Highly advective upwelling systems along the western margins of continents are widely believed to transport larvae far offshore in surface currents resulting in larval wastage, limited recruitment, and increased population connectivity. However, suites of larval behaviors effectively mediate interspecific differences in the extent of cross-shelf migrations between nearshore adult habitats and offshore larval habitats. Interspecific differences in behavior determining whether larvae complete development in estuaries or migrate to the continental shelf are evident in large estuaries, but they sometimes may be disrupted by turbulent tidal flow or the absence of a low-salinity cue in shallow, low-flow estuaries, which are widespread in upwelling systems. Larvae of most species on the continental shelf complete development in the coastal boundary layer of reduced flow, whereas other species migrate to the mid- or outer shelf depending on how much time is spent in surface currents. These migrations are maintained across latitudinal differences in the strength and persistence of upwelling, in upwelling jets at headlands, over upwelling-relaxation cycles, and among years of varying upwelling intensity. Incorporating larval behaviors into numerical models demonstrates that larvae recruit closer to home and in higher numbers than when larvae disperse passively or remain in surface currents.
Eastern boundary upwelling systems have been studied intensively, because they are one of the most productive marine ecosystems producing ~20% of the fish catch from less than 1% of the global ocean [
Schematic block diagram of generalized circulation. Prevailing winds blow equatorward toward the south with brief periods of relaxation or reversal. Surface waters flow offshore in the Ekman layer, which is weak and a few meters deep nearshore and stronger and about 15 to 30 m deep offshore. Cold, deep waters flow onshore and upwell to the surface often forming a front with warmer surface waters. Nearshore, prevailing currents flow poleward, as indicated by the circle with a dot in middle. Offshore, currents flow equatorward near the surface, as indicated by the circle with a cross in middle, and poleward at depth. Cross-shelf and alongshore transport is regulated by the amount of time larvae spend near the surface and bottom in stratified currents.
Larval transport may be affected by differences in the strength of prevailing winds, which are highly dynamic in space and time. At lower latitudes, Ekman transport is greater generating a wider band of persistent upwelling, the thermocline is shallower, oxygen is lower, mixing by weather systems is less, and river discharge is greater [
Larvae of nearshore species in upwelling systems must avoid being swept downstream and offshore to replenish adult populations, and behaviors regulating transport could be overwhelmed by strong upwelling conditions [
Despite the important implications for the ecology and evolution and conservation and management of species in upwelling regimes, these hypotheses have been difficult to test for mobile species, such as fishes, which have received the most attention due to their commercial importance. However, insights have come from studying more tractable sedentary intertidal and shallow-water benthic species. Because adults are fairly fixed along a narrow ribbon of shoreline, the starting and ending points of the planktonic phase of the life cycle are more restricted than for species inhabiting dynamic currents. Surveys of cross-shore distributions of progressively later larval stages indicate the extent of offshore transport. Surveys of the vertical distributions of progressively later larval stages over diel and tidal cycles coupled with concurrent profiles of current velocity and water column structure indicate how vertical swimming behavior may mediate cross-shore distributions. Complementary approaches, such as numerical oceanographic models, are needed to determine alongshore transport because larvae could have originated from many locations along the coast.
I review evidence for the behavioral regulation of larval transport of nearshore and estuarine benthic species in upwelling systems. I begin by summarizing generalized larval behaviors that are known to mediate transport in diverse systems. I then briefly review similarities and differences in the characteristics of the three upwelling systems where larval surveys of nearshore benthic species have been conducted: CCS, HCS, and ICS. With this background, I briefly characterize circulation in each upwelling system before reviewing the evidence for the behavioral mediation of larval transport by nearshore benthic species. I focus on evidence from the horizontal and vertical distributions of larvae in the water column rather than inferences drawn from the extensive literature on larval settlement onshore, which is beyond the scope of this review. Next, I synthesize this evidence to characterize shared physical and behavioral processes mediating larval transport across upwelling systems. I conclude by highlighting future directions for investigating larval transport in upwelling systems in an era of climate change.
The extent of larval transport is largely determined by the vertical distributions of larvae in flow [
Depth regulation by larvae mediating cross-shore transport: depth preferences and vertical migrations. Larvae of some species prefer to occur in surface waters, and larvae of other species prefer to occur in bottom waters. Larvae also may undertake three types of vertical migrations: ontogenetic (descend late in development), diel (ascend at night and descend during the daytime), and tidal (descend during ebb tide and ascend during flood tide). Larvae of other species undertake reverse vertical migrations in the opposite directions.
Behaviorally mediated cross-shore migrations by larvae (L) of estuarine and coastal species from adult populations (A; subscripts represent different species). Larvae of some estuarine species may complete development in the estuary while other species migrate to the inner, mid-, or outer shelf (or open ocean). Larvae of intertidal and shallow-water coastal species may complete development on the inner shelf or migrate either to the mid- or outer shelf (or beyond).
