## Abstract

Larvae have been difficult to study because their small size limits our ability to understand their behavior and the conditions they experience. Questions about larval transport focus largely on (a) where they go [dispersal] and (b) where they come from [connectivity]. Mechanisms of transport have been intensively studied in recent decades. As our ability to identify larval sources develops, the consequences of connectivity are garnering more consideration. Attention to transport and connectivity issues has increased dramatically in the past decade, fueled by changing motivations that now include management of fisheries resources, understanding of the spread of invasive species, conservation through the design of marine reserves, and prediction of climate-change effects. Current progress involves both technological advances and the integration of disciplines and approaches. This review focuses on insights gained from physical modeling, chemical tracking, and genetic approaches. I consider how new findings are motivating paradigm shifts concerning (1) life-history consequences; (2) the openness of marine populations, self-recruitment, and population connectivity; (3) the role of behavior; and (4) the significance of variability in space and time. A challenge for the future will be to integrate methods that address dispersal on short (intragenerational) timescales such as elemental fingerprinting and numerical simulations with those that reflect longer timescales such as gene flow estimates and demographic modeling. Recognition and treatment of the continuum between ecological and evolutionary timescales will be necessary to advance the mechanistic understanding of larval and population dynamics.

## Introduction

Interest in the dispersal of larvae dates back to the seminal ideas of Hjort (1926) and Thorson (1946), who advocated the importance of larval transport and survival in determining the dynamics of fish and invertebrate populations, respectively. Since the 1980s there has been an increased awareness of “supply side” ecology (Gaines and Roughgarden 1985; Lewin 1986; Young 1987; Fairweather 1991), granting larval studies a central position in the field of marine ecology. The number of articles addressing larval dispersal increased greatly during the 1990s (Fig. 1). A Web of Science search for articles using the key word “larvaldispersal” shows 2003 (the last year surveyed) to be a peak year with 62 publications.

Fig. 1

The number of articles published over the last 25 years whose title or abstract contained the term larval dispersal. Based on a Web of Science survey.

Fig. 1

The number of articles published over the last 25 years whose title or abstract contained the term larval dispersal. Based on a Web of Science survey.

Much of the larval work conducted during the last quarter of the twentieth century focused on mechanisms of transport (for example, see reviews by Shanks 1995), rates of mortality (Rumrill 1990), larval trajectories (Levin 1984), settlement behaviors and cues (Pawlik 1992), and rates of gene flow (Burton 1983; Hedgecock 1986; Grosberg and Cunningham 2001; Hellberg and others 2002). The primary motivation was the idea that larval supply was a key determinant of adult population dynamics.

There has been a resurgence of interest in larval dispersal, in part fueled by relatively new motivations and by new imperatives for more traditional motivations. For example, understanding the dynamics of fish and shellfish resources has long spurred interest in the dispersal of commercially valuable species such as oysters (Nelson 1924, Mazzarelli 1992). Overfishing, eutrophication, and destruction of fisheries habitats have increased the importance of understanding which populations act as sources, which populations act as sinks, and how sites are connected by larval exchange. The design of marine protected areas (MPAs) has provided major impetus for the assessment of dispersal and its role in conservation (Botsford and others 2001; Lubchenco and others 2003). As coastal ecosystems are degraded, restoration plays a more prominent role in the ecological management agenda. Recovery of restored (or disturbed) habitats may initially be controlled by the structure of the patches (Connel and Keough 1985; Sousa 1985) or the dispersal abilities of colonizing species (for example, Levin and others 1996). Thus, understanding dispersal mechanisms, rates, and distances can help scientists to determine the optimal size, configuration, and location of MPAs and restored habitats such as wetlands. Attempts to understand and control the spread of invasive species have led to a new genre of dispersal studies focusing on newly colonized, non-indigenous populations (Neubert and Caswell 2000). The growing recognition that climate change may alter species ranges on interannual (Fields and others 1993; Roy and others 2001) and much longer timescales has prompted scientists to look at the role of dispersal in this process. Finally, a general desire to maintain and sometimes maximize regional and local biodiversity has generated curiosity about the role of dispersal in this process (Stuart and others 2003).

Throughout his career, Larry McEdward's research offered invaluable insights into the evolution and consequences of invertebrate life histories. Although Larry did not directly study the dispersal of larvae, many facets of his work, from the provisioning of eggs and parental care to release times (McEdward and Janies 1997; McEdward and Morgan 2001; Reitzel and others 2004), greatly enhanced understanding of larval survival and transport.

The goal of this review is to provide an overview of how understanding of larval dispersal has changed in the past 5–10 years. I will examine the primary questions addressed, the new tools and approaches that have been developed to tackle these questions, and the insights that have emerged from these approaches. Rather than covering the multitude of articles that have been published in an exhaustive fashion, I will focus on examples that illustrate paradigm shifts and novel methodologies. A significant number of comprehensive reviews have been published recently on different aspects of larval dispersal and its consequences. I will attempt to synthesize some of the main insights resulting from these reviews, highlighting those issues that appear to advance (or at least move) the field.

It should be emphasized that while larvae are the focus of this article, they are not the only, or always the most important, dispersive phase in animal life histories. Sperm dispersal and post-larval dispersal by drifting, rafting, dislodgement, or adult migrations can contribute to the patterns of connectivity and gene flow often attributed to larvae (Havenhand 1995).

## Key questions

I maintain that the two most important questions in the study of larval dispersal are the age-old queries “Where do larvae go?” and “Where do settling larvae come from?” The first of these is the more traditional view of larval dispersal. We ask how far do larvae travel and what are the factors that influence transport? What are the roles of developmental traits, timing and location of release, nutrition, behavior, and physical processes in determining larval transport distances? In modern jargon we speak of dispersal kernels, to reflect the probability distribution of larvae as a function of their starting location (Neubert and Caswell 2000). As mentioned earlier, considerable focus in the past decades has been on determining the underlying transport mechanisms (for example, Epifanio and Garvine 2001).

The opposite side of the coin considers where settlers or recruits in a population originate. Taken in a spatial context, this is a key component in the modern concept of connectivity (Moilanen and Hanski 2001). Questions about whether populations are open or closed (Caley and others 1996; Mora and Sale 2002), the importance of retention and self-recruitment (Swearer and others 2002), the existence of sources and sinks within a metapopulation (Hanski and Gilpin 1991), and the complexity of these patterns all derive from knowing the sources (and sometimes trajectories) of settling larvae. As our ability to evaluate the origins of recruits develops, we can also begin to ask about the importance of the origin of planktonic larvae to subsequent success in the benthos.

To understand changes in the field it is necessary to view the dominant paradigms that have developed with the onset of a “supply side” mindset. The concept of “open populations,” with plentiful exchange of larvae, was pervasive in the late twentieth century (Caley and others 1996). In combination, the widespread existence of planktonic larvae among invertebrates and fish, the broad distribution of larvae in the plankton, extended planktonic periods, poor swimming abilities of most larvae, and observations of gene flow among isolated patches suggest that larval exchange among subpopulations should be the rule. These observations, combined with the typical disconnection between local larval production and settlement at any one site (Dixon and others 1999), provide evidence for open populations (Swearer and others 2002). Over time exceptions have been noted (for example, Todd and others 1998) that preview shifts in the paradigm of well-mixed populations.

Recent work suggests that retention of larvae in the natal habitat is more frequent than suspected and, thus, that populations may be less open (or more closed) than originally thought. Later sections of this article demonstrate how diverse studies of dispersal utilizing physical models, genetic studies, elemental fingerprinting, and natural observations all suggest that retention is common. Taken together, these methodologies appear to be altering the “connectivity” paradigm.

That the larval dispersal phase is advantageous was also viewed by many as a fact during much of the past century. The key roles of dispersal in founding new populations; in habitat selection; in gene flow; and for possibly placing larvae in a safer, food-rich, predator-free setting (relative to the benthos) argued strongly for selection to promote the planktonic larval phase. However, it is now recognized that planktonic larvae offer many disadvantages and that trade-offs are clearly involved (Palmer and Strathmann 1981; Strathmann 1982; Strathmann and others 2002). Ontogenetic (life-stage) migrations provide a more balanced framework for viewing the trade-offs between transport and larval loss.

The passive nature of larval dispersal, particularly for marine invertebrates, is another assumption that had pervaded the study of transport and application of physical models until recently (Stobutzski 2001). The absence of information about behavior of larvae in the field (Young 1995) and of techniques to study their behavior in the field has been partly responsible for this, although Young and Chia (1987) earlier highlighted the potential importance of larval behavior in determining the distribution of larvae. Some of the most thoughtful treatment of how behavior can influence dispersal or settlement comes from studies of poecilogonous species with developmental and behavioral dimorphisms (for example, Levin and Huggett 1990; Krug and Zimmer 2004).

