Larval Transport and Dispersal in the Coastal Ocean and Consequences for Population Connectivity

M a r i n e P o p u l at i o n C o nn e c t i v i t y

larval Transport and Dispersal in the Coastal Ocean and Consequences for Population Connectivity

By Jesús Pi n e d a , J o n at h a n A . H a r e , a nd S u s P o n a u g l e

M a n y m a r i n e s p e c i e s have small, pelagic early life stages. For those species, knowledge of population connectivity requires understanding the origin and trajectories of dispersing eggs and larvae among subpopulations. Researchers have used various terms to describe the movement of eggs and larvae in the marine environment, including larval dispersal, dispersion, drift, export, retention, and larval transport. Though these terms are intuitive and relevant for understanding the spatial dynamics of populations, some may be nonoperational (i.e., not measur- able), and the variety of descriptors and approaches used makes studies difficult to compare. Furthermore, the assumptions that underlie some of these concepts are rarely identified and tested. Here, we describe two phenomenologi- cally relevant concepts, larval transport and larval dispersal. These concepts have corresponding operational definitions, are relevant to understanding population connectivity, and have a long history in the literature, although they are sometimes confused and used interchangeably. After defining and discussing larval transport and dispersal, we consider the relative importance of planktonic processes to the overall understanding and measurement of population connectivity. The ideas considered in this contribution are applicable to most benthic and pelagic species that undergo transforma- tions among life stages. In this review, however, we focus on coastal and nearshore benthic invertebrates and fishes.

22 Oceanography Vol. 20, No. 3 Larval transport is defined as the hori- a certain distance, herein referred to invasive species, and other phenomena zontal translocation of a larva between as dispersal distance. Larval transport (Cowen et al., 2006, this issue; Levin, points x1,y1 and x2,y2, where x and y are is an important component of larval 2006). By this definition, if the exchange horizontal axes, say, perpendicular and dispersal, and broad dispersal requires is measured at the time of settlement, parallel to the coastline. In larval trans- significant larval transport. Restricted connectivity is essentially larval dispersal port, only the spatial dimensions mat- dispersal, however, does not imply little from one population to another (e.g., ter. Although this definition ignores larval transport (Figure 1). Further, pro- Webster et al., 2002). Not all settlers will the vertical axis (z) for simplicity, this cesses and factors associated with the survive, however, and survival may be dimension is critical for larval transport end of larval transport (i.e., settlement) influenced by larval experience. Thus, because larvae can modify their hori- also influence dispersal, including settle- connectivity is frequently measured at zontal distribution by swimming verti- ment behavior, distribution of suitable some point after settlement, once set- cally, thereby encountering different settlement sites, and refuge availability tlers survive to enter, or recruit to, the currents (Nelson, 1912; Crisp, 1976). To (Figure 2). Similarly, because spawning juvenile population. Functionally, how- transfer from point x1,y1 to point x2,y2, a initiates larval dispersal, spawning time ever, this point is somewhat arbitrary larva can swim horizontally and may be and location are important, as are factors and differs among taxa. A more precise transported by diffusive and advective influencing spawning, including season demographic milestone is reproduction. processes (Scheltema, 1986). Defined as and synchronicity of spawning, age and If settlers die without reproducing, dis- the translocation of a larva between two condition of spawners, and fertiliza- persal is of questionable importance to points, larval transport appears decep- tion success. In addition to the spatial population growth or spread of invasive tively simple. However, the wide range dimensions inherent in larval transport, species. In this contribution we differen- of larval behaviors and physical mecha- larval dispersal involves a survival prob- tiate between population connectivity, nisms, together with their variability at ability, and thus food availability and measured at the time of settlement, and multiple scales, makes larval transport predation are important. The highest reproductive population connectivity, exceedingly difficult to measure. The mortality in marine populations occurs defined as the dispersal of individu- temporal and spatial scales of variability are enormous (Scheltema, 1986), even when considering a single physical transport mechanism (see Box 1). the fundamental challenge in population In contrast, larval dispersal refers to connectivity studies is to determine the the spread of larvae from a spawning source populations of settling larvae and source to a settlement site. This definition is consistent with the terrestrial lit- the settlement sites of dispersing larvae. erature (natal dispersal in Clobert et al., 2001; Begon et al., 2006) that describes seed dispersal as the probability den- during the early life stages, so mortal- als among subpopulations that survive sity function of the number of seeds ity plays a large, but understudied, to reproduce. Reproductive population versus distance from the adult source role in larval dispersal. connectivity encompasses larval dis- (i.e., the dispersal kernel) (Nathan and Population connectivity has been persal but is also influenced by post- Muller-Landau, 2000; see Gerrodette, defined as the exchange of individuals settlement mortality (e.g., Hunt and 1981, for a rare marine example). Using among geographically separated subpop- Scheibling, 1997; Doherty et al., 2004), the dispersal kernel, dispersal can be ulations (see Cowen et al., this issue) and growth, and condition from settlement viewed as a probability that a released is thought to be a key process for popu- to successful reproduction. By the defini- zygote will make it to settlement over lation replenishment, genetics, spread of tion above, although dispersal of larvae

Oceanography September 2007 23 that do not survive to reproduce can play (e.g., Roughgarden et al., 1988; Siegel et this and similar observations, combined a role in population and community al., 2003). An increasing number of stud- with recent modeling and genetic studies ecology, their contributions to reproduc- ies, however, conclude that a significant (Cowen et al., 2000; Gerlach et al., 2007) tive population connectivity are minimal amount of self-recruitment occurs in (Figures 1 and 2). marine populations (Jones et al., 2005; Jesús Pineda ([email protected]) is Almany et al., 2007). These conclusions Associate Scientist, Department of Biology, Larval transport are not in and of themselves surprising: Woods Hole Oceanographic Institution, Reconsideration of the a population is defined as a self-sustain- Woods Hole, MA, USA. Jonathan Scales of Larval Transport ing component of a species, and thus A. Hare is Research Marine Scientist, The term larval transport brings to self-recruitment is a defining attribute National Oceanic and Atmospheric mind small, passive larvae being moved of a population (Sinclair, 1988). What is Administration, National Marine Fisheries throughout the ocean by meso- and surprising is the relatively small spatial Service, Northeast Fisheries Service Center, large-scale physical processes (Johnson, scales over which self-recruitment has Narragansett Laboratory, Narragansett, 1939). This view has become a para- been observed. For example, despite a RI, USA. Su Sponaugle is Associate digm—larvae are released, trans- planktonic stage of 9–12 days, approxi- Professor, Marine Biology and Fisheries ported by mesoscale processes, mixed mately 30% of settling panda clown- Division, Rosenstiel School of Marine and in a larval pool, and then randomly fish self-recruited to an area of 0.5 km2 Atmospheric Science, University of Miami, recruited to juvenile or adult habitat (Jones et al., 2005). The implication of Miami, FL, USA.

BOX 1. Variability in Spatial and Temporal Scales of Larval Transport

The movement of larvae in internal bores is an example of the variety of Robertson, 1985). Thus, temporal scales relevant for understanding lar- spatial and temporal scales involved in larval transport. Larval accumula- val transport by internal tidal bores range from seconds to years. Other tion at surface-propagating convergences is critical for effective transport temporal scales important to internal tidal bore larval transport that are in internal bore warm fronts, and the time scales of these convergences not depicted here include fortnightly periodicity (~ 14.4 days), and the are from a few seconds to a few hours. On the other hand, water-col- periodicity of coastally trapped waves (a few weeks; Pineda and López, umn stratification, a seasonal phenomenon, modulates the energy of 2002). In the literature, larval transport generally encompasses horizontal internal bores and therefore also impacts larval transport (Pineda and distances ranging from tens to hundreds of kilometers, a usage we follow López, 2002). At even larger scales, stratification and internal bores are in this contribution. modulated by El Niño, an interannual phenomenon (Zimmerman and

24 Oceanography Vol. 20, No. 3 and the constrained nearshore larval dis- flows mainly because of the shoreline topographic guide for coastally trapped tributions of littoral species (Barnett and barrier, shallow depths, bathymetric waves and tends to steer flows in the Jahn, 1987; Tapia and Pineda, 2007), is features associated with the continental alongshore direction (see Box 2). Tidal that the spatial scales of larval transport shelf, and nearshore inputs of fresh- ellipses that tend to be isomorphic in may be much smaller than previously water.1 Moreover, flows in nearshore the open ocean become compressed recognized. These results indicate that waters tend to be more complex than near the coast, and large-scale flows such small-scale and nearshore physical pro- in the deep and coastal ocean because as the Gulf Stream and the Humboldt cesses play an important role in larval many processes operate there, includ- Current flow parallel to the shoreline, transport (Kingsford, 1990; Willis and ing surface gravity waves, buoyancy- not perpendicular. Freshwater runoff Oliver, 1990; Pineda, 1999). driven flows, wind-forcing, surface and and large-scale currents running paral- internal tides, large-amplitude internal lel to the coastline produce characteristic Nearshore, Coastal, and waves and bores, and boundary-layer stratification in the nearshore, such as Oceanic Currents effects. These differences between near- shallowing of the thermocline near the Flows in nearshore, shallow environ- shore and coastal/open ocean hydrody- coastline in response to the California ments, including the surf zone, are dif- namics are important for larval trans- Current (Hickey, 1979) and the Florida ferent from coastal and deep-ocean port. The shoreline barrier serves as a Current/Gulf Stream (Leaman et al.,

1In this contribution we use the term nearshore to describe (a) the shallow waters where surface and bottom Ekman layers interact, the nearshore of Mitchum and Clarke (1986), and the inner shelf of Lentz (1995), and (b) the surfzone, while the coastal region includes mid- and outer-shelf areas.

