Larval quality is shaped by matrix effects: implications for connectivity in a marine metapopulation

Abstract

Variation in the phenotype or "quality" of dispersing individuals can shape colonization success and thus local dynamics and patterns of connectivity in a metapopulation. In marine reef systems, larval dispersal typically connects fragmented populations, and larval quality may be shaped by developmental history at the natal reef (e.g., parental effects) and/or by conditions in the pelagic environment (e.g., food, temperature, hydrodynamics, predator regime). We extract information recorded within the incremental bands of fish "ear stones" (otoliths) to reconstruct the early life histories of reef fish, to evaluate whether larval quality is a function of natal populations, dispersal histories, or both. We sampled sagittal otoliths from 282 common triplefins (Forsterygion lapillum) collected at approximately weekly, intervals between December 2003 and March 2004, from three sites within Wellington Harbor (New Zealand) and three sites along the adjacent Wellington South Coast. We used image analysis to quantify otolith traits and to reconstruct five larval phenotypes (pelagic larval duration, size-at-hatch, early larval growth, late larval growth, and an instantaneous larval growth rate), followed by a principal components analysis to derive a composite measure of larval quality. We used laser ablation-inductively coupled plasma-mass spectrometry to quantify otolith microchemistry, followed by a set of cluster analyses (based upon 13 statistical descriptors of time series for each of 11 elemental ratios) to identify and characterize two putative natal "source populations" and two putative "larval dispersal histories." We evaluated the relationship between larval quality, source populations, and dispersal histories using two-way ANOVA and MANOVA, and determined that larval quality of F. lapillum is a function of larval dispersal history and not source population identity. Specifically, larvae of F. lapillum with microchemical signatures consistent with retention and/or entrainment in the nutrient-enriched Wellington Harbor had traits associated with elevated larval quality (i.e., short pelagic larval durations, small size-at-hatch, fast larval growth, and fast instantaneous growth rates). Our results suggest that conditions in the pelagic larval environment shape larval quality and potentially mediate metapopulation connectivity. In the case of F. lapillum from Wellington Harbor, environmentally induced heterogeneity in larval quality may limit connectivity by favoring successful replenishment by locally retained larvae over long-distance dispersers.

Regional variation in larval retention and dispersal drives recruitment patterns in a temperate reef fish

“…Females spawn benthic egg clutches that are cared for by territorial males for 2 wk until hatching (Thompson 1979, Francis 2001. Larvae develop in the pelagic environment for ~50 d (Shima & Swearer 2009a) before settling to fronds of macroalgae (McDermott & Shima 2006).…”

“…To reconstruct larval dispersal history and source population identity, sagittal otoliths from a subsample of 321 fish (a random sample of up to 10 recruits per site per collection date) were cleaned, mounted, and polished to within 20 µm of the core following the methods of Patterson & Swearer (2007), Barbee & Swearer (2007), and Shima & Swearer (2009a Pb (0.0357) in recruit otoliths was performed on a Varian inductively-coupled plasma mass spectrometer (ICP-MS) fitted with a HelEx (Laurin Technic and the Australian National University) laser ablation (LA) system constructed around a Compex 110 (Lamda Physik) excimer laser operating at 193 nm (see Eggins et al 1998 for a description of the LA system and Barbee & Swearer 2007 for details of LA-ICP-MS methods).…”

“…For both the source population and dispersal history analyses, the time series were truncated to only include analyses of pre-hatch and pre-settlement otolith material, respectively (see Shima & Swearer 2009a for details).…”

Local retention, dispersal and fluctuating connectivity among populations of a coral reef fish

“…This metric is much harder to estimate as it requires information about larval exchange among a network of populations. Few studies have tracked larval dispersal among populations (Miller and Shanks 2004;Becker et al 2007;Planes et al 2009;Shima and Swearer 2009); fewer still have empirically estimated temporal variation in dispersal (Miller and Shanks 2004); and none have empirically investigated the degree of temporal stability in connectivity among a network of populations.…”

Chlorophyll-a and the Supply Side Ecology: Lessons from the Rocky Shores

“…Larval responses to the variability in phytoplankton abundance and diversity are species-speciic. Larval itness is inluenced by environmental conditions experienced by adults and larvae [10,11]. The efects of phytoplankton on larval dynamics depend on the phase of larval development [12][13][14][15] and may be stronger when variations in phytoplankton occur on temporal scales that larvae or breeding adults are able to respond [16].…”