A fourth paradigm concerns the idea that larval supply has key consequences for both the dynamics and genetic structure of marine populations. Using bivalve biomass data, Thorson (1950) demonstrated that species with long-lived planktonic larvae exhibit larger abundance fluctuations than species with non-planktonic larvae. For the next 40 years the belief that dispersive larvae contribute to population variability in invertebrates was dominant. A number of treatments questioned this over the years (Josefson 1986; Levin and Huggett 1990; Olaffson and others 1994). By far the most definitive of these is a recent review by Eckert (2003) in which 570 invertebrate time series were examined for adult density variation. Species with no planktonic period were found to exhibit the greatest coefficients of variation, but taxa with short (<3 days), intermediate (3–10 days), and long (>2 weeks) planktonic periods did not differ in variability of benthic populations. Eckert (2003) argued that rather than promoting variability, the planktonic period may dampen fluctuations by spreading larvae over heterogeneous environments. Botsford and colleagues (1998) noted that dispersal allows spatially separated populations to fluctuate in phase.

Interest in the influence of dispersal on genetic structure also has a long history (Hedgecock 1986; Palumbi 2001). Planktonic dispersal was considered to play a key role in homogenizing gene frequencies, and the lack of larval exchange was thought to promote differentiation and increase genetic structure. Reviews by Palumbi (2001), Hellberg and colleagues (2002), and Palumbi (2003) look at the scales over which dispersal distance and genetic structure appear linked. These authors conclude that the greatest influence of larval transport on genetic structure occurs at intermediate scales (∼100 km). They observed little differentiation on small scales (10 m) and domination by historical influences at much larger scales (1000 km).

### The link between larval development, dispersal, and its consequences

There has been a general understanding that egg size is correlated with planktonic development time and thus to dispersal potential (Thorson 1950). Two recent compilations show a positive relationship between propagule duration in the plankton and measures of dispersal distance.

Shanks and colleagues (2003; Fig. 2) drew data from studies in which planktonic period was derived from direct observations, studies of distributions in nature, genetic and experimental studies, as well as from tracking of introduced species. Siegel and colleagues (2003; Fig. 2) examined studies for which a genetic-based average dispersal scale was estimated. Both revealed a bimodal distance distribution, comparable to observations of bimodal egg sizes (Vance 1973; Sewell and Young 1997). Few species exhibited dispersal distances between 1 and 20 km/year. Both studies also identified a number of species whose observed dispersal distances fell well below the predicted values; these were identified as possibly reflecting retention within the natal habitat.

Fig. 2

The relationship between planktonic duration of propagules and dispersal distance. A: from Shanks and colleagues (2003), B: from Siegel and colleagues (2003).

Fig. 2

The relationship between planktonic duration of propagules and dispersal distance. A: from Shanks and colleagues (2003), B: from Siegel and colleagues (2003).

The positive relationship between propagule duration (planktonic larval duration [PLD]) and dispersal distance was used by Grantham and colleagues (2003) to calculate habitat-specific dispersal potential. They examined a range of ecosystems in the U.S. Pacific Northwest, collating development mode, rafting potential, and planktonic duration. From this information they inferred that assemblages in sandy intertidal habitats, which have the highest proportion of non-dispersing and non-planktonic taxa, should exhibit the most limited dispersal. Assemblages in subtidal soft-bottom habitats, which have the highest proportion of taxa with planktonic feeding and larval lifespans >30 days, should exhibit the greatest dispersal. Rocky shore assemblages in California, Oregon, and Washington were intermediate in dispersal potential.

Large eggs, the absence of feeding, and aplanktonic development or short PLDs are associated with limited dispersal potential, and thus should enhance the probability of self-recruitment (settlement at the natal site). However, comparison of larval dispersal by demersal-versus pelagic-spawning fishes revealed no inshore retention in species with non-pelagic eggs (Hickford and Schiel 2003). Two groups that rely on self-recruitment for persistence are endemic species and newly introduced species. Swearer and colleagues (2002) examined articles addressing the life histories of these groups and found no bias toward development with reduced PLDs. Pelagic larvae are well represented among endemic tropical fishes and marine mollusks, as well as among introduced Hawaiian fishes and marine invertebrates (Swearer and others 2002). Thus, retention is clearly not solely a function of life history. We must recognize, however, that endemic and introduced species are more likely to have originated from founder events associated with long distance dispersal than other species. Thus, a focus on these groups may bias the assessment of the link between life history and self-recruitment.

While the questions about dispersal are not new, the context in which they are addressed and the methods of study are changing. A combination of thoughtful ideas, increased accessibility to computing power, advances in analytical chemistry and genetics, and even a little bit of magic have made the twenty-first century a more creative milieu for dispersal studies. Below, I focus on three methodological approaches to assess connectivity: physical modeling of larval dispersal, use of geochemical tracers, and genetic studies of isolation by distance.

### Physical modeling

The past 5 years has seen an exponential increase in the application of numerical simulations to larval dispersal problems. The focus is often on the development of dispersal kernels (probability distributions of spread), estimation of self-recruitment rates, generation of site-specific data for MPA design, and the construction of null hypotheses for connectivity studies (Siegel and others 2003). Circulation models may be used to study the consequences of specific hydrographic features and are often combined with realistic estimates of mortality or behavior. Lagrangian particle tracking models and diffusion models of tracer dispersion are both used extensively. Both 2D and 3D approaches have been adopted.

A number of key insights have emerged from numerical simulations and physical models. One very prominent idea is the finding that retention (near source habitat) is more likely than expected when models incorporate mortality. This was demonstrated by Cowen and colleagues (2000) for Caribbean reef fish. Studies of the polychaete Pectenaria koreni in the English channel (Ellien and others 2004) and the brittle star Ophiothris fragilis (Lefebvre and others 2003) both reveal a greater role for mortality than hydrodynamics in determining recruitment patterns, and suggest that retention is significant.

Early modeling efforts typically assumed passive dispersal by currents, even for fish larvae (Roberts 1997). Models that incorporate vertical migration often show that vertical movements have a significant effect on transport and can lead to retention or export, which would not otherwise occur. By using a 2D TRIM (tidal residual intertidal mudflat) simulation for San Diego Bay, DiBacco and colleagues (2001) demonstrated that for larvae release in the back half of the Bay, migration to the seabed during flood tide (as occurs for Pachygrapsus crassipes) will enhance transport out of the bay within 24–30 h, whereas larvae that do not migrate (such as zoeae of Lophopanopeus spp.) are effectively retained within the Bay. Particle simulations by Witman and colleagues (2003) mimicking crab and seastar larvae in the Gulf of Maine revealed that 15–75% are retained within the study area over 2–5 weeks. This fraction is 0 at the surface, but increases dramatically with increasing water depth. For example, 2-week retention rates were 30, 54, and 75% at 5, 10, and 15 m water depth, respectively. Paris and Cowen (2004) used CTD/ADCP (acoustic doppler current profiler)-based models to study the effect of vertical swimming by bicolor damselfish larvae. In combination with field collections, they ascertained that retention on the natal reef can be high when larvae swim downward in a directed fashion.

Another key insight is the clear role of variability in physical transport. ROMS (regional oceanic modeling system) simulations of tracer/larvae movements in a release from the mouth of San Diego Bay illustrates that larvae may move northward during periods of slope instabilities, and transport may be southward during periods when circulation is dominated by offshore eddies (E. DiLorenzo and B. Cornuelle, unpublished data). Clearly, transport is far from static, and will vary with tidal phase, season, and year as well as external forcing factors.

Physical models are often used to address how far larvae travel. Particle tracking models suggest that larvae of the shrimp Pandalus borealus may travel 74–122 km, with variability controlled by migration of the polar front that determines inflow of Atlantic water to the Barents Sea (Pederson and others 2003). In contrast, satellite tracking of coral larvae at Flower Garden Banks in the Gulf of Mexico suggests that larvae encounter reefs and settle in <40 m (Lugo-Fernandez and others 2001).

When used in combination with other techniques, physical models can provide powerful results. Marsh and colleagues (2001) combined physiological studies of metabolic rates, energy content, and potential larval lifespan in the vent tubeworm Riftia pachyptila with measurements of along-axis water movement to estimate dispersal distances of <100 km. Two-dimensional circulation models were combined with genetic studies of Mytilus hybrid dispersal (into pure zones) to estimate dispersal distances of 30–64 km in the United Kingdom (Gilg and Hilbish 2003).

### How far do larvae go?

Scientists have been trying to answer this question since larvae were first recognized as being alternative phases of adult forms (Wallace 1876; Young 1990). Methods for tracking marine invertebrate larvae or for estimating dispersal distances have included direct observation of larvae, laboratory rearing experiments, analysis of distributions of larvae and recruits around isolated sources, studies of the spread of newly invasive species, numerical simulations based on physical transport, genetic isolation by distance studies, and use of natural and artificial markers (see reviews in Levin 1990; Thorrold and others 2002). Dispersal distance estimates compiled by Kinlan and Gaines (2003) and by Shanks and colleagues (2003) suggest that results are highly dependent on the mode of study. Direct observations focus on larvae that disperse a few centimeters to 100 m, whereas invasion studies identify dispersal distances of 10 to >100 km, and genetic methods produce a range that spans the other two approaches.

An unexpected tool for studying dispersal distance has been the spread of newly arrived invasive species. Founder populations of exotic species typically represent an isolated source whose dispersal can be evaluated by monitoring annual changes in distribution. An isolated population of the invasive mussel Mytilus galloprovincialis in South Africa was found by McQuaid and Phillips (2000) to experience wind-driven dispersal distances of 12–97 km depending on direction. However, they found that 90% of recruits settled within 5 km of their release site. Natural dispersal is not always the operating transport mechanism. The gastropod species Ocinebrellus inornatus was found by Martel and colleagues (2004) to exhibit limited differentiation despite the lack of planktonic larvae, largely because oyster farming actively dispersed the populations and enhanced gene flow.