Accumulation in internal tidal bore warm fronts (seconds to hours)

Seasonal stratiﬁcation (months)

El Niño (several years)

Oceanography September 2007 25 larval transport x2,y2 ,t2 mocline. A shallow thermocline creates larval dispersal site vertically sheared environments that may g reproductive population restrict larval transport for species with x ,y ,t 1 1 1 connectivity diel vertical migration; thus, interan-

spawnin x ,y ,t nual variability in the strength of these 3 3 3 x ,y ,t x ,y ,t m 4 4 4 4 4 5 large-scale current systems might lead to fro variability in dispersal, an untested spec-

dispersal distance

e ulation. Consider the effects of coastal x0,y0 ,t0 upwelling, El Niño, and coastally trapped Distanc waves on shallow water stratification spawning Time after spawning settlement reproduction and cross-shore transport along the west coasts of North and South America. The Figure 1. Relationship between the spatial and temporal components of larval transport, lar- combination of strong coastal upwelling val dispersal, and reproductive population connectivity for a sessile species. Survivorship is not depicted. Note that the sum of larval transport distances can be larger than the dispersal dis- and El Niño produces weak nearshore tance. White circles are locations in space with coordinates x-y at times t. All locations are pelagic stratification due to the upwelling of except x ,y and x and y , which are benthic. Distance could also be represented in two dimen- o 0 4 4 unstratified cold waters and the piling sions (e.g., x,y as cross- and alongshore axes.) up of mixed surface warm waters in the nearshore (Simpson, 1984; Zimmerman and Robertson, 1985). Both upwelling 1989). Salinity (Thièbaut et al., 1992) from the shoreline (e.g., Lentz et al., and El Niño result in decreased water- and water-column stratification (Pineda 1999; Largier, 2003). column stratification, suppressing the and López, 2002) contribute to larval shallowing of the thermocline by the transport because sharper stratification Modulation of Nearshore internal tide and the internal tidal bores, in shallow waters (e.g., Hickey, 1979) Cross-Shore Transport by which, in turn, may result in decreased allows larvae of coastal species to exploit Large-Scale Processes onshore larval transport (recent work vertically sheared flow to control hori- Clearly meso- and large-scale processes of author Pineda and Manuel López, zontal distributions (Paris and Cowen, affect larval transport, and most stud- Centro de Investigación Cientifica y de 2004), and internal motions such as ies emphasize these effects. Large-scale Educación Superior de Ensenada). In internal tidal bores may transport larvae physical processes also influence the contrast, coastally trapped waves pro- onshore. Surface waves that break near smaller-scale processes discussed above. duce a transient, small drop in sea level the shore produce some mass transport, Many large-scale circulation systems that is compensated by a large uplift- and storm systems that originate in the and processes, such as eastern and west- ing of the nearshore thermocline. This deep ocean sometimes move onshore. ern boundary currents, El Niño, coastal results in the shallowing of the ther- Flows in the nearshore are broken by upwelling, and coastally trapped waves, mocline by the internal tide and larval coastline topographic features such as are energetic and coherent in the along- transport by internal bore warm fronts bays and capes, resulting in complex shore direction, but can also modulate (Pineda and López, 2002). flows with smaller spatial coherence smaller-scale processes in ways that (see discussion in Okubo, 1994). This is enhance or suppress larval transport. Small-Scale Processes and true for cross-shore coastal flows, whose For example, as pointed out above, the Event-Type Larval Transport coherence scales are much smaller than strength of the California Current deter- Spatial and temporal scales are linked the alongshore coastal flows (Brink, mines the depth of the thermocline in in the ocean (Stommel, 1963), so the 1999). The relative importance of these shallow nearshore waters, with a stron- importance of small-spatial-scale pro- processes varies with depth and distance ger current resulting in a shallow ther- cesses underscores the significance of

26 Oceanography Vol. 20, No. 3 small-temporal-scale processes to larval Larval transport = ƒ(physical transport, larval behavior) transport. Moreover, meso- and large- scale processes can exhibit small-tem- Advection, diﬀusion poral-scale variability (Stommel, 1963) and be episodic (e.g., hurricanes). Larval settlement from the plankton for many

marine organisms is episodic, and it is Larval behavior not uncommon to have the majority of a season’s settlement occur in a handful of days (Forward et al., 2004; Sponaugle Dispersal = ƒ(larval transport, survival, spawning and settlement) et al., 2005). Even though settlement records imply transport events and are often correlated with various physical factors, the observation of event- driven larval transport remains elusive. Similarly, larval distributions are often used to infer transport and the influence of events (e.g., the occurrence of Connectivity = ƒ(larval dispersal, post-larval survival) an eddy; Limouzy-Paris et al., 1997), but few studies have measured the movement of larvae in the water over time by event-type processes. When larval distributions are sampled repeatedly over time, they offer excellent views of the processes involved in larval transport (Pepin and Helbig, 1997; Natunewicz Figure 2. The concepts of larval transport, larval dispersal, and reproductive popu- and Epifanio, 2001), but due to sampling lation connectivity. Colors of arrows distinguish each concept. For example, the limitations, such studies are rarely able green arrow in the connectivity box means dispersal is involved in reproductive population connectivity. to observe the influence of smaller-scale processes. Examining the effect of events on transport is more straightforward in a modeling context—a well-mod- Behavior and Larval Transport cept that vertical swimming behavior, eled example is the effect of wind- As our appreciation of small-scale physi- changes in buoyancy, and ontogenetic driven events on settlement (Garvine cal processes grows, so does our appre- changes in vertical position influence et al., 1997; Brown et al., 2004)—but ciation for the role of larval behavior in the horizontal movement of larvae; this most circulation models do not cap- influencing larval transport. For many view was adopted early in estuarine and ture smaller-scale physical processes, years, larvae were considered planktonic, coastal lagoon systems (Nelson, 1912; frontogenesis, frontal convergence and that is, moving at the whim of ocean Pritchard, 1953; Bousfield, 1955) and divergence, intrusions, internal waves, currents but using feeding and preda- later in shelf and open-ocean systems and topographic effects, particularly tor avoidance behaviors that resulted in (Kelly et al., 1982; Cowen et al., 1993). in the nearshore. small-scale (millimeters to centimeters) Additionally, the influence of larval set- movements (Blaxter, 1969). The view tlement behavior on the specific location of passive larvae gave way to the con- of settlement, at scales of meters to tens

Oceanography September 2007 27 of meters, was recognized as important sound, smell, and possibly magnetism, mechanisms involved in larval transport, (e.g., Crisp, 1976; Raimondi, 1991). electric fields, and wave swell (e.g., and ignorance of other potential trans- More recent research shows that Kingsford et al., 2002; Gerlach et al., port mechanisms (see Cowen, 2002, for a larvae also have horizontal swimming 2007). Clearly, larvae are complex and review). Physical mechanisms that could capabilities that improve with develop- capable organisms that develop the abil- affect transport include surface grav- ment (see review by Leis, 2006). For ity to feed, avoid predation, and move ity waves (Monismith and Fong, 2004), example, larvae of a damselfish swam within the pelagic environment. Thus, in submeso- and mesoscale eddies (Bassin continuously for 39 hours without food, the equation of larval transport, behav- et al., 2005; Sponaugle et al., 2005), baro- covering a distance equivalent to 19 km ior plays an equally important role as tropic tidal currents (Hare et al., 2005; (Stobutzki, 1997). Similarly, larval lob- advection and diffusion. Queiroga et al., 2006), and cross-shore sters and early pelagic stages of cepha- winds (Tapia et al., 2004). lopods are good swimmers (Villanueva Larval Transport: Some proposed mechanisms have not et al., 1996; Jeffs and Holland, 2000). Research Needs been tested rigorously in field condi- In combination with the capability to Identification of Nearshore Larval tions. Moreover, the logistical difficulty swim vertically and horizontally, larvae Transport Mechanisms of studying transport sometimes can of both invertebrates and vertebrates Knowledge of larval transport in near- push researchers to use weak inferen- can orient and potentially navigate shore environments is very limited. tial approaches, such as inferring larval over short (meter-to-kilometer) to long Major drawbacks include lack of rigor- transport mechanisms from settlement (10-to-100-km) distances, using light, ous knowledge of the suspected physical data (Pineda, 2000; Queiroga et al.,

BOX 2. Along- and Cross-Shore Physical Transport Processes

Larval transport in nearshore and shelf species is often split into cross- as Atlantic menhaden (Quinlan et al., 1999), larvae must move onshore and alongshore components (e.g., Hare et al., 1999; Ma and Grassle, to recruit to juvenile habitats. Although cross-shelf transport is often 2005). This distinction follows a convention in coastal physical oceanog- emphasized in studies of larval transport, it is obvious that alongshore raphy and is convenient because cross- and alongshore hydrodynamic processes also play a role (Hare et al., 1999), particularly in population processes have different temporal and spatial scales (Winant, 1983), connectivity. Nearshore and coastal marine populations are generally different physical processes dominate cross- and alongshore transport arrayed along coasts, and the alongshore movement of lar- (e.g., Winant and Bratkovich, 1981), and momentum balances in these vae between these populations can keep these two axes are accounted for by different terms (e.g., Lentz et al., 1999). geographically isolated populations Also, plankton patches have widely different dimensions in the two axes connected. (Mullin, 1993). Because the strongest gradients in water properties and ecological variables are in the cross-shore dimension, transport on this axis has a disproportionately large effect on the distribution of larvae. For nearshore species whose later developmental stages move pro- gressively offshore with time, such as the southern California barnacle nauplii (Tapia and Pineda, 2007), cross-shore transport is the most critical process, as older larvae tend to be farther away from the shore and must return nearshore to settle and reproduce. Similarly, for species that move offshore to spawn but have nearshore settlement habitats, such

