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Strong Maternal Effects and Extreme Heterogeneity of Progeny Development in the Caridean Shrimp Sclerocrangon Boreas (Crangonidae)

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Strong Maternal Effects and Extreme Heterogeneity of Progeny Development in the Caridean Shrimp Sclerocrangon Boreas (Crangonidae) See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/257377197 Strong maternal effects and extreme heterogeneity of progeny development in the caridean shrimp Sclerocrangon boreas (Crangonidae) ARTICLE in MARINE BIOLOGY · DECEMBER 2011 Impact Factor: 2.39 · DOI: 10.1007/s00227-011-1782-8 CITATIONS READS 4 16 3 AUTHORS, INCLUDING: Bernard Sainte-Marie Jean-Claude Brêthes Fisheries and Oceans Canada Université du Québec à Rimouski UQAR 80 PUBLICATIONS 2,224 CITATIONS 44 PUBLICATIONS 598 CITATIONS SEE PROFILE SEE PROFILE Available from: Bernard Sainte-Marie Retrieved on: 15 January 2016 Mar Biol (2011) 158:2835–2845 DOI 10.1007/s00227-011-1782-8 ORIGINAL PAPER Strong maternal eVects and extreme heterogeneity of progeny development in the caridean shrimp Sclerocrangon boreas (Crangonidae) Cynthia Guay · Bernard Sainte-Marie · Jean-Claude Brêthes Received: 26 May 2011 / Accepted: 19 August 2011 / Published online: 11 September 2011 © Her Majesty the Queen in Rights of Canada 2011 Abstract Sclerocrangon boreas is uncommon among marine species. Maternal eVects are varied and may marine coastal carideans in having a non-dispersing, abbre- include: oVspring provisioning (size) which may be inXu- viated (2-stage) larval phase. We investigated the implica- enced by female size and nutritional condition, or season; tions of this strategy in terms of fecundity, oVspring mate choice; manipulation of oVspring sex/phenotype in provisioning and brood care in S. boreas from the St. Law- response to environmental stimuli; brood care; and selec- rence Gulf and Estuary in 2009–2010. Fecundity scaled tion of sites and times for oVspring release. Maternal eVects positively to female body size but was low due to the pro- are major factors inXuencing population dynamics and evo- duction of large, lipid-rich eggs. OVspring size at all stages lutionary trajectories (Marshall and Keough 2008; Marshall of development was positively related to female size. Lar- et al. 2008). val traits and lipid dynamics indicate obligatory lecitho- Maternal investment patterns determine how the Wnite trophic development from hatching to juvenile. The larva amount of energy devoted to gamete production is parti- becomes a juvenile on the mother and remains associated tioned among reproductive events (clutches) and between with her for sometime after. The co-occurrence of early egg the number and size of oocytes within individual clutches stages among many juveniles in some clutches raises the (Marshall and Keough 2008). Crustacean maternal invest- possibility that maternal care of juveniles includes the pro- ment patterns at the species level are largely constrained by visioning of trophic eggs or eggs reclaimed from other phylogeny and habitat (e.g., Sainte-Marie 1991), whereas at females. the individual level they may be modiWed by local environ- mental (e.g., temperature) eVects on physiological pro- cesses (e.g., maternal growth, oogenesis, embryogenesis) Introduction and maternal genotype and phenotype (e.g., size, age). With respect to phenotype, it is generally the case among crusta- Knowledge of maternal eVects is important for understand- ceans that larger females produce more eggs per clutch than ing the ecology, biology and aquaculture potential of smaller females (e.g., Hines 1982; Clarke 1993a). Larger females also may produce bigger and presumed better qual- ity (i.e., better performing) oVspring, at the expense of a Communicated by X. Irigoien. proportional reduction of fecundity (size–number tradeoV) but with the possible return of greater oVspring and/or C. Guay · J.-C. Brêthes maternal Wtness (Marshall and Keough 2008; but see Mar- Institut des sciences de la mer (ISMER), Université du Québec à Rimouski, shall et al. 2010). 300 allée des Ursulines, Rimouski, QC G5L 3A1, Canada Marine crustacean eggs are in general relatively largest in species with abbreviated (advanced or direct) develop- B. Sainte-Marie (&) ment (Rabalais and Gore 1985; Anger 2001; Bauer 2004). Direction des sciences halieutiques et aquaculture, X Institut Maurice-Lamontagne, Pêches et Océans Canada, The larger egg size re ects larger nutrient (yolk) reserves C.P. 1000, Mont-Joli, QC G5H 3Z4, Canada which are essential for extended lecithotrophic develop- e-mail: [email protected] ment (Clarke 1993b; Graeve and Wehrtmann 2003; Thatje 123 2836 Mar Biol (2011) 158:2835–2845 et al. 2004). Lipids are the main energetic reserve for diameter and female size in S. boreas, but noticed no diVer- embryos of all marine crustaceans, contributing at least ence in larval size between small and