Recovery following catastrophic disturbance may also provide clues about dispersal distances, often with results that are counterintuitive. On local scales, Nucella lapillus recolonizes disturbance rapidly despite a non-planktonic larval stage (Colson and Hughes 2004). At intermediate scales, the rapid recovery of genetic diversity of manta shrimp cytochrome oxidase c-1 on Krakatau suggested dispersal distance of 10 to 100 km (Barber and others 2002). On very large scales, Marko (2004) found that ecology was more important than dispersal in generating the genetic structure of Nucella species following the first glacial maximum. Based on genetic structure, Nucella ostrina appears to have gone locally extinct and reinvaded, whereas Nucella lamellosa appears to have been retained in a Northern refuge.

Genetic isolation by distance models has proven to be a powerful tool for estimating larval dispersal distances. Isolation by distance is most evident when comparing populations separated by two to five times the mean dispersal distance (Palumbi 2003). Estimates of this mean range from 0.5 km in corals (Hellberg 1994) to 150 km in sole (Kotoulas and others 1995), with littorine gastropods (25 km, Johnson and Black 1998), Pacific urchins (50 km, Palumbi and others 1997), and vent tube worms (70 km, Vrijenhoek 1997) falling in between. However there can be a lot of scatter in the relationship between population distances and Fst, as shown for south Pacific urchins (Palumbi and others 1997).

### Where do larvae come from?

If we knew how many larvae were produced, where all larvae dispersed to, and which ones survived to settle, it would be possible to know where larvae originated from, among any cohort of settlers. This pattern of larval exchange, and the degree to which larvae originate from outside the target population, is one definition of connectivity in a metapopulation sense (Moilanen and Hanski 2001). A large amount of self-seeding leads to low connectivity; high rates of larval exchange with other populations generate high connectivity. Interest in connectivity on land and in the sea has increased as scientists realized its importance in effective resource management (Crooks and Sanjayan 2006) and MPA design (Palumbi 2001). There has been considerable recent development of tools for examining population connectivity. Below I offer examples illustrating the application of physical modeling, natural and applied geochemical markers, and genetics to elucidate patterns of connectivity.

#### Connectivity matrices and physical modeling

Lagrangian particle tracking models or advection diffusion tracer models that map dispersal probability distributions for larvae originating at distinct sites can be used to create a connectivity matrix. By gathering the incoming larvae at a particular target site to determine the distribution of sources, one can establish (1) the likelihood of self-recruitment [pij where i = j], (2) the proportion of larvae originating outside the target site ($∑pij$ where ij), and (3) the diversity of sources ($∑pijlnpij$). James and colleagues (2002) created a connectivity matrix for coral larvae using a numerical hydrodynamic model to compute the 2D depth-integrated current field for the shelf-reef complex between 14° and 19°S on the Great Barrier Reef. They simulated 240 million (fish) larval trajectories in an examination of 321 reefs and dispersal over 20 years, illustrating the statistical power and expansive scale of computer methods. Behavior involving early passive and later active phases was combined with mortality estimates in an advective larval tracking model. The simulations predicted that <9% of recruits would settle on the natal reef, and indicated that a small number of populations supplied most of the recruits. One can test computer-generated dispersal predictions against distance-based predictions and against actual data for realized dispersal (M. Neubert and H. Caswell, personal communication). This is being attempted for bivalves dispersing in New England and southern California (Levin and others 2005).

#### Environmental markers

To obtain information about realized connectivity patterns on ecological timescales for species whose larvae cannot be observed, it is necessary to employ a marker. Larvae may be marked artificially or natural tags may be used (Levin 1990; Thorrold and others 2002). Artificial markers are often used to label carbonate structures such as shells or otoliths, though tissues may be marked as well. Common markers include fluorescent dyes such as tetracycline and calcein, elemental tags such as SrCl2 or rare earth elements, radiolabels, and even applied thermal stress marks (Levin and others 1993; Anastasia and others 1998; Thorrold and others 2002). The first direct evidence of larval retention in marine fish was provided by marking large numbers of damselfish eggs with tetracycline on Lizard Island, Australia. Jones and colleagues (1999) found that 15 of the 5000 recruiting larvae they examined were marked. Based on an estimate of the total percent of the population marked, they inferred that anywhere from 15 to 60% of juveniles may return to their natal population. This is one of the few true marking success stories. Typically dilution rates in nature are too great to yield significant numbers of marked larvae.

For this reason scientists have sought natural tags that mark all larvae exposed to a particular environment. Structural attributes, stable isotopic signatures, and trace elements can function in this mode. Gaines and Bertness (1992) used size to distinguish larvae originating in Narragansett Bay from those on the open coast. They were able to detect flushing of the larger Bay larvae to the outer coast during years of high rainfall.

Stable isotope signatures of tissues reflect consumer diets (δ13C, δ15N) or water temperature (δ18O). Killingley and Rex (1985) first used oxygen isotopes to document differences in developmental zones of planktotrophic and lecithotrophic larvae of deep-sea gastropods. δ18O signatures of benthic planktotrophic species clearly revealed a warm-water signature in the retained larval shell but cold-water signatures in the adult shell. In contrast, lecithotrophic species with supposedly demersal development had similar adult and larval shell signatures. Surprisingly little has been done since this landmark study to use isotopes to study the water masses occupied by deep-sea larvae.

When larval habitat shifts involve a change in food sources, distinct isotope signatures should develop. Herzka and colleagues (2002) found that the red drum habitat shift from open water (as larvae) to seagrass beds (after settlement) in the Gulf of Mexico estuaries yielded a distinct increase in δ13C and a decrease in δ15N, and that the changes stabilized within 10 days of settlement. Based on this information she was able to model the size and time of settlement of red drum larvae in a seagrass ecosystem. Similar applications should be useful in assessing larval transitions from open water to wetland ecosystems and mangrove to coral reef ecosystems.

An emerging methodology is the use of trace elemental fingerprinting to assess larval origins or trajectories. This is based on the idea that the elemental composition of larval tissues or hard parts reflects the chemistry of the water in which they were formed. If one knows the multi-elemental signatures imparted by source waters, and these are distinct among natal regions, then it should be possible to reconstruct larval origins and possibly trajectories. To apply this method it is necessary to either test the source signatures imparted while larvae are in the water or to establish that these signatures are stable over time (Gillanders 2002; Becker and others 2005). One must also know the trace elemental signatures for all possible sources.

Instrument development has played a pivotal role in making the use trace elemental fingerprinting to study larvae possible (Campana and others 1997). Different kinds of mass spectrometers and ion microprobes have been used to measure trace element concentrations in larvae. Early systems required putting the larval structures (otoliths, tissues, shells) into solution. The use of laser ablation with a highly sensitive inductively coupled plasma mass spectrometer now allows scientists to detect multiple trace elements simultaneously at ppb and ppt concentrations in individual larvae (Gunther and others 2000) or even parts of larvae at scales of 10–50 µm. From trace elements and isotope ratios of trace elements in carbonate structures it is now possible to infer much about the larval environment including salinity, temperature, proximity to land, exposure to hypoxia, pollution, upwelling, and storm events (Table 1).

Table 1

Use of trace elements to infer environmental characteristics from carbonate structures (mainly fish otoliths)

Factor Elements or isotopes References
Temperature Sr, Mg, 18/16O, 88/87Sr Kalish (1989)
Fowler and colleagues (1995)
Klein and colleagues (1996)
Thorrold, Campana, and colleagues (1997), Thorrold, Jones, and colleagues (1997)
Salinity Sr, Ba, U Fowler and colleagues (1995)
Terrestrial influence
Proximity to land Sr, Mg, Pb, Mn, Ba Swearer and colleagues (1999)
Estuarine conditions Mg, Mn, Sr, Ba, Li Thorrold and colleagues (1998)
Inshore/offshore Ba, Sr Thorrold, Campana, and colleagues (1997); Thorrold, Jones, and colleagues (1997)
Estuary/offshore Pb, Ba Forrester and Swearer (2002)
Pollutants Cu, Sn, Pb Pitts and Wallace (1994)
Hypoxia Mn Thorrold and Shuttleworth (2000)
Upwelling Ba, Cd Segovia-Zavala and colleagues (1998)
Gillanders and Kingsford (2000, 2003)
Storm events Cd
DIC, diet δ13Herzka and colleagues (2002)
Factor Elements or isotopes References
Temperature Sr, Mg, 18/16O, 88/87Sr Kalish (1989)
Fowler and colleagues (1995)
Klein and colleagues (1996)
Thorrold, Campana, and colleagues (1997), Thorrold, Jones, and colleagues (1997)
Salinity Sr, Ba, U Fowler and colleagues (1995)
Terrestrial influence
Proximity to land Sr, Mg, Pb, Mn, Ba Swearer and colleagues (1999)
Estuarine conditions Mg, Mn, Sr, Ba, Li Thorrold and colleagues (1998)
Inshore/offshore Ba, Sr Thorrold, Campana, and colleagues (1997); Thorrold, Jones, and colleagues (1997)
Estuary/offshore Pb, Ba Forrester and Swearer (2002)
Pollutants Cu, Sn, Pb Pitts and Wallace (1994)
Hypoxia Mn Thorrold and Shuttleworth (2000)
Upwelling Ba, Cd Segovia-Zavala and colleagues (1998)
Gillanders and Kingsford (2000, 2003)
Storm events Cd
DIC, diet δ13Herzka and colleagues (2002)

To apply this technique to new recruits, the larval structure must be retained by the settled individual. This occurs in fishes which retain otoliths, in squid which retain statoliths, in gastropods which retain statoliths and prodissoconch (larval shell), and in bivalves which retain the prodissoconch at settlement.