28 Oceanography Vol. 20, No. 3 2006). The lure of mesoscale processes in larger-scale models, thereby capturing detail. Furthermore, surveys by research and satellite oceanography has proved the large-scale aspects of larval trans- vessels diligently planned in advance irresistible for some shallow-water port, the modulation of small-scale pro- do not guarantee that larval-transport ecologists, resulting in an overempha- cesses by large-scale forcing, and the very events will happen during the surveys. sis on explanations based on mesoscale small-scale processes (e.g., turbulence) Adaptive sampling, defined as sampling processes while disregarding nearshore where larval swimming capabilities in response to an event, is a solution to processes and mechanisms that cannot and behavior become overly important these dilemmas; it has been used suc- be studied remotely. Unambiguous iden- (see discussion in Metaxas, 2001). Even cessfully to sample hydrodynamics and tification of the mechanisms of larval modeling a single, relatively straight- larval distributions during transport transport is rare, and testing alternative forward process, such as the accumula- by internal tidal bores (Pineda, 1994, explanations is almost unheard of. Thus, tion of particles in gravity currents, can 1999). Adaptive sampling is challenging, there is a serious need to follow up some be extremely complex (e.g., Scotti and however, because it is hypothesis based; of these weakly founded hypotheses with Pineda, 2007). Thus, using numerical sampling is initiated in response to a rigorous tests. With limited knowledge models for inferring larval transport real-time change in a time-dependent of nearshore larval transport, it seems when poorly studied processes may be variable, such as temperature or wind that assessing the relative contributions important, or where the physical forcing direction, that is integral to the hypoth- of various physical transport mecha- is unknown, is dire. On the other hand, it esized larval transport mechanism. nisms in larval transport for a given case is clear that numerical models are pow- Adaptive sampling is therefore a strin- study is, so far, only a utopian hope. The erful tools in settings where processes gent hypothesis test, because if larval field will be mature when such a study are well known and in cases where field transport does not occur as expected, the can be proposed and accomplished. hydrodynamics are well simulated by the hypothesis is rejected. Adaptive sampling Understanding the role of small-scale model (e.g., Reyns et al., 2006). Thus, we is also logistically difficult. If the events processes in larval transport is also lim- suggest that bottlenecks in understand- are sporadic, and the sampling is ship- ited by modeling capabilities. Large-scale ing larval transport are less related to board, adaptive sampling requires hav- and mesoscale models forced by winds numerical modeling than to the mecha- ing a vessel and crew on standby ready and the surface tide are now common- nistic knowledge of larval transport. to sample for long periods, an expen- place (see Werner et al., this issue). The sive prospect for anxious researchers. spatial resolution of these models is Challenges of Adaptive Sampling Conceivably, remote sampling systems increasing and extending into nearshore It is unclear how much larval transport initiated in response to events could be areas (e.g., Chen et al., 2006). Decreased occurs during episodic events and how constructed with off-the-shelf gear and grid size, however, is only one aspect of much occurs during “mean” condi- new technologies currently under devel- resolving smaller-scale processes. Small- tions. Sharp peaks in settlement time opment such as in situ molecular detec- scale processes, such as surface waves, series and studies of larval transport tion of larvae (e.g., Goffredi et al., 2006). internal waves, and propagating conver- by wind and internal motions suggest Thus, similar to the limitations in mod- gences, need to be included. Currently, that transport can be sporadic, larvae eling larval transport, adaptive sampling no numerical model appears capable extremely patchy, or both (see Pineda, is limited in part by technology and in of simultaneously resolving Lagrangian 2000, for discussion). Time-series mea- part by the development of testable, transport caused by, for example, shal- surements of relevant hydrodynamics mechanistic hypotheses. lowing internal tides, sea breeze, large- and larval distributions during larval amplitude internal waves, and sur- transport are of limited use when mea- Breaking the Behavioral Black Box face gravity waves. Further, accurately surements cannot be taken with the nec- The incorporation of larval behavior modeling larval transport will require essary frequency and spatial resolution fully into the larval transport equation embedding these small-scale processes to describe the processes with sufficient requires several important advances.

Oceanography September 2007 29 First, hypotheses on the role of behavior the trade-offs between feeding and pre- Third, most research has focused on in transport need to be developed and dation; these rules result in vertical (and how larval behavior affects advection, tested. Colby (1988) argued that passive potentially horizontal) responses to vari- but the influence of behavior on diffu- advection and diffusion should be the null ous cues (Titelman and Fiksen, 2004; sion requires more emphasis. Using an hypothesis for studies of larval transport. Fiksen et al., in press). Although the advection-diffusion-mortality model, In an early example of this approach, importance of time-dependent behav- Cowen et al. (2000) estimate that suc- Woods and Hargis (1971) compared iors, such as diel, tidal, and ontogenetic, cessful larval transport to coral reef habi- the distribution of coal particles with is well recognized, little is known about tats diminishes sharply when diffusion that of similarly sized oyster larvae and “adaptive” behavior on scales of seconds rates increase from 0 to 100 m2 s-1 (the concluded that larvae were not being to minutes, where larvae might respond latter is a typical diffusion rate used in transported passively. A study on ascid- to transient physical and biological larval transport studies; see also Okubo, ian tadpole larvae found that dispersal features. We know that larvae respond 1994). However, the assumption that distance was shorter in swimming lar- behaviorally to a number of factors, such larvae diffuse passively in the marine vae than in nonswimming individuals as time of day, light, temperature, tur- environment likely does not hold, par- of similar size and shape (Bingham and bulence, pressure, and food availability, ticularly for older larval stages. Peaks Young, 1991). Similarly, Arnold et al. and that some of these responses influ- in settlement must result from high- (2005) followed a cohort of larval hard ence transport, but only a few behaviors density patches of larvae reaching adult clams and found their distribution dif- facilitating transport have been identi- habitats, and these coherent patches fered from dye distributions and from fied (e.g., Boehlert and Mundy, 1988; run counter to hypothesized diffusion. modeled distributions based on passive DiBacco et al., 2001). For example, field Natunewicz and Epifanio (2001) fol- particles. There are other examples of observations, modeling, and labora- lowed discrete patches of crab larvae the use of a hypothesis-testing approach tory experiments imply that “swimming for up to six days and hypothesized that for evaluating the processes that affect up” behaviors in response to transient associative swimming behaviors might larval transport (e.g., Hare et al., 2002). downwelling flows in propagating fea- be responsible for patch maintenance. This approach should be expanded to tures determine efficient larval transport A U-shaped patchiness-at-age function take advantage of advances in modeling (Pineda, 1999; Scotti and Pineda, 2007). has been described for the larval stages as well as in field and laboratory studies. To incorporate our understanding of of several fish species, and this shape has Behavioral hypotheses from laboratory behavior into rule-based models will been interpreted as initial diffusion with studies are attractive because quantifica- require a hypothesis-based approach. subsequent schooling (Matsuura and tion of hydrodynamics and behavior is Without hypotheses, we run the risk of Hewitt, 1995). In addition, larvae may feasible, but these hypotheses should be evaluating the effect of multiple irrel- remain in thin layers of food (Lasker, tested in field conditions, and vice versa. evant behavioral scenarios on larval 1975) and reduce their diffusion owing Second, the incorporation of behav- transport. This rule-based approach to vertical differences in flow (shear dif- iors into models of transport needs to be coupled with more studies on adaptive fusion). Larvae can also accumulate at rule-based rather than deterministic, and behavior and well-developed biophysi- upwelling and downwelling fronts by individual variability should be consid- cal, individual-based models (e.g., Lough swimming into the current (e.g., Franks, ered. Most transport models that include et al., 2005, and recent observations of 1992; Metaxas, 2001), thereby reducing larval behavior use population-level Claudio DiBacco of Bedford Institute diffusion. Thus, small-scale vertical and descriptions of distributions or swim- of Oceanography, author Pineda, and horizontal larval behavioral responses ming speeds and apply them to particles Karl Helfrich of WHOI), will greatly may limit diffusion and greatly affect released in the model (Hare et al., 1999). advance our understanding of the com- larval transport. Consequently, the use Another approach is to provide a set of bined roles of advection, diffusion, of advection-diffusion models to under- behavioral rules that attempt to capture and larval behavior. stand larval transport requires great

30 Oceanography Vol. 20, No. 3 care. For example, Hill (1991) under- ing behaviors have long been thought to 10–15 km of known habitat have suc- scored the limitations of an advection- maximize larval survival (e.g., Hughes et cessfully settled (Hare et al., 1999; Paris diffusion-mortality model in cases when al., 2000), the overall effect of localized et al., 2005). How larvae transverse these active vertical positioning of larvae was and punctuated spawning on larval dis- last 10 km is unknown largely because of expected, and Okubo (1994) warned that persal is unclear. the exclusion of smaller-scale processes a horizontal diffusive model would not Moreover, where individuals end their in models and the inability to include work in settings with strong convergent planktonic stage is also an important realistic behaviors (see above). flows, a widespread phenomenon in coastal and nearshore settings.