The California Current can be ~1000 km wide flowing from the North Pacific Current off Washington, USA (~20°N to ~50°N), to the subtropical waters off Baja California, Mexico (~15°N to ~25°N), where it turns westward as the North Equatorial Current (Figure
Satellite images of sea surface temperature during the peak upwelling season in three upwelling regions: California (CCS), Humboldt (HCS), and Iberia Current Systems (ICS). Images are for 1 month during the peak upwelling season and were obtained from the National Oceanic and Atmospheric Admistration Coastwatch website (
A review of the spawning “strategies” of fishes provides keen insights into the potential losses of eggs and larvae from advection across three regions of the CCS [
This review helped set the stage for benthic ecologists to focus on the importance of upwelling in regulating populations for the next several decades by monitoring spatial and temporal variation in larval settlement of nearshore species [
Upwelling also affects alongshore transport of larvae raising the fundamental question of how populations persist in prevailing equatorward flow. Shanks and Eckert [
Coastal topography generates mesoscale variation in circulation, thereby affecting larval transport and recruitment. Urchin recruitment is consistently less at four headlands (Cape Blanco, Cape Mendocino, Point Arena, and Point Reyes) than elsewhere along the coast suggesting that many larvae are swept offshore by jets [
Retentive recruitment hotspots also occur in the lee of small headlands [
The variation in coastline topography and bathymetry generates fronts, which concentrate phytoplankton and invertebrate larvae, at scales of approximately 50 m across the CCS during the upwelling season [
At a smaller scale, coves may form retentive hotspots during the peak upwelling season [
It is now clear that offshore transport of larvae is not the cause of the well-documented latitudinal gradients in larval recruitment across the CCS. Characteristic circulation of upwelling regions enables invertebrate larvae to limit cross-shelf and alongshore transport by regulating their depth in stratified flow (offshore transport near the surface and onshore return flow at depth) to maintain their position over the continental shelf, as first shown for copepods [
Suites of behaviors maintain the interspecific differences of crustacean larvae in the vertically stratified, opposing flows over the shelf (Figure
Representative horizontal and vertical distributions of larvae of nearshore benthic crustaceans during the daytime off Bodega Bay, northern California. (a) Barnacle larvae (
Similar cross-shelf distributions of the same species of crustacean larvae occur elsewhere in the CCS, indicating that behavior may effectively mediate transport across different upwelling regimes. In the intermittent upwelling regime off the coast of Oregon, interspecific differences in cross-shelf distributions of benthic crustaceans are similar to those off northern California: the highest densities of larvae occur within 5 km of the coast and larvae are rare beyond 18 km [
In the comparatively weak upwelling in the southern California Bight, barnacle larvae (
The interspecific differences in cross-shelf distributions do not appreciably shift in response to variability in upwelling intensity. Larvae are not swept farther offshore during upwelling than during relaxation conditions in either the persistent upwelling regime off northern California [
Although interspecific differences in cross-shelf distributions do not appear to change appreciably in response to upwelling intensity, alongshore distributions do. European green crabs (
Evidence for the behavioral regulation of cross-shelf distributions of fish larvae during the peak upwelling season is limited, but consistent cross-shelf structure in larval fish assemblages occurs. Larvae of sculpins, lingcod, and flatfishes with short larval durations occur on the inner shelf (<28 km from shore) and larvae of rockfishes, myctophids, and flatfishes with very long larval durations occur on the outer shelf [
Transport was shown to be inherently unpredictable due to the chaotic nature of coastal circulation, especially eddy dynamics, by using numerical particle tracking models of passive larval dispersal during one year of idealized circulation [
A three-dimensional ROMS model coupled with particle tracking for Monterey Bay showed that simulated zooplankton remaining below the surface throughout the day had high levels of self-recruitment even in this advective region [
In a second study for Monterey Bay, larval dispersal by the barnacle,
Several studies have been conducted using ROMS models to investigate the effect of the depth of larval release or subsequent depth preferences on larval dispersal and connectivity. Kim and Barth [
Petersen et al. [
Drake et al. [
To examine the effect of larval behavior on transport and connectivity, Drake et al. [
Numerical model of larval dispersion and connectivity for larvae (
Larvae regulate depth effectively in San Francisco Bay, California, which is the largest estuary on the west coast of the USA [
Larvae also regulate depth effectively in San Diego Bay, California, and Willipa Bay, Washington, where RTVM occurs in several species [
Interspecific differences in cross-shore distributions occur in low-flow estuaries along the West Coast even though larval behaviors can be disrupted by turbulent tidal flows or the lack of a low-salinity cue. In Bodega Harbor, barnacle and pinnotherid larvae complete development in nearshore coastal waters by either remaining below the shallow Ekman layer throughout development (barnacles) or rising to the surface at night after winds have subsided (pinnotherids) [
The Humboldt Current can be ~1000 km wide flowing from southern Chile (~45°S) to northern Peru (~4°S; Figure
Depth regulation by larvae determines transport in the HCS with the same or congeneric species showing the same larval transport patterns as in the CCS. RDVM was found to play a role in nearshore larval retention by conducting complementary larval surveys at different spatial and temporal scales on the central coast of Chile [