Use of otolith microchemistry to assess larval environments was pioneered among fish larvae—initially using Sr/Ca ratios by Radtke and colleagues (1990) for herring larvae. The first successful application of multiple elemental fingerprinting (to assess larval fish habitat) was accomplished by Swearer and colleagues (1999). They found that elevated concentrations of Mn, Ba, and Pb in blueheaded wrasse larvae reflected development near land (St Croix) rather than in open water. This study was among the earliest to report retention of larvae near natal sources. While some very exciting fingerprinting has been done with fish juveniles (Gillanders and Kingsford 1996; Thorrold and others 2001; Forrester and Swearer 2002), and some of these studies strongly indicate natal homing or retention, applications to fish larvae remain limited.

The first application of elemental fingerprinting to invertebrate larvae came a decade after the first work on fish larvae. DiBacco and Levin (2000) identified zoea larvae of the crab P. crassipes originating inside versus outside San Diego Bay, CA. Discriminant function analysis clearly identified larval source based on multiple elemental concentrations. By combining measurements of larval distributions at different times of the tide and in different depth zones in the water column, elemental fingerprinting of origins, and ADCP measurements of water transport, DiBacco and Chadwick (2001) were able to quantify the flux of larvae of different crab species into and out of San Diego Bay.

In the crab fingerprinting studies, larvae were not tracked beyond zoea stage 1, because elemental signals are lost as the larvae molt. Thus, it was not possible to determine where larvae of different origins actually settle. Elemental fingerprinting efforts now focus on species that retain a larval structure after settlement. An important precursor to the application of fingerprinting to determine settler origins is the identification of spatial variation in elemental signatures sufficient to distinguish sources. Zacherl, Manriquez, and colleagues (2003), Zacherl, Paradis, and colleagues (2003) and Zacherl (2005) document such variation for statoliths and prodissoconch in Kelletia kelletia and Concholepas concholepas, species that brood their larvae. Becker and colleagues (2005) documented distinct chemical variation in shells of newly recruited mytilid mussels in bay versus open-coast habitats and along 20-km zones of the southern California coastline. They also documented temporal stability of signatures on weekly and monthly scales. Because the shell of settled Mytilus is made up of calcite and the shells of larvae are of aragonite, it is desirable to obtain source signatures for larvae directly. By outplanting laboratory-spawned larvae for short periods in PVC homes on moorings placed in locations of interest, it is possible to generate the “map” of larval signatures required for determination of origins. Outplanting studies by Becker (manuscript in preparation) documented patterns in larval shells similar to those described for recruit shell (Becker and others 2005). Mapping of the prodissoconch elemental signatures for settled individuals onto the outplanting signatures revealed distinct connectivity patterns for two Mytilus species in southern California (Becker, manuscript in preparation). Other larvae for which fingerprinting techniques are under development include soft shell clam (L. Mullineaux, personal communication), oysters (D. Zacherl, personal communication), other mytilids (C. DiBacco, personal communication), rockfish (R. Warner and S. Morgan, personal communication) and halibut (J. Fodrie, personal communication).

The potential of elemental fingerprinting for revealing patterns of larval dispersal is yet to be fully exploited. Promising applications include the detection of larval associations with hydrographic features (for example, salinity or turbidity fronts, upwelling areas, eddies, and oxygen minimum zones) and tests of larval origins for abyssal populations (Rex and others 2005). Nutritional clues, derived from isotopic or fatty acid analysis, may offer information about waters and habitats occupied by larvae. Isotopic signatures of larvae can potentially indicate utilization of symbionts (chemosynthetic or photosynthetic) as a nutritional source to prolong planktonic duration.

#### Gene frequencies

Genetic structure also can provide valuable information about the movements of larvae, typically integrated over multigeneration timescales that are notably longer than those for elemental fingerprinting. Valuable reviews by Palumbi (2001, 2003), and Hellberg and colleagues (2002) examine the use of genetic information to study larval dispersal distances. Short-term tracking has been done with distinct markers. Lambert and colleagues (2003) transplanted genetically distinct nudibranchs and found that they altered gene frequencies for subsequent generations of recruits, indicating that populations are not completely open. Multiyear studies of changes in barnacle (Balanus glandula) gene frequencies on the central California coast have illustrated the importance of regional oceanography and its variability, as well as regional history (Sotka and others 2004).

On very long timescales, historical influence (pre ice age) is shown to preclude high dispersal in structuring population genetics in the holothurian Holothuria nobilis (Uthicke and Benzie 2003), in the sea star Coscinasterias muricata (Skold and others 2003), and in Macoma balthica (Luttikhuizen and others 2003). Large-scale studies of vent annelids (Hurtado and others 2004) and mussels (Won and others 2003) illustrate the importance of biogeographic filters to dispersal. Transform faults and mid-ocean ridges form clear boundaries to larval dispersal, but have different effects on different species.

Genetic structure suggests surprisingly high levels of dispersal in some species with aplanic development, for example Abra tenuis (Holmes and others 2004) and Amphipholis squamata (Sponer and Roy 2002). In contrast, unexpectedly high levels of differentiation have been observed in species with teleplanic development (Staton and Rice 1999, Apionsoma misakianum), in corals with broadcast spawning (Whitaker 2004), and in spider crabs (Weber and others 2000) and bryozoans (Goldson and others 2001) with broadly dispersing larvae having obligate planktonic phases lasting for weeks. From these genetic studies it is clear that intuition about dispersal based on development mode and larval PLD cannot provide the whole story.

## Where are we now?

Changing paradigms are key to scientific progress. The last 5 years of published results and overviews provide growing evidence for significant amounts of retention in marine species with planktonic larvae (Warner and Cowen 2002). This evidence comes from observations of persistence of upstream populations (Gaylord and Gaines 2000), the persistence of pelagic larvae on islands (Bell and others 1995), strong stock-recruitment relationships (Swearer and others 2002), studies in which restocked species persist (Peterson and others 1996), numerical simulations based on physical measurements and behavior (Cowen and others 2000; Paris and Cowen 2004), mark recapture studies (Jones and others 1999), trace elemental fingerprinting (Swearer and others 1999), and genetic studies (reviewed in Hellberg and others 2002).

The occurrence of retention and restricted dispersal may have strong consequences for the ability of populations to adapt to local ecological habitat change (Kawecki and Ebert 2004), on rates of differentiation, and species evolution (Jablonski and Lutz 1983). The phenomenon of local adaptation in marine systems has been reported mainly for species with brooded or short-lived lecithotrophic larvae, but it also occurs in several species with longer-lived pelagic larvae (Sotka 2005). If retention is widespread then local adaptation may be more prevalent than expected (Sotka 2005). Generally, the evolutionary consequences of restricted dispersal may be significant (Jablonski and Lutz 1983). High rates of intraspecific genetic variation and population differentiation parallel the occurrence of high species diversity on the continental margin (Etter and others 2005). Whether limited dispersal (relative to shelf or abyssal depths) contributes to these patterns remains to be determined.

Most recent articles published about dispersal emphasize retention, but tend to ignore those larvae that are not retained. If even a small fraction of these successfully recruit elsewhere, their significance for connectivity may be great. One can ask whether the pendulum has swung too far toward a new paradigm of self-recruitment as a rule. I suggest it is a matter of the cup being half full or half empty. If one is interested in the persistence of stocks within a marine reserve or the establishment of a new invader, self-recruitment may be the focus and a half-full cup of recruits may provide the needed input. However, if one is concerned with maintenance of genetic or biotic diversity, novel species invasions, or evolutionary change, those larvae that travel and recruit elsewhere (leaving a half-empty cup at home) may be of greater significance.

Another changing paradigm involves recognition of the significance of behavior to dispersal outcomes. Not long ago invertebrate larvae were thought to behave as passive plankton, moving within the water column at the direction of ocean physics. Behavior was considered important mainly as larvae approached the seabed to settle (Butman 1987). Although the potential significance of vertical migration was reviewed some time ago by Young and Chia (1987), and has been well studied in crustacean larvae (Cronin and Forward 1986), better understanding of sensory cues and responses (Kingsford and others 2002), more sophisticated field sampling (DiBacco and others 2001), and physical studies integrating behavior (Armsworth 2000; Paris and Cowen 2004; Largier 2004) have raised awareness about the roles of behavior in dispersal and recruitment (Metaxas 2001). Greater flexibility of behavior in response to hydrologic conditions and even sound (Leis and others 2003) gives larvae unexpected latitude in controlling their movements.