Larval Dispersal ...all the research needs identified under Defining Dispersal Kernels the larval transport and dispersal sections Most attempts to describe dispersal ker- sum together as research needs for nels have emphasized larval transport (e.g., Botsford et al., 1994), but other population connectivity. processes such as spawning, settlement, pelagic larval duration, and survival also influence larval dispersal (Edwards et al., component of larval dispersal. Larval The dispersal kernel also is dependent in press). Many marine species release durations of some species are fixed on larval mortality. Most studies of larval their offspring at specific locations and while others are flexible (Pechenik, 1986; dispersal, however, either do not con- times, using specific behaviors. For Cowen, 1991). Some species have very sider larval mortality (Hare et al., 1999), example, relatively sedentary bluehead narrow habitat requirements for the con- consider spatially homogenous mortal- wrasse spawn daily at particular reef tinuation of the life cycle, such as river ity (Cowen et al., 2000), or assume low spawning sites that have been used for mouths on isolated oceanic islands for mortality (Gaylord and Gaines, 2000). years (Warner, 1988). Similarly, several some gobies, wave-beaten rocky points Modeling studies that assume low mor- fish species spawn in circular motions for gooseneck barnacles, and specific talities should be reconsidered in light that may create hydrodynamic vortexes species of anemones for some reef fish of observed higher mortalities (e.g., (Okubo, 1988; Heyman et al., 2005). The (Radtke et al., 1988; Cruz, 2000; Jones Rumrill, 1990); use of high mortalities influence of these small-scale events on et al., 2005). Other species have broad in dispersal models frequently yields larval dispersal over periods of weeks is habitat requirements such as eurytopic lower maximum dispersal estimates than unknown. On a larger scale, a number of Pachygrapsus crabs (Hiatt, 1948) and those obtained assuming low mortality motile species, including snappers, her- flounders of the genus Etropus (Walsh et (Cowen et al., 2000; Ellien et al., 2004; ring, and blue crabs, move to particular al., 2006). For most species, only a subset Tapia and Pineda, 2007). Differential locations for spawning (Carr et al., 2004; of locations will support the continu- survival of larvae during transport con- Heyman et al., 2005). In the temporal ation of the life cycle; these locations tributes to defining the dispersal kernel domain, many coral species participate must be reached within the time window in potentially numerous species-specific in annual mass spawning events, with of possible settlement. Understanding ways. The ecological literature is rich more than 60% of species spawning over these habitat and time constraints will with examples and models in which the the course of several days (Babcock et be necessary to observe and model dis- role of spatial heterogeneity in mortal- al., 1994), and crabs and barnacles tend persal kernels. A number of models have ity shapes subsequent patterns in abun- to release their larvae at certain phases included such considerations at a rela- dance, distribution, and demographics. of the tide or the day (Morgan, 1995; tively large scale, for example, assum- These concepts, however, have yet to be Macho et al., 2005). While such spawning modeled larvae that arrive within applied to mortality in pelagic early life

Oceanography September 2007 31 stages. It is also clear that not all larvae else is equal (i.e., same daily mortality the dispersal of planula larvae from are equal, and the range of traits will for species with short and long PLD; see adults in a temperate solitary coral and result in selective survival (see later sec- Hare and Cowen, 1997). It is also unclear found that mean dispersal distance from tion on Population Connectivity). how variables influencing PLD, such as the parent was < 50 cm. Similar work Larval duration also influences sur- temperature and food (Scheltema and with ascidians quantified dispersal from vival probability. Pelagic larval dura- Williams, 1982), may influence the dis- spawning to settlement, but the pelagic tion (PLD) must be correlated with the persal kernel (see O’Connor et al., 2007, stage of ascidians is short (hours), larvae dispersal kernel for the simple reason for model predictions). Thus, the rela- are large (millimeters), and mortality is that species with short PLD must have tionship between PLD and dispersal is low (< 90%) (Olson and McPherson, reduced larval transport and relatively ambiguous except for species with very 1987), making it possible to follow indi- “short” dispersal kernels; PLD is a short larval durations (see discussion in viduals from the beginning to the end of constraining variable for dispersal. In Sponaugle et al., 2002). the pelagic stage (see also Bingham and contrast, long PLDs do not necessarily Young, 1991). Work on an isolated reef yield broad dispersal kernels, as larval Dispersal Estimates in the indicated that most acroporid and pocil- behavior breaks the direct-proportional Coastal Ocean loporid corals recruited in experimental relationship between PLD and dispersal Given the complexity of larval dispersal, moorings within 300 m from the reef, distance, both for fish and invertebrates it is not surprising that measurement of and that spat mortality decreased with (Sponaugle et al., 2002). Of course, long a dispersal kernel in the marine environ- distance from the reef (Sammarco and PLD yields higher cumulative mortali- ment is extraordinarily rare (Shanks et Andrews, 1989). Several studies followed ties than short PLD when everything al., 2003). Gerrodette (1981) measured patches of more typical marine larvae

Eventually, long-term, labor-intensive studies will be needed to increase our understanding of reproductive population connectivity of longer-lived mobile species.

32 Oceanography Vol. 20, No. 3 (PLD of weeks, size < 1–10 mm, and Larval behavior was not as important, persal models in locations where physical high mortality), but these efforts are not but horizontal swimming behavior was processes are well known. true measures of larval dispersal because not included and depth-stratified cur- When empirical estimates of disper- the spawning and ending locations rents were minimal through most of the sal are obtained, it is crucial that they be were inferred (Pepin and Helbig, 1997; modeling domain, limiting the effect of used to test the assumptions and hypoth- Natunewicz and Epifanio, 2001; Paris different vertical positions. eses resulting from both simple and and Cowen, 2004). Other studies marked complex models. Robust measurements spawned eggs and then collected off- Larval Dispersal: of dispersal will be rare and opportuni- spring at the end of their planktonic stage Research Needs ties to evaluate and test models must not (Jones et al., 2005; Almany et al., 2007); Field Observations of Dispersal be lost. In this way, the skill of models these studies provide a partial measure, The paradigm of broad dispersal of can be assessed and improved through but not a complete description, of the fish and invertebrate larvae is giving an iterative process of observation and dispersal kernel because all potential way to the notion of restricted disper- modeling, and the resulting dispersal ending locations could not be sampled. sal, mainly because of studies find- kernels can be part of larger studies of Although dispersal kernels will eventually ing: (1) unexpected high levels of self- connectivity with increasing confidence. be fully quantified for some species in recruitment, (2) high larval mortality Although the challenges are immense, we some systems, the measurement of these rates, and (3) restricted scales of larval emphasize that solid empirical estimates probability distributions in the marine transport (see above). Still, the domi- of dispersal are necessary to guide fur- environment will remain extremely rare. nant scales of dispersal are not known. ther field studies and numerical model- It is easier to obtain dispersal kernels Solid empirical estimates of dispersal ing; theoretical developments and mod- with models than with field measure- are needed to guide field and numeri- eling of spatial population processes and ments. Some models consider simpli- cal modeling studies to address ques- connectivity may be futile unless we gain fied situations using advection-diffusion tions such as: What regions of the ocean more observationally based knowledge models. More complex numerical circu- should researchers focus on? What pro- of larval dispersal. lation models coupled with Lagrangian cesses must be included in the models? particle-tracking algorithms follow Studying dispersal is challenging, and for Population Connectivity particles released at multiple locations fish and invertebrate species with long The Concept of Population and multiple times and have proven and typical larval durations (i.e., about Connectivity instrumental in estimating dispersal ker- four weeks for temperate invertebrates; A mechanistic understanding of larval nels in the marine environment (Cowen Levin and Bridges, 1995), knowledge will dispersal is sufficient for determining et al., 2000; see also Werner et al., this be gained incrementally by using mul- population connectivity at time of settle- issue). Edwards et al. (in press) used a tiple approaches, including: (1) empirical ment. Knowledge of population con- fully orthogonal approach to examine estimates of larval origin, such as natu- nectivity at the time of settlement or the effects of different factors on generic ral and artificial tags and genetic dis- shortly thereafter may be adequate for two-dimensional dispersal kernels esti- tance and structure, (2) a mechanistic some objectives because subadult indi- mated from a three-dimensional circu- understanding of larval transport, viduals use resources, interact with adults lation model of the Southeast United (3) assessment of how the space and time and other members of the community States shelf. This study found that time of spawning and settlement influence and in some instances, sustain fisher- and place of initial release were most dispersal, (4) trophodynamic studies to ies. Reproductive population connectiv- important in determining the position of address the influence of pelagic patchi- ity, on the other hand, is the exchange of the dispersal kernel, and that dispersion ness and structure on the larval jour- individuals that eventually reproduce. and PLD were most critical in determin- ney from spawning to settlement, and Accordingly, for benthic marine species, ing the spread of the dispersal kernel. (5) improved mortality estimates in dis- it is not only a function of larval dispersal