large females. Posi- 60% of the total energy used for development, but they also tive associations between egg diameter and female size in are important for metabolic processes and the formation of S. boreas reported in Lacoursière-Roussel and Sainte-Marie cellular membranes (Wehrtmann and Kattner 1998; Anger (2009) are inconclusive due to small sample size. These 2001; Figueiredo et al. 2008). The two major lipid compo- two last studies and Birkely and Gulliksen (2003a) casually nents of embryos and larvae are triacylglycerol (TAG), a remarked on the co-occurrence of at least two oVspring class of reserve lipids, and phospholipids which may have developmental stages in S. boreas clutches. multiple roles (Clarke 1977; Heras et al. 2000; Graeve and This study explores aspects of maternal investment in Wehrtmann 2003). The change in proportions of TAG and S. boreas. We tested the hypothesis that maternal oVspring phospholipids in successive oVspring developmental stages size eVects are apparent at every stage of progeny develop- can indicate at which stage oVspring shift from lecithotro- ment, including larvae and juveniles. We also wanted to phy to exogenous feeding (Ouellet et al. 1992; Graeve and better characterize the female size–fecundity relationship, Wehrtmann 2003). Among invertebrates with direct devel- heterogeneity of progeny development within clutches, opment, moreover, the nutritional needs of emerging juve- and site of transformation from postlarva to juvenile. niles may be met temporarily by nurse eggs, sibling Finally, we qualiWed and quantiWed the lipid classes cannibalism or partial predation on maternal body parts present in progeny stages to conWrm lecithotrophic devel- (Perry and Roitberg 2006; Marshall et al. 2008). opment. The sculptured shrimp Sclerocrangon boreas (Phipps 1774) is a boreal-arctic species of the family Crangonidae. This large marine caridean may be found in coarse sedi- Materials and methods ments from the intertidal down to 450 m depth (e.g., Squires 1990; Klekowski and Wdsiawski 1991; Bukin Field collections and laboratory analyses 1992). This species is gonochoric, but females become much larger and live longer than males (Birkely and Gullik- Sclerocrangon boreas were collected from two localities of sen 2003a; Sainte-Marie et al. 2006; Lacoursière-Roussel the St. Lawrence Gulf and Estuary: Baie Sainte-Marguerite and Sainte-Marie 2009). Crangonids, and in particular (BSM; ca. 50°06ЈN, 66°35ЈW) on 14–19 May 2009, and S. boreas, are highly benthic and their grooming appendages Bic Island (BIC; ca. 48°24ЈN, 68°50ЈW) on 15–16 October and behaviors are usually not as well developed as in other 2009 and 6–11 May 2010. A beam trawl with a 3-m wide caridean families (Bauer 2004). Consequently, female cran- horizontal opening and a codend lined with 17-mm netting gonids may accumulate epibioses on their carapace (illus- was used to collect shrimp. We collected premature and trated for S. boreas in Sainte-Marie et al. 2006) and may brooding female S. boreas of the broadest size range possi- host various worms and mollusks beneath their abdomen ble for determination of fecundity, progeny size and lipid (e.g., Fontaine 1977; Miglavs et al. 1993). composition, and eventually genetic parentage analysis. There is little information on fecundity, oVspring provi- Each trawl set lasted 2–5 min at a speed of 1.5–2.0 knots at sioning and brood care in S. boreas. Females spawn in the depths between 15 and 35 m. Trawl contents were promptly period April to August hundreds of large eggs that are sorted and brooding S. boreas females were placed into reportedly incubated over winter (ca 1 year) beneath the individual pots to minimize loss of progeny. abdomen (Ingram 1979; Klekowski and Wdsiawski 1991; At BSM, 109 brooding females were preserved individu- Birkely and Gulliksen 2003a). Larval development of ally in 4% formalin (n = 62) or 100% ethanol (n =47). S. boreas is abbreviated to two, presumably lecithotrophic Twenty-Wve premature females, recognizable by green ova- stages (one zoea and one “postlarva”) which cling to the ries showing through the cephalothorax exoskeleton, were mother’s pleopods with their subcheliform Wrst pereiopods preserved in 4% formalin. Uncertainty about our ability to and hooked dactyls of pereiopods 2–5 (Makarov 1968; discern developmental stage of eggs preserved in ethanol, a Ingram 1979; Haynes 1985). The zoea stage is ephemeral, required preservation method for genetic paternity analy- while the postlarval stage may last for only 3–5 days (at ses, motivated the partitioning of brooding females between 5°C) and separate from its mother before or at “metamor- formalin and ethanol. However, subsequent examination phosis” and transform to a juvenile on the bottom (Ingram revealed that we could distinguish egg developmental 1979). However, juveniles have been found on females stages
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