Finally, as our understanding of ocean physics improves, and as physicists begin to study the time and space scales relevant to larvae (Sponuaugle and others 2002), a deep appreciation for the dual importance of advection and diffusion (Largier 2003), and the significance of variability, has emerged. Along a coastline, points, jets, and retention zones cause variable transport (Richards and others 1995; Gaylord and Gaines 2000; Largier 2004). El Niño events, which transport species long distances, shift species ranges (Fields and others 1993), and alter recruitment patterns (Connoly and Roughgarden 1999; Davis 2000), have captured the most attention. However, seasonal shifts in current patterns and episodic events such as relaxation of upwelling (Largier 2004) may also have large consequences for the transport and recruitment success of larvae.

## Where next?

Can we enter a new dimension in our understanding of larval dispersal with advances in fingerprinting, modeling, and genetics? I believe that an entire array of novel questions will become tractable within the coming decade. The deep sea, for example, is one realm where relatively little is known about dispersal. Geochemical techniques may be applied to address the following questions:

• What are the origins of abyssal recruits––are they vagrants from the slope or do they originate in the abyss? (Rex and others 2005).

• How much larval exchange occurs within and among reducing ecosystems such as vents, seeps, and whale falls? Analysis of short-term larval exchange among seep or hydrothermal vent ecosystems might be tractable if these impart distinct trace element signatures to larval shells.

• Can we evaluate transport from hydrographic signatures? Larval movements through upwelling zones, oxygen minima, turbidity plumes, warm or cold eddies, or salinity fronts might impart distinct elemental signatures to larval shells.

• Can isotopic signatures of individual larvae provide evidence of functional photosynthesis or chemosynthesis in larvae and a nutritional basis for long planktonic phases? While photosynthesis is known to occur via zooxanthellae in coral larvae (Weiss and others 2001), activity of chemosynthetic sulfide oxidizing or methane oxidizing bacteria has not been documented for larval symbionts in reducing ecosystems.

An integration of approaches across space and timescales (Fig. 3) offers the greatest potential for advances in understanding. Combination of numerical simulations with field measurements of physics, larval distributions, fingerprinting, behavioral studies, and genetic studies will be a challenge. Such combinations will undoubtedly provide unexpected results, raise new questions, and dispel some incorrect beliefs. This will also require more interdisciplinary interaction among scientists within and outside the field of biology.

Fig. 3

Time and space scales relevant to different approaches to the study of larval dispersal. A challenge for the future is to integrate these methods.

Fig. 3

Time and space scales relevant to different approaches to the study of larval dispersal. A challenge for the future is to integrate these methods.

Always inherent in our view of dispersal will be the limitations imposed by our study taxa and methodologies. For example, far more is known about echinoderm and bivalve development than for most invertebrates, and as such our theories of life histories are based on echinoderm and bivalve patterns. Much of the trace elemental fingerprinting work has focused on fish, and new results will emerge mainly for mollusks that retain larval structures. This cannot help but bias our understanding of dispersal patterns. Within these limitations we can strive to work with species having diverse life histories, but cannot get around certain developmental and morphological biases and constraints. Genetic studies do not have these limitations, but often constrain us to looking across rather than within generations. While a critical understanding of these limitations is necessary, innovative breakthroughs that surmount them should be a focus in the coming decade.

Portions of this presentation were given at the 2005 Society of Integrative and Comparative Biology meeting in San Diego and at the 2004 Larval Ecology Conference in Hong Kong. The author thanks Larry McEdward for the scientific inspiration underlying the SICB symposium “Complex Life-Histories in Marine Benthic Invertebrates,” Ben Miner and Dianna Padilla for pulling together a wonderful series of presentations, and Pei Yuan Qian for stimulating me to think about these issues for the 2004 Larval Ecology Conference in Hong Kong. My fellow bivalve connectivity researchers, B. J. Becker, F. J. Fodrie, and P. A. McMillan, have contributed much to my understanding of the issues. I offer all the dispersal researchers (those cited and those not) heartfelt thanks for their exciting contributions to the field. D. Siegel and A. Shanks kindly provided their figures. Preparation of this review and my recent research on connectivity have been supported by NSF Grant OCE 0327209. The author thanks J. Gonzalez for assistance with manuscript preparation and F. J. Fodrie, C. DiBacco, J. Havenhand, and one anonymous reviewer for helpful comments on earlier versions of the manuscript.

## References

Anastasia
JR
Morgan
SG
Fisher
NS
Tagging crustacean larvae: assimilation and retention of trace elements
Limnol Oceanogr
,
1998
, vol.
43
(pg.
362
-
8
)
Armsworth
PR
Modeling the swimming response of late stage larval reef fish to different stimuli
Mar Ecol Prog Ser
,
2000
, vol.
195
(pg.
231
-
47
)
Barber
PH
Moosa
MK
Palumbi
SR
Rapid recovery of genetic diversity of stomatopod populations on Krakatau: Temporal and spatial scales of marine larval dispersal
Proc Biol Sci
,
2002
, vol.
269
(pg.
1591
-
7
)
Becker
BJ
The regional population variability and larval connectivity of mytilid mussels: conserving the populations of Cabrillo National Monument (San Diego, CA).
2005
San Diego
Scripps Institution of Oceanography, University of California

[PhD Dissertation]
Becker
BJ
Fodrie
FJ
McMillan
PA
Levin
LA
Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: A precursor to invertebrate larval tracking
Limnol Oceanogr
,
2005
, vol.
50
(pg.
48
-
61
)
Bell
KN
Pepin
P
Brown
JA
Seasonal, inverse cycling of length- and age at recruitment in the diadromous gobies Sicydium punctatum and Sicydium antillarum in Dominica, West Indies
Can J Fish Aquat Sci
,
1995
, vol.
52
(pg.
1535
-
45
)
Botsford
LW
Moloney
CL
Largier
JL
Hastings
A
Metapopulation dynamics of meroplanktonic invertebrates: the Dungeness crab (Cancer magister) as an example
Can Spec Publ Fish Aquat Sci
,
1998
, vol.
125
(pg.
295
-
306
)
Botsford
LW
Hastings
A
Gaines
SD
Dependence of sustainability on the configuration of marine reserves and larval dispersal distances
Ecol Lett
,
2001
, vol.
4
(pg.
144
-
50
)
Burton
RS
Protein polymorphisms and genetic differentiation of marine invertebrate populations
Mar Biol Lett
,
1983
, vol.
4
(pg.
193
-
206
)
Butman
CA
Larval settlement of soft-sediment invertebrates: the spatial scale of pattern explained by active habitat selection and the emerging role of hydrodynamical processes
Oceanogr Mar Biol Ann Rev
,
1987
, vol.
25
(pg.
13
-
165
)
Caley
MJ
Carr
MH
Hixon
MA
Hughes
TP
Jones
GP
Menge
BA
Recruitment and the local dynamics of open marine populations
Ann Rev Ecol Syst
,
1996
, vol.
27
(pg.
477
-
500
)
Campana
SE
Thorrold
SR
Jones
CM
Günther
D
Tubrett
M
Longerich
H
Jackson
S
Halden
NM
Kalish
JM
Piccoli
P
others
Comparison of accuracy, precision, and sensitivity in elemental assays of fish otoliths using the electron microprobe, proton-induced X-ray emission, and laser ablation inductively coupled plasma mass spectrometry
Can J Fish Aquat Sci
,
1997
, vol.
54
(pg.
2068
-
79
)
Colson
I
Hughes
RN
Rapid recovery of genetic diversity of dogwhelk (Nucella lapillus L.) populations after local extinction and recolonization contradicts predictions from life-history characteristics
Mol Ecol
,
2004
, vol.
13
(pg.
2223
-
33
)
Connel
JH
Keough
MJ
Pickett
STA
White
PS
Disturbance and patch dynamics of subtidal marine animals on hard substrata
The ecology of natural disturbance and patch dynamics
,
1985
Orlando, FL
(pg.
125
-
52
)
Connolly
SR
Roughgarden
J
Increased recruitment of northeast Pacific barnacles during the 1997 El Niño
Limnol Oceanogr
,
1999
, vol.
44
(pg.
466
-
9
)
Cowen
RK
Lwiza
KM
Sponaugle
S
Paris
CB
Olson
DB
Connectivity of marine populations: open or closed?
Science
,
2000
, vol.
287
(pg.
857
-
9
)
Crooks
KR
Sanjayan
MA
Connectivity conservation
2006
Cambridge University Press