Oceanography September 2007 33 (including survivorship of larvae during Variation in Larval Traits and mortality hypotheses” (reviewed in transit), but also of post-settlement and Survival During the Pelagic Stage Anderson, 1988). Theoretically, survivors juvenile survival to the point of repro- Most larvae exhibit variation in early should be those larvae that are larger at a duction (Figures 1 and 2). Reproductive life history (ELH) traits, such as size at given age (“bigger is better” hypothesis; population connectivity can be expressed a given age and growth rate. This varia- Miller et al., 1988), grow faster (“growth- as the number of individuals from site a tion can be introduced as early as the egg rate” hypothesis; Bailey and Houde, and population A that disperse to site b stage, when differential size, age, condi- 1989), and/or move through an early containing population B and reproduce tion, or stress level of the mother can stage more rapidly (“stage-duration” there per unit time. Thus, during devel- influence quality of the spawned eggs hypothesis; Anderson, 1988). Larvae of opment to the adult stage (which var- (Berkeley et al., 2004; McCormick, 2006). a diversity of marine fish (e.g., Meekan ies greatly among species, from days to Larval encounter with variable pelagic and Fortier, 1996; Hare and Cowen, multiple years), juveniles must survive, environments also influences larval 1997; Meekan et al., 2006) appear to grow, mature, and reproduce. As charac- growth and survival. Water temperature adhere (to varying degrees) to aspects of teristics of settlers are often variable and plays a central role in regulating metabo- these overarching concepts. Differential those surviving to reproduce may not be lism and growth (Houde, 1989), with survival of larvae due to their pelagic a random sample of the settlers, simply larvae in different temperatures exhibit- experience and ELH traits can influ- tracking larval trajectories from spawning variable ELH traits (Meekan et al., ence the magnitude of larval settlement ing to settlement is insufficient to quan- 2003; Sponaugle et al., 2006). Sustained pulses. Variation in the magnitude of tify reproductive population connectivity. growth requires adequate food; there- settlement events has been related to The remainder of this discussion consid- fore, variable access to food also affects variable larval growth throughout or ers the ecological processes contributing larval traits and survival. Transit across during particular periods of larval life to reproductive population connectivity. nutrient-poor open oceans may be par- (e.g., Bergenius et al., 2002; Jenkins and For a population to be ecologically ticularly difficult for species with high King, 2006; Sponaugle et al., 2006) sustained, a minimum number of off- growth rates. Access to food and avoid- spring must mature and reproduce over ance of predation or other develop- Influence of Larval Traits on time intervals dictated by species’ longev- mental conditions may be related to the Juvenile Survival ity. Identifying this number is essential timing of spawning, such that particular Settlement of larvae to the benthos is to parameterize population models, but “windows” of time result in higher larval a risky event plagued with high levels an equally important consideration is the survivorship (Cushing, 1990; Baumann of predation mortality (e.g., Hunt and composition of the survivors that make et al., 2006). Encounter with oceano- Scheibling, 1997; Doherty et al., 2004); up this number: What are the character- graphic features such as fronts or meso- thus, additional selective loss typically istics of dispersers that lead to successful scale eddies can also influence food sup- occurs during this period. Most marine recruitment? Which of those recruits will ply and exposure to predators (Grimes species undergo a metamorphosis then survive to reproduce? Recent evi- and Kingsford, 1996; Sponaugle and between the larval and juvenile stages as dence points to important influences of Pinkard, 2004). Thus, a complex oceano- they move between radically different spawning patterns, maternal effects, and graphic environment coupled with environments. While metamorphosis pelagic experience on larval size, growth, variable egg quality at spawning results enables closer adaptation to stage-spe- condition, and survival. Furthermore, in a pool of larvae with variable traits cific environments (Wilbur, 1980), larval many of these larval traits “carry over” (Jarrett, 2003; Lee et al., 2006; Sponaugle history is not erased and accompanies and influence juvenile survival. However, and Grorud-Colvert, 2006). this transition (Pechenik et al., 1998). comparatively little is known about the Survival of pelagic larvae is typically Importantly, recent studies have begun linkages between these early life phenom- nonrandom and proceeds according to linking these two stages and investigating ena and adult survival and reproduction. three general concepts of the “growth- how larval traits influence juvenile sur-

34 Oceanography Vol. 20, No. 3 vival. Traits exhibited by settling larvae first few days or weeks as juveniles. We ships likely influence the outcome. When as a consequence of pelagic constraints know little about the settlers that eventu- carryover effects occur, they may persist, and selective pressures have the potential ally survive to reproduce. It is generally become amplified, or, instead, be com- to “carry over” and influence survival of substantially more time-consuming and pensated for during subsequent stages juveniles. For example, larval growth, logistically challenging to track cohorts (Podolsky and Moran, 2006). In short, size, and condition influence the survi- of settlers all the way to reproduction. A simply reaching a settlement site does vorship of juvenile sponges, molluscs, few recent studies have had some success not guarantee that larvae will possess the barnacles, bryozoans, and fishes (e.g., following species that mature rapidly. necessary traits to survive to reproduce. Searcy and Sponaugle, 2001; Pechenik et al., 2002; Jarrett, 2003; McCormick and Hoey, 2004; Phillips, 2004; Marshall et al., 2006; Sponaugle and Grorud-Colvert, …simply reaching a settlement site does 2006). The potential exists for some not guarantee that larvae will possess the traits that are advantageous to larvae to become subsequently detrimental to necessary traits to survive to reproduce. juveniles or vice versa. For example, crab zoeae reared at reduced salinities suffer higher mortality as larvae, but metamor- Pineda et al. (2006) sampled barnacles Population Connectivity: phose into larger juveniles (Giménez and that settled over an 89-day period until Research Needs Anger, 2003), and a short pelagic larval they reproduced 11 months later and The fundamental challenge in popula- duration enables fish larvae to escape the found that survivors settled during a tion connectivity studies is to determine predation in the plankton, but results narrow 21-day “recruitment window.” the source populations of settling larvae in smaller settlers (e.g., Sponaugle et al. Meekan et al. (2006) tracked a single and the settlement sites of dispersing lar- 2006), which in some cases may be more cohort of a fast-growing coastal fish and vae. In short, all the research needs iden- susceptible to predation (Anderson, found that despite strong selective loss tified under the larval transport and dis- 1988). Most studies have focused on con- during early stages, there was no addi- persal sections sum together as research sequences to juveniles and somewhat less tional selective mortality between the needs for population connectivity. In on the trade offs associated with conflict- juvenile and adult stages. For bryozoans addition, there is a need to link maternal ing constraints in complex life histories. in an experimental manipulation, how- effects and larval processes to early juve- ever, adults that were larger as larvae nile survival and, in the case of repro- Survivorship Beyond the had higher survival rates and produced ductive population connectivity, to the Juvenile Stage larger larvae themselves than those that point of reproduction. Because repro- Although events during larval life can were smaller as larvae, although delaying ductive population connectivity per se play an important role in early juve- metamorphosis erased this relationship is defined as the exchange of individuals nile survival, much less is known about (Marshall and Keough, 2006). Optimal that eventually reproduce, tracking dis- how these traits are carried through or traits may vary with the environment persing larvae to the point of settlement lost from individuals that survive to encountered by the larval, juvenile, or or juvenile recruitment, while important reproduce. Studies on larval dispersal or adult stages, as evident for a snail (Moran for some purposes, is functionally insuf- population connectivity typically define and Emlet, 2001) and colonial ascid- ficient. New efforts to track settlers to recruitment as entry into the juvenile ian (Marshall et al., 2006). Thus, traits reproduction will initially advance with population, not to the adult popula- obtained during early stages have the shorter-lived sessile species. Eventually, tion. Thus, settlers are tracked at most to potential for long-term effects on later long-term, labor-intensive studies will the point of settlement or through the stages, but many complex interrelation- be needed to increase our understanding

Oceanography September 2007 35 of reproductive population connectivity if settlers that survive to reproduction Bailey, K.M., and E.D. Houde. 1989. Predation on eggs and larvae of marine fishes and the recruitment of longer-lived mobile species. There is are only spawned at time t and site x,y, problem. Advances in Marine Biology 25:1–83. a rich history of marine ecological work or if successful individuals only settle Barnett, A.M., and A.E. Jahn. 1987. Pattern and per- sistence of a nearshore planktonic ecosystem off examining the relative importance of in recruitment windows coinciding Southern California. Continental Shelf Research recruitment versus density-dependent, with physical-transport processes p and 7:1–25. post-settlement processes in structuring feeding and prey environments e, the Bassin, C.J., L. Washburn, M. Brzezinski, and E. McPhee-Shaw. 2005. Sub-mesoscale coastal eddies benthic populations (Caley et al., 1996), vast parameter space that potentially observed by high frequency radar: A new mecha- but we need to move beyond numeri- affects pelagic eggs and larvae, and vexes nism for delivering nutrients to kelp forests in the Southern California Bight. Geophysical Research Letters 32 (L12604):doi:10.1029/2005GL023017. Baumann, H., H.H. Hinrichsen, R. Voss, D. Stepputtis, W. Grygiel, L.W. Clausen, and A. Temming. 2006. Real measures of reproductive population Linking growth to environmental histories in central Baltic young-of-the-year sprat, Sprattus sprat- connectivity require an understanding of tus: An approach based on otolith microstructure analysis and hydrodynamic modelling. Fisheries who is surviving to reproduce and why. Oceanography 15(6):465–476. Begon, M., J.L. Harper, and C.R. Townsend. 2006. Ecology. From individuals to ecosystems, 4th ed. Blackwell Publishing, Malden, MA, 738 pp. Bergenius, M.A.J., M.G. Meekan, D.R. Robertson, and cal responses and refine the question to researchers, may be effectively reduced to M.I. McCormick. 2002. Larval growth predicts the recruitment success of a coral reef fish.Oecologia focus on trait-based ecological linkages a more manageable set. 131(4):521–525. among all stages. Real measures of repro- Berkeley, S.A., C. Chapman, and S.M. Sogard. 2004. Maternal age as a determinant of larval growth and ductive population connectivity require Acknowledgements survival in a marine fish. Sebastes melanops. Ecology an understanding of who is surviving to We thank the National Oceanic and 85(5):1,258–1,264. Bingham, B.L., and C.M. Young. 1991. Larval behavior reproduce and why. Atmospheric Administration, the of the ascidian Ecteinascidia turbinata Herdman: As there is ample evidence that larval National Science Foundation, and the An in situ experimental study of the effects of growth and condition can influence per- Woods Hole Oceanographic Institution swimming of dispersal. Journal of Experimental Marine Biology and Ecology 145:189–204. formance in later stages, from a practi- for supporting our work, and John Blaxter, J.H.S. 1969. Development: Eggs and larvae. cal point of view we need more reliable Manderson, David Mountain, Nathalie Pp. 177–252 in Fish Physiology, W.S. Hoar and D. J. Randall, eds, Academic Press, New York, NY. measures of condition. The coarsest Reyns, Vicke Starczak, Fabián Tapia, Boehlert, G.W., and B.C. Mundy. 1988. Roles of behav- measures of condition often use size as Simon Thorrold, and an anonymous ioral and physical factors in larval and juvenile fish recruitment to estuarine nursery areas. Pp. 51–67 a proxy (e.g., many invertebrates), while reviewer for constructive criticisms. in Transport of Larval Fish and Shellfish Through others measure organic (Jarrett, 2003) Coastal Inlets, M.P. Weinstein, ed., Transactions of or lipid content (Hentschel and Emlet, References the American Fisheries Society Symposium 3. Botsford, L.W., C.L. Moloney, A. Hastings, J.L. Largier, Almany, G.R., M.L. Berumen, S.R. Thorrold, S. Planes, 2000), RNA/DNA ratios (Suthers et al., T.M. Powell, K. Higgins, and J.F. Quinn. 1994. and G.F. Jones. 2007. Local replenishment of coral The influence of spatially and temporally vary- 1996; Lee et al., 2006), or (for fishes) reef fish populations in a Marine Reserve. Science ing oceanographic conditions on meroplanktonic 316:742–744. otolith-based measures (e.g., Sponaugle metapopulations. Deep-Sea Research II 41:107–145. et al., 2006), all of which have some limi- Anderson, J.T. 1988. A review of size dependent Bousfield, E.L. 1955. Ecological control of the occur- survival during pre-recruitment stages of fishes tations. As new genomic techniques are rence of barnacles in the Miramichi estuary. in relation to recruitment. Journal of Northwest National Museum of Canada Bulletin 137:1–69. developed, perhaps new measures of per- Atlantic Fishery Science 8:55–66. Brink, K.H. 1999. Observational coastal oceanog- Arnold, W.S., G.L. Hitchcock, M.E. Frischer, R. formance can be incorporated into both raphy. Pp. 137–158 in The Future of Physical Wanninkhof, and Y.P. Sheng. 2005. Dispersal of Oceanography: Report of the APROPOS Workshop. observational and manipulative studies. an introduced larval cohort in a coastal lagoon. UCAR/JOSS. Finally, focusing on the individu- Limnology and Oceanography 50:587–597. Brown, C.A., S.A. Holt, G.A. Jackson, D.A. Brooks, Babcock, R.C., B.L. Wills, and C.J. Simpson. 1994. and G.J. Holt. 2004. Simulating larval supply to als that survive to reproduce may guide Mass spawning of corals on a high latitude coral estuarine nursery areas: How important are physi- larval transport and dispersal studies; reef. Coral Reefs 13:161–169. cal processes to the supply of larvae to the Aransas

