Field test of the behavioral regulation of larval transport

Abstract

The maintenance of marine populations depends on the completion of larval migrations between adult and larval habitats, but the ability of microscopic larvae to regulate their movements in such a dynamic environment has been debated. Using a comparative hypothesis testing approach and intensive hourly sampling throughout the water column, we determined the ability of larvae of 6 species with different swimming abilities (2 gastropods, 2 crabs, 2 fishes) to overcome strong tidal mixing during spring tides and regulate their vertical, and hence, horizontal position, in opposing depth-stratified currents in the upper Hudson River estuary, USA. The vertical distributions of nonmotile eggs and swimming larvae generally differed, suggesting that larvae regulated depth. Eggs were passively mixed by tidal currents, but larvae typically aggregated in stratified portions of the water column, which fostered retention in the upper estuary. However, the capacity to regulate depth depended on swimming ability and the degree of mixing. In a predominantly mixed tidal environment upstream, mixing overcame most larvae when current velocities were maximal during mid-ebb or mid-flood tides; tidal vertical migrations were not evident for any species, and diel vertical migrations were apparent for only 1 species. In a partially stratified water column downstream, diel vertical migrations were apparent for larvae of 3 of 4 invertebrate species, and tidal vertical migrations were apparent for the 2 fish species. The presence of all larval stages showed that all species regulated depth sufficiently well to remain in the upper estuary. Regardless of swimming ability, larvae were retained in the estuary by occurring near the level of no net motion, even without completing tidal vertical migrations. Continuous profiling of larvae and hydrodynamics is necessary to reveal the ability of larvae to regulate depth in tidal mixing and recruit to adult populations.

Transport of Crustacean Larvae Between a Low-Inflow Estuary and Coastal Waters

“…The absence of lowsalinity water is typical in low-inflow estuaries from late spring to fall along the West Coast, and the effects of turbulence and the lack of a low-salinity cue on larval depth regulation should be examined. If turbulent mixing is important in disrupting vertical migrations, then (1) weakly swimming ciliated larvae, such as mollusks and echinoderms, should be even less able to regulate depth effectively while stronger swimming fish larvae should be better able to do so (Kunze et al 2013) and (2) larvae should be better able to regulate depth in deeper well-mixed estuaries. If freshwater inflow and lower salinity is important, then tidal vertical migrations should occur in estuaries with substantial freshwater inflow, but not in low-flow estuaries when larvae are abundant, regardless of estuary depth.…”

“…Specifically, we determined the effectiveness of larval behavior by benthic crustaceans in regulating larval transport between a low-inflow estuary and coastal waters. We hypothesize that previously documented larval behaviors in adjacent coastal waters may not be evident in the estuary due to tidal vertical mixing and turbulence in shallow water (Breckenridge and Bollens 2011;Kunze et al 2013) or the lack of low salinity or pronounced salinity fluctuations to cue tidal vertical migrations (Miller and Morgan 2013a). Thus, we concurrently looked for vertical migrations in adjacent nearshore waters where salinity fluctuations are similar, but tidal flows and the strength of vertical mixing are weaker.…”

“…The timing of vertical swimming may be controlled by endogenous clocks with free-running periods that approximate tidal and diel cycles, thereby enabling larvae and postlarvae to anticipate and reliably time vertical migrations (Forward and Tankersley 2001;Kingsford et al 2002;Gibson 2003;Morgan and Anastasia 2008;López-Duarte et al 2011). Thus, larvae of some species are retained in estuaries despite net seaward flow by migrating vertically between residual currents that generally flow seaward near the surface and landward near the bottom or by remaining at mid-depth near the level of no net motion; whereas larvae of other species leave estuaries by rising into outflowing surface currents and return later in development in inflowing bottom currents (reviewed by Forward and Tankersley 2001;Queiroga and Blanton 2005;Morgan 2006; Kunze et al 2013;Miller and Morgan 2013a). Once on the open coast, larvae of some species complete larval development close to shore while larvae of other species are transported across the continental shelf (reviewed by Morgan 1995aMorgan , 2006Epifanio and Garvine 2001;Queiroga and Blanton 2005).…”

Tidal shifts in the vertical distribution of bivalve larvae: Vertical advection vs. active behavior

“…Numerous field studies have identified vertical shifts in larval distribution that coincide with tidal (Carriker 1951(Carriker , 1961Kunkle 1957;Wood and Hargis 1971;Booth 1972;Maru et al 1973;Andrews 1983;Gregg 2002;Baker and Mann 2003;Knights et al 2006;Kunze et al 2013;Peteiro and Shanks 2015) and diel (Quayle 1952;Maru et al 1973;Tremblay and Sinclair 1990a;Raby et al 1994; cycles. Such distribution shifts occur in taxa with both strongly (e.g., crustaceans ;Queiroga 1998;Forward and Tankersley 2001) and weakly (e.g., mollusks, echinoderms, bryozoans, and sponges; Young and Chia 1987;Kingsford et al 2002) swimming larvae, as well as in holoplankton (Southward and Barrett 1983;Harding et al 1986;Scrope-Howe and Jones 1986).…”

The influence of discharge, current speed, and development on the downstream dispersal of larval nase (Chondrostoma nasus) in the River Danube

“…Reef fish larvae, for example, orientate towards odours and sounds of their natal reef and use directional currents to get there (Paris and Cowen 2004;Leis et al 2011;Paris et al 2013). Observations of larvae moving along hydraulic gradients (Stoll and Beeck 2012), adapting swimming and drifting speeds to the prevailing flow regime (Hogan and Mora 2005) or regulating depth distribution according to currents (Kunze et al 2013), further emphasize an active response to the hydrodynamic environment. The interactive effects of temporally unstable hydrodynamics and ontogenetically variable larval behaviour are increasingly being used in oceanic dispersal models to gain more realistic simulation results (Vikebo et al 2011;Sponaugle et al 2012;Nolasco et al 2013).…”