In press
Cronin
TW
Forward
RB
Vertical migration cycles of crab larvae and their role in larval dispersal
Bull Mar Sci
,
1986
, vol.
39
(pg.
192
-
201
)
Davis
JLD
Changes in a tidepool fish assemblage on two scales of environmental variation: Seasonal and El Nino Southern Oscillation
Limnol Oceanogr
,
2000
, vol.
45
(pg.
1368
-
79
)
DiBacco
C
DB
Assessing the dispersal and exchange of brachyuran larvae between regions of San Diego Bay, California and nearshore coastal habitats using elemental fingerprinting
J Mar Res
,
2001
, vol.
59
(pg.
53
-
78
)
DiBacco
C
Levin
LA
Development and application of elemental fingerprinting to track the dispersal of marine invertebrate larvae
Limnol Oceanogr
,
2000
, vol.
45
(pg.
871
-
80
)
DiBacco
C
Sutton
D
McConnico
L
Vertical migration behavior and horizontal distribution of brachyuran larvae in a low inflow estuary: Implications for bay-ocean exchange
Mar Ecol Prog Ser
,
2001
, vol.
217
(pg.
191
-
206
)
Dixon
PA
Milicich
MJ
Sugihara
G
Episodic fluctuation in larval supply
Science
,
1999
, vol.
283
(pg.
1528
-
30
)
Eckert
GL
Effects of the planktonic period on marine population fluctuations
Ecology
,
2003
, vol.
84
(pg.
372
-
83
)
Ellien
C
Thiebaut
E
Dumas
F
Salomon
JC
Nival
P
A modeling study of the respective role of hydrodynamic processes and larval mortality on larval dispersal and recruitment of benthic invertebrates: Example of Pectinaria koreni (Annelida: Polychaeta) in the Bay of Seine (English Channel)
J Plank Res
,
2004
, vol.
26
(pg.
117
-
32
)
Epifanio
CE
Garvine
RW
Larval transport on the Atlantic continental shelf of North America: a review
Est Coast Shelf Sci
,
2001
, vol.
52
(pg.
51
-
77
)
Etter
RJ
Rex
MA
Chase
MR
Quattro
JM
Population differentiation decreases with depth in deep-sea bivalves
Evolution
,
2005
, vol.
59
(pg.
1479
-
91
)
Fairweather
PG
Implications of ‘supply-side’ ecology for environmental assessment and management
Trends Ecol Evol
,
1991
, vol.
6
(pg.
60
-
3
)
Fields
PA
Graham
JB
Rosenblatt
RH
Somero
GN
Effects of expected global climate change on marine faunas
Trends Ecol Evol
,
1993
, vol.
8
(pg.
361
-
7
)
Forrester
GE
Swearer
SE
Trace elements in otoliths indicate the use of open-coast versus bay nursery habitats by juvenile California halibut
Mar Ecol Prog Ser
,
2002
, vol.
241
(pg.
201
-
13
)
Fowler
AJ
Campana
SE
Jones
CM
Thorrold
SR
Experimental assessment of the effect of temperature and salinity on elemental composition of otoliths using solution-based ICPMS
Can J Fish Aquat Sci
,
1995
, vol.
52
(pg.
1421
-
30
)
Gaines
SD
Bertness
MD
Dispersal of juveniles and variable recruitment in sessile marine species
Nature
,
1992
, vol.
360
(pg.
579
-
80
)
Gaines
S
Roughgarden
J
Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone
,
1985
, vol.
82
(pg.
3707
-
11
)
Gaylord
B
Gaines
SD
Temperature or transport? Range limits in marine species mediated solely by flow
Am Nat
,
2000
, vol.
155
(pg.
769
-
89
)
Gilg
MR
Hilbish
TJ
The geography of marine larval dispersal: coupling genetics with fine-scale physical oceanography
Ecology
,
2003
, vol.
84
(pg.
2989
-
98
)
Gillanders
BM
Temporal and spatial variability in elemental composition of otoliths: implications for determining stock identity and connectivity of populations
Can J Fish Aquat Sci
,
2002
, vol.
59
(pg.
669
-
79
)
Gillanders
BM
Kingsford
MJ
Elements in otoliths may elucidate the contribution of estuarine recruitment to sustaining coastal reef populations of a temperate reef fish
Mar Ecol Prog Ser
,
1996
, vol.
141
(pg.
13
-
20
)
Gillanders
BM
Kingsford
MJ
Elemental fingerprints of otoliths of fish may distinguish estuarine ‘nursery’ habitats
Mar Ecol Prog Ser
,
2000
, vol.
201
(pg.
273
-
86
)
Gillanders
BM
Kingsford
MJ
Spatial variation in elemental composition of otoliths of three species of fish (family Sparidae)
Est Coast Shelf Sci
,
2003
, vol.
57
(pg.
1049
-
64
)
Goldson
AJ
Hughes
RN
Gliddon
CJ
Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans
Mar Biol
,
2001
, vol.
138
(pg.
1037
-
42
)
Grantham
BA
Eckert
GL
Shanks
AL
Dispersal potential of marine invertebrates in diverse habitats
Ecol Appl
,
2003
, vol.
13
(pg.
S108
-
16
)
Grosberg
RK
Cunningham
CW
Bertness
MD
Gaines
SD
Hay
ME
Genetic structure in the sea from populations to communities
Marine community ecology
,
2001
Sunderland, Massachusetts
Sinauer
(pg.
61
-
84
)
Gunther
D
Horn
I
Hattendorf
B
Recent trends and developments in laser ablation-ICP-mass spectrometry
Fresenius J Anal Chem
,
2000
, vol.
368
(pg.
4
-
14
)
Hanski
I
Gilpin
M
Metapopulation dynamics: empirical and theoretical investigations
1991
San Diego, California
Havenhand
JN
McEdward
L
Evolutionary ecology of larval types
Ecology of marine invertebrate larvae
,
1995
Boca Raton, FL
CRC Press
(pg.
79
-
122
)
Hedgecock
D
Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates?
Bull Mar Sci
,
1986
, vol.
39
(pg.
550
-
64
)
Hellberg
ME
Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans
Evolution
,
1994
, vol.
48
(pg.
1829
-
54
)
Hellberg
ME
Burton
RS
Neigel
JE
Palumbi
SR
Genetic assessment of connectivity among marine populations
Bull Mar Sci
,
2002
, vol.
70
(pg.
S273
-
90
)
Herzka
SZ
Holt
SA
Holt
GJ
Characterization of settlement patterns of red drum Sciaenops ocellatus larvae to estuarine nursery habitat: a stable isotope approach
Mar Ecol Prog Ser
,
2002
, vol.
226
(pg.
143
-
56
)
Hickford
MJH
Schiel
DR
Comparative dispersal of larvae from demersal versus pelagic spawning fishes
Mar Ecol Prog Ser
,
2003
, vol.
252
(pg.
255
-
71
)
Hjort
J
Fluctuations in the year classes of important food fishes
J du Conseil
,
1926
, vol.
1
(pg.
5
-
38
)
Holmes
SP
Dekker
R
Williams
ID
Population dynamics and genetic differentiation in the bivalve mollusk Abra tenius: aplanic dispersal
Mar Ecol Prog Ser
,
2004
, vol.
268
(pg.
131
-
40
)
LA
Lutz
RA
Vrijenhoek
RC
Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents
Mol Ecol
,
2004
, vol.
13
(pg.
2603
-
15
)
Jablonski
D
Lutz
RA
Larval ecology of marine benthic invertebrates: Paleobiological implications
Biol Rev
,
1983
, vol.
58
(pg.
21
-
89
)
James
MK
Armsworth
PR
Mason
LB
Bode
L
The structure of reef fish metapopulations: Modeling larval dispersal and retention patterns
Proc Biol Sci
,
2002
, vol.
269
(pg.
2079
-
86
)
Johnson
MS
Black
R
Effects of isolation by distance and geographical discontinuity on genetic subdivision of Littorina cingulata
Mar Biol
,
1998
, vol.
132
(pg.
295
-
303
)
Jones
GP
Milicich
MJ
Emslie
MJ
Lunow
C
Self recruitment in a coral-reef fish population
Nature
,
1999
, vol.
402
(pg.
802
-
4
)
Josefson
AB
Temporal heterogeneity in deep-water soft-sediment benthos: an attempt to reveal temporal structure
Est Coast Shelf Sci
,
1986
, vol.
23
(pg.
147
-
69
)
Kalish
JM
Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition
J Exp Mar Biol Ecol
,
1989
, vol.
132
(pg.
151
-
78
)
Kawecki
TJ
Ebert
D
Ecol Lett
,
2004
, vol.
7
(pg.
1225
-
41
)
Killingley
JS
Rex
MA
Mode of larval development in some deep-sea gastropods indicated by oxygen-18 values of their carbonate shells
Deep-Sea Res
,
1985
, vol.
32
(pg.
809
-
18
)
Kingsford
MJ
Leis
JM
Shanks
A
Lindeman
KC
Morgan
SG
Pineda
J
Sensory environments, larval abilities and local self-recruitment
Bull Mar Sci
,
2002
, vol.
70
(pg.
S309
-
40
)
Kinlan
BP
Gaines
SD
Propagule dispersal in marine and terrestrial environments: A community perspective
Ecology
,
2003
, vol.
84
(pg.
2007
-
20
)
Klein
RT
Lohmann
KC
Thayer
CW
Bivalve skeletons record sea-surface temperature and δ18O via Mg/Ca and 18O/16O ratios
Geology
,
1996
, vol.
24
(pg.
415
-
8
)
Kotoulas
G
Bonhomme
F
Borsa
P
Genetic structure of the common sole Solea vulgaris at different geographic scales
Mar Biol
,
1995
, vol.
122
(pg.
361
-
75
)
Krug
PJ
Zimmer
RK
Developmental dimorphism: consequences for larval behavior and dispersal potential in a marine gastropod
Biol Bull
,
2004
, vol.
207
(pg.
233
-
46
)
Lambert
WJ
Todd
CD
Thorpe
JP
Genetic population structure of two intertidal nudibranch molluscs with contrasting larval types: Temporal variation and transplant experiments
Mar Biol
,
2003
, vol.
142
(pg.
461
-
71
)
Largier
JL
Considerations in estimating larval dispersal distances from oceanographic data
Ecol Appl
,
2003
, vol.
13
(pg.
S71
-
89
)
Largier
J
The importance of retention zones in the dispersal of larvae
Am Fish Soc Symp
,
2004
, vol.
42
(pg.
105
-
22
)
Lefebvre
A
Ellien
C
Davoult
D
Thiébaut
E
Salomon
JC
Pelagic dispersal of the brittle-star Ophiothrix fragilis larvae in a megatidal area (English Channel, France) examined using an advection-diffusion model
Est Coast Shelf Sci
,
2003
, vol.
57
(pg.
421
-
33
)
Leis
JM
Carson-Ewart
BM
Hay
AC
Cato
DH
Coral-reef sounds enable nocturnal navigation by some reef-fish larvae in some places and at some times
J Fish Biol
,
2003
, vol.
63
(pg.
724
-
37
)
Levin
LA
Life history and dispersal patterns in a dense infaunal polychaete assemblage: Community structure and response to disturbance
Ecology
,
1984
, vol.
65
(pg.
1185
-
200
)
Levin
LA
A review of methods for labeling and tracking marine invertebrate larvae
Ophelia
,
1990
, vol.
32
(pg.
115
-
44
)
Levin
LA
Huggett
DV
Implications of alternative development modes for seasonality and demography in an estuarine polychaete
Ecology
,
1990
, vol.
71
(pg.
2191
-
208
)
Levin
LA
Huggett
D
Myers
P
Bridges
T
Weaver
J
Rare earth tagging methods for the study of larval dispersal by marine invertebrates
Limnol Oceanogr
,
1993
, vol.
38
(pg.
346
-
60
)
Levin
LA
Talley
D
Thayer
G
Succession of macrobenthos in a created salt marsh
Mar Ecol Prog Ser
,
1996
, vol.
141
(pg.
67
-
82
)
Levin
LA
Becker
B
Fodrie
F
McMillan
P
Rasmussen
L
Cornuelle
B
DiBacco
C
Mullineaux
L
Strasser
C
Lerczak
J
others
Connectivity of bivalve populations: assessing sources of larval recruits
2005
International Ocean Research Conference
June
Paris, France
pg.
111