36 Oceanography Vol. 20, No. 3 Pass Inlet? Fisheries Oceanography 13(3):181–196. press. Using two-dimensional dispersal kernels to Ecology 78:2,415–2,431. Caley, M.J., M.H. Carr, M.A. Hixon, T.P. Hughes, identify the dominant influences on larval disper- Hare, J.A., J.A. Quinlan, F.E. Werner, B.O. Blanton, J.J. G.P. Jones, and B.A. Menge. 1996. Recruitment sal on continental shelves. Marine Ecology Progress Govoni, R.B. Forward, L.R. Settle, and D.E. Hoss. and the local dynamics of open marine popula- Series. 1999. Larval transport during winter in the SABRE tions. Annual Review of Ecology and Systematics Ellien, C., E. Thièbaut, F. Dumas, J.C. Salomon, and study area: Results of a coupled vertical larval 27:477–500. P. Nival. 2004. A modelling study of the respec- behavior-three-dimensional circulation model. Carr, S.D., R.A. Tankersley, J.L. Hench, R.B. Forward tive role of hydrodynamic processes and larval Fisheries Oceanography 8(supplement 1):57–76. Jr., and R.A. Luettich Jr. 2004. Movement patterns mortality on larval dispersal and recruitment of Hare, J.A., S.R. Thorrold, H. Walsh, C. Reiss, A. and trajectories of ovigerous blue crabs Callinectes benthic invertebrates: Example of Pectinaria koreni Valle-Levinson, and C. Jones. 2005. Routes and sapidus during the spawning migration. Estuarine, (Annelida: Polychaeta) in the Bay of Seine (English rates of larval fish transport from the southeast Coastal and Shelf Science 60:567–579. Channel). Journal of Plankton Research 26:117–132. to the northeast United States continental shelf. Chen, C., R.C. Beardsley, and G. Cowles. 2006. Fiksen, Ø., C. Jørgensen, T. Kristiansen, F. Vikebø, and Biophysical Mechanisms of Larval Fish Ingress into An unstructured-grid, finite-volume coastal G. Huse. In press. Linking behavioural ecology Chesapeake Bay 303:295–310. ocean model (FVCOM) system. Oceanography and oceanography: Larval behaviour determines Hentschel, B.T., and R.B. Emlet. 2000. Metamorphosis 19(1):78–89. growth, mortality and dispersal. Marine Ecology of barnacle nauplii: Effects of food variability and Clobert, J., E. Danchin, A.A. Dhondt, and J.D. Nichols, Progress Series. a comparison with amphibian models. Ecology eds. 2001. Dispersal. Oxford University Press, Forward, R.B., J.H. Cohen, R.D. Irvine, J.L. Lax, 81:3,495–3,508. 452 pp. R. Mitchell, A.M. Schick, M.M. Smith, J.M. Heyman, W.D., B. Kjerfve, R.T. Graham, K.L. Rhodes, Colby, D.R. 1988. Null hypotheses, models, and sta- Thompson, and J.I. Venezia. 2004. Settlement of and L. Garbutt. 2005. Spawning aggregations tistical designs in the study of larval transport. blue crab Callinectes sapidus megalopae in a North of Lutjanus cyanopterus (Cuvier) on the Belize American Fisheries Society Symposium 3:149–162. Carolina estuary. Marine Ecology Progress Series Barrier Reef over a 6 year period. Journal of Fish Cowen, R.K. 1991. Variation in the planktonic larval 269:237–247. Biology 67:83–101. duration of the temperate wrasse Semicossyphus Franks, P.J.S. 1992. Sink or swim: Accumulation of Hiatt, R.W. 1948. The biology of the lined shore crab, pulcher. Marine Ecology Progress Series 69:9–15. biomass on fronts. Marine Ecology Progress Series Pachygrapsus crassipes Randall. Pacific Science Cowen, R.K. 2002. Larval dispersal and retention and 82:1–12. 2:135–213. consequences for population connectivity. Pp. 149– Garvine, R.W., C.E. Epifanio, C.C. Epifanio, and K.C. Hickey, B.M. 1979. The California Current System— 170 in Coral Reef Fishes. Dynamics and Diversity in Wong. 1997. Transport and recruitment of blue hypotheses and facts. Progress in Oceanography a Complex Ecosystem. P.F. Sale, ed., Academic Press, crab larvae: A model with advection and mortality. 8:191–279. San Diego, CA. Estuarine Coastal and Shelf Science 45(1):99–111. Hill, A.E. 1991. Advection-diffusion-mortality solu- Cowen, R.K., J.A. Hare, and M.P. Fahay. 1993. Beyond Gaylord, B., and S.D. Gaines. 2000. Temperature or tions for investigating pelagic larval dispersal. hydrography: Can physical processes explain larval transport? Range limits in marine species mediated Marine Ecology Progress Series 70:117–128. fish assemblages within the Middle Atlantic Bight. solely by flow. American Naturalist 55:769–789. Houde, E.D. 1989. Comparative growth, mortality, Bulletin of Marine Science 53(2):567–587. Gerlach, G., J. Atema, M.J. Kingsford, K.P. Black, and V. and energetics of marine fish larvae: Temperature Cowen, R.K., K.M.M. Lwiza, S. Sponaugle, C.B. Paris, Miller-Sims. 2007. Smelling home can prevent dis- and implied latitudinal effects. Fishery Bulletin and D.B. Olson. 2000. Connectivity of marine persal of reef fish larvae.Proceedings of the National 87(3):471–495. populations: Open or closed? Science 287:857–859. Academy of Sciences of United States of America Hughes, T.P., A.H. Baird, E.A. Dinsdale, N.A. Cowen, R.K., C.B. Paris, and A. Srinivasan. 2006. 104:858–863. Moltschaniwskyj, M.S. Pratchett, J.E. Tanner, and Scaling of population connectivity in marine pop- Gerrodette, T. 1981. Dispersal of the solitary coral B.L. Willis. 2000. Supply-side ecology works both ulations. Science 311:522–527. Balanophyllia elegans by demersal planular larvae. ways: The link between benthic adults, fecundity, Crisp, D.J. 1976. Settlement responses in marine Ecology 62:611–619. and larval recruits. Ecology 81:2,241–2,249. organisms. Pp. 83–124 in Adaptation to Giménez, L., and K. Anger. 2003. Larval performance Hunt, H.L., and R.E. Scheibling. 1997. Role of early Environment: Essays on the Physiology of Marine in an estuarine crab, Chasmagnathus granulata, is a post-settlement mortality in recruitment of ben- Animals, R.C. Newell, ed., Butterworths, London. consequence of both larval and embryonic experi- thic marine invertebrates. Marine Ecology Progress Cruz, T. 2000. Biologia e ecologia do percebe Pollicipes ence. Marine Ecology Progress Series 249:251–264. Series 155:269–301. pollicipes (Gmelin, 1790) no litoral sudoeste Goffredi, S. K., W.J. Jones, C.A. Scholin, R. Marin, and Jarrett, J.N. 2003. Seasonal variation in larval condition português. Ph.D. Dissertation, Universidade R.C. Vrijenhoek. 2006. Molecular detection of and postsettlement performance of the barnacle de Évora, Évora. marine invertebrate larvae. Marine Biotechnology Semibalanus balanoides. Ecology 84(2):384–390. Cushing, D.H. 1990. Plankton production and year- 8:149–160. Jeffs, A.G., and R.C. Holland. 2000. Swimming behav- class strength in fish populations: An update of the Grimes, C.B., and M.J. Kingsford. 1996. How do riv- iour of the puerulus of the spiny lobster Jasus match/mismatch hypothesis. Advances in Marine erine plumes of different sizes influence fish lar- edwardsii (Hutton, 1875) (Decapoda, Palinuridae). Biology 26:249–293. vae: Do they enhance recruitment? Marine and Crustaceana 73:847–856. DiBacco, C., D. Sutton, and L. McConnico. 2001. Freshwater Research 47(2):191–208. Jenkins, G.P., and D. King. 2006. Variation in larval Vertical migration behavior and horizontal distri- Hare, J.A., J.H. Churchill, R.K. Cowen, T.J. Berger, growth can predict the recruitment of a temperate, bution of brachyuran larvae in a low-inflow estu- P.C. Cornillon, P. Dragos, S.M. Glenn, J.J. Govoni, seagrass-associated fish.Oecologia 147(4):641–649. ary: Implications for bay-ocean exchange. Marine and T.N. Lee. 2002. Routes and rates of larval fish Johnson, M.W. 1939. The correlation of water move- Ecology Progress Series 217:191–206. transport from the southeast to the northeast ments and dispersal of pelagic larval stages of Doherty, P.J., V. Dufour, R. Galzin, M.A. Hixon, M.G. United States continental shelf. Limnology and certain littoral animals, especially the sand crab, Meekan, and S. Planes. 2004. High mortality dur- Oceanography 47:1,774–1,789. Emerita. Journal of Marine Research 2:236–245. ing settlement is a population bottleneck for a Hare, J.A., and R.K. Cowen. 1997. Size, growth, devel- Jones, G.P., S. Planes, and S.R. Thorrold. 2005. Coral tropical surgeonfish. Ecology 85:2,422–2,428. opment, and survival of the planktonic larvae reef fish larvae settle close to home. Current Biology Edwards, K.P., J.A. Hare, F.E. Werner, and H. Seim. In of Pomatomus saltatrix (Pisces: Pomatomidae). 15:1,314–1,318.

