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Offspring Size and Maternal Environments Mediate the Early Juvenile Performance of Two Congeneric Whelks

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Offspring Size and Maternal Environments Mediate the Early Juvenile Performance of Two Congeneric Whelks Vol. 459: 73–83, 2012 MARINE ECOLOGY PROGRESS SERIES Published July 12 doi: 10.3354/meps09763 Mar Ecol Prog Ser Offspring size and maternal environments mediate the early juvenile performance of two congeneric whelks Sergio A. Carrasco1,*, Nicole E. Phillips1, Alejandro Pérez-Matus2 1School of Biological Sciences and Coastal Ecology Laboratory, Victoria University of Wellington, Wellington 6140, New Zealand 2Laboratorio de Ecología Marina, Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaíso, Casilla 5080, Avenida Borgoño 16344, Viña del Mar, Chile ABSTRACT: Offspring size variation can have pervasive ecological and evolutionary implications for both offspring and mother, affecting an organism’s performance throughout its life. Using 2 marine intertidal whelk species Cominella virgata and C. maculosa as model organisms, we examined how different maternal environments and contrasting hatchling size influence juvenile performance. The average size of field-collected hatchlings greatly differed between the species and at different scales of variation (i.e. among sites). Species-specific differences in hatching size were reflected in juvenile performance. Overall, C. virgata with larger hatchlings (~3 mm), exhib- ited faster growth rates and higher survival than the smaller C. maculosa (~1.5 mm). Desiccation treatment did not affect the performance of fed juveniles; however, large hatchlings had higher growth rates than small conspecifics for both species. Starved hatchlings of both species per- formed more poorly than fed ones; however, species- specific and size differences were less signif- icant for the evaluated traits, suggesting a non- size-related allocation of resources and similar resource utilization during starvation conditions (i.e. within species). As has been described for many taxa, large offspring often perform better than small conspecifics; however, because this performance is likely context-dependent, understanding the importance of different scales of vari- ation is crucial for determining when variation in size is an advantage or a disadvantage in terms of an organism’s performance. KEY WORDS: Progeny size · Reproductive strategies · Environmental variation · Phenotypic plasticity · Offspring size-fitness · Cominella Resale or republication not permitted without written consent of the publisher INTRODUCTION jan et al. 2003), ascidians (Marshall et al. 2003, 2006), beetles (Fox 2000, Clark et al. 2011), isopods (Tsai & Offspring size is a key trait for most organisms, Dai 2001), spiders (Walker et al. 2003), fish (Green & influencing an individual’s subsequent performance McCormick 2005, Fisher et al. 2007), and birds (Krist and having direct consequences in fitness for both 2011). Therefore, intraspecific variation in offspring the offspring and mother. For a range of taxa across a size is of fundamental ecological and evolutionary variety of habitats, individuals that start juvenile life importance (Marshall & Keough 2008). Offspring size with a large size often perform better than smaller often varies spatially (i.e. among and within popula- conspecifics. This pattern has been shown for gas- tions, clutches, or siblings) and temporally (Bernardo tropods (Spight 1976, Gosselin 1997, Moran & Emlet 1996). Several explanations have been proposed for 2001), mussels (Phillips 2002), barnacles (Thiyagara- these scales of variation, but they are often attributed *Email: [email protected] © Inter-Research 2012 · www.int-res.com 74 Mar Ecol Prog Ser 459: 73–83, 2012 to either non-adaptive stochastic variation in provi- time of spawning is the primary source of nutrition sioning or to a maternal bet-hedging strategy in until the offspring enter juvenile life (Spight 1976, unpredictable environments (see Kamel et al. 2010). Rivest 1983). This characteristic makes direct-devel- The ability of mothers to anticipate the environ- oping invertebrates an interesting model system to ment that their offspring will experience may there- evaluate how maternal environments and initial fore mediate variation in offspring size. When moth- maternal-derived resources affect offspring traits ers are able to predict their offspring’s environment, (e.g. size, growth rate, and overall survival) and to the expectation is that plasticity in mean offspring determine the scales of variation at which these size will be favored (‘anticipatory’ maternal effects; maternal effects are evident and comparable within Marshall & Uller 2007). Conversely, when mothers or among populations. To date, few studies have are unable to predict the environment, the expected examined this