A brief study on the assemblage of decapod larvae in the Gulf of Arauco during the upwelling season indicates that interspecific differences in vertical distribution in two-layer flow facilitate nearshore retention or offshore export [
The distribution and abundance of decapod larvae were surveyed at six stations along each of 11 transects across the continental shelf (35 to 37°S) during the upwelling and downwelling seasons [
Larvae of the squat lobster (
In a follow-up study of larval dispersal and connectivity along the coast of central Chile, Aiken et al. [
The Portugal Current flows equatorward along the Iberian Peninsula (Figure
Behaviorally mediated larval transport has been well studied off the coast of the Iberian Peninsula. Barnacles and some species of decapods complete development on the inner shelf, whereas green crabs and other species of decapods migrate farther onto the shelf [
Numerical modeling studies of the Iberian Shelf indicate that DVM contributes to retaining green crab larvae on the shelf and establishing population connectivity [
Both larvae and postlarvae of green crabs effectively regulate depth in small estuaries. Newly hatched larvae undertake RTVM upon hatching during spring tides, thereby expediting transport onto the shelf, whereas the nocturnal TVM by postlarvae expedites transport up the estuary [
Sole (
The long-standing view that larvae are transported offshore in upwelling conditions has become entrenched even though it was based on the results of a single larval survey coupled with settlement studies and its intuitive appeal [
Subsequent larval surveys have demonstrated that larval behavior effectively regulates cross-shelf transport in upwelling regimes as it does elsewhere in the world. Similar interspecific differences in the extent of cross-shelf transport have been documented for many species across the CCS, including the strong persistent upwelling regime off northern California, the intermittent upwelling regime off Oregon, and the weaker upwelling regime off southern California. Furthermore, interspecific distances of cross-shelf transport have been maintained off northern California and Oregon over the years despite interannual differences in the intensity of upwelling. Moreover, larvae do not appear to be advected farther offshore by the upwelling jet from major headlands. Interspecific differences in the extent of cross-shelf transport also are evident in both persistent and intermittent upwelling regimes in the ICS and HCS. Although cross-shelf larval surveys of nearshore benthic species have yet to be conducted in the Benguela Current System, it is highly likely that consistent interspecific differences in cross-shelf larval transport will be found there too.
Passive larval advection and diffusion alone cannot account for the interspecific differences in cross-shelf distributions. Behavior must be important in mediating these migrations, because larvae of different species and different stages of the same species migrate in opposite directions at the same time. Concentrations offshore are dramatically lower than those onshore right after hatching, even when corrected for vertical mixing into the higher volume of a deepening water column. Further, larval concentrations of later larval stages of some taxa remain similar or increase on the middle and outer shelf rather than diminishing offshore (Figure
Copepods and larvae of nearshore benthic species share the same basic behaviors (depth preference, OVM, and DVM) for regulating cross-shelf transport. Reverse vertical migrations (ROVM, RDVM) and additional combinations of behaviors mediating transport have been identified for larvae regulating transport of nearshore benthic species (Figure
Models exploring larval transport and connectivity usually assume passive dispersal or dispersal in surface currents. These models have provided valuable insights into the role of stochasticity in larval transport as well as a first order approximation of potential dispersal and connectivity. However, neither passive dispersal nor simple dispersal in surface currents adequately characterizes larval dispersal in upwelling regions. The recent inclusion of selected behaviors into models for the CCS and ICS is now showing that larval behavior greatly reduces the alongshore and cross-shore extent of dispersal resulting in more realistic estimates of dispersal and connectivity matrices.
The same interspecific differences in larval behavior mediating larval retention and export in estuaries occur in both the CCS and ICS. However, larval behaviors are best defined in larger, stratified estuaries in the CCS and in small estuaries in the ICS where low-salinity may cue larvae to regulate depth. The lack of a low-salinity signal or turbulent mixing in shallow, low-flow estuaries in the CCS appears to disrupt depth regulation by larvae. In these low-flow estuaries, RTVM facilitating seaward transport requires migration to the bottom boundary layer (next to the seabed) to be effective, and TVM facilitating larval retention has not been detected. Therefore, larval retention in low-inflow estuaries may occur primarily at the head of estuaries, where tidal exchange is weak and longer retention times are observed [
Considerable progress has been made in understanding the behavioral mediation of larval transport, recruitment, and connectivity in upwelling systems. However, there are number of areas that would benefit from more attention, and I briefly highlight seven of them below.
The author declares that there is no conflict of interests regarding the publication of this paper.
The author thanks of all his co-authors working on larval transport in the CCS over the years for their contributions to the development of the research summarized here (see cited references). This research was funded by the National Science Foundation (Biological Oceanography OCE-0326110) and California Sea Grant (R/FISH-2018) and is a contribution of the Bodega Marine Laboratory.