genus Sclerocrangon G.O. Sars (Caridea, Crangonidae). Crustaceana Suppl 2:27–37

    Google Scholar 

  • Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60

    Article  Google Scholar 

  • Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. Oceanogr Mar Biol Ann Rev 46:203–250

    Article  Google Scholar 

  • Marshall DJ, Heppell SS, Munch SB, Warner RR (2010) The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring? Ecology 91:2862–2873

    Article  Google Scholar 

  • Miglavs IJ, Sneli JA, Waren A (1993) Brood protection of Oenopota (Gastropoda: Turridae) eggs by the shrimp Sclerocrangon boreas (Phipps). J Mollusc Stud 59:363–365

    Article  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 P. elegans (Decapoda; Palaemonidae): relation to metabolic consumption. Mar Ecol Prog Ser 242:195–204

    Article  CAS  Google Scholar 

  • Oh C-W, Hartnoll RG (1999) Brood loss during incubation in Philocheras trispinosus (Decapoda) in Port Erin Bay, Isle of Man. J Crustac Biol 19:467–476

    Article  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

    Article  Google Scholar 

  • Ouellet P, Taggart CT, Frank KT (1995) Early growth, lipid composition, and survival expectations of shrimp Pandalus borealis larvae in the northern Gulf of St. Lawrence. Mar Ecol Prog Ser 126:163–175

    Article  CAS  Google Scholar 

  • Pandian TJ (1967) Changes in chemical composition and caloric content of developing eggs of the shrimp Crangon crangon. Helgoland Meeresunters 16:216–224

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Patterson L, Dick JTA, Elwood RW (2008) Embryo retrieval and kin recognition in an amphipod (Crustacea). Anim Behav 76:717–722

    Article  Google Scholar 

  • Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714

    Article  Google Scholar 

  • Quiroga EJ, Soto RM (1997) Relaciones biométricas y fecundidad de Glyphocrangon alata (Faxon, 1893) en la zona norte de Chile (21°19′S; 70°20′W). Invest Mar Valparaíso 25:281–285

    Google Scholar 

  • Rabalais NN, Gore RH (1985) Abbreviated development in decapods. In: Wenner A (ed) Larval growth. Crustac issues 2. AA Balkema, Rotterdam, pp 67–126

    Google Scholar 

  • Rodríguez A, Cuesta JA (2011) Morphology of larval and first juvenile stages of the kangaroo shrimp Dugastella valentina (Crustacea, Decapoda, Caridea), a freshwater atyid with abbreviated development and parental care. Zootaxa 2867:43–58

    Google Scholar 

  • Sainte-Marie B (1991) A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223:189–227

    Article  Google Scholar 

  • Sainte-Marie B, Bérubé I, Brillon S, Hazel F (2006) Observations on the growth of the sculptured shrimp Sclerocrangon boreas (Decapoda: Caridea). J Crustac Biol 26:55–62

    Article  Google Scholar 

  • Sibert V, Ouellet P, Brêthes J-C (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 

  • Smith HL, Gibson GD (1999) Nurse egg origin in the polychaete Boccardia proboscidea (Spionidae). Invertebr Reprod Dev 35:177–185

    Article  Google Scholar 

  • Squires HJ (1990) Decapod crustacea of the Atlantic coast of Canada. Can Bull Fish Aquat Sci 221:532

    Google Scholar 

  • Thatje S, Lovrich GA, Anger K (2004) Egg production, hatching rates, and abbreviated larval development of Campylonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea), in subantarctic waters. J Exp Mar Biol Ecol 301:15–27

    Article  Google Scholar 

  • Torati LS, Mantelatto FL (2008) Uncommon mechanism of egg incubation in the endemic Southern hermit crab Loxopagurus loxochelis: how is this phenomenon related to egg production? Acta Zool 89:79–85

    Article  Google Scholar 

  • Wehrtmann IS, Graeve M (1998) Lipid composition and utilization in developing eggs of two tropical marine caridean shrimps (Decapoda: Caridea: Alpheidea, Palaemonidae). Comp Bioch Physiol Part B Biochem Mol Biol 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

    Article  Google Scholar 

  • Zarenkov N (1965) Revision of the genera Crangon Fabricius and Sclerocrangon G.O. Sars (Decapoda, Crustacea). Zool Zh Mosc 44:1761–1775 (In Russian, translated to English in Fish Res Bd Can Transl Serv 1465)

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Acknowledgments

This study was supported by postgraduate scholarships from Natural Sciences and Engineering Research Council of Canada (NSERC), Fonds québécois de la recherche sur la nature et les technologies (FQRNT) and Institut des sciences de la mer de Rimouski (ISMER) to C. Guay. Field work and laboratory analyses were funded by Fisheries and Oceans Canada and an NSERC Discovery Grant to B. Sainte-Marie. We thank H. Dionne for her assistance during field and laboratory work, and P. Ouellet for guidance in lipid analyses. The manuscript was improved by comments from Y. Lambert, P. Ouellet, J.-M. Sévigny and two anonymous reviewers.

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Authors and Affiliations

  1. Institut des sciences de la mer (ISMER), Université du Québec à Rimouski, 300 allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

    Cynthia Guay & Jean-Claude Brêthes

  2. Direction des sciences halieutiques et aquaculture, Institut Maurice-Lamontagne, Pêches et Océans Canada, C.P. 1000, Mont-Joli, QC, G5H 3Z4, Canada

    Bernard Sainte-Marie

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  1. Cynthia Guay
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  2. Bernard Sainte-Marie
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  3. Jean-Claude Brêthes
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Correspondence to Bernard Sainte-Marie.

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Communicated by X. Irigoien.

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Guay, C., Sainte-Marie, B. & Brêthes, JC. Strong maternal effects and extreme heterogeneity of progeny development in the caridean shrimp Sclerocrangon boreas (Crangonidae). Mar Biol 158, 2835–2845 (2011). https://doi.org/10.1007/s00227-011-1782-8

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