Oceanography September 2007 37 Kelly, P., S.D. Sulkin, and W.F van Heukelem. 1982. A Iberian Peninsula. Marine Ecology Progress Series Nathan, R., and H. Muller-Landau. 2000. Spatial pat- dispersal model for larvae of the deep sea red crab 298:251–260. terns of seed dispersal, their determinants and Geryon quinquedens based on behavioral regula- Marshall, D.J., C.N. Cook, and R.B. Emlet. 2006. consequences for recruitment. Trends in Ecology tion of vertical migration in the hatching stage. Offspring size effects mediate competitive interac- and Evolution 15:278–285. Marine Biology 72:35–43. tions in a colonial marine invertebrate. Ecology Natunewicz, C.C., and C.E. Epifanio. 2001. Spatial and Kingsford, M.J. 1990. Linear oceanographic features: 87(1):214–225. temporal scales of patches of crab larvae in coastal A focus for research on recruitment processes. Marshall, D.J., and M.J. Keough. 2006. Complex waters. Marine Ecology Progress Series 212:217–222. Australian Journal of Ecology 15:391–401. life cycles and offspring provisioning in marine Nelson, J. 1912. Report of the biologist. Pp. 269–309 Kingsford, M.J., J. Leis, A.L. Shanks, K. Lindeman, S. invertebrates. Integrative and Comparative Biology in Report of the Department of Biology, New Jersey Morgan, and J. Pineda. 2002. Sensory environ- 46(5):643–651. Agricultural College Experimental Station for 1911. ments, larval abilities and local self-recruitment. Matsuura, Y., and R. Hewitt. 1995. Changes in the spa- O’Connor, M.I., J.F. Bruno, S.D. Gaines, B.S. Halpern, Bulletin of Marine Science 49:309–340. tial patchiness of Pacific mackerel, Scomber japoni- S.E. Lester, B.P. Kinlan, and J.M. Weiss. 2007. Largier, J.G. 2003. Considerations in estimating lar- cus, larvae with increasing age and size. Fishery Temperature control of larval dispersal and val dispersal distances from oceanographic data. Bulletin 93:172–178. the implications for marine ecology, evolution, Ecological Applications 13:S71–S89. McCormick, M.I. 2006. Mothers matter: Crowding and conservation. Proceedings of the National Lasker, R. 1975. Field criteria for survival of anchovy leads to stressed mothers and smaller offspring in Academy of Sciences of the United States of America larvae: The relation between inshore chlorophyll marine fish. Ecology 87(5):1,104–1,109. 104:1,266–1,271. maximum and successful feeding. U.S. Fish and McCormick, M.I., and A.S. Hoey. 2004. Larval growth Okubo, A. 1988. Biological vortex rings fertiliza- Wildlife Service Fishery Bulletin 73:453–462. history determines juvenile growth and survival in tion and dispersal of fish eggs. Pp. 270–283 in Leaman, K.D., E. Johns, and T. Rossby. 1989. The aver- a tropical marine fish. Oikos 106(2):225–242. Mathematical Ecology, T.G. Hallam, L.J. Gross, and age distribution of volume transport and potential Meekan, M.G., J.H. Carleton, A.D. McKinnon, K. S.A. Levin, eds, World Scientific, Singapore. vorticity with temperature at 3 sections across Flynn, and M. Furnas. 2003. What determines the Okubo, A. 1994. The role of diffusion and related the Gulf Stream. Journal of Physical Oceanography growth of tropical reef fish larvae in the plankton: physical processes in dispersal and recruitment of 19:35–51. Food or temperature? Marine Ecology Progress marine populations. Pp. 5–32 in The Bio-Physics Lee, O., B.S. Danilowicz, and M. Dickey-Collas. 2006. Series 256:193–204. of Marine Larval Dispersal, P.W. Sammarco and Temporal and spatial variability in growth and Meekan, M.G., and L. Fortier. 1996. Selection for fast M.L. Heron, eds, American Geophysical Union, condition of dab (Limanda limanda) and sprat growth during the larval life of Atlantic cod Gadus Washington, D.C. (Sprattus sprattus) larvae in the Irish Sea. Fisheries morhua on the Scotian Shelf. Marine Ecology Olson, R.R., and R. McPherson. 1987. Potential vs. Oceanography 15(6):490–507. Progress Series 137(1–3):25–37. realized larval dispersal: Fish predation on larvae Leis, J. 2006. Are larvae of demersal fishes plankton or Meekan, M.G., L. Vigliola, A. Hansen, P.J. Doherty, A. of the ascidian Lissoclinum patella (Gottschaldt). nekton? Advances in Marine Biology 51:57–141. Halford, and J.H. Carleton. 2006. Bigger is better: Journal of Experimental Marine Biology and Ecology Lentz, S.J. 1995. Sensitivity of the inner-shelf circu- Size-selective mortality throughout the life his- 110:245–256. lation to the form of the eddy viscosity profile. tory of a fast-growing clupeid, Spratelloides gracilis. Paris, C.B., R.K. Cowen, R. Claro, and K.C. Lindeman. Journal of Physical Oceanography 25:19–28. Marine Ecology Progress Series 317:237–244. 2005. Larval transport pathways from Cuban snap- Lentz, S.J., R.T. Guza, S. Elgar, F. Feddersen, and Metaxas, A. 2001. Behaviour in flow: Perspectives on per (Lutjanidae) spawning aggregations based on T.H.C. Herbes. 1999. Momentum balances in the the distribution and dispersion of meroplanktonic biophysical modeling. Marine Ecology Progress North Carolina inner shelf. Journal of Geophysical larvae in the water column. Canadian Journal of Series 296:93–106. Research 104:18,205–18,226. Fisheries and Aquatic Sciences 58:86–98. Paris, C.B., and R.K. Cowen. 2004. Direct evidence Levin, L.A. 2006. Recent progress in understanding Miller, T.J., L.B. Crowder, J.A. Rice, and E.A. Marschall. of a biophysical retention mechanism for coral larval dispersal: New directions and digressions. 1988. Larval size and recruitment mechanisms reef fish larvae.Limnology and Oceanography Integrative and Comparative Biology 282–297. in fishes: Towards a conceptual framework. 49:1,964–1,979. Levin, L.A., and T.S. Bridges. 1995. Pattern and Canadian Journal of Fisheries and Aquatic Sciences Pechenik, J.A. 1986. Field evidence for delayed meta- diversity in reproduction and development. Pp. 45:1,657–1,670. morphosis of larval gastropods: Crepidula plana 1–48 in Ecology of Marine Invertebrate Larvae, L. Mitchum, G.T., and A.J. Clarke. 1986. The fric- Say, C. fornicata (L.) and Bittium alternatum (Say). McEdward, ed., CRC Press, Boca Raton, FL. tional nearshore response to forcing by synoptic Journal of Experimental Marine Biology and Ecology Limouzy-Paris, C.B., H.C. Graber, D.L. Jones, A.W. scale winds. Journal of Physical Oceanography 97:313–319. Röpke, and W.J. Richards. 1997. Translocation of 16:934–946 Pechenik, J.A., J.N. Jarrett, and J. Rooney. 2002. larval coral reef-fishes via sub-mesoscale spin-off Monismith, S.G., and D.A. Fong. 2004. A note on Relationships between larval nutritional experi- eddies from the Florida Current. Bulletin of Marine the potential transport of scalars and organisms ence, larval growth rates, juvenile growth rates, and Science 60:966–983. by surface waves. Limnology and Oceanography juvenile feeding rates in the prosobranch gastropod Lough, R.G., L.J. Buckley, F.E. Werner, J.A. Quinlan, 49:1,214–1,217. Crepidula fornicata. Journal of Experimental Marine and K. Pehrson Edwards. 2005. A general biophysi- Moran, A.L., and R.B. Emlet. 2001. Offspring size and Biology and Ecology 280(1–2):63–78. cal model of larval cod (Gadus morhua) growth performance in variable environments: Field stud- Pechenik, J.A., D.E. Wendt, and J.N. Jarrett. 1998. applied to populations on Georges Bank. Fisheries ies on a marine snail. Ecology 82(6):1,597–1,612. Metamorphosis is not a new beginning. Bioscience Oceanography 14:241–262. Morgan, S.G. 1995. The timing of larval release. Pp. 48:901–910. Ma, H., and J.P. Grassle. 2005. Invertebrate larval avail- 157–191 in Ecology of Marine Invertebrate Larvae, Pepin, P., and J.A. Helbig. 1997. Distribution and ability during summer upwelling and downwelling L. McEdward, ed., CRC Press, Boca Raton, FL. drift of Atlantic cod (Gadus morhua) eggs and on the inner continental shelf off New Jersey. Mullin, M.M. 1993. Webs and Scales: Physical and larvae on the northeast Newfoundland Shelf. Journal of Marine Research 62:837–865. Ecological Processes in Marine Fish Recruitment. Canadian Journal of Fisheries and Aquatic Sciences Macho, G., J. Molares, and E. Vásquez. 2005. Timing Washington Sea Grant Program, University of 54:670–685. of larval release by three barnacles from the NW Washington Press, Seattle, WA, 135 pp. Phillips, N.E. 2004. Variable timing of larval food has