()
Lewin
R
Supply-side ecology
Science
,
1986
, vol.
234
(pg.
25
-
7
)
Lubchenco
J
Palumbi
SR
Gaines
SD
Andelman
S
Plugging a hole in the ocean: the emerging science of marine reserves
Ecol Appl
,
2003
, vol.
13
(pg.
S3
-
7
)
Lugo-Fernández
A
Deslarzes
KJP
Price
JM
Boland
GS
Morin
MV
Inferring probable dispersal of Flower Garden Banks coral larvae (Gulf of Mexico) using observed and simulated drifter trajectories
Cont Shelf Res
,
2001
, vol.
21
(pg.
47
-
67
)
Luttikhuizen
PC
Drent
J
Baker
AJ
Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal
Mol Ecol
,
2003
, vol.
12
(pg.
2215
-
29
)
Marko
PB
‘What's larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential
Mol Ecol
,
2004
, vol.
13
(pg.
597
-
611
)
Marsh
AG
Mullineaux
LS
Young
CM
Manahan
DT
Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents
Nature
,
2001
, vol.
411
(pg.
77
-
80
)
Martel
C
Viard
F
Bourguet
D
Garcia-Meunier
P
Invasion by the marine gastropod Ocinebrellus inornatus in France. II. Expansion along the Atlantic coast
Mar Ecol Prog Ser
,
2004
, vol.
273
(pg.
163
-
72
)
Mazzarelli
G
Note sulla biologia dell'Ostrica Ostrea edulis L. I. Nascia delle larve e durata del periodo larvale
Boll Soc Nat Napoli
,
1992
, vol.
34
(pg.
151
-
9
)
McEdward
LR
Janies
DA
Relationships among development, ecology, and morphology in the evolution of echinoderm larvae and life cycles
Biol J Linn Soc
,
1997
, vol.
60
(pg.
381
-
400
)
McEdward
LR
Morgan
KH
Interspecific relationship between egg size and the level of parental investment per offspring in echinoderms
Biol Bull
,
2001
, vol.
200
(pg.
33
-
50
)
McQuaid
CD
Phillips
TE
Limited wind-driven dispersal of the intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa
Mar Ecol Prog Ser
,
2000
, vol.
201
(pg.
211
-
20
)
Metaxas
A
Behaviour in flow: perspectives on the distribution and dispersion of meroplanktonic larvae in the water column
Can J Fish Aquat Sci
,
2001
, vol.
58
(pg.
86
-
98
)
Moilanen
A
Hanski
I
On the use of connectivity measures in spatial ecology
Oikos
,
2001
, vol.
95
(pg.
147
-
51
)
Mora
C
Sale
PF
Are populations of coral reef fish open or closed?
Trends Ecol Evol
,
2002
, vol.
17
(pg.
422
-
28
)
Nelson
TC
The attachment of oyster larvae
Biol Bull
,
1924
, vol.
46
(pg.
143
-
51
)
Neubert
MG
Caswell
H
Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations
Ecology
,
2000
, vol.
81
(pg.
1613
-
28
)
Olaffson
EB
Peterson
CH
Ambrose
WG
Does recruitment limitation structure populations and communities of macroinvertebrates in marine soft sediments? The relative significance of pre and post settlement processes
Oceanogr Mar Biol Ann Rev
,
1994
, vol.
32
(pg.
65
-
109
)
Palmer
AR
Strathmann
RR
Scale of dispersal in varying environments and its implications for life histories of marine invertebrates
Oecologia
,
1981
, vol.
48
(pg.
308
-
18
)
Palumbi
SR
Bertness
M
Gaines
SD
Hay
ME
The ecology of marine protected areas
Marine ecology: The new synthesis
,
2001
Sunderland, Massachusetts
Sinauer
(pg.
509
-
30
)
Palumbi
SR
Population genetics, demographic connectivity, and the design of marine reserves
Ecol Appl
,
2003
, vol.
13
(pg.
S146
-
58
)
Palumbi
SR
Grabowsky
G
Duda
T
Tachino
N
Geyer
L
Speciation and the evolution of population structure in tropical Pacific sea urchins
Evolution
,
1997
, vol.
51
(pg.
1506
-
17
)
Paris
CB
Cowen
RK
Direct evidence of a biophysical retention mechanism for coral reef fish larvae
Limnol Oceanogr
,
2004
, vol.
49
(pg.
1964
-
79
)
Pawlik
J
Chemical ecology of the settlement of benthic marine invertebrates
Oceanogr Mar Biol Annu Rev
,
1992
, vol.
30
(pg.
273
-
335
)
Pedersen
OP
Aschan
M
Rasmussen
T
Tande
KS
D
Larval dispersal and mother populations of Pandalus borealis investigated by a Lagrangian particle-tracking model
Fish Res
,
2003
, vol.
65
(pg.
173
-
90
)
Peterson
CH
Summerson
HC
Leuttich
RA
Jr.
Response of bay scallops to spawner transplants: a test of recruitment limitation
Mar Ecol Prog Ser
,
1996
, vol.
132
(pg.
93
-
107
)
Pitts
LC
Wallace
GT
Lead deposition in the shell of the bivalve, Mya arenaria: an indicator of dissolved lead in seawater
Estuar Coast Shelf Sci
,
1994
, vol.
39
(pg.
93
-
104
)
RL
Townsend
DW
Folsom
SD
Morrison
MA
Strontium: calcium concentration ratios in larval herring otoliths as indicators of environmental histories
Environ Biol Fish
,
1990
, vol.
27
(pg.
51
-
61
)
Reitzel
AM
Miner
BG
McEdward
LR
Relationships between spawning date and larval development time for benthic marine invertebrates: A modeling approach
Mar Ecol Prog Ser
,
2004
, vol.
280
(pg.
13
-
23
)
Rex
MA
McClain
CR
Johnson
NA
Etter
RJ
Allen
JA
Bouchet
P
Waren
A
A source-sink hypothesis for abyssal biodiversity
Am Nat
,
2005
, vol.
165
(pg.
163
-
78
)
Richards
SR
Possingham
HP
Noye
B
Larval dispersion along a straight coast with tidal currents: complex distribution patterns from a simple model
Mar Ecol Prog Ser
,
1995
, vol.
122
(pg.
59
-
71
)
Roberts
CM
Connectivity and management of Caribbean coral reefs
Science
,
1997
, vol.
278
(pg.
1454
-
7
)
Roy
K
Jablonski
D
Valentine
J
Climate change, species range limits and body size in marine bivalves
Ecol Lett
,
2001
, vol.
4
(pg.
366
-
70
)
Rumrill
SS
Natural mortality of marine invertebrate larvae
Ophelia
,
1990
, vol.
32
(pg.
163
-
98
)
Segovia-Zavala
JA
F
Alvarez-Borrego
S
Estuar Coast Shelf Sci
,
1998
, vol.
46
(pg.
475
-
481
)
Sewell
MA
Young
CM
Are echinoderm egg size distributions bimodal?
Biol Bull
,
1997
, vol.
193
(pg.
297
-
305
)
Shanks
AL
McEdward
l
Mechanisms of cross-shelf dispersal of larval invertebrates and fish
Ecology of marine invertebrate larvae
,
1995
Boca Raton, FL
CRC Press
(pg.
323
-
68
)
Shanks
AL
Grantham
BA
Carr
MH
Propagule dispersal distance and the size and spacing of marine reserves
Ecol Appl
,
2003
, vol.
13
(pg.
S159
-
69
)
Siegel
DA
Kinlan
BP
Gaylord
B
Gaines
SD
Lagrangian descriptions of marine larval dispersion
Mar Ecol Prog Ser
,
2003
, vol.
260
(pg.
83
-
96
)
Skold
M
Wing
SR
PV
Genetic subdivision of a sea star with high dispersal capability in relation to physical barriers in a fjordic seascape
Mar Ecol Prog Ser
,
2003
, vol.
250
(pg.
163
-
74
)
Sotka
EE
Local adaptation in host use among marine invertebrates
Ecol Lett
,
2005
, vol.
8
(pg.
448
-
59
)
Sotka
EE
Wares
JP
Barth
JA
Grosberg
RK
Palumbi
SR
Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula
Mol Ecol
,
2004
, vol.
13
(pg.
2143
-
56
)
Sousa
WP
A. Pickett
ST
White
PS
Disturbance and patch dynamics on rocky intertidal shores
The ecology of natural disturbance and patch dynamics
,
1985
Orlando, FL
(pg.
101
-
24
)
Sponaugle
S
Cowen
RK
Shanks
A
Morgan
SG
Leis
JM
Pineda
J
Boehlert
GW
Kingsford
MJ
Lindeman
KC
Grimes
C
Munro
JL
Predicting self-recruitment in marine populations: biophysical correlates and mechanisms
Bull Mar Sci
,
2002
, vol.
70
(pg.
341
-
75
)
Sponer
R
Roy
MS
Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential
Evolution
,
2002
, vol.
56
(pg.
1954
-
67
)
Staton
JL
Rice
ME
Genetic differentiation despite teleplanic larval dispersal: Allozyme variation in sipunculans of the Apionsoma species-complex
Bull Mar Sci
,
1999
, vol.
65
(pg.
467
-
80
)
Stobutzki
IC
Marine reserves and the complexity of larval dispersal
Rev Fish Biol Fish
,
2001
, vol.
10
(pg.
515
-
8
)
Strathmann
RR
Kennedy
VS
Selection for retention or export of larvae in estuaries
Estuarine comparisons
,
1982
New York
(pg.
521
-
36
)
Strathmann
RR
Hughes
TP
Kuris
AM
Lindeman
KC
Morgan
SG
Pandolfi
JM
Warner
RR
Evolution of local recruitment and its consequences for marine populations
Bull Mar Sci
,
2002
, vol.
70
(pg.
S377
-
96
)
Stuart
CT
Rex
MA
Etter
RJ
Tyler
PA
Large-scale spatial and temporal patterns of deep-sea benthic species diversity
Ecosystems of the World
,
2003
Amsterdam
Elsevier
(pg.
295
-
312
)
Swearer
SE
Caselle
JE
Lea
DW
Warner
RR
Larval retention and recruitment in an island population of coral-reef fish
Nature
,
1999
, vol.
402
(pg.
799
-
802
)
Swearer
SE
Shima
JS
Hellberg
ME
Thorrold
SR
Jones
GP
Robertson
DR
Morgan
SG
Selkoe
KA
Ruiz
GM
Warner
RR
Evidence of self-recruitment in demersal marine populations
Bull Mar Sci
,
2002
, vol.
70
(pg.
S251
-
71
)
Thorrold
SR
Shuttleworth
S
In situ analysis of trace elements and isotope ratios in fish otoliths using laser ablation sector field inductively coupled plasma mass spectrometry
Can J Fish Aquat Sci
,
2000
, vol.
57
(pg.
1232
-
42
)
Thorrold
SR
Campana
SE
Jones
CM
Swart
PK
Factors determining δ13C and δ18O fractionation in aragonitic otoliths of marine fish
Geochim Cosmochim Acta
,
1997
, vol.
61
(pg.
2909
-
19
)
Thorrold
SR
Jones
CM
Campana
SE
Response of otolith microchemistry to environmental variations experienced by larval and juvenile Atlantic croaker (Micropogonias undulates)
Limnol Oceanogr
,
1997
, vol.
42
(pg.
102
-
11
)
Thorrold
SR
Jones
CM
Campana
SE
McLaren
JW
Lam
JWH
Trace element signatures in otoliths record natal river of juvenile American shad (Alosa sapidissima)
Limnol Oceangr
,
1998
, vol.
43
(pg.
1826
-
35
)
Thorrold
SR
Latkoczy
C
Swart
PK
Jones
CM
Natal homing in a marine fish metapopulation
Science
,
2001
, vol.
291
(pg.
297
-
9
)
Thorrold
SR
Jones
GP
Hellberg
ME
Burton
RS
Swearer
SE
Neigel
JE
Morgan
SG
Warner
RR
Quantifying larval retention and connectivity in marine populations with artificial and natural markers
Bull Mar Sci
,
2002
, vol.
70
(pg.
S291
-
308
)
Thorson
G
Reproduction and larval development of Danish marine bottom invertebrates
Meddelelser fra Kommissionen for Hovundersoegelser Serie Plankton
,
1946
, vol.
4
(pg.
1
-
523
)
Thorson
G
Reproductive and larval ecology of marine bottom invertebrates
Biol Rev
,
1950
, vol.
25
(pg.
1
-
45
)
Todd
CD
Lambert
WJ
Thorpe
JP
The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae “for” dispersal?
J Exp Mar Biol Ecol
,
1998
, vol.
228
(pg.
1
-
28
)
Uthicke
S
Benzie
JAH
Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific
Mol Ecol
,
2003
, vol.
12
(pg.
2635
-
48
)
Vance
RR
On reproductive strategies in marine invertebrates
Am Nat
,
1973
, vol.
107
(pg.
339
-
52
)
Vrijenhoek
R
Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals
J Hered
,
1997
, vol.
88
(pg.
285
-
93
)
Wallace
AR
The geographical distribution of animals
1876
New York
Harpers
Warner
RR
Cowen
RK
Local retention of production in marine populations: evidence, mechanisms, and consequences
Bull Mar Sci
,
2002
, vol.
70
(pg.
S245
-
9
)
Weber
LI
Hartnoll
RG
Thorpe
JP
Genetic divergence and larval dispersal in two spider crabs (Crustacea:Decapoda)
Hydrobiologia
,
2000
, vol.
420
(pg.
211
-
9
)
Weis
VM
Reynolds
WS
de Boer
MD
Krupp
D
Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria
Coral Reefs
,
2001
, vol.
20
(pg.
301
-
8
)
Whitaker
K
Non-random mating and population genetic subdivision of two broadcasting corals at Ningaloo Reef, Western Australia
Mar Biol
,
2004
, vol.
144
(pg.
593
-
603
)
Witman
JD
Genovese
SJ
Bruno
JF
McLaughlin
JW
Pavlin
BI
Massive prey recruitment and the control of rocky subtidal communities on large spatial scales
Ecol Monogr
,
2003
, vol.
73
(pg.
441
-
62
)
Won
Y
Young
CR
Lutz
RA
Vrijenhoek
RC
Dispersal barriers and isolation among deep-sea mussel populations (Mytilidae: Bathymodiolus) from eastern Pacific hydrothermal vents
Mol Ecol
,
2003
, vol.
12
(pg.
169
-
84
)
Young
CM
On the novelty of “supply-side ecology”
Science
,
1987
, vol.
235
(pg.
415
-
6
)
Young
CM
Field inferences in the ecology of marine invertebrate larvae
Ophelia
,
1990
, vol.
32

