The potential effects of pre-settlement processes on post-settlement growth and survival of juvenile northern rock sole (Lepidopsetta polyxystra) in Gulf of Alaska nursery habitats
Graphical abstract
Introduction
Marine fish species such as flatfish have a complex life cycle with discrete pelagic larval and benthic juvenile stages. Settlement to the benthos following metamorphosis in flatfish exposes individuals to a novel habitat and a distinct suite of predators. Predation is considered the primary source of mortality in nursery grounds and individuals that grow slowly and settle at small sizes are often the most vulnerable to growth- and size-selective predation (Ellis and Gibson, 1996, Nash and Geffen, 2000, Joh et al., 2013). These observations indicate that nursery conditions promoting fast growth and large body size are especially important in maximizing survival during post-settlement life stages. Growth in nursery grounds is influenced by density-dependent processes and environmental factors, including temperature and prey availability (Gibson, 1994, Sogard et al., 2001, Ciotti et al., 2013).
Flatfishes are considered particularly vulnerable to density-dependent effects on growth because large concentrations of recently settled juveniles present in nurseries can often result in increased competition (van der Veer, 1986, Bergman et al., 1988). Studies on several flatfish species have observed significant negative effects of high abundance on growth rates and post-settlement size (Steele and Edwards, 1970, Modin and Pihl, 1994, Nash et al., 1994). However, in other cases evidence for density-dependent processes in flatfish nurseries is limited, suggesting that environmental factors play a larger role in explaining growth variation. The “maximum growth/optimal food condition” hypothesis predicts that if there is no competition for food then temperature will be the primary driver of growth (Karakiri et al., 1991, van der Veer and Witte, 1993). Although the relative importance of food versus temperature on flatfish growth dynamics remains poorly understood, a large number of studies have documented positive correlations between post-settlement growth and temperature (e.g. Zijlstra et al., 1982, May and Jenkins, 1992, Teal et al., 2008).
Increasing attention has been paid to the relationships and interdependency of early life history stages with the recognition that conditions experienced during the larval stage may have lasting effects on the characteristics of post-settlement juveniles. Life history stages are linked through the processes of “carry-over effects” and selection. For example, environmentally-induced body size variation within and between cohorts tends to persist independent of subsequent growth rate variation (O'Connor et al., 2014). Because predation on juvenile fishes is generally inversely related to size (Ellis and Gibson, 1996, Sogard, 1997), size advantages gained during the larval stage can influence performance and survival in post-settlement periods (Searcy and Sponaugle, 2001, Vigliola and Meekan, 2002, Smith and Shima, 2011). These relationships are complicated by potential changes in magnitude and direction of selective pressures with ontogeny (Gagliano et al., 2007a, Johnson and Hixon, 2010). Correspondingly, while selection operates on phenotypes expressed in the juvenile stage, the covariation in traits across life history stages can effectively act as selection on traits expressed in the larval stage. Ultimately, a better understanding of individual growth histories and patterns of co-variation in early life history characteristics is necessary to provide insight into trait-mediated survival of individuals as well as population-level ramifications of selection (McCormick, 1998).
Recent research directed toward understanding the effects of nursery habitat factors and potential carry-over effects on post-settlement growth and survival has focused on reef species (e.g. Shima and Findlay, 2002, McCormick and Hoey, 2004, Smith and Shima, 2011). Early life history processes of many North Pacific species, however, are not well understood despite their economic importance. Northern rock sole (Lepidopsetta polyxystra) is a flatfish species of high commercial value in the Gulf of Alaska and Bering Sea. In mid-winter to early spring, adult northern rock sole (NRS) spawn demersal eggs in nearshore bays (Stark and Somerton, 2002). Pelagic larvae metamorphose and settle in shallow nursery grounds in May and June (Norcross et al., 1995, Laurel et al., 2015). While research on the early life history stages of NRS has focused primarily on the post-settlement nursery period (Moles and Norcross, 1998, Hurst and Abookire, 2006, Ryer and Hurst, 2008, Ryer et al., 2012), larval growth exhibits significant interannual variation (Fedewa et al., 2016). Hurst et al. (2010) demonstrated that temperatures in the late-larval period explained >80% of the variation in post-settlement size of NRS and contributed to variation that persisted throughout the first growing season. Furthermore, post-settlement growth was more variable across years than across nursery sites and not related to NRS densities in the nurseries. These observations highlight the need to identify larval traits that may be carried over to post-settlement stages to influence growth and survival.
Consequently, we quantified spatial and temporal variation in post-settlement growth of NRS in relation to water temperature and juvenile NRS densities in two nursery sites in the Gulf of Alaska using otolith structural analysis. Pre- and post-settlement traits of NRS individuals were also examined to determine if relative patterns of covariation in size and growth were maintained across life stages. In addition, we determined if there was evidence for selection related to timing of metamorphosis, growth or size in the nursery grounds between July and August during the early post-settlement period. Reconstructing and integrating pre- and post-settlement growth histories of “settlers” (July-captured fish) and “survivors” (August-captured fish) enabled the comparison of traits between the two months to determine if pre-settlement growth and size patterns were preserved during juvenile residence in nurseries. We therefore hypothesized that NRS that are larger at hatch, grow faster as larvae, and are larger at metamorphosis will display faster growth and experience greater survival during the early post-settlement period.
Section snippets
Fish collection and site characterization
Age-0 NRS were collected off the northeast coast of Kodiak Island, Alaska, USA, at two nurseries: Holiday Beach (57°41.2′ N, 152°27.7′ W) in Middle Bay and Pillar Creek Cove (57°49′ N, 152°25′ W) in Monashka Bay (Fig. 1). Sampling for post-settlement NRS has been conducted annually since 2004 by the Fisheries Behavioral Ecology Program of the Alaska Fisheries Science Center (AFSC) (Hurst and Abookire, 2006, Laurel et al., 2015). Sampling was conducted using a 2-m beam trawl with a 3-mm mesh
Environmental variation in nursery sites
Seasonal patterns in Trident Basin nursery temperatures were characterized by minimum temperatures in February and March with an increase in mid-April and a maximum in late-July. Interannual variation in post-settlement temperatures was characterized by higher temperatures in 2005 which were at least 1.5 °C warmer than average temperatures in all other study years (Fig. 3, one-way ANOVA, F4,360 = 4.28, p < 0.01) as well as all 17 years in the Trident Bay temperature record. 2007 was the coldest
Discussion
Variation in growth and development during the larval stage can carry over to subsequent post-settlement stages, potentially influencing future growth and survival (Shima and Findlay, 2002, McCormick and Hoey, 2004). To the best of our knowledge, this study is the first to integrate pre- and post-settlement processes of a North Pacific flatfish in relation to growth and survival during the early post-settlement period. Overall, post-metamorphic and August recent growth of NRS were positively
Acknowledgments
We thank the staff of AFSC's Fisheries Behavioral Ecology Program for access to archival field collections of northern rock sole as well as Ashley Silver and Thomas Murphy for assistance with otolith removal and preparation. This manuscript benefitted greatly from valuable comments and insight from Janet Duffy-Anderson, Su Sponaugle, and two anonymous reviewers. Field sampling was supported by AFSC's Habitat and Ecological Processes Research Program and the North Pacific Research Board. EJF was
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