38 Oceanography Vol. 20, No. 3 consequences for early juvenile performance in a larvae of benthic invertebrates: An eclectic over- rates. Marine Ecology Progress Series 342:177–190. marine mussel. Ecology 85(8):2,341–2,346. view and summary of problems. Bulletin of Marine Tapia, F., J. Pineda, F. Ocampo-Torres, H. Fuchs, E. Pineda, J. 1994. Internal tidal bores in the nearshore: Science 39:290–322. Parnell, P. Montero, and S. Ramos. 2004. High-fre- Warm-water fronts, seaward gravity currents and Scheltema, R.S., and I.P. Williams. 1982. Significance quency observations of wind-forced onshore trans- the onshore transport of neustonic larvae. Journal of temperature to larval survival and length of port at a coastal site in Baja California. Continental of Marine Research 52:427–458. development in Balanus eburneus (Crustacea: Shelf Research 24:1,573–1,585. Pineda, J. 1999. Circulation and larval distribution Cirripedia). Marine Ecology Progress Series 9:43–49. Thièbaut, E., J.C. Dauvin, and Y. Lagadeuc. 1992. in internal tidal bore warm fronts. Limnology and Scotti, A., and J. Pineda. 2007. Plankton accumulation Transport of Owenia fusiformis larvae (Annelida: Oceanography 44:1,400–1,414. and transport in propagating nonlinear internal Polychaeta) in the Bay of Seine. I. Vertical distri- Pineda, J. 2000. Linking larval settlement to larval fronts. Journal of Marine Research 65:117–145. bution in relation to water column stratification transport: Assumptions, potentials, and pitfalls. Searcy, S.P., and S. Sponaugle. 2001. Selective mortality and ontogenic vertical migration. Marine Ecology Oceanography of the Eastern Pacific I:84–105. during the larval-juvenile transition in two coral Progress Series 80:29–39. Pineda, J., and M. López. 2002. Temperature, strati- reef fishes.Ecology 82(9):2,452–2,470. Titelman, J., and O. Fiksen. 2004. Ontogenetic verti- fication and barnacle larval settlement in two Shanks, A.L., B.A. Grantham, and M.E. Carr. 2003. cal distribution patterns in small copepods: Field Californian sites. Continental Shelf Research Propagule dispersal distance and the size and spac- observations and model predictions. Marine 22:1,183–1,198. ing of marine reserves. Ecological Applications 13: Ecology Progress Series 284:49–63. Pineda, J., V.R. Starczak, and T. Stueckle. 2006. Timing S159–S169. Villanueva, R., C. Nozais, and S. v. Boletzky. 1996. of successful settlement: Demonstration of a Siegel, D.A., B.P. Kinlan, B. Gaylord, and S.D. Gaines. Swimming behaviour and food searching in plank- recruitment window in Semibalanus balanoides. 2003. Lagrangian descriptions of marine larval dis- tonic Octopus vulgaris Cuvier from hatching to Marine Ecology Progress Series 320:233–237. persion. Marine Ecology Progress Series 260:83–96. settlement. Journal of Experimental Marine Biology Podolsky, R.D., and A.L. Moran. 2006. Integrating Simpson, J.J. 1984. El Niño-induced onshore trans- and Ecology 208:169–184. function across marine life cycles. Integrative and port in the California Current during 19821983. Walsh, H.J., K.E. Marancik, and J.A. Hare. 2006. Comparative Biology 46(5):577–586. Geophysical Research Letters 11:233–266. Juvenile fish assemblages collected on unconsoli- Pritchard, D.W. 1953. Distribution of oyster larvae in Sinclair, M. 1988. Marine Populations: An Essay on dated sediments of the southeast United States relation to hydrographic conditions. Proceedings Population Regulation and Speciation. Washington continental shelf. Fishery Bulletin 104:256–277. of the Gulf and Caribbean Fisheries Institute Sea Grant Program, Seattle, WA, 252 pp. Warner, R.R. 1988. Traditionality of mating- 5:123–132. Sponaugle, S., T. Lee, V. Kourafalou, and D. Pinkard. site preferences in a coral-reef fish. Nature Queiroga, H., M.J. Almeida, T. Alpuim, A.A.V. Flores, 2005. Florida Current frontal eddies and the 335(6,192):719–721. S. Francisco, I. Gonzàlez-Gordillo, A.I. Miranda, I. settlement of coral reef fishes.Limnology and Webster, M.S., P.P. Marra, S.M. Haig, S. Bensch, Silva, and J. Paula. 2006. Tide and wind control of Oceanography 50:1,033–1,048. and R.T. Holmes. 2002. Links between worlds: megalopal supply to estuarine crab populations on Sponaugle, S., R.K. Cowen, A.L. Shanks, S.G. Morgan, Unraveling migratory connectivity. Trends in the Portuguese west coast. Marine Ecology Progress J. Leis, J. Pineda, G. Boehlert, M.J. Kingsford, Ecology and Evolution 17:76–83. Series 307:21–36. K. Lindeman, C. Grimes, and J.L. Munro. 2002. Wilbur, H.M. 1980. Complex life cycles. Annual Review Quinlan, J.A., B.O. Blanton, T.J. Miller, and F.E. Predicting self-recruitment in marine populations: of Ecology and Systematics 11:67–93. Werner. 1999. From spawning grounds to estuary: Biophysical correlates and mechanisms. Bulletin of Willis, B.L., and J.K. Oliver. 1990. Direct tracking of Using linked individual-based and hydrodynamic Marine Science 49:341–375. coral larvae: Implications for dispersal studies of models to interpret patterns and processes in the Sponaugle, S., and K. Grorud-Colvert. 2006. planktonic larvae in topographically complex envi- oceanic phase of Atlantic menhaden Brevoortia Environmental variability, early life-history ronments. Ophelia 32:145–162. tyrannus life history. Fisheries Oceanography traits, and survival of new coral reef fish recruits. Winant, C.D. 1983. Longshore coherence of currents 8(s2):224–246. Integrative and Comparative Biology 46:623–633. on the Southern California shelf during the sum- Radtke, R.L., R.A. Kinzie, and S.D. Folsom. 1988. Age Sponaugle, S., K. Grorud-Colvert, and D. Pinkard. mer. Journal of Physical Oceanography 13:54–64. at recruitment of Hawaiian freshwater gobies. 2006. Temperature-mediated variation in early life Winant, C.D., and A. Bratkovich. 1981. Temperature Environmental Biology of Fishes 23:205–213. history traits and recruitment success of the coral and currents in the southern California shelf: A Raimondi, P.T. 1991. Settlement behavior of reef fishThalassoma bifasciatum in the Florida description of the variability. Journal of Physical Chthamalus anisopoma larvae largely deter- Keys. Marine Ecology Progress Series 308:1–15. Oceanography 11:71–86. mines the adult distribution. Oecologia (Berl.) Sponaugle, S., and D.R. Pinkard. 2004. Impact of vari- Woods, L., and W.J. Hargis. 1971. Transport of bivalve 85:349–360. able pelagic environments on natural larval growth larvae in a tidal estuary. Pp. 29–44 in Fourth Reyns, N.B., D.B. Eggleston, and R.A. Luettich. 2006. and recruitment of the reef fishThalassoma bifas- European Marine Biology Symposium, D.J. Crisp, Secondary dispersal of early juvenile blue crabs ciatum. Journal of Fish Biology 64(1):34–54. ed., Cambridge University Press. within a wind-driven estuary. Limnology and Stobutzki, I.C. 1997. Energetic cost of sustained swim- Zimmerman, R.C., and D.L. Robertson. 1985. Effects Oceanography 51:1,982–1,995. ming in the late pelagic stages of reef fishes.Marine of El Niño on local hydrography and growth of the Roughgarden, J., S. Gaines, and H. Possingham. 1988. Ecology Progress Series 152(1–3):249–259. giant kelp, Macrocystis pyrifera, at Santa Catalina Recruitment dynamics in complex life cycles. Stommel, H. 1963. Varieties of oceanographic experi- Island, California. Limnology and Oceanography Science 241:1,460–1,466. ence. Science 139:572–576. 30:1,298–1,302. Rumrill, S.S. 1990. Natural mortality of marine inver- Suthers, I.M., J.J. Cleary, S.C. Battaglene, and R. Evans. tebrate larvae. Ophelia 32:163–198. 1996. Relative RNA content as a measure of con- Sammarco, P.W., and J.C. Andrews. 1989. The Helix dition in larval and juvenile fish. Marine and experiment: Differential localized dispersal and Freshwater Research 47 (2):301–307. recruitment patterns in Great Barrier reef corals. Tapia, F., and J. Pineda. 2007. Stage-specific distri- Limnology and Oceanography 34:896–912. bution of barnacle larvae in nearshore waters: Scheltema, R.S. 1986. On dispersal and planktonic Potential for limited dispersal and high mortality

Oceanography September 2007 39