Nos 1 and 2
Young
CM
McEdward
L
Behavior and locomotion during the dispersal phase of larval life
Ecology of marine invertebrate larvae
,
1995
Boca Raton
CRC Press
(pg.
249
-
77
)
Young
CM
Chia
FS
Giese
AC
Pearse
JS
Pearse
VB
Abundance and distribution of pelagic larvae as influenced by predation, behavior and hydrographic factors
Reproduction of marine invertebrates. Vol. 9. General Aspects: Seeking Unity in Diversity
,
1987
Palo Alto
Blackwell/Boxwood
(pg.
385
-
463
)
Zacherl
DC
Spatial and temporal variation in statolith and protoconch trace elements as natural tags to track larval dispersal
Mar Ecol Prog Ser
,
2005
, vol.
290
(pg.
145
-
63
)
Zacherl
DC
Manríquez
PH
G
Day
RW
Castilla
JC
Warner
RR
Lea
DW
Gaines
SG
Trace elemental fingerprinting of gastropod statoliths to study larval dispersal trajectories
Mar Ecol Prog Ser
,
2003
, vol.
248
(pg.
297
-
303
)
Zacherl
DC
G
Lea
DW
Barium and strontium uptake in larval protoconch and statolith of the marine neogastropod Kelletia kelletii
Geochim Cosmochim Acta
,
2003
, vol.
67
(pg.
4091
-
9
)

## Author notes

From the symposium “Complex Life-Histories of Marine Benthic Invertebrates: A Symposium in Memory of Larry McEdward” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, San Diego, CA.