system; however, they have found outcome is that increases in the variation of offspring consistent relationships between hatchling size and size will ensure that some offspring will be optimal performance (e.g. larger hatchlings showing better for the environment (Crean & Marshall 2009). Re- growth and survival than small conspecifics; Moran gardless of the strategy, the division of finite repro- & Emlet 2001), hatchling size and maternal habitat ductive resources should ultimately result in an opti- (e.g. smaller hatchling sizes from more protected mal equilibrium between the offspring fitness and habitats; Lloyd & Gosselin 2007), and maternal the maximization of the parental fitness, and there- resources and offspring performance (e.g. higher fore, simple models have typically suggested that as growth of juveniles from mothers in better food con- the relationship between progeny size and progeny ditions; van der Sman et al. 2009). fitness changes, the optimal size of progeny is also Because maternal food resources can ultimately expected to change as environmental conditions vary limit the energy available for allocation, variation in (Fox 2000, Walker et al. 2003). Examples provided by food availability can be an important factor influenc- Allen et al. (2008) for marine invertebrates suggest ing the amount of energy available for reproduction that harsh environmental conditions have a steeper (Du 2006). One coastal region where resources vary offspring size-fitness relationship than more benign between 2 neighboring locations is at the southern conditions. Hence, an evolutionary response would end of the North Island of New Zealand, first de - result in larger offspring sizes in adverse conditions scribed by Morton & Miller (1968), i.e. the semi- (e.g. highly competitive environments, high preda- enclosed and nutrient-rich Wellington Harbor vs. the tion pressure, or high wave exposure), whereas off- exposed and low productivity Wellington southern spring size would be less important in more favorable coast. Compared to the nearby southern coast, environments. Wellington Harbour has denser and more species- Spight (1976) suggested predation as a component rich intertidal communities with greater recruitment of environmental severity for early juvenile benthic rates of fish and invertebrates (Phillips & Hutchison invertebrates. Food limitation, especially in the be - 2008, Shima & Swearer 2009, Demello & Phillips ginning of benthic life, is also a critical factor that can 2011), higher standing stocks of phytoplankton and influence the growth and survival of juveniles (Gal- concentrations of particulates (Gardner 2000, Helson lardo et al. 2004b, Moran & Manahan 2004). For juve- et al. 2007), higher quality and faster growing larval nile intertidal organisms, however, vulnerability also reef fish (Shima & Swearer 2009, 2010, Swearer & includes other physical factors that do not occur in Shima 2010), and higher growth rates for several most terrestrial and freshwater habitats, such as species of whelks (N. Phillips unpubl. data). wave exposure, desiccation, and temperature fluctu- Here, we used sympatric direct-developing whelks ations, which often result in mortality and affect the with different reproductive strategies, using Comi- distributional limits of the species (Gosselin & Chia nella virgata (1 large hatchling per capsule) and 1995a,b, Helmuth et al. 2002). C. maculosa (multiple small hatchlings per capsule) Several studies of invertebrates with larval stages as models to examine how maternal environments have shown that larger sizes are often correlated influence the size and performance of juveniles. with better performance in terms of feeding rate, There were 2 major aims: (1) to examine variation in duration of planktonic period, settlement rate, hatchling size within and among different C. virgata growth rate, and survival (Phillips 2002, Marshall et and C. maculosa populations and (2) to determine al. 2003, Marshall & Keough 2004, 2009). In contrast, whether initial hatchling size mediates the per - for direct developers that lack a planktonic larval formance of juveniles when exposed to different stage, maternal provisioning to the embryos at the stressors (i.e. desiccation and starvation). We hypo - Carrasco et al.: Offspring size mediates performance of juvenile marine snails 75 thesized that (1) hatchlings from different maternal the rocks using a scalpel and then transported in sea- environments will perform differently, i.e. hatchlings water to the laboratory, where each of them was from productive maternal environments (i.e. Wel- placed in a 500 ml jar fitted with mesh sides (500 µm ling ton Harbour) will perform better than hatchlings mesh) that allowed for water flow. The jars were half from less productive maternal conditions (i.e. the submerged in a large shallow tank supplied with southern coast), and (2)
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